Hypoxia-induced autophagy reduces radiosensitivity by the HIF-1α/miR-210/Bcl-2 pathway in colon cancer cells

International Journal of Oncology

Volumn 46, Issue 2, 2015, Pages 750-756

  Sun, Yong ^a,b   Xing, Xing ^a,b   Liu, Qi ^a,b   Wang, Zheng ^a,b   Xin, Yuhu ^a,b   Zhang, Ping ^a,b   Hu, Chaosu ^a,b   Liu, Yong ^a,b  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

Autophagy; Colon cancer; Hypoxia; Radiosensitivity

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA 210; PROTEIN BCL 2; SMALL INTERFERING RNA; MICRORNA; MIRN210 MICRORNA, HUMAN;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; COLORECTAL CANCER CELL LINE; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPOXIA INDUCED AUTOPHAGY; PROTEIN EXPRESSION; RADIOSENSITIVITY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; X IRRADIATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL HYPOXIA; CELL PROLIFERATION; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; RADIATION DOSE; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

APOPTOSIS; AUTOPHAGY; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICRORNAS; PROTO-ONCOGENE PROTEINS C-BCL-2; RADIATION TOLERANCE; SIGNAL TRANSDUCTION;

EID: 84918583818     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2745     Document Type: Article

References (43)

1. Avivar-Valderas A, Bobrovnikova-Marjon E, Alan Diehl J, Bardeesy N, Debnath J and Aguirre-Ghiso JA: Regulation of autophagy during ECM detachment is linked to a selective inhibition of mTORC1 by PERK. Oncogene 32: 4932-4940, 2013.
2. Liu B, Wen X and Cheng Y: Survival or death: disequilibrating the oncogenic and tumor suppressive autophagy in cancer. Cell Death Dis 4: e892, 2013.
3. Goda N and Kanai M: Hypoxia-inducible factors and their roles in energy metabolism. Int J Hematol 95: 457-463, 2012.
4. Chaachouay H, Ohneseit P, Toulany M, Kehlbach R, Multhoff G and Rodemann HP: Autophagy contributes to resistance of tumor cells to ionizing radiation. Radiother Oncol 99: 287-292, 2011.
5. He WS, Dai XF, Jin M, Liu CW and Rent JH: Hypoxia-induced autophagy confers resistance of breast cancer cells to ionizing radiation. Oncol Res 20: 251-258, 2012.
6. Peitzsch C, Perrin R, Hill RP, Dubrovska A and Kurth I: Hypoxia as a biomarker for radioresistant cancer stem cells. Int J Radiat Biol 90: 636-652, 2014.
7. Lin SC, Liao WL, Lee JC and Tsai SJ: Hypoxia-regulated gene network in drug resistance and cancer progression. Exp Biol Med (Maywood) 239: 779-792, 2014.
8. Semenza GL: Hypoxia and cancer. Cancer Metastasis Rev 26: 223-224, 2007.
9. Majmundar AJ, Wong WJ and Simon MC: Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40: 294-309, 2010.
10. Bellot G, Garcia-Medina R, Gounon P, et al: Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29: 2570-2581, 2009.
11. Zhang H, Bosch-Marce M, Shimoda LA, et al: Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283: 10892-10903, 2008.
12. Saito S and Nakashima A: The role of autophagy in extravillous trophoblast function under hypoxia (Review). Placenta 34 (Suppl): S79-S84, 2013.
13. Janga SC and Vallabhaneni S: MicroRNAs as post-transcriptional machines and their interplay with cellular networks. Adv Exp Med Biol 722: 59-74, 2011.
14. Camps C, Buffa FM, Colella S, et al: hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 14: 1340-1348, 2008.
15. Fasanaro P, D'Alessandra Y, Di Stefano V, et al: MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 283: 15878-15883, 2008.
16. Maejima Y, Kyoi S, Zhai P, et al: Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat Med 19: 1478-1488, 2013.
17. Pattingre S, Tassa A, Qu X, et al: Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939, 2005.
18. Mathew R, Karantza-Wadsworth V and White E: Role of autophagy in cancer. Nat Rev Cancer 7: 961-967, 2007.
19. Wu S, Chu Y, Yang Y, et al: Inhibition of macrophage autophagy induced by Salmonella enterica serovar typhi plasmid. Front Biosci 19: 490-503, 2014.
20. Nakatogawa H, Suzuki K, Kamada Y and Ohsumi Y: Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10: 458-467, 2009.
21. Apel A, Herr I, Schwarz H, Rodemann HP and Mayer A: Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 68: 1485-1494, 2008.
22. Sannigrahi MK, Singh V, Sharma R, Panda NK and Khullar M: Role of autophagy in head and neck cancer and therapeutic resistance. Oral Dis: June 3, 2014 (Epub ahead of print) doi: 10.1111/ odi.12254.
23. Wang J and Wu GS: Role of autophagy in cisplatin resistance in ovarian cancer cells. J Biol Chem 289: 17163-17173, 2014.
24. Klionsky DJ and Emr SD: Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721, 2000.
25. Ruan K, Song G and Ouyang G: Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 107: 1053-1062, 2009.
26. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC and Huang LE: HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23: 1949-1956, 2004.
27. Agani F and Jiang BH: Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets 13: 245-251, 2013.
28. Clara CA, Marie SK, de Almeida JR, et al: Angiogenesis and expression of PDGF-C, VEGF, CD105 and HIF-1alpha in human glioblastoma. Neuropathology 34: 343-352, 2014.
29. Liu Y, Li YM, Tian RF, et al: The expression and significance of HIF-1alpha and GLUT-3 in glioma. Brain Res 1304: 149-154, 2009.
30. Devlin C, Greco S, Martelli F and Ivan M: miR-210: More than a silent player in hypoxia. IUBMB Life 63: 94-100, 2011.
31. Chan YC, Banerjee J, Choi SY and Sen CK: miR-210: the master hypoxamir. Microcirculation 19: 215-223, 2012.
32. Grosso S, Doyen J, Parks SK, et al: MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis 4: e544, 2013.
33. Qu A, Du L, Yang Y, et al: Hypoxia-inducible MiR-210 is an independent prognostic factor and contributes to metastasis in colorectal cancer. PLoS One 9: e90952, 2014.
34. Chio CC, Lin JW, Cheng HA, et al: MicroRNA-210 targets antiapoptotic Bcl-2 expression and mediates hypoxia-induced apoptosis of neuroblastoma cells. Arch Toxicol 87: 459-468, 2013.
35. Zhou F, Yang Y and Xing D: Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 278: 403-413, 2011.
36. Kitada S, Takayama S, De Riel K, Tanaka S and Reed JC: Reversal of chemoresistance of lymphoma cells by antisensemediated reduction of bcl-2 gene expression. Antisense Res Dev 4: 71-79, 1994.
37. Kaminskyy VO and Zhivotovsky B: Free radicals in cross talk between autophagy and apoptosis. Antioxid Redox Signal 21: 86-102, 2014.
38. Ni Z, Wang B, Dai X, et al: HCC cells with high levels of Bcl-2 are resistant to ABT-737 via activation of the ROS-JNK-autophagy pathway. Free Radic Biol Med 70: 194-203, 2014.
39. Akar U, Chaves-Reyez A, Barria M, et al: Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 4: 669-679, 2008.
40. Mukhopadhyay S, Panda PK, Sinha N, Das DN and Bhutia SK: Autophagy and apoptosis: where do they meet? Apoptosis 19: 555-566, 2014.
41. Wei Y, Sinha S and Levine B: Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 4: 949-951, 2008.
42. Oberstein A, Jeffrey PD and Shi Y: Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 282: 13123-13132, 2007.
43. Maiuri MC, Criollo A, Tasdemir E, et al: BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 3: 374-376, 2007.