Mechanisms and biology of B-cell leukemia/lymphoma 2/adenovirus E1B interacting protein 3 and Nip-like protein X

Antioxidants and Redox Signaling

Volumn 14, Issue 10, 2011, Pages 1959-1969

  Zhang, Ji ^a   Ney, Paul A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; NIP LIKE PROTEIN X; PROTEIN BCL 2; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AGING; AUTOPHAGY; CANCER GROWTH; CELL DEATH; DEGENERATIVE DISEASE; DOWN REGULATION; ENDOPLASMIC RETICULUM; HEART DISEASE; HUMAN; IN VIVO STUDY; ISCHEMIA; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RETICULOCYTE; REVIEW;

ANIMALS; AUTOPHAGY; BCL-2-ASSOCIATED X PROTEIN; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTO-ONCOGENE PROTEINS; TUMOR SUPPRESSOR PROTEINS;

ADENOVIRIDAE;

EID: 79954568268     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3772     Document Type: Review

References (112)

1. Aerbajinai W, Giattina M, Lee YT, Raffeld M, and Miller JL. The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. Blood 102: 712-717, 2003. (Pubitemid 36841996)
2. Althaus J, Bernaudin M, Petit E, Toutain J, Touzani O, and Rami A. Expression of the gene encoding the pro-apoptotic BNIP3 protein and stimulation of hypoxia-inducible factor-1alpha (HIF-1alpha) protein following focal cerebral ischemia in rats. Neurochem Int 48: 687-695, 2006.
3. Aouacheria A, Brunet F, and Gouy M. Phylogenomics of life-or-death switches in multicellular animals: Bcl-2, BH3-Only, and BNip families of apoptotic regulators. Mol Biol Evol 22: 2395-2416, 2005. (Pubitemid 41662342)
4. Azad MB, Chen Y, Henson ES, Cizeau J, Millan-Ward E, Israels SJ, and Gibson SB. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 4: 195-204, 2008. (Pubitemid 351231183)
5. Band M, Joel A, Hernandez A, and Avivi A. Hypoxiainduced BNIP3 expression and mitophagy: in vivo comparison of the rat and the hypoxia-tolerant mole rat, Spalax ehrenbergi. FASEB J 23: 2327-2335, 2009.
6. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, and Mazure NM. 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.
7. Bocharov EV, Pustovalova YE, Pavlov KV, Volynsky PE, Goncharuk MV, Ermolyuk YS, Karpunin DV, Schulga AA, Kirpichnikov MP, Efremov RG, Maslennikov IV, and Arseniev AS. Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J Biol Chem 282: 16256-16266, 2007. (Pubitemid 47100372)
8. Boyd JM, Malstrom S, Subramanian T, Venkatesh LK, Schaeper U, Elangovan B, Sa-Eipper C, and Chinnadurai G. Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79: 341-351, 1994. (Pubitemid 24324923)
9. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci USA 97: 9082-9087, 2000. (Pubitemid 30626677)
10. Burton TR, Henson ES, Baijal P, Eisenstat DD, and Gibson SB. The pro-cell death Bcl-2 family member, BNIP3, is localized to the nucleus of human glial cells: implications for glioblastoma multiforme tumor cell survival under hypoxia. Int J Cancer 118: 1660-1669, 2006. (Pubitemid 43376429)
11. Calvisi DF, Ladu S, Gorden A, Farina M, Lee JS, Conner EA, Schroeder I, Factor VM, and Thorgeirsson SS. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest 117: 2713-2722, 2007. (Pubitemid 47494371)
12. Carreira RS, Lee Y, Ghochani M, Gustafsson AB, and Gottlieb RA. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 6: 462-472, 2010.
13. Chen G, Cizeau J, Vande VC, Park JH, Bozek G, Bolton J, Shi L, Dubik D, and Greenberg A. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J Biol Chem 274: 7-10, 1999. (Pubitemid 29035022)
14. Chen G, Ray R, Dubik D, Shi L, Cizeau J, Bleackley RC, Saxena S, Gietz RD, and Greenberg AH. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 186: 1975-1983, 1997. (Pubitemid 28013681)
15. Chen Y, Lewis W, Diwan A, Cheng EH, Matkovich SJ, and Dorn GW. Dual autonomous mitochondrial cell death pathways are activated by Nix/BNip3L and induce cardiomyopathy. Proc Natl Acad Sci USA 107: 9035-9042, 2010.
16. Cuconati A and White E. Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev 16: 2465-2478, 2002.
17. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, and Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 64: 4286-4293, 2004. (Pubitemid 38802435)
18. Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, and Mazure NM. The oxygen sensor factor-inhibiting hypoxiainducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1alpha. Cancer Res 66: 3688-3698, 2006.
19. Deas E, Plun-Favreau H, and Wood NW. PINK1 function in health and disease. EMBO Mol Med 1: 152-165, 2009.
20. Ding WX, Ni HM, Li M, Liao Y, Chen X, Stolz DB, Dorn GW, and Yin XM. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J Biol Chem 285: 27879-27890, 2010.
21. Diwan A, Koesters AG, Odley AM, Pushkaran S, Baines CP, Spike BT, Daria D, Jegga AG, Geiger H, Aronow BJ, Molkentin JD, Macleod KF, Kalfa TA, and Dorn GW. Unrestrained erythroblast development in Nix-/-mice reveals a mechanism for apoptotic modulation of erythropoiesis. Proc Natl Acad Sci USA 104: 6794-6799, 2007. (Pubitemid 47175580)
22. Diwan A, Krenz M, Syed FM, Wansapura J, Ren X, Koesters AG, Li H, Kirshenbaum LA, Hahn HS, Robbins J, Jones WK, and Dorn GW. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J Clin Invest 117: 2825-2833, 2007. (Pubitemid 47529613)
23. Diwan A, Matkovich SJ, Yuan Q, Zhao W, Yatani A, Brown JH, Molkentin JD, Kranias EG, and Dorn GW. Endoplasmic reticulum-mitochondria crosstalk in NIX-mediated murine cell death. J Clin Invest 119: 203-212, 2009.
24. Diwan A, Wansapura J, Syed FM, Matkovich SJ, Lorenz JN, and Dorn GW. Nix-mediated apoptosis links myocardial fibrosis, cardiac remodeling, and hypertrophy decompensation. Circulation 117: 396-404, 2008.
25. Dorn GW. Mitochondrial pruning by Nix and BNip3: an essential function for cardiac-expressed death factors. J Cardiovasc Transl Res 3: 374-383, 2010.
26. Elmore SP, Qian T, Grissom SF, and Lemasters JJ. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15: 2286-2287, 2001.
27. Erkan M, Kleeff J, Esposito I, Giese T, Ketterer K, Buchler MW, Giese NA, and Friess H. Loss of BNIP3 expression is a late event in pancreatic cancer contributing to chemoresistance and worsened prognosis. Oncogene 24: 4421-4432, 2005. (Pubitemid 40961765)
28. Fei P, Wang W, Kim SH, Wang S, Burns TF, Sax JK, Buzzai M, Dicker DT, McKenna WG, Bernhard EJ, and El-Deiry WS. Bnip3L is induced by p53 under hypoxia, and its knockdown promotes tumor growth. Cancer Cell 6: 597-609, 2004. (Pubitemid 40017703)
29. Frazier DP, Wilson A, Graham RM, Thompson JW, Bishopric NH, and Webster KA. Acidosis regulates the stability, hydrophobicity, and activity of the BH3-only protein Bnip3. Antioxid Redox Signal 8: 1625-1634, 2006. (Pubitemid 44726337)
30. Frezza C, Cipolat S, Martins de BO, Micaroni M, Beznoussenko GV, Rudka T, Bartoli D, Polishuck RS, Danial NN, De SB, and Scorrano L. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-189, 2006.
31. Galvez AS, Brunskill EW, Marreez Y, Benner BJ, Regula KM, Kirschenbaum LA, and Dorn GW. Distinct pathways regulate proapoptotic Nix and BNip3 in cardiac stress. J Biol Chem 281: 1442-1448, 2006.
32. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, and Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12: 119-131, 2010.
33. Giatromanolaki A, Koukourakis MI, Sowter HM, Sivridis E, Gibson S, Gatter KC and Harris AL. BNIP3 expression is linked with hypoxia-regulated protein expression and with poor prognosis in non-small cell lung cancer. Clin Cancer Res 10: 5566-5571, 2004. (Pubitemid 39100497)
34. Gronowicz G, Swift H, and Steck TL. Maturation of the reticulocyte in vitro. J Cell Sci 71: 177-197, 1984.
35. Guo K, Searfoss G, Krolikowski D, Pagnoni M, Franks C, Clark K, Yu KT, Jaye M, and Ivashchenko Y. Hypoxia induces the expression of the pro-apoptotic gene BNIP3. Cell Death Differ 8: 367-376, 2001. (Pubitemid 32409607)
36. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, and Gustafsson AB. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14: 146-157, 2007. (Pubitemid 44911902)
37. Haworth RA and Hunter DR. The Ca2 + -induced membrane transition in mitochondria. II. Nature of the Ca2 + trigger site. Arch Biochem Biophys 195: 460-467, 1979. (Pubitemid 9235078)
38. Heynen MJ, Tricot G, and Verwilghen RL. Autophagy of mitochondria in rat bone marrow erythroid cells. Relation to nuclear extrusion. Cell Tissue Res 239: 235-239, 1985.
39. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, and Ohsumi Y. A ubiquitin-like system mediates protein lipidation. Nature 408: 488-492, 2000.
40. Imazu T, Shimizu S, Tagami S, Matsushima M, Nakamura Y, Miki T, Okuyama A, and Tsujimoto Y. Bcl-2/E1B 19 kDa-interacting protein 3-like protein (Bnip3L) interacts with bcl-2/Bcl-xL and induces apoptosis by altering mitochondrial membrane permeability. Oncogene 18: 4523-4529, 1999. (Pubitemid 29405883)
41. Kanki T, Wang K, Cao Y, Baba M, and Klionsky DJ. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 17: 98-109, 2009.
42. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y, and Kondo S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 24: 980-991, 2005. (Pubitemid 40313875)
43. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, and Cheng EH. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8: 1348-1358, 2006. (Pubitemid 44835109)
44. Kim I, Rodriguez-Enriquez S, and Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462: 245-253, 2007. (Pubitemid 46876640)
45. Kim JY, Cho JJ, Ha J, and Park JH. The carboxy terminal Ctail of BNip3 is crucial in induction of mitochondrial permeability transition in isolated mitochondria. Arch Biochem Biophys 398: 147-152, 2002. (Pubitemid 34848580)
46. Kirkin V, McEwan DG, Novak I, and Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 34: 259-269, 2009.
47. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, and Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608, 1998. (Pubitemid 28207717)
48. Kong DK, Georgescu SP, Cano C, Aronovitz MJ, Iovanna JL, Patten RD, Kyriakis JM, and Goruppi S. Deficiency of the transcriptional regulator p8 results in increased autophagy and apoptosis, and causes impaired heart function. Mol Biol Cell 21: 1335-1349, 2010.
49. Koop EA, van LT, van Wichen DF, de Weger RA, Wall E, and van Diest PJ. Expression of BNIP3 in invasive breast cancer: correlations with the hypoxic response and clinicopathological features. BMC Cancer 9: 175, 2009.
50. Koury MJ, Koury ST, Kopsombut P, and Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood 105: 2168-2174, 2005. (Pubitemid 40731809)
51. Kubasiak LA, Hernandez OM, Bishopric NH, and Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 99: 12825-12830, 2002.
52. Kubli DA, Quinsay MN, Huang C, Lee Y, and Gustafsson AB. Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 295: H2025-H2031, 2008.
53. KunduM, Lindsten T, Yang CY,WuJ, Zhao F, Zhang J, Selak MA, Ney PA, and Thompson CB. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112: 1493-1502, 2008.
54. Lai J, Flanagan J, Phillips WA, Chenevix-Trench G, and Arnold J. Analysis of the candidate 8p21 tumour suppressor, BNIP3L, in breast and ovarian cancer. Br J Cancer 88: 270-276, 2003. (Pubitemid 36255847)
55. Lam M, Oleinick NL, and Nieminen AL. Photodynamic therapy-induced apoptosis in epidermoid carcinoma cells. Reactive oxygen species and mitochondrial inner membrane permeabilization. J Biol Chem 276: 47379-47386, 2001.
56. Landes T, Emorine LJ, Courilleau D, Rojo M, Belenguer P and Arnaune-Pelloquin L. The BH3-only Bnip3 binds to the dynamin Opa1 to promote mitochondrial fragmentation and apoptosis by distinct mechanisms. EMBO Rep 11: 459-465, 2010.
57. Lee JY, Nagano Y, Taylor JP, Lim KL, and Yao TP. Diseasecausing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J Cell Biol 189: 671-679, 2010.
58. Li Y, Wang Y, Kim E, Beemiller P, Wang CY, Swanson J, You M, and Guan KL. Bnip3 mediates the hypoxia-induced inhibition on mammalian target of rapamycin by interacting with Rheb. J Biol Chem 282: 35803-35813, 2007. (Pubitemid 350277153)
59. Liu W, Xie CC, Zhu Y, Li T, Sun J, Cheng Y, Ewing CM, Dalrymple S, Turner AR, Sun J, Isaacs JT, Chang BL, Zheng SL, Isaacs WB, and Xu J. Homozygous deletions and recurrent amplifications implicate new genes involved in prostate cancer. Neoplasia 10: 897-907, 2008.
60. Low BC, Seow KT, and Guy GR. Evidence for a novel Cdc42GAP domain at the carboxyl terminus of BNIP-2. J Biol Chem 275: 14415-14422, 2000. (Pubitemid 30339727)
61. Maiuri MC, Le TG, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, and Kroemer G. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26: 2527-2539, 2007. (Pubitemid 46788315)
62. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del PP, Burden SJ, Di LR, Sandri C, Zhao J, Goldberg AL, Schiaffino S, and Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471, 2007. (Pubitemid 350163055)
63. Manka D, Spicer Z, and Millhorn DE. 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, 2005. (Pubitemid 41821729)
64. Matsui M, Yamamoto A, Kuma A, Ohsumi Y, and Mizushima N. Organelle degradation during the lens and erythroid differentiation is independent of autophagy. Biochem Biophys Res Commun 339: 485-489, 2006. (Pubitemid 41739693)
65. Matsushima M, Fujiwara T, Takahashi E, Minaguchi T, Eguchi Y, Tsujimoto Y, Suzumori K, and Nakamura Y. Isolation, mapping, and functional analysis of a novel human cDNA (BNIP3L) encoding a protein homologous to human NIP3. Genes Chromosomes Cancer 21: 230-235, 1998. (Pubitemid 28136440)
66. Metukuri MR, Beer-Stolz D, Namas RA, Dhupar R, Torres A, Loughran PA, Jefferson BS, Tsung A, Billiar TR, Vodovotz Y, and Zamora R. Expression and subcellular localization of BNIP3 in hypoxic hepatocytes and liver stress. Am J Physiol Gastrointest Liver Physiol 296: G499-G509, 2009.
67. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, and Ohsumi Y. A protein conjugation system essential for autophagy. Nature 395: 395-398, 1998. (Pubitemid 28450691)
68. Mortensen M, Ferguson DJ, Edelmann M, Kessler B, Morten KJ, Komatsu M, and Simon AK. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA 107: 832-837, 2010.
69. Murai M, Toyota M, Satoh A, Suzuki H, Akino K, Mita H, Sasaki Y, Ishida T, Shen L, Garcia-Manero G, Issa JP, Hinoda Y, Tokino T, and Imai K. Aberrant DNA methylation associated with silencing BNIP3 gene expression in haematopoietic tumours. Br J Cancer 92: 1165-1172, 2005. (Pubitemid 40546685)
70. Murai M, Toyota M, Suzuki H, Satoh A, Sasaki Y, Akino K, Ueno M, Takahashi F, Kusano M, Mita H, Yanagihara K, Endo T, Hinoda Y, Tokino T, and Imai K. Aberrant methylation and silencing of the BNIP3 gene in colorectal and gastric cancer. Clin Cancer Res 11: 1021-1027, 2005. (Pubitemid 40175749)
71. Nakajima K, Hirose H, Taniguchi M, Kurashina H, Arasaki K, Nagahama M, Tani K, Yamamoto A, and Tagaya M. Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion. EMBO J 23: 3216-3226, 2004. (Pubitemid 39209146)
72. Narendra D, Tanaka A, Suen DF, and Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803, 2008.
73. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, and Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8: e1000298, 2010.
74. Narendra DP, Kane LA, Hauser DN, Fearnley IM, and Youle RJ. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 6: 1090-1106, 2010.
75. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, and Shimizu S. Discovery of Atg5/Atg7- independent alternative macroautophagy. Nature 461: 654-658, 2009.
76. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Lohr F, Popovic D, Occhipinti A, Reichert AS, Terzic J, Dotsch V, Ney PA, and Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51, 2010.
77. Nutt LK, Pataer A, Pahler J, Fang B, Roth J, McConkey DJ, and Swisher SG. Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2 + stores. J Biol Chem 277: 9219-9225, 2002. (Pubitemid 34953002)
78. Ohi N, Tokunaga A, Tsunoda H, Nakano K, Haraguchi K, Oda K, Motoyama N, and Nakajima T. A novel adenovirus E1B19K-binding protein B5 inhibits apoptosis induced by Nip3 by forming a heterodimer through the C-terminal hydrophobic region. Cell Death Differ 6: 314-325, 1999. (Pubitemid 29186875)
79. Okami J, Simeone DM, and Logsdon CD. Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer. Cancer Res 64: 5338-5346, 2004. (Pubitemid 39006554)
80. Okamoto K, Kondo-Okamoto N, and Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17: 87-97, 2009.
81. Papandreou I, Krishna C, Kaper F, Cai D, Giaccia AJ, and Denko NC. Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment. Cancer Res 65: 3171-3178, 2005. (Pubitemid 40524598)
82. Papandreou I, Lim AL, Laderoute K, and Denko NC. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ 15: 1572-1581, 2008.
83. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, and Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939, 2005. (Pubitemid 41345209)
84. Quinsay MN, Lee Y, Rikka S, Sayen MR, Molkentin JD, Gottlieb RA, and Gustafsson AB. Bnip3 mediates permeabilization of mitochondria and release of cytochrome c via a novel mechanism. J Mol Cell Cardiol 48: 1146-1156, 2010.
85. Quinsay MN, Thomas RL, Lee Y, and Gustafsson AB. Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6: 17-24, 2010.
86. Ray R, Chen G, Vande VC, Cizeau J, Park JH, Reed JC, Gietz RD, and Greenberg AH. 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, 2000. (Pubitemid 30051204)
87. Regula KM, Ens K, and Kirshenbaum LA. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 91: 226-231, 2002. (Pubitemid 34875677)
88. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, and Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008.
89. Scherz-Shouval R and Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36: 30-38, 2010.
90. Schwarten M, Mohrluder J, Ma P, Stoldt M, Thielmann Y, Stangler T, Hersch N, Hoffmann B,Merkel R, andWillboldD. Nix directly binds toGABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 5: 690-698, 2009.
91. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, and Ney PA. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 104: 19500-19505, 2007.
92. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, and Korsmeyer SJ. BAX and BAK regulation of endoplasmic reticulum Ca2 + : a control point for apoptosis. Science 300: 135-139, 2003. (Pubitemid 36423046)
93. Shaida N, Launchbury R, Boddy JL, Jones C, Campo L, Turley H, Kanga S, Banham AH, Malone PR, Harris AL, and Fox SB. Expression of BNIP3 correlates with hypoxiainducible factor (HIF)-1alpha, HIF-2alpha and the androgen receptor in prostate cancer and is regulated directly by hypoxia but not androgens in cell lines. Prostate 68: 336-343, 2008. (Pubitemid 351273062)
94. Sowter HM, Ferguson M, Pym C, Watson P, Fox SB, Han C, and Harris AL. 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, 2003. (Pubitemid 38256406)
95. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, and Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res 61: 6669-6673, 2001. (Pubitemid 32896483)
96. Sulistijo ES, Jaszewski TM, and MacKenzie KR. Sequencespecific dimerization of the transmembrane domain of the "BH3-only" protein BNIP3 in membranes and detergent. J Biol Chem 278: 51950-51956, 2003. (Pubitemid 38020442)
97. Sulistijo ES and MacKenzie KR. Sequence dependence of BNIP3 transmembrane domain dimerization implicates sidechain hydrogen bonding and a tandem GxxxG motif in specific helix-helix interactions. J Mol Biol 364: 974-990, 2006. (Pubitemid 44765043)
98. Tracy K, Dibling BC, Spike BT, Knabb JR, Schumacker P, and Macleod KF. BNIP3 is an RB/E2F target gene required for hypoxia-induced autophagy. Mol Cell Biol 27: 6229-6242, 2007. (Pubitemid 47326709)
99. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, LasG,Alroy J,WuM, Py BF, Yuan J, Deeney JT, Corkey BE, and Shirihai OS. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27: 433-446, 2008. (Pubitemid 351161653)
100. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, Hakem R, and Greenberg AH. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 20: 5454-5468, 2000. (Pubitemid 30482883)
101. Wang J, Ni H, Chen L, Liu YX, Chen CB, and Song WQ. Preparation and analysis of cSNP chip on hepatocellular carcinoma-related genes. Hepatobiliary Pancreat Dis Int 4: 398-402, 2005. (Pubitemid 41207542)
102. Xie Z and Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9: 1102-1109, 2007. (Pubitemid 47500484)
103. Yang Z and Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 12: 814-822, 2010.
104. Yasuda M, Han JW, Dionne CA, Boyd JM, and Chinnadurai G. BNIP3alpha: a human homolog of mitochon-drial proapoptotic protein BNIP3. Cancer Res 59: 533-537, 1999. (Pubitemid 29076045)
105. Yasuda M, Sa-Eipper C, Gong XL, and Chinnadurai G. Regulation of apoptosis by a Caenorhabditis elegans BNIP3 homolog. Oncogene 17: 2525-2530, 1998. (Pubitemid 28544722)
106. Yasuda M, Theodorakis P, Subramanian T, and Chinnadurai G. Adenovirus E1B-19K/BCL-2 interacting protein BNIP3 contains a BH3 domain and a mitochondrial targeting sequence. J Biol Chem 273: 12415-12421, 1998. (Pubitemid 28240613)
107. Yussman MG, Toyokawa T, Odley A, Lynch RA, Wu G, Colbert MC, Aronow BJ, Lorenz JN, and Dorn GW. Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy. Nat Med 8: 725-730, 2002. (Pubitemid 34778726)
108. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, and Semenza GL. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283: 10892-10903, 2008.
109. Zhang J and Ney PA. NIX induces mitochondrial autophagy in reticulocytes. Autophagy 4: 354-356, 2008. (Pubitemid 351458098)
110. Zhang J, Randall MS, Loyd MR, Dorsey FC, Kundu M, Cleveland JL, and Ney PA. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 114: 157-164, 2009.
111. Zhang Z, Yang X, Zhang S, Ma X, and Kong J. BNIP3 upregulation and EndoG translocation in delayed neuronal death in stroke and in hypoxia. Stroke 38: 1606-1613, 2007. (Pubitemid 46684181)
112. Zhu X, Zhou W, Cui Y, Zhu L, Li J, Feng X, Shao B, Qi H, Zheng J, Wang H, and Chen H. Pilocarpine protects cobalt chloride-induced apoptosis of RGC-5 cells: involvement of muscarinic receptors and HIF-1 alpha pathway. Cell Mol Neurobiol 30: 427-435, 2010.