Abstract
Anaplastic thyroid cancer is one of the most aggressive forms of malignancies which grow very rapidly. Several conventional methods have been applied for the treatment of anaplastic thyroid cancer, but most of them were not successful in complete recovery of the patients. Therefore, a combination of two or more conventional modalities is being applied nowadays for the treatment of this type of cancer. In this present study, the combination of photodynamic therapy (PDT) and chemotherapy has been studied in anaplastic thyroid cancer. Human anaplastic thyroid cancer cells FRO were treated with a chemotherapy drug, carboplatin (cis-diammine-1,1-cyclobutanedicarboxyl-ateplatinum II (CBDCA)), and radachlorin-mediated PDT individually and in combination. Several parameters like cytotoxicity assay by MTT, apoptosis study by annexin V and propidium iodide, cell cycle analysis by flow cytometry, confocal microscopic study, and Western blot analysis for different apoptosis-related proteins like Bax, cytochrome c, caspases 3, 9, 8, and 12, etc. were studied to check the efficacy of the combination treatment as well as to find out the mechanism of this enhanced efficacy. Results showed that both PDT and CBDCA can induce apoptosis in FRO cells. However, a synergistic efficacy was observed when the cells were treated with CBDCA and PDT in combination. Changes in mitochondrial membrane potential and an increase in reactive oxygen species generation were observed in combination treatments. The enhanced expression of different apoptotic pathway-related proteins like Bax, cytochrome c, caspase 3, caspase 8, caspase 12, etc. also confirmed the higher efficacy of combination treatment. Therefore, with this combination treatment, not only a higher efficacy can be achieved but also the effective dose of the chemotherapy drug can be reduced, and hence, the adverse side effects of the chemotherapy drugs can also be controlled.
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References
Nagaiah G, Hossain A, Mooney CJ, Parmentier J, Remick SC (2011) Anaplastic thyroid cancer: a review of epidemiology, pathogenesis, and treatment. J oncol 2011:542358. doi:10.1155/2011/542358
Are C, Shaha A (2006) Anaplastic thyroid carcinoma: biology, pathogenesis, prognostic factors, and treatment approaches. Ann Surg Oncol 13(4):453–464. doi:10.1245/aso.2006.05.042
Ain KB (1998) Anaplastic thyroid carcinoma: behavior, biology, and therapeutic approaches. Thyroid off j Am Thyroid Assoc 8(8):715–726
Nagaiah G, Hossain A, Mooney CJ, Parmentier J, Remick SC (2011) Anaplastic thyroid cancer: a review of epidemiology, pathogenesis, and treatment. J oncol. doi:10.1155/2011/542358
Pasieka JL (2003) Anaplastic thyroid cancer. Curr opin oncol 15(1):78–83
Shaha AR, Ferlito A, Rinaldo A (2001) Distant metastases from thyroid and parathyroid cancer. ORL j oto-rhino-laryngol relat spec 63(4):243–249
Dolmans DE, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat rev Cancer 3(5):380–387. doi:10.1038/nrc1071
Dolmans DEJGJ, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat rev Cancer 3(5):380–387
Wilson BC (2002) Photodynamic therapy for cancer: principles. Can j gastroenterol 16(6):393–396
Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q (1998) Photodynamic therapy. J Natl Cancer Inst 90(12):889–905
Henderson BW, Dougherty TJ (1992) How does photodynamic therapy work? Photochem photobiol 55(1):145–157
Lam M, Oleinick NL, Nieminen AL (2001) Photodynamic therapy-induced apoptosis in epidermoid carcinoma cells. Reactive oxygen species and mitochondrial inner membrane permeabilization. J biol chem 276(50):47379–47386. doi:10.1074/jbc.M107678200
Brown SB, Brown EA, Walker I (2004) The present and future role of photodynamic therapy in cancer treatment. lancet oncol 5(8):497–508. doi:10.1016/S1470-2045(04)01529-3
Hopper C (2000) Photodynamic therapy: a clinical reality in the treatment of cancer. lancet oncol 1:212–219
Huang Z (2005) A review of progress in clinical photodynamic therapy. Technol cancer res treat 4(3):283–293
Douillard S, Lhommeau I, Olivier D, Patrice T (2010) In vitro evaluation of radachlorin sensitizer for photodynamic therapy. J photochem photobiol B Biol 98(2):128–137. doi:10.1016/j.jphotobiol.2009.11.011
Bae SM, Kim YW, Lee JM, Namkoong SE, Han SJ, Kim JK, Lee CH, Chun HJ, Jin HS, Ahn WS (2004) Photodynamic effects of Radachlorin on cervical cancer cells. Cancer res treat off j Korean Cancer Assoc 36(6):389–394. doi:10.4143/crt.2004.36.6.389
Filonenko EV, Sokolov VV, Chissov VI, Lukyanets EA, Vorozhtsov GN (2008) Photodynamic therapy of early esophageal cancer. Photodiagn photodyn ther 5(3):187–190. doi:10.1016/j.pdpdt.2008.06.001
Kochneva EV, Filonenko EV, Vakulovskaya EG, Scherbakova EG, Seliverstov OV, Markichev NA, Reshetnickov AV (2010) Photosensitizer Radachlorin(R): skin cancer PDT phase II clinical trials. Photodiagn photodyn ther 7(4):258–267. doi:10.1016/j.pdpdt.2010.07.006
Kelland L (2007) The resurgence of platinum-based cancer chemotherapy. Nat rev Cancer 7(8):573–584
Decatris MP, Sundar S, O’Byrne KJ (2004) Platinum-based chemotherapy in metastatic breast cancer: current status. Cancer treat rev 30(1):53–81. doi:10.1016/s0305-7372(03)00139-7
Forastiere A, Koch W, Trotti A, Sidransky D (2001) Head and neck cancer. N Engl j med 345(26):1890–1900. doi:10.1056/NEJMra001375
Kelly K, Crowley J, Bunn PA Jr, Presant CA, Grevstad PK, Moinpour CM, Ramsey SD, Wozniak AJ, Weiss GR, Moore DF, Israel VK, Livingston RB, Gandara DR (2001) Randomized phase III trial of paclitaxel plus carboplatin versus vinorelbine plus cisplatin in the treatment of patients with advanced non-small-cell lung cancer: a Southwest Oncology Group trial. J clin oncol off j Am Soc Clin Oncol 19(13):3210–3218
du Bois A, Luck HJ, Meier W, Adams HP, Mobus V, Costa S, Bauknecht T, Richter B, Warm M, Schroder W, Olbricht S, Nitz U, Jackisch C, Emons G, Wagner U, Kuhn W, Pfisterer J (2003) A randomized clinical trial of cisplatin/paclitaxel versus carboplatin/paclitaxel as first-line treatment of ovarian cancer. J Natl Cancer Inst 95(17):1320–1329
Wheate NJ, Walker S, Craig GE, Oun R (2010) The status of platinum anticancer drugs in the clinic and in clinical trials. Dalton Trans 39(35):8113–8127. doi:10.1039/c0dt00292e
Bhuvaneswari R, Gan YY, Soo KC, Olivo M (2009) Targeting EGFR with photodynamic therapy in combination with Erbitux enhances in vivo bladder tumor response. Mol cancer 8:94. doi:10.1186/1476-4598-8-94
Bhuvaneswari R, Yuen GY, Chee SK, Olivo M (2011) Antiangiogenesis agents avastin and erbitux enhance the efficacy of photodynamic therapy in a murine bladder tumor model. Lasers surg med 43(7):651–662. doi:10.1002/lsm.21109
Compagnin C, Mognato M, Celotti L, Canti G, Palumbo G, Reddi E (2010) Cell proliferation and cell cycle alterations in oesophageal p53-mutated cancer cells treated with cisplatin in combination with photodynamic therapy. Cell prolif 43(3):262–274. doi:10.1111/j.1365-2184.2010.00673.x
Datta SN, Allman R, Loh C, Mason M, Matthews PN (1997) Effect of photodynamic therapy in combination with mitomycin C on a mitomycin-resistant bladder cancer cell line. Br j cancer 76(3):312–317
Ma LW, Moan J, Steen HB, Iani V (1995) Anti-tumour activity of photodynamic therapy in combination with mitomycin C in nude mice with human colon adenocarcinoma. Br j cancer 71(5):950–956
Ahn J-C, Biswas R, Chung P-S (2012) Combination with genistein enhances the efficacy of photodynamic therapy against human anaplastic thyroid cancer cells. Lasers surg med 44(10):840–849. doi:10.1002/lsm.22095
Skirnisdottir I, Lindborg K, Sorbe B (2007) Adjuvant chemotherapy with carboplatin and taxane compared with single drug carboplatin in early stage epithelial ovarian carcinoma. Oncol rep 18(5):1249–1256
Gervais R, Robinet G, Clement-Duchene C, Denis F, Kouri CE, Martin P, Chouaki N, Bourayou N, Morere JF (2013) Pemetrexed and carboplatin, an active option in first-line treatment of elderly patients with advanced non-small cell lung cancer (NSCLC): a phase II trial. Lung Cancer. doi:10.1016/j.lungcan.2013.01.008
Fury MG, Sherman E, Ho A, Katabi N, Sima C, Kelly KW, Nwankwo O, Haque S, Pfister DG (2012) A phase I study of temsirolimus plus carboplatin plus paclitaxel for patients with recurrent or metastatic (R/M) head and neck squamous cell cancer (HNSCC). Cancer chemother pharmacol 70(1):121–128. doi:10.1007/s00280-012-1894-y
Rizvi I, Celli JP, Evans CL, Abu-Yousif AO, Muzikansky A, Pogue BW, Finkelstein D, Hasan T (2010) Synergistic enhancement of carboplatin efficacy with photodynamic therapy in a three-dimensional model for micrometastatic ovarian cancer. Cancer res 70(22):9319–9328. doi:10.1158/0008-5472.CAN-10-1783
Chou TC (2010) Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer res 70(2):440–446. doi:10.1158/0008-5472.CAN-09-1947
Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol rev 58(3):621–681. doi:10.1124/pr.58.3.10
Pozarowski P, Darzynkiewicz Z (2004) Analysis of cell cycle by flow cytometry. Methods Mol Biol 281:301–311. doi:10.1385/1-59259-811-0:301
Elisei R (2012) Anaplastic thyroid cancer therapy: dream or reality? Endocrine. doi:10.1007/s12020-012-9785-x
Yu GP, Li JC, Branovan D, McCormick S, Schantz SP (2010) Thyroid cancer incidence and survival in the National Cancer Institute surveillance, epidemiology, and end results race/ethnicity groups. Thyroid off j Am Thyroid Assoc 20(5):465–473. doi:10.1089/thy.2008.0281
Rajeswaran A, Trojan A, Burnand B, Giannelli M (2008) Efficacy and side effects of cisplatin- and carboplatin-based doublet chemotherapeutic regimens versus non-platinum-based doublet chemotherapeutic regimens as first line treatment of metastatic non-small cell lung carcinoma: a systematic review of randomized controlled trials. Lung Cancer 59(1):1–11. doi:10.1016/j.lungcan.2007.07.012
Ofner JG, Schlogl H, Kostron H (1996) Unusual adverse reaction in a patient sensitized with Photosan 3. J photochem photobiol B Biol 36(2):183–184
Chen H-H, Chen T-W, Lin H (2010) Pravastatin attenuates carboplatin-induced nephrotoxicity in rodents via peroxisome proliferator-activated receptor α-regulated heme oxygenase-1. Mol Pharmacol 78(1):36–45. doi:10.1124/mol.109.061101
Sharma A, Bhat MK (2011) Enhancement of carboplatin- and quercetin-induced cell death by roscovitine is Akt dependent and p53 independent in hepatoma cells. Integr cancer ther 10(4):NP4–NP14. doi:10.1177/1534735411423922
Bevis KS, McNally LR, Sellers JC, Della Manna D, Londono Joshi A, Amm H, Straughn JM Jr, Buchsbaum DJ (2011) Anti-tumor activity of an anti-DR5 monoclonal antibody, TRA-8, in combination with taxane/platinum-based chemotherapy in an ovarian cancer model. Gynecol oncol 121(1):193–199. doi:10.1016/j.ygyno.2010.11.046
Panzarini E, Inguscio V, Dini L (2011) Timing the multiple cell death pathways initiated by Rose Bengal acetate photodynamic therapy. Cell death dis 2:e169. doi:10.1038/cddis.2011.51
Granville DJ, Carthy CM, Jiang H, Shore GC, McManus BM, Hunt DWC (1998) Rapid cytochrome c release, activation of caspases 3, 6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated with photodynamic therapy. FEBS Lett 437(1–2):5–10. doi:10.1016/S0014-5793(98)01193-4
Singh S, Chhipa RR, Vijayakumar MV, Bhat MK (2006) DNA damaging drugs-induced down-regulation of Bcl-2 is essential for induction of apoptosis in high-risk HPV-positive HEp-2 and KB cells. Cancer lett 236(2):213–221. doi:10.1016/j.canlet.2005.05.024
Lee CS, Kim YJ, Jang ER, Myung SC, Kim W (2010) Akt inhibitor enhances apoptotic effect of carboplatin on human epithelial ovarian carcinoma cell lines. Eur j pharmacol 632(1–3):7–13. doi:10.1016/j.ejphar.2010.01.004
Robertson CA, Evans DH, Abrahamse H (2009) Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J Photochem Photobiol B Biol 96(1):1–8. doi:10.1016/j.jphotobiol.2009.04.001
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This research was supported by Leading Foreign Research Institute Recruitment Program through the National Research Foundation of Korea funded by the Ministry of Education, Science and Technology (2012K1A4A3053142).
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Biswas, R., Chung, PS., Moon, J.H. et al. Carboplatin synergistically triggers the efficacy of photodynamic therapy via caspase 3-, 8-, and 12-dependent pathways in human anaplastic thyroid cancer cells. Lasers Med Sci 29, 995–1007 (2014). https://doi.org/10.1007/s10103-013-1452-9
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DOI: https://doi.org/10.1007/s10103-013-1452-9