Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains

Molecular and Cellular Biology

Volumn 29, Issue 10, 2009, Pages 2570-2581

  Bellot, Grégory ^a   Garcia Medina, Raquel ^a   Gounon, Pierre ^a,b   Chiche, Johanna ^a   Roux, Danièle ^a   Pouysségur, Jacques ^a   Mazure, Nathalie M ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b Universite Co te d'Azur Parc Valrose   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; BH3 PROTEIN; BNIP3L PROTEIN; HYPOXIA INDUCIBLE FACTOR; PROTEIN BCL 2; PROTEIN BNIP3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BAX PROTEIN (53 86); BAX PROTEIN (53-86); BECN1 PROTEIN, HUMAN; BNIP3 PROTEIN, HUMAN; BNIP3L PROTEIN, HUMAN; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MEMBRANE PROTEIN; ONCOPROTEIN; PEPTIDE FRAGMENT; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; AUTOPHAGY; CELL ACTIVATION; CELL DEATH; CELL HYPOXIA; CELL SURVIVAL; CONTROLLED STUDY; GENE DISRUPTION; GENE INDUCTION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOLOGY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE, TUMOR; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; TUMOR SUPPRESSOR PROTEINS;

EID: 66349121718     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00166-09     Document Type: Article

References (41)

1. Adams, J. M., and S. Cory. 2007. Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr. Opin. Immunol. 19:488-496.
2. Berra, E., E. Benizri, A. Ginouves, V. Volmat, D. Roux, and J. Pouyssegur. 2003. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J. 22:4082-4090.
3. Biederbick, A., H. F. Kern, and H. P. Elsasser. 1995. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur. J. Cell Biol. 66:3-14.
4. Boyd, J. M., S. Malstrom, T. Subramanian, L. K. Venkatesh, U. Schaeper, B. Elangovan, C. D'Sa-Eipper, and G. Chinnadurai. 1994. Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341-351.
5. Brugarolas, J., K. Lei, R. L. Hurley, B. D. Manning, J. H. Reiling, E. Hafen, L. A. Witters, L. W. Ellisen, and W. G. Kaelin, Jr. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18:2893-2904.
6. Certo, M., V. Del Gaizo Moore, M. Nishino, G. Wei, S. Korsmeyer, S. A. Armstrong, and A. Letai. 2006. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9:351-365.
7. Chen, G., J. Cizeau, C. Vande Velde, J. H. Park, G. Bozek, J. Bolton, L. Shi, D. Dubik, and A. Greenberg. 1999. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J. Biol. Chem. 274:7-10.
8. Dayan, F., D. Roux, M. C. Brahimi-Horn, J. Pouyssegur, and N. M. Mazure. 2006. The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1alpha. Cancer Res. 66:3688-3698.
9. Debnath, J., E. H. Baehrecke, and G. Kroemer. 2005. Does autophagy contribute to cell death? Autophagy 1:66-74.
10. de Bruijn, W. C. 1973. Glycogen, its chemistry and morphologic appearance in the electron microscope. I. A modified OsO 4 fixative which selectively contrasts glycogen. J. Ultrastruct. Res. 42:29-50.
11. Goldsmith, K. C., X. Liu, V. Dam, B. T. Morgan, M. Shabbout, A. Cnaan, A. Letai, S. J. Korsmeyer, and M. D. Hogarty. 2006. BH3 peptidomimetics potently activate apoptosis and demonstrate single agent efficacy in neuroblastoma. Oncogene 25:4525-4533.
12. Guo, K., G. Searfoss, D. Krolikowski, M. Pagnoni, C. Franks, K. Clark, K. T. Yu, M. Jaye, and Y. Ivashchenko. 2001. Hypoxia induces the expression of the pro-apoptotic gene BNIP3. Cell Death Differ. 8:367-376.
13. Kondo, Y., T. Kanzawa, R. Sawaya, and S. Kondo. 2005. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 5:726-734.
14. Lee, H., and S. G. Paik. 2006. Regulation of BNIP3 in normal and cancer cells. Mol. Cells 21:1-6.
15. Levine, B., S. Sinha, and G. Kroemer. 2008. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4:600-606.
16. Li, Y., Y. Wang, E. Kim, P. Beemiller, C. Y. Wang, J. Swanson, M. You, and K. L. Guan. 2007. Bnip3 mediates the hypoxia-induced inhibition on mammalian target of rapamycin by interacting with Rheb. J. Biol. Chem. 282:35803-35813.
17. Liang, X. H., S. Jackson, M. Seaman, K. Brown, B. Kempkes, H. Hibshoosh, and B. Levine. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676.
18. Maiuri, M. C., G. Le Toumelin, A. Criollo, J. C. Rain, F. Gautier, P. Juin, E. Tasdemir, G. Pierron, K. Troulinaki, N. Tavernarakis, J. A. Hickman, O. Geneste, and G. Kroemer. 2007. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 26:2527-2539.
19. Mathew, R., V. Karantza-Wadsworth, and E. White. 2007. Role of autophagy in cancer. Nat. Rev. Cancer 7:961-967.
20. Mizushima, N., and T. Yoshimori. 2007. How to interpret LC3 immunoblotting. Autophagy 3:542-545.
21. Munafo, D. B., and M. I. Colombo. 2001. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J. Cell Sci. 114:3619-3629.
22. Murai, M., M. Toyota, H. Suzuki, A. Satoh, Y. Sasaki, K. Akino, M. Ueno, F. Takahashi, M. Kusano, H. Mita, K. Yanagihara, T. Endo, Y. Hinoda, T. Tokino, and K. Imai. 2005. Aberrant methylation and silencing of the BNIP3 gene in colorectal and gastric cancer. Clin. Cancer Res. 11:1021-1027.
23. Oberstein, A., P. D. Jeffrey, and Y. Shi. 2007. Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J. Biol. Chem. 282:13123-13132.
24. Papandreou, I., C. Krishna, F. Kaper, D. Cai, A. J. Giaccia, and N. C. Denko. 2005. Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment. Cancer Res. 65:3171-3178.
25. Pattingre, S., A. Tassa, X. Qu, R. Garuti, X. H. Liang, N. Mizushima, M. Packer, M. D. Schneider, and B. Levine. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939.
26. Pouyssegur, J., F. Dayan, and N. M. Mazure. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437-443.
27. Ray, R., G. Chen, C. Vande Velde, J. Cizeau, J. H. Park, J. C. Reed, R. D. Gietz, and A. H. Greenberg. 2000. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J. Biol. Chem. 275:1439-1448.
28. Rual, J. F., K. Venkatesan, T. Hao, T. Hirozane-Kishikawa, A. Dricot, N. Li, G. F. Berriz, F. D. Gibbons, M. Dreze, N. Ayivi-Guedehoussou, N. Klitgord, C. Simon, M. Boxem, S. Milstein, J. Rosenberg, D. S. Goldberg, L. V. Zhang, S. L. Wong, G. Franklin, S. Li, J. S. Albala, J. Lim, C. Fraughton, E. Llamosas, S. Cevik, C. Bex, P. Lamesch, R. S. Sikorski, J. Vandenhaute, H. Y. Zoghbi, A. Smolyar, S. Bosak, R. Sequerra, L. Doucette-Stamm, M. E. Cusick, D. E. Hill, F. P. Roth, and M. Vidal. 2005. Towards a proteome-scale map of the human protein-protein interaction network. Nature 437:1173-1178.
29. Ryan, H. E., M. Poloni, W. McNulty, D. Elson, M. Gassmann, J. M. Arbeit, and R. S. Johnson. 2000. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res. 60:4010-4015.
30. Sandoval, H., P. Thiagarajan, S. K. Dasgupta, A. Schumacher, J. T. Prchal, M. Chen, and J. Wang. 2008. Essential role for Nix in autophagic maturation of erythroid cells. Nature 454:232-235.
31. Sarkar, S., E. O. Perlstein, S. Imarisio, S. Pineau, A. Cordenier, R. L. Maglathlin, J. A. Webster, T. A. Lewis, C. J. O'Kane, S. L. Schreiber, and D. C. Rubinsztein. 2007. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat. Chem. Biol. 3:331-338.
32. Schofield, C. J., and P. J. Ratcliffe. 2004. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:343-354.
33. Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer. 3:721-732.
34. Shintani, T., and D. J. Klionsky. 2004. Autophagy in health and disease: a double-edged sword. Science 306:990-995.
35. Shintani, T., and D. J. Klionsky. 2004. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J. Biol. Chem. 279:29889-29894.
36. Tanida, I., T. Ueno, and E. Kominami. 2004. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36:2503-2518.
37. Tracy, K., B. C. Dibling, B. T. Spike, J. R. Knabb, P. Schumacker, and K. F. Macleod. 2007. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol. Cell. Biol. 17:6229-6242.
38. van de Wetering, M., I. Oving, V. Muncan, M. T. Pon Fong, H. Brantjes, D. van Leenen, F. C. Holstege, T. R. Brummelkamp, R. Agami, and H. Clevers. 2003. Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector. EMBO Rep. 4:609-615.
39. Webster, K. A., R. M. Graham, and N. H. Bishopric. 2005. BNip3 and signal-specific programmed death in the heart. J. Mol. Cell Cardiol. 38:35-45.
40. Willis, S. N., and J. M. Adams. 2005. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17:617-625.
41. Zhang, H., M. Bosch-Marce, L. A. Shimoda, Y. S. Tan, J. H. Baek, J. B. Wesley, F. J. Gonzalez, and G. L. Semenza. 2008. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283:10892-10903.