MicroRNA-30a sensitizes tumor cells to cis-platinum via suppressing beclin 1-mediated autophagy

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4148-4156

  Zou, Zhenyou ^a   Wu, Linping ^a   Ding, Hanying ^a   Wang, Yang ^a   Zhang, Yaqin ^a   Chen, Xuejiao ^a   Chen, Xi ^a   Zhang, Chen Yu ^a   Zhang, Qipeng ^a   Zen, Ke ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGOSOMES; AUTOPHAGY; CANCER CELL APOPTOSIS; CANCER CELLS; IN-VIVO; KEY REGULATORS; MOUSE MODELS; PROBE-BASED; QUANTITATIVE RT-PCR; TUMOR CELLS;

CELL DEATH; CHEMOTHERAPY; PLATINUM; POLYMERASE CHAIN REACTION;

TUMORS;

3 METHYLADENINE; BECLIN 1; CISPLATIN; MICRORNA; MICRORNA 30A; PACLITAXEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER TRANSPLANTATION; CHEMOSENSITIZATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LENTIVIRINAE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SCREENING; SOLID TUMOR;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CISPLATIN; DRUG RESISTANCE, NEOPLASM; HEK293 CELLS; HELA CELLS; HEP G2 CELLS; HUMANS; LENTIVIRUS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICRORNAS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASMS; RNA, NEOPLASM; TRANSDUCTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS;

LENTIVIRUS;

EID: 84863011747     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.307405     Document Type: Article

References (49)

1. Gottesman, M. M. (2002) Mechanisms of cancer drug resistance. Annu. Rev. Med. 53, 615-627
2. Khan, S. A., Thomas, H. C., Davidson, B. R., and Taylor-Robinson, S. D. (2005) Cholangiocarcinoma. Lancet 366, 1303-1314 (Pubitemid 41416587)
3. White, E., Karp, C., Strohecker, A. M., Guo, Y., and Mathew, R. (2010) Role of autophagy in suppression of inflammation and cancer. Curr. Opin. Cell Biol. 22, 212-217
4. Klionsky, D. J., and Emr, S. D. (2000) Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721 (Pubitemid 32004796)
5. O'Donovan, T. R., O'Sullivan, G. C., and McKenna, S. L. (2011) Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 7, 509-524
6. Longo, L., Platini, F., Scardino, A., Alabiso, O., Vasapollo, G., and Tessitore, L. (2008) Autophagy inhibition enhances anthocyanin-induced apoptosis in hepatocellular carcinoma. Mol. Cancer Ther. 7, 2476-2485
7. Mathew, R., Karantza-Wadsworth, V., and White, E. (2007) Role of autophagy in cancer. Nat. Rev. Cancer 7, 961-967 (Pubitemid 350165856)
8. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., and White, E. (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21, 1621-1635 (Pubitemid 47026367)
9. Sato, K., Tsuchihara, K., Fujii, S., Sugiyama, M., Goya, T., Atomi, Y., Ueno, T., Ochiai, A., and Esumi, H. (2007) Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67, 9677-9684 (Pubitemid 47621214)
10. Hou, Y. J., Dong, L. W., Tan, Y. X., Yang, G. Z., Pan, Y. F., Li, Z., Tang, L., Wang, M., Wang, Q., and Wang, H. Y. (2011) Inhibition of active autophagy induces apoptosis and increases chemosensitivity in cholangiocarcinoma. Lab. Invest. 91, 1146-1157
11. Hornstein, E., Mansfield, J. H., Yekta, S., Hu, J. K., Harfe, B. D., McManus, M. T., Baskerville, S., Bartel, D. P., and Tabin, C. J. (2005) The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 438, 671-674 (Pubitemid 41740577)
12. Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350-355
13. Bartel, D. P. (2004) MicroRNAs. Genomics, biogenesis, mechanism, and function. Cell 116, 281-297
14. Garzon, R., Calin, G. A., and Croce, C. M. (2009) MicroRNAs in Cancer. Annu. Rev. Med. 60, 167-179
15. Medina, P. P., Nolde, M., and Slack, F. J. (2010) OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 467, 86-90
16. Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs. MicroRNAs with a role in cancer. Nat. Rev. Cancer 6, 259-269
17. White, N. M., Fatoohi, E., Metias, M., Jung, K., Stephan, C., and Yousef, G. M. (2011) Metastamirs. A stepping stone towards improved cancer management. Nat. Rev. Clin. Oncol. 8, 75-84
18. Fabbri, M., Croce, C. M., and Calin, G. A. (2008) MicroRNAs. Cancer J. 14, 1-6
19. Nakatani, F., Ferracin, M., Manara, M. C., Ventura, S., Del Monaco, V., Ferrari, S., Alberghini, M., Grilli, A., Knuutila, S., Schaefer, K. L., Mattia, G., Negrini, M., Picci, P., Serra, M., and Scotlandi, K. (2011) MiR-34a predicts survival of Ewing's sarcoma patients and directly influences cell chemosensitivity and malignancy. J. Pathol. doi: 10.1002/path.3007
20. Kastl, L., Brown, I., and Schofield, A. C. (2011) MiRNA-34a is associated with docetaxel resistance in human breast cancer cells. Breast Cancer Res. Treat. doi: 10.1007/s10549-011-1424-3
21. Tao, J., Lu, Q., Wu, D., Li, P., Xu, B., Qing, W., Wang, M., Zhang, Z., and Zhang, W. (2011) MicroRNA-21 modulates cell proliferation and sensitivity to doxorubicin in bladder cancer cells. Oncol. Rep. 25, 1721-1729
22. Dong, J., Zhao, Y. P., Zhou, L., Zhang, T. P., and Chen, G. (2011) Bcl-2 up-regulation induced by miR-21 via a direct interaction is associated with apoptosis and chemoresistance in MIA PaCa-2 pancreatic cancer cells. Arch. Med. Res. 42, 8-14
23. Song, B., Wang, Y., Xi, Y., Kudo, K., Bruheim, S., Botchkina, G. I., Gavin, E., Wan, Y., Formentini, A., Kornmann, M., Fodstad, O., and Ju, J. (2009) Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 28, 4065-4074
24. Mukhopadhyay, P., Pacher, P., and Das, D. K. (2011) MicroRNA signatures of resveratrol in the ischemic heart. Ann. N.Y. Acad. Sci. 1215, 109-116
25. Zhu, H., Wu, H., Liu, X., Li, B., Chen, Y., Ren, X., Liu, C. G., and Yang, J. M. (2009) Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 5, 816-823
26. Brest, P., Lapaquette, P., Souidi, M., Lebrigand, K., Cesaro, A., Vouret- Craviari, V., Mari, B., Barbry, P., Mosnier, J. F., Hébuterne, X., Harel- Bellan, A., Mograbi, B., Darfeuille-Michaud, A., and Hofman, P. (2011) A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat. Genet. 43, 242-245
27. Xiao, J., Zhu, X., He, B., Zhang, Y., Kang, B., Wang, Z., and Ni, X. (2011) MiR-204 regulates cardiomyocyte autophagy induced by ischemia-reperfusion through LC3-II. J. Biomed. Sci. 18, 35
28. Chaney, S. G., Campbell, S. L., Temple, B., Bassett, E., Wu, Y., and Faldu, M. (2004) J. Inorg. Biochem. 98, 1551-1559
29. Hou, X. M., Zhang, X. H., Wei, K. J., Ji, C., Dou, S. X., Wang, W. C., Li, M., and Wang, P. Y. (2009) Cisplatin induces loop structures and condensation of single DNA molecules. Nucleic Acids Res. 37, 1400-1410
30. Chen, C. F., Ridzon, D. A., Broomer, A. J., Zhou, Z. H., Lee, D. H., Nguyen, J. T., Barbisin, M., Xu, N. L., Mahuvakar, V. R., Andersen, M. R., Lao, K. Q., Livak, K. J., and Guegler, K. J. (2005) Real-time quantification of micro-RNAs by stem-loop RT-PCR. Nucleic Acids Research 33, e179
31. Kota, J., Chivukula, R. R., O'Donnell, K. A., Wentzel, E. A., Montgomery, C. L., Hwang, H. W., Chang, T. C., Vivekanandan, P., Torbenson, M., Clark, K. R., Mendell, J. R., and Mendell, J. T. (2009) Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137, 1005-1017
32. Tang, R., Li, L., Zhu, D., Hou, D., Cao, T., Gu, H., Zhang, J., Chen, J., Zhang, C. Y., and Zen, K. (2011) Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res. doi: 10.1038/cr.2011.137
33. Li, L. M., Hou, D. X., Guo, Y. L., Yang, J. W., Liu, Y., Zhang, C. Y., and Zen, K. (2011) Role of microRNA-214-targeting phosphatase and tensin homolog in advanced glycation end product-induced apoptosis delay in monocytes. J. Immunol. 186, 2552-2560
34. Sun, Q., Fan, W., and Zhong, Q. (2009) Regulation of Beclin 1 in autophagy. Autophagy 5, 713-716
35. Lee, A. J., Roylance, R., Sander, J., Gorman, P., Endesfelder, D., Kschischo, M., Jones, N. P., East, P., Nicke, B., Spassieva, S., Obeid, L. M., Birkbak, N. J., Szallasi, Z., McKnight, N. C., Rowan, A. J., Speirs, V., Hanby, A. M., Downward, J., Tooze, S. A., and Swanton, C. (2011) CERT depletion predicts chemotherapy benefit and mediates cytotoxic and polyploid-specific cancer cell death through autophagy induction. J. Pathol. doi: 10.1002/path.2998
36. Li, J., Hou, N., Faried, A., Tsutsumi, S., Takeuchi, T., and Kuwano, H. (2009) Inhibition of autophagy by 3-MA enhances the effect of 5-FU-induced apoptosis in colon cancer cells. Ann. Surg. Oncol. 16, 761-771
37. Zhang, Y., Cheng, Y., Ren, X., Zhang, L., Yap, K. L., Wu, H., Patel, R., Liu, D., Qin, Z. H., Shih, I. M., and Yang, J. M. NACl modulates sensitivity of ovarian cancer cells to cisplatin by altering the HMGB1-mediated autophagic response. Oncogene doi: 10.1038/onc.2011.290
38. Amaravadi, R. K., Lippincott-Schwartz, J., Yin, X. M., Weiss, W. A., Takebe, N., Timmer, W., DiPaola, R. S., Lotze, M. T., and White, E. (2011) Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 17, 654-666
39. Livesey, K. M., Tang, D., Zeh, H. J., and Lotze, M. T. (2009) Autophagy inhibition in combination cancer treatment. Curr. Opin. Investig. Drugs 10, 1269-1279
40. Rabik, C. A., and Dolan, M. E. (2007) Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat. Rev. 33, 9-23 (Pubitemid 46137553)
41. Stronach, E. A., Alfraidi, A., Rama, N., Datler, C., Studd, J. B., Agarwal, R., Guney, T. G., Gourley, C., Hennessy, B. T., Mills, G. B., Mai, A., Brown, R., Dina, R., and Gabra, H. (2011) HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res. 71, 4412-4422
42. Miracco, C., Cosci, E., Oliveri, G., Luzi, P., Pacenti, L., Monciatti, I., Mannucci, S., De Nisi, M. C., Toscano, M., Malagnino, V., Falzarano, S. M., Pirtoli, L., and Tosi, P. (2007) Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int. J. Oncol. 30, 429-436
43. Chen, Y., Lu, Y., Lu, C., and Zhang, L. (2009) Beclin-1 expression is a predictor of clinical outcome in patients with esophageal squamous cell carcinoma and correlated to hypoxia-inducible factor (HIF)-1α expression. Pathol. Oncol. Res. 15, 487-493
44. Shen, Y., Li, D. D., Wang, L. L., Deng, R., and Zhu, X. F. (2008) Decreased expression of autophagy-related proteins in malignant epithelial ovarian cancer. Autophagy 4, 1067-1068
45. Ahn, C. H., Jeong, E. G., Lee, J. W., Kim, M. S., Kim, S. H., Kim, S. S., Yoo, N. J., and Lee, S. H. (2007) Expression of beclin-1, an autophagy-related protein, in gastric and colorectal cancers. APMIS 115, 1344-1349
46. Hoppe-Seyler, F., and Butz, K. (1993) Repression of endogenous p53 transactivation function in HeLa cervical carcinoma cells by human papillomavirus type 16 E6, human mdm-2, and mutant p53. J. Virol. 67, 3111-3117 (Pubitemid 23143679)
47. Koivusalo, R., Krausz, E., Ruotsalainen, P., Helenius, H., and Hietanen, S. (2002) Chemoradiation of cervical cancer cells. Targeting human papillomavirus E6 and p53 leads to either augmented or attenuated apoptosis depending on the platinum carrier ligand. Cancer Res. 62, 7364-7371 (Pubitemid 36025260)
48. Fan, S., Smith, M. L., Rivet, D. J., 2nd, Duba, D., Zhan, Q., Kohn, K. W., Fornace, A. J., Jr., and O'Connor, P. M. (1995) Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res. 55, 1649-1654
49. Vollmer, C. M., Ribas, A., Butterfield, L. H., Dissette, V. B., Andrews, K. J., Eilber, F. C., Montejo, L. D., Chen, A. Y., Hu, B., Glaspy, J. A., McBride, W. H., and Economou, J. S. (1999) p53 selective and nonselective replication of an E1B-deleted adenovirus in hepatocellular carcinoma. Cancer Res. 59, 4369-4374 (Pubitemid 29418756)