Skip to main content

Advertisement

Log in

Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update

  • Review Article
  • Published:
Archives of Toxicology Aims and scope Submit manuscript

Abstract

Heat shock proteins (HSP) are a subset of the molecular chaperones, best known for their rapid and abundant induction by stress. HSP genes are activated at the transcriptional level by heat shock transcription factor 1 (HSF1). During the progression of many types of cancer, this heat shock transcriptional regulon becomes co-opted by mechanisms that are currently unclear, although evidently triggered in the emerging tumor cell. Concerted activation of HSF1 and the accumulation of HSPs then participate in many of the traits that permit the malignant phenotype. Thus, cancers of many histologies exhibit activated HSF1 and increased HSP levels that may help to deter tumor suppression and evade therapy in the clinic. We review here the extensive work that has been carried out and is still in progress aimed at (1) understanding the oncogenic mechanisms by which HSP genes are switched on, (2) determining the roles of HSF1/HSP in malignant transformation and (3) discovering approaches to therapy based on disrupting the influence of the HSF1-controlled transcriptome in cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarwal M, Pandita S, Hunt CR, Gupta A, Yue X, Khan S, Pandita RK, Pratt D, Shay JW, Taylor JS, Pandita TK (2008) Inhibition of telomerase activity enhances hyperthermia-mediated radiosensitization. Cancer Res 68:3370–3378

    Article  PubMed  CAS  Google Scholar 

  • Aghdassi A, Phillips P, Dudeja V et al (2007) Heat shock protein 70 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res 67(2):616–625

    Article  PubMed  CAS  Google Scholar 

  • Ahmad MF, Raman B, Ramakrishna T, Rao Ch M (2008) Effect of phosphorylation on alpha B-crystallin: differences in stability, subunit exchange and chaperone activity of homo and mixed oligomers of alpha B-crystallin and its phosphorylation-mimicking mutant. J Mol Biol 375(4):1040–1051

    Article  PubMed  CAS  Google Scholar 

  • Al-Madhoun AS, Chen YX, Haidari L et al (2007) The interaction and cellular localization of HSP27 and ERbeta are modulated by 17beta-estradiol and HSP27 phosphorylation. Mol Cell Endocrinol 270(1–2):33–42

    Article  PubMed  CAS  Google Scholar 

  • Aloy MT, Hadchity E, Bionda C, Diaz-Latoud C, Claude L, Rousson R, Arrigo AP, Rodriguez-Lafrasse C (2008) Protective role of Hsp27 protein against gamma radiation-induced apoptosis and radiosensitization effects of Hsp27 gene silencing in different human tumor cells. Int J Radiat Oncol Biol Phys 70:543–553

    Article  PubMed  CAS  Google Scholar 

  • Altieri DC (2003) Validating survivin as a cancer therapeutic target. Nat Rev Cancer 3(1):46–54

    Article  PubMed  CAS  Google Scholar 

  • Andrieu C, Taieb D, Baylot V et al (2010) Heat shock protein 27 confers resistance to androgen ablation and chemotherapy in prostate cancer cells through eIF4E. Oncogene 29(13):1883–1896

    Article  PubMed  CAS  Google Scholar 

  • Aoyama A, Frohli E, Schafer R, Klemenz R (1993) Alpha B-crystallin expression in mouse NIH 3T3 fibroblasts: glucocorticoid responsiveness and involvement in thermal protection. Mol Cell Biol 13(3):1824–1835

    PubMed  CAS  Google Scholar 

  • Aquilina JA, Benesch JL, Ding LL, Yaron O, Horwitz J, Robinson CV (2004) Phosphorylation of alphaB-crystallin alters chaperone function through loss of dimeric substructure. J Biol Chem 279(27):28675–28680

    Article  PubMed  CAS  Google Scholar 

  • Arispe N, Doh M, Simakova O, Kurganov B, De Maio A (2004) Hsc70 and Hsp70 interact with phosphatidylserine on the surface of PC12 cells resulting in a decrease of viability. FASEB J 18(14):1636–1645

    Article  PubMed  CAS  Google Scholar 

  • Arrigo AP (2000) sHsp as novel regulators of programmed cell death and tumorigenicity. Pathol Biol (Paris) 48(3):280–288

    CAS  Google Scholar 

  • Arrigo AP (2001) Hsp27: novel regulator of intracellular redox state. IUBMB Life 52(6):303–307

    Article  PubMed  CAS  Google Scholar 

  • Arrigo AP (2005) In search of the molecular mechanism by which small stress proteins counteract apoptosis during cellular differentiation. J Cell Biochem 94(2):241–246

    Article  PubMed  CAS  Google Scholar 

  • Arrigo AP (2011) Structure-functions of HspB1 (Hsp27). Methods Mol Biol 787:105–119

    Article  PubMed  CAS  Google Scholar 

  • Arteaga CL (2011) Why is this effective HSP90 inhibitor not being developed in HER2+ breast cancer? Clin Cancer Res 17(15):4919–4921

    Article  PubMed  CAS  Google Scholar 

  • Barbash O, Lin DI, Diehl JA (2007) SCF Fbx4/alphaB-crystallin cyclin D1 ubiquitin ligase: a license to destroy. Cell Div 2:2

    Article  PubMed  CAS  Google Scholar 

  • Bauer K, Nitsche U, Slotta-Huspenina J, Drecoll E, von Weyhern CH, Rosenberg R, Höfler H, Langer R (2012) High HSP27 and HSP70 expression levels are independent adverse prognostic factors in primary resected colon cancer. Cell Oncol (Dordr) 3:197–205

    Google Scholar 

  • Bausero MA, Page DT, Osinaga E, Asea A (2004) Surface expression of Hsp25 and Hsp72 differentially regulates tumor growth and metastasis. Tumour Biol 25(5–6):243–251

    Article  PubMed  CAS  Google Scholar 

  • Bausero MA, Bharti A, Page DT et al (2006) Silencing the hsp25 gene eliminates migration capability of the highly metastatic murine 4T1 breast adenocarcinoma cell. Tumour Biol 27(1):17–26 (Epub 2005 Dec 8)

    Article  PubMed  CAS  Google Scholar 

  • Beere HM, Wolf BB, Cain K et al (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the apaf-1 apoptosome. Nat Cell Biol 2(8):469–475

    Article  PubMed  CAS  Google Scholar 

  • Behnsawy HM, Miyake H, Kusuda Y, Fujisawa M (2011) Small interfering RNA targeting heat shock protein 70 enhances chemosensitivity in human bladder cancer cells. Urol Oncol [Epub ahead of print]

  • Bellyei S, Szigeti A, Pozsgai E et al (2007) Preventing apoptotic cell death by a novel small heat shock protein. Eur J Cell Biol 86(3):161–171

    Article  PubMed  CAS  Google Scholar 

  • Beresford PJ, Jaju M, Friedman RS, Yoon MJ, Lieberman J (1998) A role for heat shock protein 27 in CTL-mediated cell death. J Immunol 161(1):161–167

    PubMed  CAS  Google Scholar 

  • Bhat SP, Nagineni CN (1989) αB subunit of lens-specific protein α-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158(1):319–325

    Article  PubMed  CAS  Google Scholar 

  • Blackburn RV, Galoforo SS, Berns CM et al (1997) comparison of tumor growth between Hsp25- and Hsp27- transfected murine L929 cells in nude mice. Int J Cancer 72:871–877

    Article  PubMed  CAS  Google Scholar 

  • Blagosklonny MV (2002) Hsp-90-associated oncoproteins: multiple targets of geldanamycin and its analogs. Leukemia 16(4):455–462

    Article  PubMed  CAS  Google Scholar 

  • Boelens WC, Croes Y, de Jong WW (2001) Interaction between alphaB-crystallin and the human 20S proteasomal subunit C8/alpha7. Biochim Biophys Acta 1544(1–2):311–319

    Article  PubMed  CAS  Google Scholar 

  • Bruey JM, Ducasse C, Bonniaud P et al (2000a) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol 2(9):645–652

    Article  PubMed  CAS  Google Scholar 

  • Bruey JM, Paul C, Fromentin A et al (2000b) Differential regulation of HSP27 oligomerization in tumor cells grown in vitro and in vivo. Oncogene 19(42):4855–4863

    Article  PubMed  CAS  Google Scholar 

  • Bruinsma IB, Bruggink KA, Kinast K et al (2011) Inhibition of alpha-synuclein aggregation by small heat shock proteins. Proteins 79(10):2956–2967

    Article  PubMed  CAS  Google Scholar 

  • Brunet Simioni M, De Thonel A, Hammann A et al (2009) Heat shock protein 27 is involved in SUMO-2/3 modification of heat shock factor 1 and thereby modulates the transcription factor activity. Oncogene 28:3332–3344

    Article  PubMed  CAS  Google Scholar 

  • Buchner J (1999) Hsp90 & Co.—a holding for folding. Trends Biochem Sci 24(4):136–141

    Article  PubMed  CAS  Google Scholar 

  • Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366

    Article  PubMed  CAS  Google Scholar 

  • Cai H, Yin S, Ma F et al (2011) ShRNA-mediated gene silencing of heat shock protein 70 inhibits human colon cancer cell growth in vitro and in vivo. Mol Cell Biochem [Epub ahead of print]

  • Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 31(3):164–172 (Epub 2006 Feb 17)

    Article  PubMed  CAS  Google Scholar 

  • Calderwood SK et al (2010) Signal transduction pathways leading to heat shock transcription. Sign Transduct Insights 2:13–24

    Article  PubMed  Google Scholar 

  • Cappello F, Bellafiore M, Palma A et al (2003) 60KDa chaperonin (HSP60) is over-expressed during colorectal carcinogenesis. Eur J Histochem 47(2):105–110

    PubMed  CAS  Google Scholar 

  • Cappello F, Czarnecka AM, La Rocca G, Di Stefano A, Zummo G, Macario AJ (2007) Hsp60 and Hspl0 as antitumor molecular agents. Cancer Biol Ther 6(4):487–489

    Article  PubMed  CAS  Google Scholar 

  • Cappello F, Conway de Macario E, Marasa L, Zummo G, Macario AJ (2008) Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol Ther 7(6):801–809

    Article  PubMed  CAS  Google Scholar 

  • Cappello F, David S, Peri G, Farina F, Conway de Macario E, Macario AJ, Zummo G (2011) Hsp60: molecular anatomy and role in colorectal cancer diagnosis and treatment. Front Biosci (Schol Ed) 3:341–351

    Article  Google Scholar 

  • Carra S (2009) The stress-inducible HspB8-Bag3 complex induces the eIF2alpha kinase pathway: implications for protein quality control and viral factory degradation? Autophagy 5(3):428–429

    Article  PubMed  CAS  Google Scholar 

  • Carra S, Sivilotti M, Chavez Zobel AT, Lambert H, Landry J (2005) HspB8, a small heat shock protein mutated in human neuromuscular disorders, has in vivo chaperone activity in cultured cells. Hum Mol Genet 14(12):1659–1669

    Article  PubMed  CAS  Google Scholar 

  • Carra S, Seguin SJ, Landry J (2008) HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 4(2):237–239

    PubMed  CAS  Google Scholar 

  • Castilla C, Congregado B, Conde JM, Medina R, Torrubia FJ, Japón MA, Sáez C (2010) Immunohistochemical expression of Hsp60 correlates with tumor progression and hormone resistance in prostate cancer. Urology 76:1017e1–1017e6

    Article  Google Scholar 

  • Cayado-Gutiérrez N, Moncalero VL, Rosales EM, Berón W, Salvatierra EE, Radrizzani M, Ciocca DR (2012) Down-regulation of Hsp27 (HSPB1) in MCF-7 human breast cancer cells induces up-regulation of PTEN. Cell Stress Chaperones (in press)

  • Chalmin F et al (2010) Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 120:457–471

    PubMed  CAS  Google Scholar 

  • Chandra D, Choy G, Tang DG (2007) Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J Biol Chem 282(43):31289–31301

    Article  PubMed  CAS  Google Scholar 

  • Charette SJ, Landry J (2000) The interaction of HSP27 with Daxx identifies a potential regulatory role of HSP27 in Fas-induced apoptosis. Ann N Y Acad Sci 926:126–131

    Article  PubMed  CAS  Google Scholar 

  • Charette SJ, Lavoie JN, Lambert H, Landry J (2000) Inhibition of daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol 20(20):7602–7612

    Article  PubMed  CAS  Google Scholar 

  • Chebotareva NA, Makeeva VF, Bazhina SG, Eronina TB, Gusev NB, Kurganov BI (2010) Interaction of Hsp27 with native phosphorylase kinase under crowding conditions. Macromol Biosci 10(7):783–789

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Dai RY, Duan CY, Liu YP, Chen SK, Yan DM, Chen CN, Wei M, Li H (2011) Unfolded protein response suppresses cisplatin-induced apoptosis via autophagy regulation in human hepatocellular carcinoma cells. Folia Biol (Praha) 57:87–95

    CAS  Google Scholar 

  • Chiosis G, Tao H (2006) Purine-scaffold Hsp90 inhibitors. IDrugs 9:778–782

    PubMed  CAS  Google Scholar 

  • Chiu CC, Lin CY, Lee LY, Chen YJ, Lu YC, Wang HM, Liao CT, Chang JT, Cheng AJ (2011) Molecular chaperones as a common set of proteins that regulate the invasion phenotype of head and neck cancer. Clin Cancer Res 17:4629–4641

    Article  PubMed  CAS  Google Scholar 

  • Choi SH, Lee YJ, Seo WD, Lee HJ, Nam JW, Lee YJ, Kim J, Seo EK, Lee YS (2011) Altered cross-linking of HSP27 by zerumbone as a novel strategy for overcoming HSP27-mediated radioresistance. Int J Radiat Oncol Biol Phys 79:1196–1205

    Article  PubMed  CAS  Google Scholar 

  • Chu B et al (1996) Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J Biol Chem 271:30847–30857

    Article  PubMed  CAS  Google Scholar 

  • Cintron NS, Toft D (2006) Defining the requirements for Hsp40 and Hsp70 in the Hsp90 chaperone pathway. J Biol Chem 281(36):26235–46224

    Article  PubMed  CAS  Google Scholar 

  • Ciocca DR, Calderwood SK (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10(2):86–103

    Article  PubMed  CAS  Google Scholar 

  • Ciocca DR, Fuqua SAW, Lock-Lim S, Toft DO, Welch WJ, Mc Guire WL (1992) Response of human breast cancer cells to heat shock and chemotherapeutic drugs. Cancer Res 52:3648–3654

    PubMed  CAS  Google Scholar 

  • Ciocca DR, Gago FE, Fanelli MA, Calderwood SK (2006) Co-expression of steroid receptors (estrogen receptor alpha and/or progesterone receptors) and Her-2/neu: clinical implications. J Steroid Biochem Mol Biol 102:32–40

    Article  PubMed  CAS  Google Scholar 

  • Ciocca DR, Fanelli MA, Cuello-Carrion FD, Castro GN (2010) Heat shock proteins in prostate cancer: from tumorigenesis to the clinic. Int J Hyperthermia 26:737–747

    Article  PubMed  CAS  Google Scholar 

  • Ciocca DR, Cuello-Carrión FD, Natoli AL, Restall C, Anderson RL (2012a) Absence of caveolin-1 alters heat shock protein expression in spontaneous mammary tumors driven by Her-2/neu expression. Histochem Cell Biol 137:187–194

    Article  PubMed  CAS  Google Scholar 

  • Ciocca DR, Cayado-Gutiérrez N, Maccioni M, Cuello-Carrión FD (2012b) Heat shock proteins (HSPs) based anti-cancer vaccines. Curr Mol Med [Epub ahead of print]

  • Colas P, Cohen B, Jessen T, Grishina I, McCoy J, Brent R (1996) Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 380:548–550

    Article  PubMed  CAS  Google Scholar 

  • Craig EA (1985) The heat shock response. CRC Crit Rev Biochem 18:239–280

    Article  PubMed  CAS  Google Scholar 

  • Cuesta R, Laroia G, Schneider RJ (2000) Chaperone Hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 14(12):1460–1470

    PubMed  CAS  Google Scholar 

  • Dai C et al (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130:1005–1018

    Article  PubMed  CAS  Google Scholar 

  • Dai S, Jiang L, Wang G et al (2010) HSP70 interacts with TRAF2 and differentially regulates TNFalpha signalling in human colon cancer cells. J Cell Mol Med 14(3):710–725

    PubMed  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Milzani A, Di Simplicio P, Colombo R (2001) The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic Biol Med 31(12):1624–1632

    Article  PubMed  CAS  Google Scholar 

  • Dall’Era MA, Oudes A, Martin DB, Liu AY (2007) HSP27 and HSP70 interact with CD10 in C4-2 prostate cancer cells. Prostate 67(7):714–721

    Article  PubMed  CAS  Google Scholar 

  • Daugaard M, Jaattela M, Rohde M (2005) Hsp70-2 is required for tumor cell growth and survival. Cell Cycle 4(7):877–880

    Article  PubMed  CAS  Google Scholar 

  • Daugaard M, Kirkegaard-Sorensen T, Ostenfeld MS et al (2007a) Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res 67(6):2559–2567

    Article  PubMed  CAS  Google Scholar 

  • Daugaard M, Rohde M, Jaattela M (2007b) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581(19):3702–3710

    Article  PubMed  CAS  Google Scholar 

  • De Bessa SA, Salaorni S, Patrao DF, Neto MM, Brentani MM, Nagai MA (2006) JDP1 (DNAJC12/Hsp40) expression in breast cancer and its association with estrogen receptor status. Int J Mol Med 17(2):363–367

    PubMed  Google Scholar 

  • De Chassey B, Mikaelian I, Mathieu AL et al (2006) An antiproliferative genetic screening identifies a peptide aptamer that targets calcineurin and upregulates its activity. Mol Cell Proteomics 4:4

    Google Scholar 

  • De Thonel A, Vandekerckhove J, Lanneau D et al (2010) HSP27 controls GATA-1 protein level during erythroid cell differentiation. Blood 116(1):85–96

    Article  PubMed  CAS  Google Scholar 

  • den Engelsman J, Keijsers V, de Jong WW, Boelens WC (2003) The small heat-shock protein alpha B-crystallin promotes FBX4-dependent ubiquitination. J Biol Chem 278(7):4699–4704

    Article  CAS  Google Scholar 

  • Deng M, Chen PC, Xie S et al (2010) The small heat shock protein alphaA-crystallin is expressed in pancreas and acts as a negative regulator of carcinogenesis. Biochim Biophys Acta 1802(7–8):621–631

    PubMed  CAS  Google Scholar 

  • Desmetz C, Bibeau F, Boissière F, Bellet V, Rouanet P, Maudelonde T, Mangé A, Solassol J (2008) Proteomics-based identification of HSP60 as a tumor-associated antigen in early stage breast cancer and ductal carcinoma in situ. J Proteome Res 7:3830–3837

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Latoud C, Buache E, Javouhey E, Arrigo AP (2005) Substitution of the unique cysteine residue of murine hsp25 interferes with the protective activity of this stress protein through inhibition of dimer formation. Antioxid Redox Signal 7(3–4):436–445

    Article  PubMed  CAS  Google Scholar 

  • Dohi T, Beltrami E, Wall NR, Plescia J, Altieri DC (2004) Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis. J Clin Invest 114(8):1117–1127

    PubMed  CAS  Google Scholar 

  • Dorard C, de Thonel A, Collura A, Marisa L, Svrcek M, Lagrange A, Jego G, Wanherdrick K, Joly AL, Buhard O, Gobbo J, Penard-Lacronique V, Zouali H, Tubacher E, Kirzin S, Selves J, Milano G, Etienne-Grimaldi MC, Bengrine-Lefèvre L, Louvet C, Tournigand C, Lefèvre JH, Parc Y, Tiret E, Fléjou JF, Gaub MP, Garrido C, Duval A (2011) Expression of a mutant HSP110 sensitizes colorectal cancer cells to chemotherapy and improves disease prognosis. Nat Med 17:1283–1289

    Article  PubMed  CAS  Google Scholar 

  • Dudeja V et al (2011) Prosurvival role of heat shock factor 1 in the pathogenesis of pancreatobiliary tumors. Am J Physiol Gastrointest Liver Physiol 300:G948–G955

    Article  PubMed  CAS  Google Scholar 

  • Dutta R, Inouye M (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25(1):24–28

    Article  PubMed  CAS  Google Scholar 

  • Eccles SA et al (2008) NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Res 68:2850–2860

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ (2006) Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31:395–401

    Article  PubMed  CAS  Google Scholar 

  • Erlichman C (2009) Tanespimycin: the opportunities and challenges of targeting heat shock protein 90. Expert Opin Investig Drugs 18(6):861–868

    Article  PubMed  CAS  Google Scholar 

  • Fanelli MA, Montt-Guevara M, Diblasi AM et al (2008) P-cadherin and beta-catenin are useful prognostic markers in breast cancer patients; beta-catenin interacts with heat shock protein Hsp27. Cell Stress Chaperones 13(2):207–220

    Article  PubMed  CAS  Google Scholar 

  • Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO (2000) The hsp90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 275(5):3305–3312

    Article  PubMed  CAS  Google Scholar 

  • Fishel R et al (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75:1027–1038

    Article  PubMed  CAS  Google Scholar 

  • Fortugno P, Beltrami E, Plescia J et al (2003) Regulation of survivin function by Hsp90. Proc Natl Acad Sci USA 100(24):13791–13796

    Article  PubMed  CAS  Google Scholar 

  • Fourie AM, Hupp TR, Lane DP et al (1997) HSP70 binding sites in the tumor suppressor protein p53. J Biol Chem 272(31):19471–19479

    Article  PubMed  CAS  Google Scholar 

  • Fu L, Liang JJ (2003) Enhanced stability of alpha B-crystallin in the presence of small heat shock protein Hsp27. Biochem Biophys Res Commun 302(4):710–714

    Article  PubMed  CAS  Google Scholar 

  • Fujita R, Ounzain S, Wang AC, Heads RJ, Budhram-Mahadeo VS (2011) Hsp-27 induction requires POU4F2/Brn-3b TF in doxorubicin-treated breast cancer cells, whereas phosphorylation alters its cellular localisation following drug treatment. Cell Stress Chaperones 16:427–439

    Article  PubMed  CAS  Google Scholar 

  • Fukagawa Y, Nishikawa J, Kuramitsu Y, Iwakiri D, Takada K, Imai S, Satake M, Okamoto T, Fujimoto M, Okita K, Nakamura K, Sakaida I (2008) Epstein-Barr virus upregulates phosphorylated heat shock protein 27 kDa in carcinoma cells using the phosphoinositide 3-kinase/Akt pathway. Electrophoresis 29:3192–3200

    PubMed  CAS  Google Scholar 

  • Fulda S, Galluzzi L, Kroemer G (2010) Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 9(6):447–464

    Article  PubMed  CAS  Google Scholar 

  • Gabai VL, Sherman MY (2005) Hsp72 and cell signaling. Cambdridge Univ. Press, Cambridge

    Google Scholar 

  • Gabai VL et al (2009) Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol Cell Biol 29:559–569

    Article  PubMed  CAS  Google Scholar 

  • Ganea E (2001) Chaperone-like activity of alpha-crystallin and other small heat shock proteins. Curr Protein Pept Sci 2(3):205–225

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Han C, Huang H et al (2010) Heat shock protein 70 together with its co-chaperone CHIP inhibits TNF-alpha induced apoptosis by promoting proteasomal degradation of apoptosis signal-regulating kinase1. Apoptosis 15(7):822–833

    Article  PubMed  CAS  Google Scholar 

  • Garrido C, Fromentin A, Bonnotte B et al (1998) Heat shock protein 27 enhances the tumorigenicity of immunogenic rat colon carcinoma cell clones. Cancer Res 58(23):5495–5499

    PubMed  CAS  Google Scholar 

  • Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E (1999) HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 13(14):2061–2070

    PubMed  CAS  Google Scholar 

  • Garrido C, Gurbuxani S, Ravagnan L, Kroemer G (2001) Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 286(3):433–442

    Article  PubMed  CAS  Google Scholar 

  • Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E, Kroemer G (2006) Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5(22):2592–2601

    Google Scholar 

  • Gastpar R, Gehrmann M, Bausero MA et al (2005) Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 65(12):5238–5247

    Article  PubMed  CAS  Google Scholar 

  • Gehrmann M, Radons J, Molls M, Multhoff G (2008) The therapeutic implications of clinically applied modifiers of heat shock protein 70 (Hsp70) expression by tumor cells. Cell Stress Chaperones 13(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Georgakis GV, Younes A (2005) Heat-shock protein 90 inhibitors in cancer therapy: 17AAG and beyond. Future Oncol 1(2):273–281

    Article  PubMed  CAS  Google Scholar 

  • George J, Srivastava AK, Singh R, Shukla Y (2011) Cypermethrin exposure leads to regulation of proteins expression involved in neoplastic transformation in mouse skin. Proteomics 11:4411–4421

    Article  PubMed  CAS  Google Scholar 

  • Ghosh JC, Dohi T, Kang BH, Altieri DC (2008) Hsp60 regulation of tumor cell apoptosis. J Biol Chem 283(8):5188–5194

    Article  PubMed  CAS  Google Scholar 

  • Ghosh JC, Siegelin MD, Dohi T, Altieri DC (2010) Heat shock protein 60 regulation of the mitochondrial permeability transition pore in tumor cells. Cancer Res 70(22):8988–8993

    Article  PubMed  CAS  Google Scholar 

  • Gibert B, Hadchity E, Czekalla A et al (2011) Inhibition of heat shock protein 27 (HspB1) tumorigenic functions by peptide aptamers. Oncogene 34:3672–3681

    Article  CAS  Google Scholar 

  • Gibert B, Eckel B, Fasquelle L et al (2012a) Knock down of heat shock protein 27 (HspB1) induces degradation of several putative client proteins. PLoS ONE 7(1):e29719

    Article  PubMed  CAS  Google Scholar 

  • Gibert B, Eckel B, Gonin et al (2012b) Targeting heat shock protein 27 (HspB1) interferes with bone metastasis and tumor formation in vivo. Br J Cancer. 24 May. doi:10.1038/bjc.2012.188 [Epub ahead of print]

  • Giordano C, Catalano S, Panza S, Vizza D, Barone I, Bonofiglio D, Gelsomino L, Rizza P, Fuqua SA, Andò S (2011) Farnesoid X receptor inhibits tamoxifen-resistant MCF-7 breast cancer cell growth through downregulation of HER2 expression. Oncogene 30:4129–4140

    Article  PubMed  CAS  Google Scholar 

  • Glaessgen A, Jonmarker S, Lindberg A et al (2008) Heat shock proteins 27, 60 and 70 as prognostic markers of prostate cancer. Apmis 116(10):888–895

    Article  PubMed  Google Scholar 

  • Golembieski WA, Thomas SL, Schultz CR, Yunker CK, McClung HM, Lemke N, Cazacu S, Barker T, Sage EH, Brodie C, Rempel SA (2008) HSP27 mediates SPARC-induced changes in glioma morphology, migration, and invasion. Glia 56:1061–1075

    Article  PubMed  Google Scholar 

  • Gray PJ Jr et al (2008) Targeting the oncogene and kinome chaperone CDC37. Nat Rev Cancer 8:491–495

    Article  PubMed  CAS  Google Scholar 

  • Gross C, Koelch W, DeMaio A, Arispe N, Multhoff G (2003) Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J Biol Chem 278(42):41173–41181

    Article  PubMed  CAS  Google Scholar 

  • Gruvberger-Saal SK, Parsons R (2006) Is the small heat shock protein alphaB-crystallin an oncogene? J Clin Invest 116(1):30–32

    Article  PubMed  CAS  Google Scholar 

  • Gullino PM (1966) The internal milieu of tumors. Prog Exp Tumor Res 8:1–25

    PubMed  CAS  Google Scholar 

  • Guo H, Bai Y, Xu P, Hu Z, Liu L, Wang F, Jin G, Wang F, Deng Q, Tu Y, Feng M, Lu D, Shen H, Wu T (2010) Functional promoter −1271G>C variant of HSPB1 predicts lung cancer risk and survival. J Clin Oncol 28:1928–1935

    Article  PubMed  CAS  Google Scholar 

  • Gurbuxani S, Bruey JM, Fromentin A et al (2001) Selective depletion of inducible HSP70 enhances immunogenicity of rat colon cancer cells. Oncogene 20(51):7478–7485

    Article  PubMed  CAS  Google Scholar 

  • Hadchity E, Aloy MT, Paulin C, Armandy E, Watkin E, Rousson R, Gleave M, Chapet O, Rodriguez-Lafrasse C (2009) Heat shock protein 27 as a new therapeutic target for radiation sensitization of head and neck squamous cell carcinoma. Mol Ther 17:1387–1394

    Article  PubMed  CAS  Google Scholar 

  • Hahn JS, Neef DW, Thiele DJ (2006) A stress regulatory network for co-ordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Mol Microbiol 60:240–251

    Article  PubMed  CAS  Google Scholar 

  • Hamelin C, Cornut E, Poirier F, Pons S, Beaulieu C, Charrier JP, Haïdous H, Cotte E, Lambert C, Piard F, Ataman-Önal Y, Choquet-Kastylevsky G (2011) Identification and verification of heat shock protein 60 as a potential serum marker for colorectal cancer. FEBS J 278:4845–4859

    Article  PubMed  CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    Article  PubMed  CAS  Google Scholar 

  • Havasi A, Li Z, Wang Z et al (2008) Hsp27 inhibits Bax activation and apoptosis via a phosphatidylinositol 3-kinase-dependent mechanism. J Biol Chem 283(18):12305–12313

    Article  PubMed  CAS  Google Scholar 

  • Hayashi N, Peacock JW, Beraldi E, Zoubeidi A, Gleave ME, Ong CJ (2012) Hsp27 silencing coordinately inhibits proliferation and promotes Fas-induced apoptosis by regulating the PEA-15 molecular switch. Cell Death Differ 19(6):990–1002

    Article  PubMed  CAS  Google Scholar 

  • Heinrich JC, Tuukkanen A, Schroeder M, Fahrig T, Fahrig R (2011) RP101 (brivudine) binds to heat shock protein HSP27 (HSPB1) and enhances survival in animals and pancreatic cancer patients. J Cancer Res Clin Oncol 137:1349–1361

    Article  PubMed  Google Scholar 

  • Hernandez MP, Sullivan WP, Toft DO (2002) The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J Biol Chem 277(41):38294–38304

    Article  PubMed  CAS  Google Scholar 

  • Hessling M, Richter K, Buchner J (2009) Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90. Nat Struct Mol Biol 16(3):287–293

    Article  PubMed  CAS  Google Scholar 

  • Hietakangas V et al (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol Cell Biol 23:2953–2968

    Article  PubMed  CAS  Google Scholar 

  • Hino M, Kurogi K, Okubo MA, Murata-Hori M, Hosoya H (2000) Small heat shock protein 27 (HSP27) associates with tubulin/microtubules in HeLa cells. Biochem Biophys Res Commun 271(1):164–169

    Article  PubMed  CAS  Google Scholar 

  • Horwitz J, Huang Q-L, Ding L-L (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    Article  PubMed  CAS  Google Scholar 

  • Horwitz J, Huang Q, Ding L (2004) The native oligomeric organization of alpha-crystallin, is it necessary for its chaperone function? Exp Eye Res 79(6):817–821

    Article  PubMed  CAS  Google Scholar 

  • Hsu HS, Lin JH, Huang WC, Hsu TW, Su K, Chiou SH, Tsai YT, Hung SC (2011) Chemoresistance of lung cancer stemlike cells depends on activation of Hsp27. Cancer 117:1516–1528

    Article  PubMed  CAS  Google Scholar 

  • Hunt CR, Dix DJ, Sharma GG, Pandita RK, Gupta A, Funk M, Pandita TK (2004) Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice. Mol Cell Biol 24:899–911

    Article  PubMed  CAS  Google Scholar 

  • Hurwitz MD, Kaur P, Nagaraja GM, Bausero MA, Manola J, Asea A (2010) Radiation therapy induces circulating serum Hsp72 in patients with prostate cancer. Radiother Oncol 95:350–358

    Article  PubMed  CAS  Google Scholar 

  • Hwang YJ, Lee SP, Kim SY et al (2009) Expression of heat shock protein 60 kDa is upregulated in cervical cancer. Yonsei Med J 50(3):399–406

    Article  PubMed  CAS  Google Scholar 

  • Ingolia TD, Craig EA (1982) Four small heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79:2360–2364

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki S, Kobayashi M, Yoda M et al (2010) Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell 39(2):292–299

    Article  PubMed  CAS  Google Scholar 

  • Jäättelä M (1995) Over-expression of Hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int J Cancer 60:689–693

    Article  PubMed  Google Scholar 

  • Jaattela M, Wissing D, Bauer PA, Li GC (1992) Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J 11(10):3507–3512

    PubMed  CAS  Google Scholar 

  • Jaattela M, Wissing D, Kokholm K, Kallunki T, Egeblad M (1998) Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J 17(21):6124–6134

    Article  PubMed  CAS  Google Scholar 

  • Jakob U, Gaestel M, Engels K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    PubMed  CAS  Google Scholar 

  • Jin X et al (2011) Heat shock transcription factor 1 is a key determinant of HCC development by regulating hepatic steatosis and metabolic syndrome. Cell Metab 14:91–103

    Article  PubMed  CAS  Google Scholar 

  • Jomary C, Cullen J, Jones SE (2006) Inactivation of the Akt survival pathway during photoreceptor apoptosis in the retinal degeneration mouse. Invest Ophthalmol Vis Sci 47(4):1620–1629

    Article  PubMed  Google Scholar 

  • Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3:415–428

    Article  PubMed  CAS  Google Scholar 

  • Kamada M, So A, Muramaki M, Rocchi P, Beraldi E, Gleave M (2007) Hsp27 knockdown using nucleotide-based therapies inhibit tumor growth and enhance chemotherapy in human bladder cancer cells. Mol Cancer Ther 6(1):299–308

    Article  PubMed  CAS  Google Scholar 

  • Kamal A et al (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425:407–410

    Article  PubMed  CAS  Google Scholar 

  • Kampinga HH et al (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111

    Article  PubMed  CAS  Google Scholar 

  • Kamradt MC, Chen F, Cryns VL (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 276(19):16059–16063

    Article  PubMed  CAS  Google Scholar 

  • Kamradt MC, Chen F, Sam S, Cryns VL (2002) The small heat shock protein alpha B-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J Biol Chem 277(41):38731–38736

    Article  PubMed  CAS  Google Scholar 

  • Kamradt MC, Lu M, Werner ME et al (2005) The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J Biol Chem 280(12):11059–11066

    Article  PubMed  CAS  Google Scholar 

  • Kanagasabai R, Krishnamurthy K, Druhan LJ, Ilangovan G (2011) Forced expression of heat shock protein 27 (Hsp27) reverses P-glycoprotein (ABCB1)-mediated drug efflux and MDR1 gene expression in Adriamycin-resistant human breast cancer cells. J Biol Chem 286:33289–33300

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa Y, Isomoto H, Oka M et al (2003) Expression of heat shock protein (Hsp) 70 and Hsp 40 in colorectal cancer. Med Oncol 20(2):157–164

    Article  PubMed  CAS  Google Scholar 

  • Kang SH, Kang KW, Kim K-H, Kwon B, Kim S-K, Lee H-Y, Kong S-Y, Lee ES, Jang S-G, Yoo BC (2008) Upregulated HSP27 in human breast cancer cells reduces Herceptin susceptibility by increasing Her2 protein stability. BMC Cancer 8:286

    Article  PubMed  CAS  Google Scholar 

  • Kanwar RK, Cheung CH, Chang JY, Kanwar JR (2010) Recent advances in anti-survivin treatments for cancer. Curr Med Chem 17(15):1509–1515

    Article  PubMed  CAS  Google Scholar 

  • Kase S, Parikh JG, Rao NA (2009) Expression of heat shock protein 27 and alpha-crystallins in human retinoblastoma after chemoreduction. Br J Ophthalmol 93(4):541–544

    Article  PubMed  CAS  Google Scholar 

  • Katoh M, Koninkx J, Schumacher U (2000) Heat shock protein expression in human tumours grown in severe combined immunodeficient mice. Cancer Lett 161(1):113–120

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann SH, Karp JE, Litzow MR, Mesa RA, Hogan W, Steensma DP, Flatten KS, Loegering DA, Schneider PA, Peterson KL, Maurer MJ, Smith BD, Greer J, Chen Y, Reid JM, Ivy SP, Ames MM, Adjei AA, Erlichman C, Karnitz LM (2011) Phase I and pharmacological study of cytarabine and tanespimycin in relapsed and refractory acute leukemia. Haematologica 96:1619–1626

    Article  PubMed  CAS  Google Scholar 

  • Kaur P, Nagaraja GM, Asea A (2011) Combined lentiviral and RNAi technologies for the delivery and permanent silencing of the hsp25 gene. Methods Mol Biol 787:121–136

    Article  PubMed  CAS  Google Scholar 

  • Khaleque MA et al (2005) Induction of heat shock proteins by heregulin beta1 leads to protection from apoptosis and anchorage-independent growth. Oncogene 24:6564–6573

    PubMed  CAS  Google Scholar 

  • Khaleque MA et al (2008) Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene 27:1886–1893

    Article  PubMed  CAS  Google Scholar 

  • Khalil AA, Kabapy NF, Deraz SF, Smith C (2011) Heat shock proteins in oncology: diagnostic biomarkers or therapeutic targets? Biochim Biophys Acta 1816(2):89–104

    PubMed  CAS  Google Scholar 

  • Kim LS, Kim JH (2011) Heat shock protein as molecular targets for breast cancer therapeutics. J Breast Cancer 14:167–174

    Article  PubMed  Google Scholar 

  • Kim JY, Son YO, Park SW, Bae JH, Chung JS, Kim HH, Chung BS, Kim SH, Kang CD (2006) Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp Mol Med 38:474–484

    PubMed  CAS  Google Scholar 

  • Kim EH, Lee HJ, Lee DH et al (2007) Inhibition of heat shock protein 27-mediated resistance to DNA damaging agents by a novel PKC delta-V5 heptapeptide. Cancer Res 67(13):6333–6341

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Jeong SJ, Kim B, Yun SM, Choi DY, Kim SH (2012) Melatonin synergistically enhances cisplatin-induced apoptosis via the dephosphorylation of ERK/p90 ribosomal S6 kinase/heat shock 27 protein in SK-OV-3 cells. J Pineal Res 52:244–252

    Article  PubMed  CAS  Google Scholar 

  • Kirkegaard T, Roth AG, Petersen NH et al (2010) Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463(7280):549–553

    Article  PubMed  CAS  Google Scholar 

  • Knapinska AM, Gratacos FM, Krause CD et al (2011) Chaperone Hsp27 modulates AUF1 proteolysis and AU-rich element-mediated mRNA degradation. Mol Cell Biol 31(7):1419–1431

    Article  PubMed  CAS  Google Scholar 

  • Kocsis J, Madaras B, Toth EK, Fust G, Prohaszka Z (2010) Serum level of soluble 70-kD heat shock protein is associated with high mortality in patients with colorectal cancer without distant metastasis. Cell Stress Chaperones 15(2):143–151

    Article  PubMed  CAS  Google Scholar 

  • Koren J III, Jinwal UK, Jin Y et al (2010) Facilitating Akt clearance via manipulation of Hsp70 activity and levels. J Biol Chem 285(4):2498–2505

    Article  PubMed  CAS  Google Scholar 

  • Koteiche HA, McHaourab HS (2003) Mechanism of chaperone function in small heat-shock proteins. Phosphorylation-induced activation of two-mode binding in alphaB-crystallin. J Biol Chem 278(12):10361–10367

    Article  PubMed  CAS  Google Scholar 

  • Kwon SM, Kim SA, Yoon JH, Ahn SG (2010) Transforming growth factor beta1-induced heat shock protein 27 activation promotes migration of mouse dental papilla-derived MDPC-23 cells. J Endod 36:1332–1335

    Article  PubMed  Google Scholar 

  • Lamb J, Crawford ED, Peck D et al (2006) The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313(5795):1929–1935

    Article  PubMed  CAS  Google Scholar 

  • Lamoureux F, Thomas C, Yin MJ, Kuruma H, Beraldi E, Fazli L, Zoubeidi A, Gleave ME (2011) Clusterin inhibition using OGX-011 synergistically enhances Hsp90 inhibitor activity by suppressing the heat shock response in castrate-resistant prostate cancer. Cancer Res 71:5838–5849

    Article  PubMed  CAS  Google Scholar 

  • Lancet JE, Gojo I, Burton M, Quinn M, Tighe SM, Kersey K, Zhong Z, Albitar MX, Bhalla K, Hannah AL, Baer MR (2010) Phase I study of the heat shock protein 90 inhibitor alvespimycin (KOS-1022, 17-DMAG) administered intravenously twice weekly to patients with acute myeloid leukemia. Leukemia 24:699–705

    Article  PubMed  CAS  Google Scholar 

  • Lander AD, Kimble J, Clevers H, Fuchs E, Montarras D, Buckingham M, Calof AL, Trumpp A, Oskarsson T (2012) What does the concept of the stem cell niche really mean today? BMC Biol 2012(10):19–34

    Article  Google Scholar 

  • Landry J, Chretien P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance confered by expression of the human HSP 27 gene in rodent cells. J Cell Biol 109:7–15

    Article  PubMed  CAS  Google Scholar 

  • Langer R, Ott K, Specht K, Becker K, Lordick F, Burian M, Herrmann K, Schrattenholz A, Cahill MA, Schwaiger M, Hofler H, Wester HJ (2008) Protein expression profiling in esophageal adenocarcinoma patients indicates association of heat-shock protein 27 expression and chemotherapy response. Clin Cancer Res 14:8279–8287

    Article  PubMed  CAS  Google Scholar 

  • Laszlo A, Fleischer I (2009) Heat-induced perturbations of DNA damage signaling pathways are modulated by molecular chaperones. Cancer Res 69:2042–2049

    Article  PubMed  CAS  Google Scholar 

  • Launay N, Tarze A, Vicart P, Lilienbaum A (2010) Serine 59 phosphorylation of {alpha}B-crystallin down-regulates its anti-apoptotic function by binding and sequestering Bcl-2 in breast cancer cells. J Biol Chem 285(48):37324–37332

    Article  PubMed  CAS  Google Scholar 

  • Lee HJ, Lee YS (2010) Repeated-dose toxicity of HSP27-binding heptapeptide in mice. Drug Chem Toxicol 33(3):284–290

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Lim KT (2012) Inhibitory effect of SJSZ glycoprotein (38 kDa) on expression of heat shock protein 27 and 70 in chromium (VI)-treated hepatocytes. Mol Cell Biochem 359:45–57

    Article  PubMed  CAS  Google Scholar 

  • Lee CC, Lin TW, Ko TP, Wang AH (2011a) The hexameric structures of human heat shock protein 90. PLoS ONE 6(5):e19961

    Article  PubMed  CAS  Google Scholar 

  • Lee HJ, Kim EH, Seo WD, Choi TH, Cheon GJ, Lee YJ, Lee YS (2011b) Heat shock protein 27-targeted heptapeptide of the PKCΔ catalytic V5 region sensitizes tumors with radio- and chemoresistance. Int J Radiat Oncol Biol Phys 80:221–230

    Article  PubMed  CAS  Google Scholar 

  • Lemieux P, Oesterreich S, Lawrence JA et al (1997) The small heat shock protein hsp27 increases invasiveness but decreases motility of breast cancer cells. Invasion Metastasis 17(3):113–123

    PubMed  CAS  Google Scholar 

  • Leu JI, Pimkina J, Pandey P, Murphy ME, George DL (2011) HSP70 inhibition by the small-molecule 2-phenylethynesulfonamide impairs protein clearance pathways in tumor cells. Mol Cancer Res 9(7):936–947

    Article  PubMed  CAS  Google Scholar 

  • Li DW, Liu JP, Mao YW et al (2005) Calcium-activated RAF/MEK/ERK signaling pathway mediates p53-dependent apoptosis and is abrogated by alpha B-crystallin through inhibition of RAS activation. Mol Biol Cell 16(9):4437–4453

    Article  PubMed  CAS  Google Scholar 

  • Liang JJ, Akhtar NJ (2000) Human lens high-molecular-weight alpha-crystallin aggregates. Biochem Biophys Res Commun 275(2):354–359

    Article  PubMed  CAS  Google Scholar 

  • Lin TY, Chang JT, Wang HM, Chan SH, Chiu CC, Lin CY, Fan KH, Liao CT, Chen IH, Liu TZ, Li HF, Cheng AJ (2010) Proteomics of the radioresistant phenotype in head-and-neck cancer: Gp96 as a novel prediction marker and sensitizing target for radiotherapy. Int J Radiat Oncol Biol Phys 78:246–256

    Article  PubMed  CAS  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631–637

    Article  PubMed  CAS  Google Scholar 

  • Liu JP, Schlosser R, Ma WY et al (2004) Human alphaA- and alphaB-crystallins prevent UVA-induced apoptosis through regulation of PKCalpha, RAF/MEK/ERK and AKT signaling pathways. Exp Eye Res 79(6):393–403

    Article  CAS  Google Scholar 

  • Lo WY, Lai CC, Hua CH, Tsai MH, Huang SY, Tsai CH, Tsai FJ (2007) S100A8 is identified as a biomarker of HPV18-infected oral squamous cell carcinomas by suppression subtraction hybridization, clinical proteomics analysis, and immunohistochemistry staining. J Proteome Res 6:2143–2151

    Article  PubMed  CAS  Google Scholar 

  • Mambula SS, Calderwood SK (2006) Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 177:7849–7857

    PubMed  CAS  Google Scholar 

  • Mantovani A et al (2008) Cancer-related inflammation. Nature 454:436–444

    Article  PubMed  CAS  Google Scholar 

  • Mao YW, Liu JP, Xiang H, Li DW (2004) Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 11(5):512–526

    Article  PubMed  CAS  Google Scholar 

  • Margel D, Pevsner-Fisher M, Baniel J, Yossepowitch O, Cohen IR (2011) Stress proteins and cytokines are urinary biomarkers for diagnosis and staging of bladder cancer. Eur Urol 59:113–119

    Article  PubMed  CAS  Google Scholar 

  • Marigo I et al (2008) Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 222:162–179

    Article  PubMed  CAS  Google Scholar 

  • Markossian KA, Yudin IK, Kurganov BI (2009) Mechanism of Suppression of Protein Aggregation by alpha-Crystallin. Int J Mol Sci 10(3):1314–13145

    Article  PubMed  CAS  Google Scholar 

  • Massey AJ, Williamson DS, Browne H et al (2010) A novel, small molecule inhibitor of Hsc70/Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother Pharmacol 66(3):535–545

    Article  PubMed  CAS  Google Scholar 

  • Matassa DS, Amoroso MR, Maddalena F, Landriscina M, Esposito F (2012) New insights into TRAP1 pathway. Am J Cancer Res 2(2):235–248

    PubMed  CAS  Google Scholar 

  • Mazumdar A et al (2001) Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol 3:30–37

    Article  PubMed  CAS  Google Scholar 

  • McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J (2007) Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell 131(1):121–135

    Article  PubMed  CAS  Google Scholar 

  • McClung HM, Golembieski WA, Schultz CR, Jankowski M, Schultz LR, Rempel SA (2012) Deletion of the SPARC acidic domain or EGF-like module reduces SPARC-induced migration and signaling through p38 MAPK/HSP27 in glioma. Carcinogenesis 33:275–284

    Article  PubMed  CAS  Google Scholar 

  • Mehlen P, Préville X, Chareyron P, Briolay J, Klemenz R, Arrigo A-P (1995) Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J Immunol 154(1):363–374

    PubMed  CAS  Google Scholar 

  • Mehlen P, Préville X, Kretz-Remy C, Arrigo A-P (1996a) Human hsp27, Drosophila hsp27 and human αB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these protein against TNFα-induced cell death. EMBO J 15:2695–2706

    PubMed  CAS  Google Scholar 

  • Mehlen P, Schulze-Osthoff K, Arrigo AP (1996b) Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271(28):16510–16514

    Article  PubMed  CAS  Google Scholar 

  • Merendino AM, Bucchieri F, Campanella C et al (2010) Hsp60 is actively secreted by human tumor cells. PLoS ONE 5(2):e9247

    Article  PubMed  CAS  Google Scholar 

  • Michels AA, Kanon B, Konings AW, Ohtsuka K, Bensaude O, Kampinga HH (1997) Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J Biol Chem 272(52):33283–33289

    Article  PubMed  CAS  Google Scholar 

  • Michiel M, Skouri-Panet F, Duprat E et al (2009) Abnormal assemblies and subunit exchange of alphaB-crystallin R120 mutants could be associated with destabilization of the dimeric substructure. Biochemistry 48(2):442–453

    Article  PubMed  CAS  Google Scholar 

  • Mickler M, Hessling M, Ratzke C, Buchner J, Hugel T (2009) The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat Struct Mol Biol 16(3):281–286

    Article  PubMed  CAS  Google Scholar 

  • Mimnaugh EG, Xu W, Vos M et al (2004) Simultaneous inhibition of hsp 90 and the proteasome promotes protein ubiquitination, causes endoplasmic reticulum-derived cytosolic vacuolization, and enhances antitumor activity. Mol Cancer Ther 3(5):551–566

    PubMed  CAS  Google Scholar 

  • Mitra A, Shevde LA, Samant RS (2009) Multi-faceted role of HSP40 in cancer. Clin Exp Metastasis 26(6):559–567

    Article  PubMed  CAS  Google Scholar 

  • Moon A, Bacchini P, Bertoni F, Olvi LG, Santini-Araujo E, Kim YW, Park YK (2010) Expression of heat shock proteins in osteosarcomas. Pathology 42:421–442

    Article  PubMed  CAS  Google Scholar 

  • Mori-Iwamoto S, Kuramitsu Y, Ryozawa S, Mikuria K, Fujimoto M, Maehara S, Maehara Y, Okita K, Nakamura K, Sakaida I (2007) Proteomics finding heat shock protein 27 as a biomarker for resistance of pancreatic cancer cells to gemcitabine. Int J Oncol 31:1345–1350

    PubMed  CAS  Google Scholar 

  • Moulick K, Ahn JH, Zong H et al (2011) Affinity-based proteomics reveal cancer-specific networks coordinated by Hsp90. Nat Chem Biol 7(11):818–826

    Article  PubMed  CAS  Google Scholar 

  • Mounier N, Arrigo AP (2002) Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7(2):167–176

    Article  PubMed  CAS  Google Scholar 

  • Moyano JV, Evans JR, Chen F et al (2006) AlphaB-crystallin is a novel oncoprotein that predicts poor clinical outcome in breast cancer. J Clin Invest 116(1):261–270

    Article  PubMed  CAS  Google Scholar 

  • Muchemwa FC, Nakatsura T, Fukushima S, Nishimura Y, Kageshita T, Ihn H (2008) Differential expression of heat shock protein 105 in melanoma and melanocytic naevi. Melanoma Res 18:166–171

    Article  PubMed  CAS  Google Scholar 

  • Multhoff G (2007) Heat shock protein 70 (Hsp70): membrane location, export and immunological relevance. Methods 43(3):229–237

    Article  PubMed  CAS  Google Scholar 

  • Murshid A et al (2010) Protein kinase A binds and activates heat shock factor 1. PLoS ONE 5:e13830

    Article  PubMed  CAS  Google Scholar 

  • Murshid A et al (2011) Heat shock proteins and cancer vaccines: developments in the past decade and chaperoning in the decade to come. Expert Rev Vaccines 10:1553–1568

    Article  PubMed  CAS  Google Scholar 

  • Nadin SA, Ciocca DR (2010) Participation of heat shock proteins in DNA repair mechanisms in cancer, Chapter 7. In: Thomas AE (ed) DNA repair: damage, repair mechanisms and aging. Nova Science Publisher, Inc, New York, pp 165–186. Hardcover ISBN 978-1-61668-914-8. eBook ISBN 978-1-61728-055-9

  • Nadin SB, Vargas-Roig LM, Drago G, Ibarra J, Ciocca DR (2007) Hsp27, Hsp70 and mismatch repair proteins hMLH1 and hMSH2 expression in peripheral blood lymphocytes from healthy subjects and cancer patients. Cancer Lett 252:131–146

    Article  PubMed  CAS  Google Scholar 

  • Nagaraja GM, Kaur P, Neumann W, Asea EE, Bausero MA, Multhoff G, Asea A (2012) Silencing Hsp25/Hsp27 gene expression augments proteasome activity and increases CD8+ T-cell-mediated tumor killing and memory responses. Cancer Prev Res (Phila) 5:122–137

    Article  CAS  Google Scholar 

  • Nakajima M, Kato H, Miyazaki T, Fukuchi M, Masuda N, Fukai Y, Sohda M, Ahmad F, Kuwano H (2009) Tumor immune systems in esophageal cancer with special reference to heat-shock protein 70 and humoral immunity. Anticancer Res 29:1595–1606

    PubMed  Google Scholar 

  • Nakajima M, Kato H, Miyazaki T, Fukuchi M, Masuda N, Fukai Y, Sohda M, Inose T, Sakai M, Sano A, Tanaka N, Ahmad F, Kuwano H (2011) Prognostic significance of heat shock protein 110 expression and T lymphocyte infiltration in esophageal cancer. Hepatogastroenterology 58:1555–1560

    PubMed  CAS  Google Scholar 

  • Nakashima M, Adachi S, Yasuda I, Yamauchi T, Kawaguchi J, Itani M, Yoshioka T, Matsushima-Nishiwaki R, Hirose Y, Kozawa O, Moriwaki H (2011) Phosphorylation status of heat shock protein 27 plays a key role in gemcitabine-induced apoptosis of pancreatic cancer cells. Cancer Lett 313:218–225

    Article  PubMed  CAS  Google Scholar 

  • Neckers L (2002) Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 8(4 Suppl):S55–S61

    Article  PubMed  CAS  Google Scholar 

  • Neckers L, Ivy SP (2003) Heat shock protein 90. Curr Opin Oncol 15:419–424

    Article  PubMed  CAS  Google Scholar 

  • Neckers L, Mimnaugh E, Schulte TW (1999) Hsp90 as an anti-cancer target. Drug Resist Updat 2(3):165–172

    Article  PubMed  CAS  Google Scholar 

  • Norton JA, Weinberger PM, Waller JL, Merkley MA, Jackson LL, Dynan WS (2010) Significance of HSPB1 expression in head and neck squamous cell carcinoma: a meta-analysis of published literatures. Laryngoscope 120 Suppl 4:S172

    Article  PubMed  Google Scholar 

  • Oba M, Yano S, Shuto T, Suico MA, Eguma A, Kai H (2008) IFN-gamma down-regulates Hsp27 and enhances hyperthermia-induced tumor cell death in vitro and tumor suppression in vivo. Int J Oncol 32:1317–1324

    PubMed  CAS  Google Scholar 

  • O’Callaghan-Sunol C, Gabai VL, Sherman MY (2007) Hsp27 modulates p53 signaling and suppresses cellular senescence. Cancer Res 67(24):11779–11788

    Article  PubMed  CAS  Google Scholar 

  • Oh HJ, Easton D, Murawski M, Kaneko Y, Subjeck JR (1999) The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J Biol Chem 274:15712–15718

    Article  PubMed  CAS  Google Scholar 

  • Oka M, Sato S, Soda H et al (2001) Autoantibody to heat shock protein Hsp40 in sera of lung cancer patients. Jpn J Cancer Res 92(3):316–320

    Article  PubMed  CAS  Google Scholar 

  • Ono A, Kumai T, Koizumi H, Nishikawa H, Kobayashi S, Tadokoro M (2009) Overexpression of heat shock protein 27 in squamous cell carcinoma of the uterine cervix: a proteomic analysis using archival formalin-fixed, paraffin-embedded tissues. Hum Pathol 40:41–49

    Article  PubMed  CAS  Google Scholar 

  • Padival AK, Crabb JW, Nagaraj RH (2003) Methylglyoxal modifies heat shock protein 27 in glomerular mesangial cells. FEBS Lett 551(1–3):113–118

    Article  PubMed  CAS  Google Scholar 

  • Pandey P, Farber R, Nakazawa A et al (2000a) Hsp27 functions as a negative regulator of cytochrome c-dependent activation of procaspase-3. Oncogene 19(16):1975–1981

    Article  PubMed  CAS  Google Scholar 

  • Pandey P, Saleh A, Nakazawa A et al (2000b) Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J 19(16):4310–4322

    Article  PubMed  CAS  Google Scholar 

  • Paraiso KH, Haarberg HE, Wood E, Rebecca VW, Chen YA, Xiang Y, Ribas A, Lo RS, Weber JS, Sondak VK, John JK, Sarnaik AA, Koomen JM, Smalley KS (2012) The HSP90 inhibitor XL888 overcomes BRAF inhibitor resistance mediated through diverse mechanisms. Clin Cancer Res 18(9):2502–2514

    Google Scholar 

  • Parcellier A, Schmitt E, Gurbuxani S et al (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23(16):5790–5802

    Article  PubMed  CAS  Google Scholar 

  • Parcellier A, Brunet M, Schmitt E et al (2006) HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells. FASEB J 20(8):1179–1181

    Article  PubMed  CAS  Google Scholar 

  • Park HS, Cho SG, Kim CK et al (2002) Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol Cell Biol 22(22):7721–7730

    Article  PubMed  CAS  Google Scholar 

  • Park HS, Park CH, Choi BR, Lim MS, Heo SH, Kim CH, Kang SG, Whang KU, Cho MK (2009) Expression of heat shock protein 105 and 70 in malignant melanoma and benign melanocytic nevi. J Cutan Pathol 36:511–516

    Article  PubMed  Google Scholar 

  • Pasta SY, Raman B, Ramakrishna T, Rao Ch M (2004) The IXI/V motif in the C-terminal extension of alpha-crystallins: alternative interactions and oligomeric assemblies. Mol Vis 10:655–662

    PubMed  CAS  Google Scholar 

  • Patil SB, Pawar MD, Bitar KN (2004) Direct association and translocation of PKC-alpha with calponin. Am J Physiol Gastrointest Liver Physiol 286(6):G954–G963

    Article  PubMed  CAS  Google Scholar 

  • Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, Arrigo AP (2002) Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 22(3):816–834

    Article  PubMed  CAS  Google Scholar 

  • Paul C, Simon S, Gibert B, Virot S, Manero F, Arrigo AP (2010) Dynamic processes that reflect anti-apoptotic strategies set up by HspB1 (Hsp27). Exp Cell Res 316(9):1535–1552

    Article  PubMed  CAS  Google Scholar 

  • Pei H, Huang L, Liu L, Zhu H, Zeng L, Xiao Z (2011) Experimental study of HSP27 differential expression in left sided colon cancer and right sided colon cancer. Zhong Nan Da Xue Xue Bao Yi Xue Ban 36:277–285

    PubMed  CAS  Google Scholar 

  • Pekarek LA et al (1995) Inhibition of tumor growth by elimination of granulocytes. J Exp Med 181:435–440

    Article  PubMed  CAS  Google Scholar 

  • Perng MD, Cairns L, van den IJssel P, Prescott A, Hutcheson AM, Quinlan RA (1999) Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci 112(Pt 13):2099–2112

    PubMed  CAS  Google Scholar 

  • Petersen NH, Kirkegaard T, Olsen OD, Jaattela M (2010) Connecting Hsp70, sphingolipid metabolism and lysosomal stability. Cell Cycle 9(12):2305–2309

    Article  PubMed  CAS  Google Scholar 

  • Pfosser A et al (2005) Liposomal Hsp90 cDNA induces neovascularization via nitric oxide in chronic ischemia. Cardiovasc Res 65:728–736

    Article  PubMed  CAS  Google Scholar 

  • Plescia J, Salz W, Xia F et al (2005) Rational design of shepherdin, a novel anticancer agent. Cancer Cell 7(5):457–468

    Article  PubMed  CAS  Google Scholar 

  • Pockley AG, Georgiades A, Thulin T, de Faire U, Frostegard J (2003) Serum heat shock protein 70 levels predict the development of atherosclerosis in subjects with established hypertension. Hypertension 42(3):235–238

    Article  PubMed  CAS  Google Scholar 

  • Powers MV et al (2008) Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 14:250–262

    Article  PubMed  CAS  Google Scholar 

  • Powers MV et al (2011) Targeting HSP70: the second potentially druggable heat shock protein and molecular chaperone? Cell Cycle 9:1542–1550

    Article  Google Scholar 

  • Preville X, Salvemini F, Giraud S et al (1999) Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp Cell Res 247(1):61–78

    Article  PubMed  CAS  Google Scholar 

  • Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417(6889):618–624

    Article  PubMed  CAS  Google Scholar 

  • Rajan A, Kelly RJ, Trepel JB, Kim YS, Alarcon SV, Kummar S, Gutierrez M, Crandon S, Zein WM, Jain L, Mannargudi B, Figg WD, Houk BE, Shnaidman M, Brega N, Giaccone G (2011) A phase I study of PF-04929113 (SNX-5422), an orally bioavailable heat shock protein 90 inhibitor, in patients with refractory solid tumor malignancies and lymphomas. Clin Cancer Res 17:6831–6839

    Article  PubMed  CAS  Google Scholar 

  • Ran R, Lu A, Zhang L et al (2004) Hsp70 promotes TNF-mediated apoptosis by binding IKK gamma and impairing NF-kappa B survival signaling. Genes Dev 18(12):1466–1481

    Article  PubMed  CAS  Google Scholar 

  • Rane MJ, Coxon PY, Powell DW et al (2001) p38 Kinase-dependent MAPKAPK-2 activation functions as 3- phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J Biol Chem 276(5):3517–3523

    Article  PubMed  CAS  Google Scholar 

  • Rane MJ, Pan Y, Singh S et al (2003) Heat shock protein 27 controls apoptosis by regulating Akt activation. J Biol Chem 278(30):27828–27835

    Article  PubMed  CAS  Google Scholar 

  • Ravagnan L, Gurbuxani S, Susin SA et al (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3(9):839–843

    Article  PubMed  CAS  Google Scholar 

  • Razandi M, Pedram A, Levin ER (2010) Heat shock protein 27 is required for sex steroid receptor trafficking to and functioning at the plasma membrane. Mol Cell Biol 30:3249–3261

    Article  PubMed  CAS  Google Scholar 

  • Rerole AL, Gobbo J, De Thonel A et al (2011) Peptides and aptamers targeting HSP70: a novel approach for anticancer chemotherapy. Cancer Res 71(2):484–495

    Article  PubMed  CAS  Google Scholar 

  • Richards EH, Hickey E, Weber LA, Master JR (1996) Effect of overexpression of the small heat shock protein HSP27 on the heat and drug sensitivities of human testis tumor cells. Cancer Res 56:2446–2451

    PubMed  CAS  Google Scholar 

  • Richardson PG, Badros AZ, Jagannath S et al (2010) Tanespimycin with bortezomib: activity in relapsed/refractory patients with multiple myeloma. Br J Haematol 150(4):428–437

    PubMed  CAS  Google Scholar 

  • Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573

    Article  CAS  Google Scholar 

  • Ritossa FM (1964) Experimental activation of specific loci in polytene chromosomes of Drosophila. Exp Cell Res 35:601–607

    Article  PubMed  CAS  Google Scholar 

  • Rocchi P, Beraldi E, Ettinger S et al (2005) Increased Hsp27 after androgen ablation facilitates androgen-independent progression in prostate cancer via signal transducers and activators of transcription 3-mediated suppression of apoptosis. Cancer Res 65(23):11083–11093

    Article  PubMed  CAS  Google Scholar 

  • Rocchi P, Jugpal P, So A et al (2006) Small interference RNA targeting heat-shock protein 27 inhibits the growth of prostatic cell lines and induces apoptosis via caspase-3 activation in vitro. BJU Int 28:28

    Google Scholar 

  • Rogalla T, Ehrnsperger M, Preville X et al (1999) Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274(27):18947–18956

    Article  PubMed  CAS  Google Scholar 

  • Rohde M, Daugaard M, Jensen MH, Helin K, Nylandsted J, Jaattela M (2005) Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev 19(5):570–582

    Article  PubMed  CAS  Google Scholar 

  • Rosenbaum EE, Brehm KS, Vasiljevic E, Liu CH, Hardie RC, Colley NJ (2011) XPORT-dependent transport of TRP and rhodopsin. Neuron 72(4):602–615

    Article  PubMed  CAS  Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396(6709):336–342

    Article  PubMed  CAS  Google Scholar 

  • Saha S, Das KP (2004) Relationship between chaperone activity and oligomeric size of recombinant human alphaA- and alphaB-crystallin: a tryptic digestion study. Proteins 57(3):610–617

    Article  PubMed  CAS  Google Scholar 

  • Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES (2000) Negative regulation of the apaf-1 apoptosome by hsp70. Nat Cell Biol 2(8):476–483

    Article  PubMed  CAS  Google Scholar 

  • Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146(3):353–358

    Article  PubMed  CAS  Google Scholar 

  • Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S (1999) Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of Jurkat cells. EMBO J 18(8):2040–2048

    Article  PubMed  CAS  Google Scholar 

  • Sangster TA, Lindquist S, Queitsch C (2004) Under cover: causes, effects and implications of Hsp90-mediated genetic capacitance. BioEssays 26(4):348–362

    Article  PubMed  CAS  Google Scholar 

  • Santagata S et al (2011) High levels of nuclear heat-shock factor 1 (HSF1) are associated with poor prognosis in breast cancer. Proc Natl Acad Sci USA 108:18378–18383

    Article  PubMed  CAS  Google Scholar 

  • Sarge KD et al (1993) Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 13:1392–1407

    PubMed  CAS  Google Scholar 

  • Sato Y, Harada K, Sasaki M, Yasaka T, Nakanuma Y (2012) Heat shock proteins 27 and 70 are potential biliary markers for the detection of cholangiocarcinoma. Am J Pathol 180:123–130

    Article  PubMed  CAS  Google Scholar 

  • Schäfer C, Seeliger H, Bader DC, Assmann G, Buchner D, Guo Y, Ziesch A, Palagyi A, Ochs S, Laubender RP, Jung A, De Toni EN, Kirchner T, Göke B, Bruns C, Gallmeier E (2011) Heat shock protein 27 as a prognostic and predictive biomarker in pancreatic ductal adenocarcinoma. J Cell Mol Med. 18 Oct 2011. doi:10.1111/j.1582-4934.2011.01473.x (Epub ahead of print)

  • Schilling D, Gehrmann M, Steinem C et al (2009) Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J 23(8):2467–2477

    Article  PubMed  CAS  Google Scholar 

  • Schlecht R, Erbse AH, Bukau B, Mayer MP (2011) Mechanics of Hsp70 chaperones enables differential interaction with client proteins. Nat Struct Mol Biol 18(3):345–351

    Article  PubMed  CAS  Google Scholar 

  • Schultz CR, Golembieski WA, King DA, Brown SL, Brodie C, Rempel SA (2012) Inhibition of HSP27 alone or in combination with pAKT inhibition as therapeutic approaches to target SPARC-induced glioma cell survival. Mol Cancer 11(1):20 [Epub ahead of print]

    Article  PubMed  CAS  Google Scholar 

  • Sedlackova L, Spacek M, Holler E, Imryskova Z, Hromadnikova I (2011) Heat-shock protein expression in leukemia. Tumour Biol 32:33–44

    Article  PubMed  CAS  Google Scholar 

  • Shan ZX et al (2010) miR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes. FEBS Lett 584:3592–3600

    Article  PubMed  CAS  Google Scholar 

  • Sharma A, Upadhyay AK, Bhat MK (2009) Inhibition of Hsp27 and Hsp40 potentiates 5-fluorouracil and carboplatin mediated cell killing in hepatoma cells. Cancer Biol Ther 8(22):2106–2113

    Article  PubMed  CAS  Google Scholar 

  • Sherman MY et al (2010) Oncogenes induce senescence with incomplete growth arrest and suppress the DNA damage response in immortalized cells. Aging Cell 10:949–961

    Article  CAS  Google Scholar 

  • Shih YY, Lee H, Nakagawara A, Juan HF, Jeng YM, Tsay YG, Lin DT, Hsieh FJ, Pan CY, Hsu WM, Liao YF (2012) Nuclear GRP75 binds retinoic acid receptors to promote neuronal differentiation of neuroblastoma. PLoS ONE 6(10):e26236

    Article  CAS  Google Scholar 

  • Simon S, Fontaine JM, Martin JL et al (2007) Myopathy-associated alpha B-crystallin mutants: abnormal phosphorylation, intracellular location, and interactions with other small heat shock proteins. J Biol Chem 82:34276–34287

    Article  Google Scholar 

  • Singh U et al (2009) A DNA sequence directed mutual transcription regulation of HSF1 and NFIX involves novel heat sensitive protein interactions. PLoS ONE 4:e5050

    Article  PubMed  CAS  Google Scholar 

  • Skalnikova H, Martinkova J, Hrabakova R, Halada P, Dziechciarkova M, Hajduch M, Gadher SJ, Hammar A, Enetoft D, Ekefjard A, Forsstrom-Olsson O, Kovarova H (2011) Cancer drug-resistance and a look at specific proteins: rho GDP-dissociation inhibitor 2, Y-box binding protein 1, and HSP70/90 organizing protein in proteomics clinical application. J Proteome Res 10:404–415

    Article  PubMed  CAS  Google Scholar 

  • Slaby O, Sobkova K, Svoboda M, Garajova I, Fabian P, Hrstka R, Nenutil R, Sachlova M, Kocakova I, Michalek J, Smerdova T, Knoflickova D, Vyzula R (2009) Significant overexpression of Hsp110 gene during colorectal cancer progression. Oncol Rep 21:1235–1241

    Article  PubMed  CAS  Google Scholar 

  • Sloan EK, Ciocca DR, Pouliot N, Natoli A, Restall C, Henderson MA, Fanelli MA, Cuello-Carrión FD, Gago FE, Anderson RL (2009) Stromal cell expression of caveolin-1 predicts outcome in breast cancer. Am J Pathol 174:2035–2043

    Article  PubMed  CAS  Google Scholar 

  • Sorger PK, Pelham HRB (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864

    Article  PubMed  CAS  Google Scholar 

  • Spizzo R et al (2009) SnapShot: MicroRNAs in cancer. Cell 137:586–586e581

    Google Scholar 

  • Srinivasan A, Nagineni C, Bhat S (1992) alpha A-crystallin is expressed in non-ocular tissues. J Biol Chem 267:23337–23341

    PubMed  CAS  Google Scholar 

  • Stangl S, Gehrmann M, Riegger J et al (2011) Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc Natl Acad Sci USA 108(2):733–738

    Article  PubMed  CAS  Google Scholar 

  • Stengel F, Baldwin AJ, Painter AJ et al (2010) Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc Natl Acad Sci USA 107(5):2007–2012

    Article  PubMed  CAS  Google Scholar 

  • Stope MB, Schubert T, Staar D, Rönnau C, Streitbörger A, Kroeger N, Kubisch C, Zimmermann U, Walther R, Burchardt M (2012) Effect of the heat shock protein HSP27 on androgen receptor expression and function in prostate cancer cells. World J Urol 30(3):327–331

    Google Scholar 

  • Straume O, Shimamura T, Lampa MJ et al (2012) Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci USA. doi:10.1073/pnas.1017909109

  • Sun TX, Liang JJ (1998) Intermolecular exchange and stabilization of recombinant human alphaA- and alphaB-crystallin. J Biol Chem 273(1):286–290

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Liao JK (2004) Induction of angiogenesis by heat shock protein 90 mediated by protein kinase Akt and endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 24:2238–2244

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Welsh MJ, Benndorf R (2006) Conformational changes resulting from pseudophosphorylation of mammalian small heat shock proteins–a two-hybrid study. Cell Stress Chaperones 11(1):61–70

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, Zhou M, Fu D et al (2011) Ubiquitination of heat shock protein 27 is mediated by its interaction with Smad ubiquitination regulatory factor 2 in A549 cells. Exp Lung Res 37:568–573

    Article  PubMed  CAS  Google Scholar 

  • Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11(7):515–528

    Article  PubMed  CAS  Google Scholar 

  • Takara K, Yamamoto K, Matsubara M, Minegaki T, Takahashi M, Yokoyama T, Okumura K (2012) Effects of α-adrenoceptor antagonists on ABCG2/BCRP-mediated resistance and transport. PLoS ONE 7:e30697

    Article  PubMed  CAS  Google Scholar 

  • Takemoto L, Emmons T, Horwitz J (1993) The C-terminal region of a-crystallin: involvement in protection against heat-induced denaturation. Biochem J 294:435–438

    PubMed  CAS  Google Scholar 

  • Tang D et al (2005) Expression of heat shock proteins and heat shock protein messenger ribonucleic acid in human prostate carcinoma in vitro and in tumors in vivo. Cell Stress Chaperones 10:46–58

    Article  PubMed  CAS  Google Scholar 

  • Tao YJ, Zheng W (2011) Chaperones and the maturation of steroid hormone receptor complexes. Oncotarget 2:104–106

    PubMed  Google Scholar 

  • Tchénio T, Havard M, Martinez LA, Dautry F (2006) Heat shock-independent induction of multidrug resistance by heat shock factor 1. Mol Cell Biol 26:580–591

    Article  PubMed  CAS  Google Scholar 

  • Teimourian S, Jalal R, Sohrabpour M, Goliaei B (2006) Down-regulation of Hsp27 radiosensitizes human prostate cancer cells. Int J Urol 13:1221–1225

    Article  PubMed  CAS  Google Scholar 

  • Theriault JR, Lambert H, Chavez-Zobel AT, Charest G, Lavigne P, Landry J (2004) Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27. J Biol Chem 279(22):23463–23471

    Article  PubMed  CAS  Google Scholar 

  • Tozawa-Ono A, Yoshida A, Yokomachi N, Handa R, Koizumi H, Kiguchi K, Ishizuka B, Suzuki N (2012) Heat shock protein 27 and p16 immunohistochemistry in cervical intraepithelial neoplasia and squamous cell carcinoma. Hum Cell 25(1):24–28

    Google Scholar 

  • Trepel J, Mollapour M, Giaccone G, Neckers L (2010) Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10(8):537–549

    Article  PubMed  CAS  Google Scholar 

  • Tutar Y (2011) Hsp70 in oncology. Recent Pat DNA Gene Seq 5:214–218

    Article  PubMed  CAS  Google Scholar 

  • Tweedle EM, Khattak I, Ang CW, Nedjadi T, Jenkins R, Park BK, Kalirai H, Dodson A, Azadeh B, Terlizzo M, Grabsch H, Mueller W, Myint S, Clark P, Wong H, Greenhalf W, Neoptolemos JP, Rooney PS, Costello E (2010) Low molecular weight heat shock protein HSP27 is a prognostic indicator in rectal cancer but not colon cancer. Gut 59:1501–1510

    Article  PubMed  CAS  Google Scholar 

  • Urushibara M, Kageyama Y, Akashi T, Otsuka Y, Takizawa T, Koike M, Kihara K (2007) HSP60 may predict good pathological response to neoadjuvant chemoradiotherapy in bladder cancer. Jpn J Clin Oncol 37:56–61

    Article  PubMed  Google Scholar 

  • Vaishampayan UN, Burger AM, Sausville EA, Heilbrun LK, Li J, Horiba MN, Egorin MJ, Ivy P, Pacey S, Lorusso PM (2010) Safety, efficacy, pharmacokinetics, and pharmacodynamics of the combination of sorafenib and tanespimycin. Clin Cancer Res 16:3795–3804

    Article  PubMed  CAS  Google Scholar 

  • Viaud S, Ullrich E, Zitvogel L, Chaput N (2008) Exosomes for the treatment of human malignancies. Horm Metab Res 40(2):82–88

    Article  PubMed  CAS  Google Scholar 

  • Visone R, Croce CM (2009) MiRNAs and cancer. Am J Pathol 174:1131–1138

    Article  PubMed  CAS  Google Scholar 

  • Walsh N, Larkin A, Swan N et al (2011) RNAi knockdown of Hop (Hsp70/Hsp90 organising protein) decreases invasion via MMP-2 down regulation. Cancer Lett 306(2):180–189

    Article  PubMed  CAS  Google Scholar 

  • Wang MH, Grossmann ME, Young CY (2004) Forced expression of heat-shock protein 70 increases the secretion of Hsp70 and provides protection against tumour growth. Br J Cancer 90(4):926–931

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Zhang P, Shi C, Yang Y, Qin H (2011a) Immunohistochemical detection of HSP27 and hnRNP K as prognostic and predictive biomarkers for colorectal cancer. Med Oncol [Epub ahead of print]

  • Wang W, Xu X, Wang W, Shao W, Li L, Yin W, Xiu L, Mo M, Zhao J, He Q, He J (2011b) The expression and clinical significance of CLIC1 and HSP27 in lung adenocarcinoma. Tumour Biol 32:1199–1208

    Article  PubMed  CAS  Google Scholar 

  • Warburg O (1956) On the origin of cancer cells. Science 123:309–314

    Article  PubMed  CAS  Google Scholar 

  • Wei L, Liu TT, Wang HH, Hong HM, Yu AL, Feng HP, Chang WW (2011) Hsp27 participates in the maintenance of breast cancer stem cells through regulation of epithelial-mesenchymal transition and nuclear factor-κB. Breast Cancer Res 13(5):R101 (Epub ahead of print)

    Article  PubMed  CAS  Google Scholar 

  • Westerheide SD et al (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323:1063–1066

    Article  PubMed  CAS  Google Scholar 

  • Westwood T, Wu C (1993) Activation of drosophila heat shock factor: conformational changes associated with monomer-to-trimer transition. Mol Cell Biol 13:3481–3486

    PubMed  CAS  Google Scholar 

  • Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5(10):761–772

    Article  PubMed  CAS  Google Scholar 

  • Whitesell L, Lindquist S (2009) Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin Ther Targets 13:469–478

    Article  PubMed  CAS  Google Scholar 

  • Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM (1994) Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci USA 91(18):8324–8328

    Article  PubMed  CAS  Google Scholar 

  • Wilhelmus MM, Boelens WC, Otte-Holler I et al (2006) Small heat shock protein HspB8: its distribution in Alzheimer’s disease brains and its inhibition of amyloid-beta protein aggregation and cerebrovascular amyloid-beta toxicity. Acta Neuropathol 111(2):139–149

    Article  PubMed  CAS  Google Scholar 

  • Workman P et al (2007) Drugging the cancer chaperone HSP90: combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann N Y Acad Sci 1113:202–216

    Article  PubMed  CAS  Google Scholar 

  • Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11:441–469

    Article  PubMed  CAS  Google Scholar 

  • Wu R, Kausar H, Johnson P, Montoya-Durango DE, Merchant M, Rane MJ (2007) Hsp27 regulates Akt activation and polymorphonuclear leukocyte apoptosis by scaffolding MK2 to Akt signal complex. J Biol Chem 282(30):21598–21608

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Liu J, Zhang Z et al (2009) HSP27 regulates IL-1 stimulated IKK activation through interacting with TRAF6 and affecting its ubiquitination. Cell Signal 21(1):143–150

    Article  PubMed  CAS  Google Scholar 

  • Wu P, Zhang H, Qi L, Tang Q, Tang Y, Xie Z, Lv Y, Zhao S, Jiang W (2012) Identification of ERp29 as a biomarker for predicting nasopharyngeal carcinoma response to radiotherapy. Oncol Rep 27:987–994

    PubMed  CAS  Google Scholar 

  • Xia Y, Liu Y, Rocchi P, Wang M, Fan Y, Qu F, Iovanna JL, Peng L (2012) Targeting heat shock factor 1 with a triazole nucleoside analog to elicit potent anticancer activity on drug-resistant pancreatic cancer. Cancer Lett 318(2):145–153

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Chen S, Bergan RC (2006) MAPKAPK2 and HSP27 are downstream effectors of p38 MAP kinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene 25:2987–2998

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Wang W, Shao W, Yin W, Chen H, Qiu Y, Mo M, Zhao J, Deng Q, He J (2011) Heat shock protein-60 expression was significantly correlated with the prognosis of lung adenocarcinoma. J Surg Oncol 104:598–603

    Article  PubMed  CAS  Google Scholar 

  • Yan LJ, Christians ES, Liu L, Xiao X, Sohal RS, Benjamin IJ (2002) Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J 21(19):5164–5172

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Yin Y, Wang F, Wang Y, Zhang L, Tang Y, Sun S (2010) miR-17–5p Promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology 51:1614–1623

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Wang J, Zhou Y, Wang Y, Wang S, Zhang W (2012) Hsp70 promotes chemoresistance by blocking Bax mitochondrial translocation in ovarian cancer cells. Cancer Lett. doi:10.1016/j.canlet.2012.01.030

  • Yeh CH, Tseng R, Zhang Z et al (2009) Circulating heat shock protein 70 and progression in patients with chronic myeloid leukemia. Leuk Res 33(2):212–217

    Article  PubMed  CAS  Google Scholar 

  • Yeh CH, Tseng R, Hannah A et al (2010) Clinical correlation of circulating heat shock protein 70 in acute leukemia. Leuk Res 34(5):605–609

    Article  PubMed  CAS  Google Scholar 

  • Yin C et al (2009) A novel role of microRNA in late preconditioning: upregulation of endothelial nitric oxide synthase and heat shock protein 70. Circ Res 104:572–575

    Article  PubMed  CAS  Google Scholar 

  • Yoon YJ, Kim JA, Shin KD, Shin DS, Han YM, Lee YJ, Lee JS, Kwon BM, Han DC (2011) KRIBB11 inhibits HSP70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. J Biol Chem 286:1737–1747

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura T, Nagahara M, Kuo C, Turner RR, Soon-Shiong P, Hoon DS (2011) Lymphovascular invasion of colorectal cancer is correlated to SPARC expression in the tumor stromal microenvironment. Epigenetics 6:1001–1011

    Article  PubMed  CAS  Google Scholar 

  • Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5(10):781–791

    Article  PubMed  CAS  Google Scholar 

  • Yu Z, Zhi J, Peng X, Zhong X, Xu A (2010) Clinical significance of HSP27 expression in colorectal cancer. Mol Med Report 3:953–958

    PubMed  CAS  Google Scholar 

  • Zanini C, Pulerà F, Carta F, Giribaldi G, Mandili G, Maule MM, Forni M, Turrini F (2008) Proteomic identification of heat shock protein 27 as a differentiation and prognostic marker in neuroblastoma but not in Ewing’s sarcoma. Virchows Arch 452:157–167

    Article  PubMed  CAS  Google Scholar 

  • Zantema A, Vries MV-D, Maasdam D, Bol S, Avd Eb (1992) Heat shock protein 27 and αB-cristallin can form a complex, which dissociates by heat shock. J Biol Chem 267(18):12936–12941

    PubMed  CAS  Google Scholar 

  • Zhang R, Luo D, Miao R et al (2005) Hsp90-Akt phosphorylates ASK1 and inhibits ASK1-mediated apoptosis. Oncogene 24(24):3954–3963

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Wong LL, Koay ES (2007) Phosphorylation of Ser78 of Hsp27 correlated with HER-2/neu status and lymph node positivity in breast cancer. Mol Cancer 6:52–57

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Murshid A, Prince T, Calderwood SK (2011a) Protein kinase A regulates molecular chaperone transcription and protein aggregation. PLoS One 6(12):e28950

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Pang E, Loo RR, Rao J, Go VL, Loo JA, Lu QY (2011b) Concomitant inhibition of HSP90, its mitochondrial localized homologue TRAP1 and HSP27 by green tea in pancreatic cancer HPAF-II cells. Proteomics 11:4638–4647

    Article  PubMed  CAS  Google Scholar 

  • Zhao YH et al (2009) Upregulation of lactate dehydrogenase A by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene 28:3689–3701

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Tassi L, Lane W, Mendelsohn ME (1994) Specific binding of the transglutaminase, platelet factor XIII, to HSP27. J Biol Chem 269(35):22379–22384

    PubMed  CAS  Google Scholar 

  • Zhuang H, Jiang W, Cheng W, Qian K, Dong W, Cao L, Huang Q, Li S, Dou F, Chiu JF, Fang XX, Lu M, Hua ZC (2010) Down-regulation of HSP27 sensitizes TRAIL-resistant tumor cell to TRAIL-induced apoptosis. Lung Cancer 68:27–38

    Article  PubMed  Google Scholar 

  • Zimmermann M, Nickl S, Lambers C, Hacker S, Mitterbauer A, Hoetzenecker K, Rozsas A, Ostoros G, Laszlo V, Hofbauer H, Renyi-Vamos F, Klepetko W, Dome B, Ankersmit HJ (2012) Discrimination of clinical stages in non-small cell lung cancer patients by serum HSP27 and HSP70: a multi-institutional case-control study. Clin Chim Acta 413(13–14):1115–1120

    Article  PubMed  CAS  Google Scholar 

  • Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G (2008) Immunological aspects of cancer chemotherapy. Nat Rev Immunol 8(1):59–73

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94(4):471–480

    Article  PubMed  CAS  Google Scholar 

  • Zoubeidi A, Zardan A, Beraldi E et al (2007) Cooperative interactions between androgen receptor (AR) and heat-shock protein 27 facilitate AR transcriptional activity. Cancer Res 67(21):10455–10465

    Article  PubMed  CAS  Google Scholar 

  • Zoubeidi A, Zardan A, Wiedmann RM, Locke J, Beraldi E, Fazli L, Gleave ME (2010) Hsp27 promotes insulin-like growth factor-I survival signaling in prostate cancer via p90Rsk-dependent phosphorylation and inactivation of BAD. Cancer Res 70:2307–2317

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

SKC was supported by NIH research grants RO-1CA047407, R0-1CA119045 and RO-1CA094397 and by DRC: Agencia Nacional de Promoción Científica y Tecnológica (PICT 1047, 2007, BID), CONICET (PIP 2428) and the Argentina Foundation for Cancer Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stuart K. Calderwood.

Additional information

Daniel R. Ciocca, Andre Patrick Arrigo and Stuart K. Calderwood contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ciocca, D.R., Arrigo, A.P. & Calderwood, S.K. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch Toxicol 87, 19–48 (2013). https://doi.org/10.1007/s00204-012-0918-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00204-012-0918-z

Keywords

Navigation