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Article

BNIP3 Is an RB/E2F Target Gene Required for Hypoxia-Induced Autophagy

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Pages 6229-6242 | Received 29 Nov 2006, Accepted 10 Jun 2007, Published online: 27 Mar 2023

REFERENCES

  • Bindra, R. S., S. L. Gibson, A. Meng, U. Westermark, M. Jasin, A. J. Pierce, R. G. Bristow, M. K. Classon, and P. M. Glazer. 2005. Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res. 65:11597–11604.
  • Bindra, R. S., and P. M. Glazer. 2007. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene 26:2048–2057.
  • Bruick, R. K. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. USA 97:9082–9087.
  • Budde, A., N. Schneiderhan-Marra, G. Petersen, and B. Brune. 2005. Retinoblastoma susceptibility product pRB activates hypoxia-inducible factor (HIF-1). Oncogene 24:1802–1808.
  • Chau, B. N., and J. Y. J. Wang. 2003. Coordinated regulation of life and death by RB. Nat. Rev. Cancer 3:130–138.
  • Degenhardt, K., G. Chen, T. Lindsten, and E. White. 2002. BAX and BAK mediate p53-independent suppression of tumorigenesis. Cancer Cells 2:193–203.
  • Degenhardt, K., R. Mathew, B. Beaudoin, K. Bray, K. L. Anderson, G. Chen, C. Mukherjee, Y. Shi, C. Gelinas, Y. Fan, D. A. Nelson, S. Jin, and E. White. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation and tumorigenesis. Cancer Cells 10:51–64.
  • DeGregori, J. 2002. The genetics of the E2F family of transcription factors. Biochim. Biophys. Acta 1602:131–150.
  • DeGregori, J., G. Leone, A. Miron, L. Jakoi, and J. R. Nevins. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94:7245–7250.
  • Denchi, E. L., and K. Helin. 2005. E2F1 is crucial for E2F-dependent apoptosis. EMBO Rep. 6:661–668.
  • Ferguson, K. L., J. L. Vanderluit, J. M. Hebert, W. C. McIntosh, E. Tibbo, J. G. MacLaurin, D. S. Park, V. A. Wallace, M. Vooijs, S. K. McConnell, and R. S. Slack. 2002. Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J. 21:3337–3346.
  • Gozuacik, D., and A. Kimchi. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891–2906.
  • Green, D. R., and G. I. Evan. 2002. A matter of life and death. Cancer Cells 1:19–30.
  • 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 Diff. 8:367–376.
  • Hamacher-Brady, A., N. R. Brady, S. E. Logue, M. R. Sayen, M. Jinno, L. A. Kirschenbaum, R. A. Gottlieb, and A. B. Gustafsson. 2006. Response to myocardial ischemia/reperfusion injury involves BNip3 and autophagy. Cell Death Diff. 13:1–12.
  • Harris, A. L. 2002. Hypoxia—a key regulatory factor in tumour growth. Nat. Rev. Cancer 2:38–47.
  • Hershko, T., and D. Ginsberg. 2004. Up-regulation of Bcl-2 homology 3 (BH3)-only proteins by E2F-1 mediates apoptosis. J. Biol. Chem. 279:8627–8634.
  • Ho, A. T., Q. H. Li, R. Hakem, T. W. Mak, and E. Zacksenhaus. 2004. Coupling of caspase-9 to Apaf1 in response to loss of pRb or cytotoxic drugs is cell-type specific. EMBO J. 23:460–472.
  • Irwin, M., M. C. Marin, A. C. Phillips, R. S. Seelam, D. I. Smith, W. Liu, E. R. Flores, K. Y. Tsai, T. Jacks, K. H. Vousden, and W. G. Kaelin. 2000. Role for the p53 homologue p73 in E2F-1 induced apoptosis. Nature 407:645–648.
  • Jin, S. 2006. Autophagy, mitochondrial quality control and oncogenesis. Autophagy 2:80–84.
  • Jin, S., and E. White. 2007. Role of autophagy in cancer. Autophagy 3:28–31.
  • Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720–5728.
  • Kim, J. Y., H. J. Ahn, J. H. Ryu, K. Suk, and J. H. Park. 2004. BH3-only protein Noxa is a mediator of hypoxic cell death induced by hypoxia inducible factor 1a. J. Exp. Med. 199:113–123.
  • 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.
  • Kothari, S., J. Cizeau, E. McMillan-Ward, S. J. Israels, M. Bailes, K. Ens, L. A. Kirshenbaum, and S. B. Gibson. 2003. BNIP3 plays a role in hypoxic cell death in human epithelial cells that is inhibited by growth factors EGF and IGF. Oncogene 22:4734–4744.
  • Kubasiak, L. A., O. M. Hernandez, N. H. Bishopric, and K. A. Webster. 2002. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc. Natl. Acad. Sci. USA 99:12825–12830.
  • Leone, G., R. Sears, E. Huang, R. Rempel, F. Nuckolls, C. Park, P. Giangrande, L. Wu, H. I. Saavedra, S. J. Field, M. A. Thompson, H. Yang, Y. Fujiwara, M. E. Greenberg, S. H. Orkin, C. Smith, and J. R. Nevins. 2001. Myc requires distinct E2F activities to induce S phase and apoptosis. Mol. Cell 8:105–113.
  • Lin, W., F. Lin, and J. R. Nevins. 2001. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 15:1833–1844.
  • Lum, J. J., D. E. Bauer, M. Kong, M. H. Harris, C. Y. Li, T. Lindsten, and C. B. Thompson. 2005. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237–249.
  • Lum, J. J., R. J. DeBerardins, and C. B. Thompson. 2005. Autophagy in metazoans: cell survival in the land of plenty. Nat. Rev. Mol. Biol. 6:439–448.
  • Macleod, K., Y. Hu, and T. Jacks. 1996. Loss of Rb activates both p53-dependent and -independent cell death pathways in the developing mouse nervous system. EMBO J. 15:6178–6188.
  • Macleod, K., and M. Plumb. 1991. Derepression of mouse β-globin gene transcription during erythroid differentiation. Mol. Cell. Biol. 11:4324–4332.
  • MacPherson, D., J. Sage, D. Crowley, A. Trumpp, R. T. Bronson, and T. Jacks. 2003. Conditional mutation of Rb causes cell cycle defects without apoptosis in the central nervous system. Mol. Cell. Biol. 23:1044–1053.
  • Manka, D., Z. Spicer, and D. E. Millhorn. 2005. Bcl-2/adenovirus E1B 19 kDa interacting protein-3 knockdown enables growth of breast cancer metastases in the lung, liver and bone. Cancer Res. 65:11689–11693.
  • Moroni, M. C., E. S. Hickman, E. L. Denchi, G. Caprara, E. Colli, F. Cecconi, H. Muller, and K. Heliin. 2001. Apaf-1 is a transcriptional target for E2F and p53. Nat. Cell Biol. 3:552–558.
  • 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.
  • Nahle, Z., J. Polakoff, R. V. Davuluri, M. E. McCurrach, M. D. Jacobson, M. Narita, M. Q. Zhang, Y. Lazebnik, D. Bar-Sagi, and S. W. Lowe. 2002. Direct coupling of the cell cycle and cell death machinery by E2F. Nat. Cell Biol. 4:859–864.
  • Okami, J., D. M. Simeone, and C. D. Logsdon. 2004. Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer. Cancer Res. 64:5338–5346.
  • 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.
  • Pattingre, S., A. Tassa, X. Qu, R. Garuti, X. H. Linag, N. Mizushima, M. Packer, M. D. Schneider, and B. Levine. 2005. Bcl-2 anti-apoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927–939.
  • Pediconi, N., A. Ianari, A. Costanzo, L. Belloni, R. Gallo, L. Cimino, A. Porcellini, I. Screpanti, C. Balsano, E. Alesse, A. Gulino, and M. Levrero. 2003. Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat. Cell Biol. 5:552–558.
  • Polager, S., Y. Kalma, E. Berkovich, and D. Ginsberg. 2002. E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene 21:437–446.
  • Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195.
  • Semenza, G. L. 2003. Targeting HIF for cancer therapy. Nat. Rev. Cancer 3:721–732.
  • Sowter, H. M., M. Ferguson, C. Pym, P. Watson, S. B. Fox, C. Han, and A. L. Harris. 2003. Expression of the cell death genes BNip3 and Nix in ductal carcinoma in situ of the breast; correlation of BNip3 levels with necrosis and grade. J. Pathol. 201:573–580.
  • Spike, B. T., A. Dirlam, B. C. Dibling, J. Marvin, B. O. Williams, T. Jacks, and K. F. Macleod. 2004. The Rb tumor suppressor is required for stress erythropoiesis. EMBO J. 23:4319–4329.
  • Stevens, C., L. Smith, and N. B. La Thangue. 2003. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 5:401–409.
  • Takahashi, Y., J. B. Rayman, and B. D. Dynlacht. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:804–816.
  • Trimarchi, J., and J. A. Lees. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11–20.
  • Vakkila, J., and M. T. Lotze. 2004. Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 4:641–648.
  • Vande Velde, C., J. Cizeau, D. Dubik, J. Alimonti, T. Brown, S. Israels, R. Hakem, and A. H. Greenberg. 2000. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell. Biol. 20:5454–5468.
  • Wu, L., A. de Bruin, H. I. Saavedra, M. Starovic, A. Trimboli, Y. Yang, J. Opavska, P. Wilson, J. C. Thompson, M. C. Ostrowski, T. J. Rosol, L. A. Woollett, M. Weinstein, J. C. Cross, M. L. Robinson, and G. Leone. 2003. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942–947.
  • Yoshida, H., K. Kawane, M. Koike, Y. Mori, Y. Uchiyama, and S. Nagata. 2005. Phosphotidlyserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437:754–758.
  • Zhang, H. M., P. Cheung, B. Yanagawa, B. M. McManus, and D. C. Yang. 2003. BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 8:229–236.
  • Zong, W., D. Ditsworth, D. E. Bauer, Z. Q. Wang, and C. B. Thompson. 2004. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18:1272–1282.
  • Zong, W., and C. B. Thompson. 2006. Necrotic death as a cell fate. Genes Dev. 20:1–15.

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