Skip to main content
Log in

Inflammatory and microenvironmental factors involved in breast cancer progression

  • Review
  • Published:
Archives of Pharmacal Research Aims and scope Submit manuscript

Abstract

The primary reason for the high mortality rate of breast cancer is metastasis, which can result in a poor survival rate. The tumor environment is important for promotion and invasion of cancer cells. Recent studies have shown that inflammation is associated with breast cancer. Therefore, it is important to investigate the role of the inflammatory and microenvironment in breast cancer progression and metastasis. The present review summarizes some of the markers for inflammation and breast cancer invasion, which may aid in the design of an appropriate therapy for metastatic breast cancer. The following four inflammatory markers are discussed in this review: (1) Tumor associated macrophages (TAMs); (2) Matrix metalloproteinases (MMPs); (3) Sphingosine 1-phosphate (S1P); (4) C-reactive protein (CRP). TAMs are commonly found in breast cancer patients, and high infiltration is positively correlated with poor prognosis and low survival rate. MMPs are well-known for their roles in the degradation of ECM components when cancer cells invade and migrate. MMPs are also associated with inflammation through recruitment of a variety of stromal cells such as fibroblasts and leukocytes. S1P is an inflammatory lipid and is involved in various cellular processes such as proliferation, survival, and migration. Recent studies indicate that S1P participates in breast cancer invasion in various ways. CRP is used clinically to indicate the outcome of cancer patients as well as acute inflammatory status. This review summarizes the current understanding on the role of S1P in CRP expression which promotes the breast epithelial cell invasion, suggesting a specific mechanism linking inflammation and breast cancer. The present review might be useful for understanding the relationship between inflammation and breast cancer for the development of pharmacological interventions that may control the primary molecules involved in the breast cancer microenvironment.

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

Similar content being viewed by others

References

  • Agarwal, S., G.V. Reddy, and P. Reddanna. 2009. Eicosanoids in inflammation and cancer: The role of COX-2. Expert Review of Clinical Immunology 5: 145–165.

    PubMed  CAS  Google Scholar 

  • Ahmed, O.I., A.M. Adel, D.R. Diab, and N.S. Gobran. 2006. Prognostic value of serum level of interleukin-6 and interleukin-8 in metastatic breast cancer patients. Egyptian Journal of Immunology 13: 61–68.

    PubMed  Google Scholar 

  • Ala-Aho, R., N. Johansson, A.H. Baker, and V.M. Kähäri. 2002. Expression of collagenase-3 (MMP-13) enhances invasion of human fibrosarcoma HT-1080 cells. International Journal of Cancer 97: 283–289.

    CAS  Google Scholar 

  • Alemany, R., C.J. van Koppen, K. Danneberg, M. Ter Braak, Zu Meyer, and D. Heringdorf. 2007. Regulation and functional roles of sphingosine kinases. Naunyn Schmiedeberg’s Archives of Pharmacology 374: 413–428.

    PubMed  CAS  Google Scholar 

  • Allavena, P., A. Sica, G. Solinas, C. Porta, and A. Mantovani. 2008. The inflammatory micro-environment in tumor progression: The role of tumor-associated macrophages. Critical Reviews in Oncology Hematology 66: 1–9.

    Google Scholar 

  • Allin, K.H., B.G. Nordestgaard, H. Flyger, and S.E. Bojesen. 2011. Elevated pre-treatment levels of plasma C-reactive protein are associated with poor prognosis after breast cancer: A cohort study. Breast Cancer Research 13: R55.

    PubMed  CAS  Google Scholar 

  • Alpaugh, M.L., J.S. Tomlinson, Z.M. Shao, and S.H. Barsky. 1999. A novel human xenograft model of inflammatory breast cancer. Cancer Research 59: 5079–5084.

    PubMed  CAS  Google Scholar 

  • Ammit, A.J., A.T. Hastie, L.C. Edsall, R.K. Hoffman, Y. Amrani, V.P. Krymskaya, S.A. Kane, S.P. Peters, R.B. Penn, S. Spiegel, and R.A. Panettieri Jr. 2001. Sphingosine 1-phosphate modulates human airway smooth muscle cell functions that promote inflammation and airway remodeling in asthma. FASEB Journal 15: 1212–1214.

    PubMed  CAS  Google Scholar 

  • Bachelot, T., I. Ray-Coquard, C. Menetrier-Caux, M. Rastkha, A. Duc, and J.Y. Blay. 2003. Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. British Journal of Cancer 88: 1721–1726.

    PubMed  CAS  Google Scholar 

  • Baglole, C.J., D.M. Ray, S.H. Bernstein, S.E. Feldon, T.J. Smith, P.J. Sime, and R.P. Phipps. 2006. More than structural cells, fibroblasts create and orchestrate the tumor microenvironment. Immunological Investigations 35: 297–325.

    PubMed  CAS  Google Scholar 

  • Balkwill, F., K.A. Charles, and A. Mantovani. 2005. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7: 211–217.

    PubMed  CAS  Google Scholar 

  • Balkwill, F., and A. Mantovani. 2001. Inflammation and cancer: Back to Virchow? Lancet 357: 539–545.

    PubMed  CAS  Google Scholar 

  • Bartsch, H., and J. Nair. 2006. Chronic inflammation and oxidative stress in the genesis and perpetuation of cancer: Role of lipid peroxidation, DNA damage, and repair. Langenbeck’s Archives of Surgery 391: 499–510.

    PubMed  Google Scholar 

  • Ben-Baruch, A. 2003. Host microenvironment in breast cancer development: Inflammatory cells, cytokines and chemokines in breast cancer progression: Reciprocal tumor-microenvironment interactions. Breast Cancer Research 5: 31–36.

    PubMed  CAS  Google Scholar 

  • Bertucci, F., P. Finetti, D. Birnbaum, and P. Viens. 2010. Gene expression profiling of inflammatory breast cancer. Cancer 116: 2783–2793.

    PubMed  CAS  Google Scholar 

  • Björklund, M., and E. Koivunen. 2005. Gelatinase-mediated migration and invasion of cancer cells. Biochimica et Biophysica Acta 1755: 37–69.

    Google Scholar 

  • Blann, A.D., G.J. Byrne, and A.D. Baildam. 2002. Increased soluble intercellular adhesion molecule-1, breast cancer and the acute phase response. Blood Coagulation and Fibrinolysis 13: 165–168.

    PubMed  CAS  Google Scholar 

  • Boland, G.P., I.S. Butt, R. Prasad, W.F. Knox, and N.J. Bundred. 2004. COX-2 expression is associated with an aggressive phenotype in ductal carcinoma in situ. British Journal of Cancer 90: 423–429.

    PubMed  CAS  Google Scholar 

  • Brasky, T.M., M.R. Bonner, K.B. Moysich, C.B. Ambrosone, J. Nie, M.H. Tao, S.B. Edge, B.V. Kallakury, C. Marian, D.S. Goerlitz, M. Trevisan, P.G. Shields, and J.L. Freudenheim. 2011. Non-steroidal anti-inflammatory drugs (NSAIDs) and breast cancer risk: Differences by molecular subtype. Cancer Causes and Control 22: 965–975.

    PubMed  Google Scholar 

  • Bronte, V., S. Cingarlini, I. Marigo, C. De Santo, G. Gallina, L. Dolcetti, S. Ugel, E. Peranzoni, S. Mandruzzato, and P. Zanovello. 2006. Leukocyte infiltration in cancer creates an unfavorable environment for antitumor immune responses: A novel target for therapeutic intervention. Immunological Investigations 35: 327–357.

    PubMed  CAS  Google Scholar 

  • Candido, J., and T. Hagemann. 2013. Cancer-related inflammation. Journal of Clinical Immunology 33: S79–S84.

    PubMed  Google Scholar 

  • Cha, Y., Y. Kang, and A. Moon. 2012. HER2 induces expression of leptin in human breast epithelial cells. BMB Report 45: 719–723.

    CAS  Google Scholar 

  • Chakrabarti, S., and K.D. Patel. 2005. Matrix metalloproteinase-2 (MMP-2) and MMP-9 in pulmonary pathology. Experimental Lung Research 31: 599–621.

    Google Scholar 

  • Chalfant, C.E., and S. Spiegel. 2005. Sphingosine 1-phosphate and ceramide 1-phosphate: Expanding roles in cell signaling. Journal of Cell Science 118: 4605–4612.

    PubMed  CAS  Google Scholar 

  • Chang, S., S.L. Parker, T. Pham, A.U. Buzdar, and S.D. Hursting. 1998. Inflammatory breast carcinoma incidence and survival: The Surveillance, Epidemiology, and End Results Program of the National Cancer Institute. Cancer 82: 2366–2372.

    PubMed  CAS  Google Scholar 

  • Chen, L.Y., G. Woszczek, S. Nagineni, C. Logun, and J.H. Shelhamer. 2008. Cytosolic phospholipase A2a activation induced by S1P is mediated by the S1P3 receptor in lung epithelial cells. American Journal of Physiology Lung Cellular and Molecular Physiology 295: L326–L335.

    Google Scholar 

  • Cole, S.W. 2009. Chronic inflammation and breast cancer recurrence. Journal of Clinical Oncology 27: 3418–3419.

    PubMed  Google Scholar 

  • Costa, C., R. Soares, J.S. Reis-Filho, D. Leitao, I. Amendoeira, and F.C. Schmitt. 2002. Cyclo-oxygenase 2 expression is associated with angiogenesis and lymph node metastasis in human breast cancer. Journal of Clinical Pathology 55: 429–434.

    PubMed  CAS  Google Scholar 

  • Coussens, L.M., and Z. Werb. 2002. Inflammation and cancer. Nature 420: 860–867.

    PubMed  CAS  Google Scholar 

  • Cox, J.H., R.A. Dean, C.R. Roberts, and C.M. Overal. 2008. Matrix metalloproteinase processing of CXCL11/I-TAC results in loss of chemoattractant activity and altered glycosaminoglycan binding. The Journal of Biological Chemistry 283: 19389–19399.

    Google Scholar 

  • Cretu, A., and P.C. Brooks. 2007. Impact of the non-cellular tumor microenvironment on metastasis: Potential therapeutic and imaging opportunities. Journal of Cellular Physiology 213: 391–402.

    PubMed  CAS  Google Scholar 

  • Crowther, M., N.J. Brown, E.T. Bishop, and C.E. Lewis. 2001. Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. Journal of Leukocyte Biology 70: 478–490.

    PubMed  CAS  Google Scholar 

  • Crumley, A.B., D.C. McMillan, M. McKernan, J.J. Going, C.J. Shearer, and R.C. Stuart. 2006. An elevated C-reactive protein concentration, prior to surgery, predicts poor cancer-specific survival in patients undergoing resection for gastro-oesophageal cancer. British Journal of Cancer 94: 1568–1571.

    PubMed  CAS  Google Scholar 

  • Davies, G., J. Salter, M. Hills, L.A. Martin, N. Sacks, and M. Dowsett. 2003. Correlation between cyclooxygenase-2 expression and angiogenesis in human breast cancer. Clinical Cancer Research 9: 2651–2656.

    PubMed  CAS  Google Scholar 

  • DeNardo, D.G., and L.M. Coussens. 2007. Inflammation and breast cancer: Balancing immune response—Crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Research 9: 212.

    PubMed  Google Scholar 

  • Denkert, C., K.J. Winzer, B.M. Muller, W. Weichert, S. Pest, M. Kobel, G. Kristiansen, A. Reles, A. Siegert, H. Guski, and S. Hauptmann. 2003. Elevated expression of cyclooxygenase-2 is a negative prognostic factor for disease free survival and overall survival in patients with breast carcinoma. Cancer 97: 2978–2987.

    PubMed  CAS  Google Scholar 

  • de Visser, K.E., A. Eichten, and L.M. Coussens. 2006. Paradoxical roles of the immune system during cancer development. Nature Reviews Cancer 6: 24–37.

    Google Scholar 

  • Dolezalova, H., G. Shankar, M.C. Huang, D.D. Bikle, and E.J. Goetzl. 2003. Biochemical regulation of breast cancer cell expression of S1P2 (Edg-5) and S1P3 (Edg-3) G protein-coupled receptors for sphingosine 1-phosphate. Journal of Cellular Biochemistry 88: 732–743.

    PubMed  CAS  Google Scholar 

  • Doronzo, G., I. Russo, L. Mattiello, M. Trovati, and G. Anfossi. 2005. CRP increases matrix metalloproteinase-2 expression and activity in cultured human vascular smooth muscle cells. Journal of Laboratory and Clinical Medicine 146: 287–298.

    PubMed  CAS  Google Scholar 

  • Du Clos, T.W. 2000. Function of C-reactive protein. Annals of Medicine 32: 274–278.

  • Duffy, M.J., T.M. Maguire, A. Hill, E. McDermott, and N. O’Higgins. 2000. Metalloproteinases: Role in breast carcinogenesis, invasion and metastasis. Breast Cancer Research 2: 252–257.

    PubMed  CAS  Google Scholar 

  • Dupuy, A.M., N. Terrier, L. Sénécal, M. Morena, H. Leray, B. Canaud, J.P. Cristol. 2003. Is C-reactive protein a marker of inflammation? Nephrologie 24: 337–341.

    Google Scholar 

  • Edge, S.B., D.R. Byrd, C.C. Compton, et al. (eds.). 2010. AJCC cancer staging manual, 7th ed, 347–376. New York: Springer.

    Google Scholar 

  • Edsparr, K., P.H. Basse, R.H. Goldfarb, and P. Albertsson. 2011. Matrix metalloproteinases in cytotoxic lymphocytes impact on tumour infiltration and immunomodulation. Cancer Microenvironment 4: 351–360.

    PubMed  CAS  Google Scholar 

  • Eiró, N., and F.J. Vizoso. 2012. Inflammation and cancer. The World Journal of Gastrointestinal Surgery 4: 62–72.

    Google Scholar 

  • Falconer, J.S., K.C. Fearon, J.A. Ross, R. Elton, S.J. Wigmore, O.J. Garden, and D.C. Carter. 1995. Acute phase protein response and survival duration of patients with pancreatic cancer. Cancer 75: 2077–2082.

    PubMed  CAS  Google Scholar 

  • Fan, S.Q., Q.Y. Wei, M.R. Li, L.Q. Zhang, and Q.C. Liang. 2003. Expression and clinical significance of MMP-2, MMP-9, TIMP-1, and TIMP-2 in breast carcinoma. Ai Zheng 22: 968–973.

    Google Scholar 

  • Federico, A., F. Morgillo, C. Tuccillo, F. Ciardiello, and C. Loguercio. 2007. Chronic inflammation and oxidative stress in human carcinogenesis. International Journal of Cancer 121: 2381–2386.

    CAS  Google Scholar 

  • Fisher, K.E., A. Pop, W. Koh, N.J. Anthis, W.B. Saunders, and G.E. Davis. 2006. Tumor cell invasion of collagen matrices requires coordinate lipid agonist-induced G protein and membrane-type matrix metalloproteinase-1-dependent signaling. Molecular Cancer 5: 1–23.

    Google Scholar 

  • Gallager, H.S., and J.E. Martin. 1970. An orientation to the concept of minimal breast cancer. Cancer 28: 1505–1507.

    Google Scholar 

  • Ganter, U., R. Arcone, C. Toniatti, G. Morrone, and G. Ciliberto. 1989. Dual control of C-reactive protein gene expression by interleukin-1 and interleukin-6. EMBO Journal 8: 3773–3779.

    PubMed  CAS  Google Scholar 

  • Goldberg, J.E., and K.L. Schwertfeger. 2010. Proinflammatory cytokines in breast cancer: Mechanisms of action and potential targets for therapeutics. Current Drug Targets 11: 1133–1146.

    PubMed  CAS  Google Scholar 

  • Gong, Y., E. Hart, A. Shchurin, and J. Hoover-Plow. 2008. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. The Journal of Clinical Investigation 118: 3012–3024.

    PubMed  CAS  Google Scholar 

  • Greene, E.R., S. Huang, C.N. Serhan, and D. Panigrahy. 2011. Regulation of inflammation in cancer by eicosanoids. Prostaglandins and Other Lipid Mediators 96: 27–36.

    PubMed  CAS  Google Scholar 

  • Hait, N.C., C.A. Oskeritzian, S.W. Paugh, S. Milstien, and S. Spiegel. 2006. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochimica et Biophysica Acta 1758: 2016–2026.

    PubMed  CAS  Google Scholar 

  • Han, Y., F. Mao, Y. Wu, X. Fu, X. Zhu, S. Zhou, W. Zhang, Q. Sun, and Y. Zhao. 2011. Prognostic role of C-reactive protein in breast cancer: A systematic review and meta-analysis. The International Journal of Biological Markers 26: 209–215.

    Google Scholar 

  • Hanahan, D., and R.A. Weinberg. 2011. Hallmarks of cancer: The next generation. Cell 144: 646–674.

    PubMed  CAS  Google Scholar 

  • Harizi, H., J.B. Corcuff, and N. Gualde. 2008. Arachidonic-acid-derived eicosanoids: Roles in biology and immunopathology. Trends in Molecular Medicine 14: 461–469.

    Google Scholar 

  • Haro, H., H.C. Crawford, B. Fingleton, K. Shinomiya, D.M. Spengler, and L.M. Matrisian. 2000. Matrix metalloproteinase-7-dependent release of tumor necrosis factor-alpha in a model of herniated disc resorption. The Journal of Clinical Investigation 105: 143–150.

    Google Scholar 

  • Harris, R.E., G.A. Alshafie, H. Abou-Issa, and K. Seibert. 2000. Chemoprevention of breast cancer in rats by celecoxib, a cyclooxygenase 2 inhibitor. Cancer Research 60: 2101–2103.

    PubMed  CAS  Google Scholar 

  • Harris, R.E. 2009. Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 17: 55–67.

    PubMed  CAS  Google Scholar 

  • Heffernan-Stroud, L.A., and L.M. Obeid. 2013. Sphingosine kinase 1 in cancer. Advances in Cancer Research 117: 201–235.

    Google Scholar 

  • Heller, R., Q. Chang, G. Ehrlich, S.N. Hsieh, S.M. Schoenwaelder, P.J. Kuhlencordt, K.T. Preissner, E. Hirsch, and R. Wetzker. 2008. Overlapping and distinct roles for PI3Kbeta and gamma isoforms in S1P-induced migration of human and mouse endothelial cells. Cardiovascular Research 80: 96–105.

    PubMed  CAS  Google Scholar 

  • Herszényi, L., G. Lakatos, I. Hritz, M.Z. Varga, G. Cierny, and Z. Tulassay. 2012. The role of inflammation and proteinases in tumor progression. Digestive Diseases 30: 249–254.

    PubMed  Google Scholar 

  • Hojilla, C.V., G.A. Wood, and R. Khokha. 2008. Inflammation and breast cancer: Metalloproteinases as common effectors of inflammation and extracellular matrix breakdown in breast cancer. Breast Cancer Research 10: 205.

    PubMed  Google Scholar 

  • Hong, G., L.M. Badudhuin, and Y. Xu. 1999. Sphingosine-1-phosphate modulates growth and adhesion of ovarian cancer cells. FEBS Letters 460: 513–518.

    PubMed  CAS  Google Scholar 

  • Honkoop, A.H., J. Wagstaff, and H.M. Pinedo. 1998. Management of stage III breast cancer. Oncology 55: 218–227.

    PubMed  CAS  Google Scholar 

  • Howe, L.R., K. Subbaramaiah, J. Patel, J.L. Masferrer, A. Deora, C. Hudis, H.T. Thaler, W.J. Muller, B. Du, A.M. Brown, and A.J. Dannenberg. 2002. Celecoxib, a selective cyclooxygenase 2 inhibitor, protects against human epidermal growth factor receptor 2 (HER-2)/neu-induced breast cancer. Cancer Research 62: 5405–5407.

    PubMed  CAS  Google Scholar 

  • Howlader, N., A.M. Noone, M. Krapcho, et al. (eds.). 2012. SEER Cancer Statistics Review, 1975–2009 (Vintage 2009 Populations). Bethesda: National Cancer Institute.

    Google Scholar 

  • Hrabec, E., J. Naduk, M. Strek, and Z. Hrabec. 2007. Type IV collagenases (MMP-2 and MMP-9) and their substrates—intracellular proteins, hormones, cytokines, chemokines and their receptors. Postepy Biochemii 53: 37–45.

    Google Scholar 

  • Huang, Y.L., W.P. Huang, and H. Lee. 2011. Roles of sphingosine 1-phosphate on tumorigenesis. The World Journal of Biological Chemistry 2: 25–34.

    Google Scholar 

  • Hsieh, H.L., C.C. Sun, C.B. Wu, C.Y. Wu, W.H. Tung, H.H. Wang, and C.M. Yang. 2008. Sphingosine 1-phosphate induces EGFR expression via Akt/NF-kappaB and ERK/AP-1 pathways in rat vascular smooth muscle cells. Journal of Cellular Biochemistry 103: 1732–1746.

    PubMed  CAS  Google Scholar 

  • Jemal, A., F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman. 2011. Global cancer statistics. A Cancer Journal for Clinicians 61: 69–90.

    Google Scholar 

  • Jinga, D.C., A. Blidaru, I. Condrea, C. Ardeleanu, C. Dragomir, G. Szegli, M. Stefanescu, and C. Matache. 2006. MMP-9 and MMP-2 gelatinases and TIMP-1 and TIMP-2 inhibitors in breast cancer: Correlations with prognostic factors. Journal of Cellular and Molecular Medicine 10: 499–510.

    Google Scholar 

  • Johnson, K.R., K.P. Becker, M.M. Facchinetti, Y.A. Hannun, and L.M. Obeid. 2002. PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). Journal of Biological Chemistry 277: 35257–35262.

    PubMed  CAS  Google Scholar 

  • Kawamori, T., W. Osta, K.R. Johnson, B.J. Pettus, J. Bielawski, T. Tanaka, M.J. Wargovich, B.S. Reddy, Y.A. Hannun, L.M. Obeid, and D. Zhou. 2006. Sphingosine kinase 1 is up-regulated in colon carcinogenesis. FASEB Journal 20: 386–388.

    Google Scholar 

  • Kessenbrock, K., V. Plaks, and Z. Werb. 2010. Matrix metalloproteinases: Regulators of the tumor microenvironment. Cell 141: 52–67.

    PubMed  CAS  Google Scholar 

  • Kim, E.S., Y. Cha, M. Ham, J. Jung, S.G. Kim, S. Hwang, R. Kleemann, and A. Moon. 2013. Inflammatory lipid sphingosine-1-phosphate upregulates C-reactive protein via C/EBPβ and potentiates breast cancer progression. Oncogene. doi:10.1038/onc.2013.319.

    Google Scholar 

  • Kim, E.S., J.B. Jeong, S. Kim, K.M. Lee, E. Ko, D.Y. Noh, K.T. Hwang, J.H. Ha, C.H. Lee, S.G. Kim, and A. Moon. 2010. The G12 family proteins upregulate matrix metalloproteinase-2 via p53 leading to human breast cell invasion. Breast Cancer Research and Treatment 124: 49–61.

    PubMed  CAS  Google Scholar 

  • Kim, E.S., J.S. Kim, S.G. Kim, S. Hwang, C.H. Lee, and A. Moon. 2011. Sphingosine 1-phosphate regulates matrix metalloproteinase-9 expression and breast cell invasion through S1P3-Gαq coupling. Journal of Cell Science 1(124): 2220–2230.

    Google Scholar 

  • Kim, I.Y., H.Y. Yong, K.W. Kang, and A. Moon. 2009. Overexpression of ErbB2 induces invasion of MCF10A human breast epithelial cells via MMP-9. Cancer Letters 18(275): 227–233.

    Google Scholar 

  • Kim, M.S., E.J. Lee, H.R. Kim, and A. Moon. 2003. p38 kinase is a key signaling molecule for H-Ras-induced cell motility and invasive phenotype in human breast epithelial cells. Cancer Research 63: 5454–5461.

    PubMed  CAS  Google Scholar 

  • Kleemann, R., P.P. Gervois, L. Verschuren, B. Staels, H.M. Princen, and T. Kooistra. 2003. Fibrates down-regulate IL-1-stimulated C-reactive protein gene expression in hepatocytes by reducing nuclear p50-NFkappa B-C/EBP-beta complex formation. Blood 101: 545–551.

    PubMed  CAS  Google Scholar 

  • Kluk, M.J., and T. Hla. 2002. Signaling of sphingosine-1-phosphate via the S1P/EDG-family of G-protein-coupled receptors. Biochimica et Biophysica Acta 1582: 72–80.

    PubMed  CAS  Google Scholar 

  • Kobayashi, N., T. Nishi, T. Hirata, A. Kihara, T. Sano, Y. Igarashi, and A. Yamaguchi. 2006. Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner. Journal of Lipid Research 47: 614–621.

    PubMed  CAS  Google Scholar 

  • Kobayashi, N., A. Yamaguchi, and T. Nishi. 2009. Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. Journal of Biological Chemistry 284: 21192–21200.

    PubMed  CAS  Google Scholar 

  • Kundu, J.K., and Y.J. Surh. 2008. Inflammation: Gearing the journey to cancer. Mutation Research 659: 15–30.

    PubMed  CAS  Google Scholar 

  • Laskin, D.L. 2009. Macrophages and inflammatory mediators in chemical toxicity: A battle of forces. Chemistry Research in Toxicology 22: 1376–1385.

    Google Scholar 

  • Lee, H., C.I. Lin, J.J. Liao, Y.W. Lee, H.Y. Yang, C.Y. Lee, H.Y. Hsu, and H.L. Wu. 2004. Lysophospholipids increase ICAM-1 expression in HUVEC through a Gi- and NF-kappaB-dependent mechanism. American Journal of Physiology Cell Physiology 287: C1657–C1666.

    PubMed  CAS  Google Scholar 

  • Leek, R.D., and A.L. Harris. 2002. Tumor-associated macrophages in breast cancer. Journal of Mammary Gland Biology and Neoplasia 7: 177–189.

    Google Scholar 

  • Leek, R.D., N.C. Hunt, R.J. Landers, C.E. Lewis, J.A. Royds, and A.L. Harris. 2000. Macrophage infiltration is associated with VEGF and EGFR expression in breast cancer. Journal of Pathology 190: 430–436.

    PubMed  CAS  Google Scholar 

  • Leek, R.D., R. Landers, S.B. Fox, F. Ng, A.L. Harris, and C.E. Lewis. 1998. Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. British Journal of Cancer 77: 2246–2251.

    PubMed  CAS  Google Scholar 

  • Leek, R.D., C.E. Lewis, R. Whithouse, M. Greenall, J. Clarke, and A.L. Harris. 1996. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Research 56: 4625–4629.

    PubMed  CAS  Google Scholar 

  • Lewis, C.E., and R. Hughes. 2007. Inflammation and breast cancer. Microenvironmental factors regulating macrophage function in breast tumours: Hypoxia and angiopoietin-2. Breast Cancer Research 9: 209.

    PubMed  Google Scholar 

  • Lewis, C.E., R. Leek, A.L. Harris, and J.O.D. McGee. 1995. Cytokine regulation of angiogenesis in breast cancer: The role of tumor associated macrophages. Journal of Leukocyte Biology 57: 747–751.

    PubMed  CAS  Google Scholar 

  • Lewis, C.E., and J.W. Pollard. 2006. Distinct role of macrophages in different tumor microenvironments. Cancer Research 66: 605–612.

    PubMed  CAS  Google Scholar 

  • Lin, C.I., C.N. Chen, J.H. Chen, and H. Lee. 2006. Lysophospholipids increase IL-8 and MCP-1 expressions in human umbilical cord vein endothelial cells through an IL-1-dependent mechanism. Journal of Cellular Biochemistry 99: 1216–1232.

    PubMed  CAS  Google Scholar 

  • Lin, E.Y., and J.W. Pollard. 2007. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Research 67: 5064–5066.

    PubMed  CAS  Google Scholar 

  • Liotta, L.A., and W.G. Stetler-Stevenson. 1991. Tumor invasion and metastasis: An imbalance of positive and negative regulation. Cancer Research 51: 5054s–5059s.

    PubMed  CAS  Google Scholar 

  • Long, J.S., J. Edwards, C. Watson, S. Tovey, K. Mair, R. Schiff, V. Natarajan, N.J. Pyne, and S. Pyne. 2010a. Sphingosine kinase 1 induces tolerance to human epidermal growth factor receptor 2 and prevents formation of a migratory phenotype in response to sphingosine 1-phosphate in estrogen receptor positive breast cancer cells. Molecular and Cellular Biology 30: 3827–3841.

    PubMed  CAS  Google Scholar 

  • Long, J.S., Y. Fujiwara, J. Edwards, C. Tannahill, G. Tigyi, S. Pyne, and N.J. Pyne. 2010b. Sphingosine 1-phosphate 4 uses HER2 (ErbB2) to regulate extracellular signal regulated kinase-1/2 in MDA-MB-453 breast cancer cells. Journal of Biological Chemistry 285: 35957–35966.

    PubMed  CAS  Google Scholar 

  • Lorusso, G., and C. Rüegg. 2008. The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochemistry and Cell Biology 130: 1091–1103.

    PubMed  CAS  Google Scholar 

  • Lu, H., W. Ouyang, and C. Huang. 2006. Inflammation, a key event in cancer development. Molecular Cancer Research 4: 221–233.

    PubMed  Google Scholar 

  • Lu, J., K.D. Marjon, L.L. Marnell, R. Wang, C. Mold, T.W. Du Clos, and P. Sun. 2011. Recognition and functional activation of the human IgA receptor (FcalphaRI) by C-reactive protein. Proceedings of the National Academy of Sciences 108: 4974–4979.

    CAS  Google Scholar 

  • Lucia, M.S., and K.C. Torkko. 2004. Inflammation as a target for prostate cancer chemoprevention: Pathological and laboratory rationale. Journal of Urology 171: S30–S34.

    PubMed  Google Scholar 

  • Malla, N., S. Sjoli, J.O. Winberg, E. Hadler-Olsen, and L. Uhlin-Hansen. 2008. Biological and pathobiological functions of gelatinase dimers and complexes. Connective Tissue Research 49: 180–184.

    PubMed  CAS  Google Scholar 

  • Manicone, A.M., and J.K. McGuire. 2008. Matrix metalloproteinases as modulators of inflammation. Seminars in Cell and Developmental Biology 19: 34–41.

    PubMed  CAS  Google Scholar 

  • Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature 454: 436–444.

    PubMed  CAS  Google Scholar 

  • Mantovani, A., B. Bottazzi, F. Colotta, S. Sozzani, and L. Ruco. 1992. The origin and function of tumor-associated macrophages. Immunology Today 13: 265–270.

    PubMed  CAS  Google Scholar 

  • Mantovani, A., F. Marchesi, C. Porta, A. Sica, and P. Allavena. 2007. Inflammation and cancer: Breast cancer as a prototype. Breast 16: S27–S33.

    PubMed  Google Scholar 

  • Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology 25: 677–686.

    Google Scholar 

  • Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. 2002. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends in Immunology 23: 549–555.

    PubMed  CAS  Google Scholar 

  • McArdle, P.A., K. Mir, A.S. Almushatat, A.M. Wallace, M.A. Underwood, and D.C. McMillan. 2006. Systemic inflammatory response, prostate-specific antigen and survival in patients with metastatic prostate cancer. Urologia Internationalist 77: 127–129.

    CAS  Google Scholar 

  • McMillan, D.C., K. Canna, and C.S. McArdle. 2003. Systemic inflammatory response predicts survival following curative resection of colorectal cancer. British Journal of Surgery 90: 215–219.

    PubMed  CAS  Google Scholar 

  • McQuibban, G.A., J.H. Gong, J.P. Wong, J.L. Wallace, I. Clark-Lewis, C.M. Overall. 2002. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100: 1160–1167.

    Google Scholar 

  • Miles, D.W., L.C. Happerfield, M.S. Naylor, L.G. Bobrow, R.D. Rubens, and F.R. Balkwill. 1994. Expression of tumour necrosis factor (TNF-α) and its receptors in benign and malignant breast tissue. International Journal of Cancer 56: 777–782.

    CAS  Google Scholar 

  • Montero, I., J. Orbe, N. Varo, O. Beloqui, J.I. Monreal, J.A. Rodríguez, J. Díez, P. Libby, and J.A. Páramo. 2006. CRP induces matrix metalloproteinase-1 and -10 in human endothelial cells: Implications for clinical and subclinical atherosclerosis. Journal of the American College of Cardiology 47: 1369–1378.

    PubMed  CAS  Google Scholar 

  • Moon, A., M.S. Kim, T.G. Kim, S.H. Kim, H.E. Kim, Y.Q. Chen, and H.R. Kim. 2000. H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: A role for MMP-2 in the H-rasinduced invasive phenotype. International Journal of Cancer 85: 176–181.

    CAS  Google Scholar 

  • Moshage, H.J., H.M. Roelofs, J.F. van Pelt, B.P. Hazenberg, M.A. van Leeuwen, P.C. Limburg, L.A. Aarden, and S.H. Yap. 1988. The effect of interleukin-1, interleukin-6 and its interrelationship on the synthesis of serum amyloid A and C-reactive protein in primary cultures of adult human hepatocytes. Biochemical and Biophysical Research Communications 155: 112–117.

    PubMed  CAS  Google Scholar 

  • Murphy, G., A. Murthy, and R. Khokha. 2008. Clipping, shedding and RIPping keep immunity on cue. Trends in Immunology 29: 75–82.

    PubMed  CAS  Google Scholar 

  • Nabata, A., M. Kuroki, H. Ueba, S. Hashimoto, T. Umemoto, H. Wada, T. Yasu, M. Saito, S. Momomura, and M. Kawakami. 2008. C-reactive protein induces endothelial cell apoptosis and matrix metalloproteinase-9 production in human mononuclear cells: Implications for the destabilization of atherosclerotic plaque. Atherosclerosis 196: 129–135.

    PubMed  CAS  Google Scholar 

  • Nakopoulou, L., E.G. Panayotopoulou, I. Giannopoulou, P. Alexandrou, S. Katsarou, P. Athanassiadou, and A. Keramopoulos. 2002. Stromelysin-3 protein expression in invasive breast cancer: Relation to proliferation, cell survival and patients’ outcome. Modern Pathology 15: 1154–1161.

    PubMed  Google Scholar 

  • Nava, V.E., J.P. Hobson, S. Murthy, S. Milstien, and S. Spiegel. 2002. Sphingosine kinase type 1 promotes estrogen-dependent tumorigenesis of breast cancer MCF-7 cells. Experimental Cell Research 281: 115–127.

    Google Scholar 

  • Nielsen, B.S., F. Rank, J.M. López, M. Balbin, F. Vizoso, L. Lund, K. Danø, and C. López-Otín. 2001. Collagenase-3 expression in breast myofibroblasts as a molecular marker of transition of ductal carcinoma in situ lesions to invasive ductal carcinomas. Cancer Research 61: 7091–7100.

    PubMed  CAS  Google Scholar 

  • Nishi, T., N. Kobayashi, Y. Hisano, A. Kawahara, and A. Yamaguchi. 2013. Molecular and physiological functions of sphingosine 1-phosphate transporters. Biochimica et Biophysica Acta S1388–1981: 00150–00159.

    Google Scholar 

  • Nishikawa, T., K. Hagihara, S. Serada, T. Isobe, A. Matsumura, J. Song, T. Tanaka, I. Kawase, T. Naka, and K. Yoshizaki. 2008. Transcriptional complex formation of c-Fos, STAT3, and hepatocyte NF-1 alpha is essential for cytokine-driven C-reactive protein gene expression. Journal of Immunology 180: 3492–3501.

    CAS  Google Scholar 

  • Nixon, G.F. 2009. Sphingolipids in inflammation: Pathological implications and potential therapeutic targets. British Journal of Pharmacology 158: 982–993.

    PubMed  CAS  Google Scholar 

  • O’Hanlon, D.M., J. Lynch, M. Cormican, and H.F. Given. 2002. The acute phase response in breast carcinoma. Anticancer Research 22: 1289–1293.

    PubMed  Google Scholar 

  • Olivera, A. 2008. Unraveling the complexities of sphingosine-1-phosphate function: The mast cell model. Prostaglandins and Other Lipid Mediators 86: 1–11.

    PubMed  CAS  Google Scholar 

  • O’Sullivan, C., and C.E. Lewis. 1994. Tumour-associated leucocytes: Friends or foes in breast carcinoma. Journal of Pathology 172: 229–235.

    PubMed  Google Scholar 

  • Paik, J.H., S. Chae, M.J. Lee, S. Thangada, and T. Hla. 2001. Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3- and beta1-containing integrins. Journal of Biological Chemistry 276: 11830–11837.

    PubMed  CAS  Google Scholar 

  • Park, C.C., M.J. Bissell, and M.H. Barcellos-Hoff. 2000. The influence of the microenvironment on the malignant phenotype. Molecular Medicine Today 6: 324–329.

    PubMed  CAS  Google Scholar 

  • Parks, W.C., C.L. Wilson, and Y.S. Lopez-Boado. 2004. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nature Reviews Immunology 4: 617–629.

    PubMed  CAS  Google Scholar 

  • Payne, S.G., S. Milstien, and S. Spiegel. 2002. Sphingosine-1-phosphate: Dual messenger functions. FEBS Letters 531: 54–57.

    Google Scholar 

  • Pchejetski, D., T. Böhler, J. Stebbing, and J. Waxman. 2011. Therapeutic potential of targeting sphingosine kinase 1 in prostate cancer. Nature Reviews Urology 8: 569–678.

    PubMed  CAS  Google Scholar 

  • Pettus, B.J., J. Bielawski, A.M. Porcelli, D.L. Reames, K.R. Johnson, J. Morrow, C.E. Chalfant, L.M. Obeid, and Y.A. Hannun. 2003. The sphingosine kinase 1/sphingosine-1 phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-a. FASEB Journal 17: 1411–1421.

    PubMed  CAS  Google Scholar 

  • Pettus, B.J., C.E. Chalfant, and Y.A. Hannun. 2004. Sphingolipids in inflammation: Roles and implications. Current Molecular Medicine 4: 405–418.

    Google Scholar 

  • Philip, M., D.A. Rowley, and H. Schreiber. 2004. Inflammation as a tumor promoter in cancer induction. Seminars in Cancer Biology 14: 433–439.

    PubMed  CAS  Google Scholar 

  • Pierce, B.L., R. Ballard-Barbash, L. Bernstein, R.N. Baumgartner, M.L. Neuhouser, M.H. Wener, K.B. Baumgartner, F.D. Gilliland, B.E. Sorensen, A. McTiernan, and C.M. Ulrich. 2009. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. Journal of Clinical Oncology 27: 3437–3444.

    PubMed  CAS  Google Scholar 

  • Pollard, J.W. 2008. Macrophages define the invasive microenvironment in breast cancer. Journal of Leukocyte Biology 84: 623–630.

    PubMed  CAS  Google Scholar 

  • Posner, M.C., and N. Wolmark. 1992. Non-invasive breast carcinoma. Breast Cancer Research and Treatment 21: 155–164.

    PubMed  CAS  Google Scholar 

  • Pyne, N.J., and S. Pyne. 2010. Sphingosine 1 phosphate and cancer. Nature Reviews Cancer 10: 489–503.

    PubMed  CAS  Google Scholar 

  • Pyne, S., and N. Pyne. 2000. Sphingosine 1-phosphate signalling in mammalian cells. The Biochemical Journal 349: 385–402.

    PubMed  CAS  Google Scholar 

  • Rahme, E., J. Ghosn, K. Dasgupta, R. Rajan, and M. Hudson. 2005. Association between frequent use of nonsteroidal anti-inflammatory drugs and breast cancer. BMC Cancer 5: 159.

    PubMed  Google Scholar 

  • Ravishankaran, P., and R. Karunanithi. 2011. Clinical significance of preoperative serum interleukin-6 and C-reactive protein level in breast cancer patients. World Journal of Surgical Oncology 6: 9–18.

    Google Scholar 

  • Rivera, R., and J. Chun. 2008. Biological effects of lysophospholipids. Reviews of Physiology Biochemistry and Pharmacology 160: 25–46.

    CAS  Google Scholar 

  • Rodrı′guez, D., C.J. Morrison, and C.M. Overall. 2010. Matrix metalloproteinases: What do they not do? New substrates and biological roles identified by murine models and proteomics. Biochimica et Biophysica Acta 1803: 39–54.

    Google Scholar 

  • Rosen, H., P.J. Gonzalez-Cabrera, M.G. Sanna, and S. Brown. 2009. Sphingosine 1-phosphate receptor signaling. Annual Review of Biochemistry 78: 743–768.

    PubMed  CAS  Google Scholar 

  • Ryu, Y., N. Takuwa, N. Sugimoto, S. Sakurada, S. Usui, H. Okamoto, O. Matsui, and Y. Takuwa. 2002. Sphingosine-1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circulation Research 90: 325–332.

    PubMed  CAS  Google Scholar 

  • Saad, S., D.J. Gottlieb, K.F. Bradstock, C.M. Overall, and L.J. Bendall. 2002. Cancer cell-associated fibronectin induces release of matrix metalloproteinase-2 from normal fibroblasts. Cancer Research 62: 283–289.

    PubMed  CAS  Google Scholar 

  • Salgado, R., S. Junius, I. Van Benoy, P. Dam, P. Vermeulen, E. Van Marck, P. Huget, and L.Y. Dirix. 2003. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. International Journal of Cancer 103: 642–646.

    CAS  Google Scholar 

  • Sarkar, S., M. Maceyka, N.C. Hait, S.W. Paugh, H. Sankala, S. Milstien, and S. Spiegel. 2005. Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Letters 579: 5313–5317.

    PubMed  CAS  Google Scholar 

  • Sbardella, D., G.F. Fasciglione, M. Gioia, C. Ciaccio, G.R. Tundo, S. Marini, and M. Coletta. 2012. Human matrix metalloproteinases: An ubiquitarian class of enzymes involved in several pathological processes. Molecular Aspects of Medicine 33: 119–208.

    PubMed  CAS  Google Scholar 

  • Schmid, M.C., and J.A. Varner. 2010. Myeloid cells in the tumor microenvironment: Modulation of tumor angiogenesis and tumor inflammation. Journal of Oncology 2010: 201026.

  • Schultz, D.R., and P.I. Arnold. 1990. Properties of four acute phase proteins: C-reactive protein, serum amyloid A protein, alpha 1-acid glycoprotein, and fibrinogen. Seminars in Arthritis and Rheumatism 20: 129–147.

    PubMed  CAS  Google Scholar 

  • Scorilas, A., A. Karameris, N. Arnogiannaki, A. Ardavanis, P. Bassilopoulos, T. Trangas, and M. Talieri. 2001. Overexpression of matrix-metalloproteinase-9 in human breast cancer: A potential favourable indicator in node-negative patients. British Journal of Cancer 84: 1488–1496.

    Google Scholar 

  • Scott, H.R., D.C. McMillan, L.M. Forrest, D.J. Brown, C.S. McArdle, and R. Milroy. 2002. The systemic inflammatory response, weight loss, performance status and survival in patients with inoperable non-small cell lung cancer. British Journal of Cancer 87: 264–267.

    PubMed  CAS  Google Scholar 

  • Shim, J.Y., H.J. An, Y.H. Lee, S.K. Kim, K.P. Lee, and K.S. Lee. 2003. Overexpression of cyclooxygenase-2 is associated with breast carcinoma and its poor prognostic factors. Modern Pathology 16: 1199–1204.

    PubMed  Google Scholar 

  • Shin, I., S. Kim, H. Song, H.R. Kim, and A. Moon. 2005. H-Ras-specific activation of Rac-MKK3/6-p38 pathway: Its critical role in invasion and migration of breast epithelial cells. Journal of Biological Chemistry 280: 14675–14683.

    PubMed  CAS  Google Scholar 

  • Sica, A., T. Schioppa, A. Mantovani, and P. Allavena. 2006. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. European Journal of Cancer 42: 717–727.

    Google Scholar 

  • Siehler, S., and D.R. Manning. 2002. Pathways of transduction engaged by sphingosine phosphate through G protein-coupled receptors. Biochimica et Biophysica Acta 1582: 94–99.

    PubMed  CAS  Google Scholar 

  • Silverstein, M.J. 1998. Ductal carcinoma in situ of the breast. BMJ 317: 734–739.

    Google Scholar 

  • Song, H., S.H. Ki, S.G. Kim, and A. Moon. 2006. Activating transcription factor 2 mediates matrix metalloproteinase-2 transcriptional activation induced by p38 in breast epithelial cells. Cancer Research 66: 10487–10496.

    PubMed  CAS  Google Scholar 

  • Spiegel, S., and S. Milstien. 2003. Sphingosine-1-phosphate: An enigmatic signaling lipid. Nature Reviews Molecular Cell Biology 4: 397–407.

    PubMed  CAS  Google Scholar 

  • Stetler-Stevenson, W.G. 1999. Matrix metalloproteinases in angiogenesis: A moving target for therapeutic intervention. The Journal of Clinical Investigation 103: 1237–1241.

    PubMed  CAS  Google Scholar 

  • Stetler-Stevenson, W.G., and A.E. Yu. 2001. Proteases in invasion: Matrix metalloproteinases. Seminars in Cancer Biology 11: 143–152.

    PubMed  CAS  Google Scholar 

  • Sun, Y., N. Lu, Y. Ling, Y. Gao, Y. Chen, L. Wang, R. Hu, Q. Qi, W. Liu, Y. Yang, Q. You, and Q. Guo. 2009. Oroxylin A suppresses invasion through down-regulating the expression of matrix metalloproteinase-2/9 in MDA-MB-435 human breast cancer cells. European Journal of Pharmacology 603: 22–28.

    PubMed  CAS  Google Scholar 

  • Swartz, M.A., N. Iida, E.W. Roberts, S. Sangaletti, M.H. Wong, F.E. Yull, L.M. Coussens, and Y.A. DeClerck. 2012. Tumor microenvironment complexity: Emerging roles in cancer therapy. Cancer Research 72: 2473–2480.

    PubMed  CAS  Google Scholar 

  • Taha, T.A., K.M. Argraves, and L.M. Obeid. 2004. Sphingosine-1-phosphate receptors: Receptor specificity versus functional redundancy. Biochimica et Biophysica Acta 1682: 48–55.

    PubMed  CAS  Google Scholar 

  • Takabe, K., S.W. Paugh, S. Milstien, and S. Spiegel. 2008. “Inside-out” signaling of sphingosine-1-phosphate: Therapeutic targets. Pharmacological Reviews 60: 181–195.

    PubMed  CAS  Google Scholar 

  • Talvensaari-Mattila, A., P. Pääkko, G. Blanco-Sequeiros, and T. Turpeenniemi-Hujanen. 2001. Matrix metalloproteinase-2 (MMP-2) is associated with the risk for a relapse in postmenopausal patients with node-positive breast carcinoma treated with antiestrogen adjuvant therapy. Breast Cancer Research and Treatment 65: 55–61.

    Google Scholar 

  • Talvensaari-Mattila, A., P. Pääkkö, and T. Turpeenniemi-Hujanen. 2003. Matrix metalloproteinase-2 (MMP-2) is associated with survival in breast carcinoma. British Journal of Cancer 89: 1270–1275.

    Google Scholar 

  • Tan, M., J. Yao, and D. Yu. 1997. Overexpression of the c-erbB-2 gene enhanced intrinsic metastasis potential in human breast cancer cells without increasing their transformation abilities. Cancer Research 57(6): 1199–1205.

    PubMed  CAS  Google Scholar 

  • Tani, M., T. Sano, M. Ito, and Y. Igarashi. 2005. Mechanisms of sphingosine and sphingosine 1-phosphate generation in human platelets. Journal of Lipid Research 46: 2458–2467.

    PubMed  CAS  Google Scholar 

  • Tauseef, M., V. Kini, N. Knezevic, M. Brannan, R. Ramchandaran, H. Fyrst, J. Saba, S.M. Vogel, A.B. Malik, and D. Mehta. 2008. Activation of sphingosine kinase-1 reverses the increase in lung vascular permeability through sphingosine-1-phosphate receptor signaling in endothelial cells. Circulation Research 103: 1164–1172.

    PubMed  CAS  Google Scholar 

  • Tillett, W.S., and T. Francis. 1930. Serological reactions in pneumonia with a nonprotein somatic fraction of pneumococcus. Journal of Experimental Medicine 52: 561–571.

    PubMed  CAS  Google Scholar 

  • Tron, K., D.E. Manolov, C. Röcker, M. Kächele, J. Torzewski, and G.U. Nienhaus. 2008. C-reactive protein specifically binds to Fcgamma receptor type I on a macrophage-like cell line. European Journal of Immunology 38: 1414–1422.

    PubMed  CAS  Google Scholar 

  • Tsung, K., J.P. Dolan, Y.L. Tsung, and J.A. Norton. 2002. Macrophages as effector cells in interleukin 12-induced T cell-dependent tumor rejection. Cancer Research 62: 5069–5075.

    PubMed  CAS  Google Scholar 

  • Ulrich, C.M., J. Bigler, and J.D. Potter. 2006. Nonsteroidal anti-inflammatory drugs for cancer prevention: Promise, perils and pharmacogenetics. Nature Reviews Cancer 6: 130–140.

    PubMed  CAS  Google Scholar 

  • Van Brocklyn, J.R., M.J. Lee, R. Menzeleev, A. Olivera, L. Edsall, O. Cuvillier, D.M. Thomas, P.J. Coopman, S. Thangada, C.H. Liu, T. Hla, and S. Spiegel. 1998. Dual actions of sphingosine-1-phosphate: Extracellular through the Gi-coupled receptor Edg-1 and intracellular to regulate proliferation and survival. Journal of Cell Biology 142: 229–240.

    PubMed  Google Scholar 

  • Van Laere, S.J., G.G. Van den Eynden, I. Van der Auwera, M. Vandenberghe, P. van Dam, E.A. Van Marck, K.L. van Golen, P.B. Vermeulen, and L.Y. Dirix. 2006. Identification of cell-of-origin breast tumor subtypes in inflammatory breast cancer by gene expression profiling. Breast Cancer Research and Treatment 95: 243–255.

    PubMed  CAS  Google Scholar 

  • Van Lint, P., and C. Libert. 2007. Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. Journal of Leukocyte Biology 82: 1375–1381.

    Google Scholar 

  • van Netten, J.P., B.J. Ashmead, D. Cavers, C. Fletcher, I.G. Thornton, B.L. Antonsen, P. Coy, and M.L. Brigden. 1992. ‘Macrophages’ and their putative significance in human breast cancer. British Journal of Cancer 66: 220–221.

    PubMed  Google Scholar 

  • Villaseñor, A., A. Ambs, R. Ballard-Barbash, K.B. Baumgartner, A. McTiernan, C.M. Ulrich, M.L. Neuhouser. 2011. Dietary fiber is associated with circulating concentrations of C-reactive protein in breast cancer survivors: The HEAL study. Breast Cancer Research and Treatment 129: 485–494.

    Google Scholar 

  • Visscher, D.W., M. Höyhtyä, S.K. Ottosen, C.M. Liang, F.H. Sarkar, J.D. Crissman, and R. Fridman. 1994. Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinomas correlates with tumor recurrence. International Journal of Cancer 59: 339–344.

    CAS  Google Scholar 

  • Volanakis, J.E. 2001. Human C-reactive protein: Expression, structure, and function. Molecular Immunology 38: 189–197.

    PubMed  CAS  Google Scholar 

  • Wang, D., and R.N. Dubois. 2010. Eicosanoids and cancer. Nature Reviews Cancer 10: 181–193.

    PubMed  CAS  Google Scholar 

  • Wang, D., Z. Zhao, A. Caperell-Grant, G. Yang, S.C. Mok, J. Liu, R.M. Bigsby, and Y. Xu. 2008. S1P differentially regulates migration of human ovarian cancer and human ovarian surface epithelial cells. Molecular Cancer Therapeutics 7: 1993–2002.

    PubMed  CAS  Google Scholar 

  • Wang, F., K. Nohara, A. Olivera, E.W. Thompson, and S. Spiegel. 1999a. Involvement of focal adhesion kinase in inhibition of motility of human breast cancer cells by sphingosine 1-phosphate. Experimental Cell Research 247: 17–28.

    PubMed  CAS  Google Scholar 

  • Wang, F., J.R. Van Brocklyn, J.P. Hobson, S. Movafagh, Z. Zukowska-Grojec, S. Milsteion, and S. Spiegel. 1999b. Sphingosine 1-phosphate stimulates cell migration through a Gi-coupled cell surface receptor: Potential involvement in angiogenesis. Journal of Biological Chemistry 274: 35343–35350.

    PubMed  CAS  Google Scholar 

  • Wang, M.T., K.V. Honn, and D. Nie. 2007. Cyclooxygenases, prostanoids, and tumor progression. Cancer and Metastasis Reviews 26: 525–534.

    PubMed  CAS  Google Scholar 

  • Watson, C., J.S. Long, C. Orange, C.L. Tannahill, E. Mallon, L.M. McGlynn, S. Pyne, N.J. Pyne, and J. Edwards. 2010. High expression of sphingosine 1-phosphate receptors, S1P1 and S1P3, sphingosine kinase 1, and extracellular signal-regulated kinase-1/2 is associated with development of tamoxifen resistance in estrogen receptor-positive breast cancer patients. American Journal of Pathology 177: 2205–2215.

    PubMed  CAS  Google Scholar 

  • Winberg, J.O., S.O. Kolset, E. Berg, and L. Uhlin-Hansen. 2000. Macrophages secrete matrix metalloproteinase 9 covalently linked to the core protein of chondroitin sulphate proteoglycans. Journal of Molecular Biology 304: 669–680.

    Google Scholar 

  • Wong, V.K., H.Z. Malik, Z.Z. Hamady, A. Al-Mukhtar, D. Gomez, K.R. Prasad, G.J. Toogood, and J.P. Lodge. 2007. C-reactive protein as a predictor of prognosis following curative resection for colorectal liver metastases. British Journal of Cancer 96: 222–225.

    PubMed  CAS  Google Scholar 

  • Wu, Z.S., Q. Wu, J.H. Yang, H.Q. Wang, X.D. Ding, F. Yang, and X.C. Xu. 2008. Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. International Journal of Cancer 122: 2050–2056.

    CAS  Google Scholar 

  • Wu, W.T., C.N. Chen, C.I. Lin, J.H. Chen, and H. Lee. 2005. Lysophospholipids enhance matrix metalloproteinase-2 expression in human endothelial cells. Endocrinology 146: 3387–3400.

    PubMed  CAS  Google Scholar 

  • Xin, C., S. Ren, B. Kleuser, S. Shabahang, W. Eberhardt, H. Radeke, M. Schäfer-Korting, J. Pfeilschifter, and A. Huwiler. 2004. Sphingosine 1-phosphate cross activates the Smad signaling cascade and mimics transforming growth factor-beta-induced cell responses. Journal of Biological Chemistry 279: 35255–35262.

    PubMed  CAS  Google Scholar 

  • Yatomi, Y., F. Ruan, S. Hakomori, and Y. Igarashi. 1995. Sphingosine-1-phosphate: A platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood 86: 193–202.

    PubMed  CAS  Google Scholar 

  • Yonemura, Y., Y. Endo, T. Takino, K. Sakamoto, E. Bandou, K. Kinoshita, S. Fushida, K. Miwa, K. Sugiyama, and T. Sasaki. 2000. Membrane-type 1 matrix metalloproteinase enhances lymph node metastasis of gastric cancer. Clinical and Experimental Metastasis 18: 321–327.

    PubMed  CAS  Google Scholar 

  • Zhao, C., M.J. Fernandes, M. Turgeon, S. Tancrède, J. Di Battista, P.E. Poubelle, and S.G. Bourgoin. 2008. Specific and overlapping sphingosine-1-phosphate receptor functions in human synoviocytes: Impact of TNF-alpha. Journal of Lipid Research 49: 2323–2337.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Duksung Women’s University Research Grant 2011.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aree Moon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ham, M., Moon, A. Inflammatory and microenvironmental factors involved in breast cancer progression. Arch. Pharm. Res. 36, 1419–1431 (2013). https://doi.org/10.1007/s12272-013-0271-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-013-0271-7

Keywords

Navigation