Induction of autophagy counteracts the anticancer effect of cisplatin in human esophageal cancer cells with acquired drug resistance

Cancer Letters

Volumn 355, Issue 1, 2014, Pages 34-45

  Yu, Le ^a   Gu, Chunping ^a   Zhong, Desheng ^a   Shi, Lili ^a   Kong, Yi ^a   Zhou, Zhitao ^a   Liu, Shuwen ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Acquired resistance; Autophagy; Cisplatin; ERK; Esophageal cancer; MTORC1

Indexed keywords

AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 7; CHLOROQUINE; CISPLATIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ATG5 PROTEIN, HUMAN; ATG7 PROTEIN, HUMAN; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MICROTUBULE ASSOCIATED PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN KINASE INHIBITOR; TARGET OF RAPAMYCIN KINASE; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER INHIBITION; CANCER RESISTANCE; CELL AGING; CONTROLLED STUDY; CYTOSTASIS; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG POTENTIATION; DRUG TREATMENT FAILURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; ESOPHAGEAL CANCER CELL LINE; ESOPHAGUS CANCER; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MONOTHERAPY; MOUSE; NONHUMAN; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; ENZYME ACTIVATION; ESOPHAGEAL NEOPLASMS; GENETIC TRANSFECTION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL AGING; CELL LINE, TUMOR; CHLOROQUINE; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; ESOPHAGEAL NEOPLASMS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; MICE, INBRED BALB C; MICE, NUDE; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSFECTION; TUMOR BURDEN; UBIQUITIN-ACTIVATING ENZYMES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84907966806     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.09.020     Document Type: Article

References (40)

1. Herszenyi L., Tulassay Z. Epidemiology of gastrointestinal and liver tumors. Eur. Rev. Med. Pharmacol. Sci 2010, 14:249-258.
2. Zhang Y. Epidemiology of esophageal cancer. World J. Gastroenterol 2013, 19:5598-5606.
3. D'Journo X.B., Thomas P.A. Current management of esophageal cancer. J. Thorac. Dis 2014, 6:S253-S264.
4. Toshimitsu H., Hashimoto K., Tangoku A., Iizuka N., Yamamoto K., Kawauchi S., et al. Molecular signature linked to acquired resistance to cisplatin in esophageal cancer cells. Cancer Lett 2004, 211:69-78.
5. Wu W.K., Coffelt S.B., Cho C.H., Wang X.J., Lee C.W., Chan F.K., et al. The autophagic paradox in cancer therapy. Oncogene 2012, 31:939-953.
6. Del Bello B., Toscano M., Moretti D., Maellaro E. Cisplatin-induced apoptosis inhibits autophagy, which acts as a pro-survival mechanism in human melanoma cells. PLoS ONE 2013, 8:e57236.
7. Sirichanchuen B., Pengsuparp T., Chanvorachote P. Long-term cisplatin exposure impairs autophagy and causes cisplatin resistance in human lung cancer cells. Mol. Cell. Biochem 2012, 364:11-18.
8. Bao L.J., Jaramillo M.C., Zhang Z.B., Zheng Y.X., Yao M., Zhang D.D., et al. Nrf2 induces cisplatin resistance through activation of autophagy in ovarian carcinoma. Int. J. Clin. Exp. Pathol 2014, 7:1502-1513.
9. Wang J., Wu G.S. Role of autophagy in cisplatin resistance in ovarian cancer cells. J. Biol. Chem 2014, 289:17163-17173.
10. Pennati M., Lopergolo A., Profumo V., De Cesare M., Sbarra S., Valdagni R., et al. miR-205 impairs the autophagic flux and enhances cisplatin cytotoxicity in castration-resistant prostate cancer cells. Biochem. Pharmacol 2014, 87:579-597.
11. Kaminskyy V.O., Piskunova T., Zborovskaya I.B., Tchevkina E.M., Zhivotovsky B. Suppression of basal autophagy reduces lung cancer cell proliferation and enhances caspase-dependent and -independent apoptosis by stimulating ROS formation. Autophagy 2012, 8:1032-1044.
12. Zhu L., Du H., Shi M., Chen Z., Hang J. ATG7 deficiency promote apoptotic death induced by cisplatin in human esophageal squamous cell carcinoma cells. Bull. Cancer 2013, 100:15-21.
13. Liu D., Yang Y., Liu Q., Wang J. Inhibition of autophagy by 3-MA potentiates cisplatin-induced apoptosis in esophageal squamous cell carcinoma. Med. Oncol 2011, 28:105-111.
14. O'Donovan T.R., O'Sullivan G.C., McKenna S.L. Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 2011, 7:509-524.
15. Wen J., Zheng B., Hu Y., Zhang X., Yang H., Luo K.J., et al. Establishment and biological analysis of the EC109/CDDP multidrug-resistant esophageal squamous cell carcinoma cell line. Oncol. Rep 2009, 22:65-71.
16. Brozovic A., Osmak M. Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett 2007, 251:1-16.
17. Klionsky D.J., Abdalla F.C., Abeliovich H., Abraham R.T., Acevedo-Arozena A., Adeli K., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
18. Maycotte P., Aryal S., Cummings C.T., Thorburn J., Morgan M.J., Thorburn A. Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy. Autophagy 2012, 8:200-212.
19. Begun J., Xavier R.J. Autophagy at the crossroads of metabolism and cellular defense. Curr. Opin. Gastroenterol 2013, 29:588-596.
20. Wang D., Lippard S.J. Cellular processing of platinum anticancer drugs. Nat. Rev. Drug Discov 2005, 4:307-320.
21. Wang X., Martindale J.L., Holbrook N.J. Requirement for ERK activation in cisplatin-induced apoptosis. J. Biol. Chem 2000, 275:39435-39443.
22. St Germain C., Nikne jad N., Ma L., Garbuio K., Hai T., Dimitroulakos J. Cisplatin induces cytotoxicity through the mitogen-activated protein kinase pathways and activating transcription factor 3. Neoplasia 2010, 12:527-538.
23. Guegan J.P., Ezan F., Theret N., Langouet S., Baffet G. MAPK signaling in cisplatin-induced death: predominant role of ERK1 over ERK2 in human hepatocellular carcinoma cells. Carcinogenesis 2013, 34:38-47.
24. Hayakawa J., Depatie C., Ohmichi M., Mercola D. The activation of c-Jun NH2-terminal kinase (JNK) by DNA-damaging agents serves to promote drug resistance via activating transcription factor 2 (ATF2)-dependent enhanced DNA repair. J. Biol. Chem 2003, 278:20582-20592.
25. Germani A., Matrone A., Grossi V., Peserico A., Sanese P., Liuzzi M., et al. Targeted therapy against chemoresistant colorectal cancers: inhibition of p38α modulates the effect of cisplatin in vitro and in vivo through the tumor suppressor Fox03A. Cancer Lett 2014, 344:110-118.
26. Wang J., Zhou J.Y., Wu G.S. ERK-dependent MKP-1-mediated cisplatin resistance in human ovarian cancer cells. Cancer Res 2007, 67:11933-11941.
27. Cagnol S., Chambard J.C. ERK and cell death: mechanisms of EKR-induced cell death-apoptosis, autophagy and senescence. FEBS J. 2010, 277:2-21.
28. Villedieu M., Deslandes E., Duval M., Heron J.F., Gauduchon P., Poulain L. Acquisition of chemoresistance following discontinuous exposures to cisplatin is associated in ovarian carcinoma cells with progressive alteration of FAK, ERK and p38 activation in response to treatment. Gynecol. Oncol 2006, 102:507-519.
29. Manabe T., Toshimori T., Henomatsu N., Tashiro Y. Inhibitors of vacuolar-type H(+)-ATPase suppresses proliferation of cultured cells. J. Cell. Physiol 1993, 157:445-452.
30. Hou W., Han J., Lu C., Goldstein L.A., Rabinowich H. Autophagic degradation of active caspase-8: a crosstalk mechanism between autophagy and apoptosis. Autophagy 2010, 6:891-900.
31. Nazio F., Strappazzon F., Antonioli M., Bielli P., Cianfanelli V., Bordi M., et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat. Cell Biol 2013, 15:406-416.
32. Kim K.W., Hwang M., Moretti L., Jaboin J.J., Cha Y.I., Lu B. Autophagy upregulation by inhibitors of caspase-3 and mTOR enhances radiotherapy in a mouse model of lung cancer. Autophagy 2008, 4:659-668.
33. Takeuchi H., Kondo Y., Fujiwara K., Kanzawa T., Aoki H., Mills G.B., et al. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res 2005, 65:3336-3346.
34. Hashimoto I., Koizumi K., Tatematsu M., Minami T., Cho S., Takeno N., et al. Blocking on the CXCR4/mTOR signaling pathway induces the anti-metastatic properties and autophagic cell death in peritoneal disseminated gastric cancer cells. Eur. J. Cancer 2008, 44:1022-1029.
35. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
36. Kim J., Kundu M., Viollet B., Guan K.-L. AMPK and mTOR regulates autophagy through direct phosphorylation of ULK1. Nat. Cell Biol 2011, 13:132-141.
37. Feng Z., Zhang H., Levine A.J., Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:8204-8209.
38. Yu L., Chen M., Li Z., Wen J., Fu J., Guo D., et al. Celecoxib antagonizes the cytotoxicity of cisplatin in human esophageal squamous cell carcinoma cells by reducing intracellular cisplatin accumulation. Mol. Pharmacol 2011, 79:608-617.
39. Maes H., Kuchnio A., Peric A., Moens S., Nys K., De Bock K., et al. Tumor vessel normalization by chloroqine independent of autophagy. Cancer Cell 2014, 26:190-206.
40. Kimura T., Takabatake Y., Takahashi A., Isaka Y. Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res 2013, 73:3-7.