Integrating stress signals at the endoplasmic reticulum: The BCL-2 protein family rheostat

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 4, 2011, Pages 564-574

  Rodriguez, Diego ^a,b   Rojas Rivera, Diego ^a,b   Hetz, Claudio ^a,b,c  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

BCL 2 family; Endoplasmic reticulum; Unfolded protein response

Indexed keywords

APOPTOSOME; CALCIUM; CYTOCHROME C; PROTEIN BCL 2;

ADAPTATION; APOPTOSIS; AUTOPHAGY; CALCIUM HOMEOSTASIS; CELL ORGANELLE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME RELEASE; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; STRESS, PHYSIOLOGICAL;

EID: 79952705597     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.11.012     Document Type: Review

References (180)

1. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat. Rev. Cancer 2004, 4:966-977.
2. Matus S., Lisbona F., Torres M., Leon C., Thielen P., Hetz C. The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr. Mol. Med. 2008, 8:157-172.
3. Scheper W., Hoozemans J.J. Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Curr. Med. Chem. 2009, 16:615-626.
4. Lipson K.L., Fonseca S.G., Urano F. Endoplasmic reticulum stress-induced apoptosis and auto-immunity in diabetes. Curr. Mol. Med. 2006, 6:71-77.
5. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454:455-462.
6. Ferri K.F., Kroemer G. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 2001, 3:E255-E263.
7. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9:47-59.
8. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
9. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
10. Zhang H.M., Cheung P., Yanagawa B., McManus B.M., Yang D.C. BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 2003, 8:229-236.
11. Chinnadurai G., Vijayalingam S., Gibson S.B. BNIP3 subfamily BH3-only proteins: mitochondrial stress sensors in normal and pathological functions. Oncogene 2008, 27(Suppl 1):S114-S127.
12. Burton T.R., Gibson S.B. The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ. 2009, 16:515-523.
13. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2002, 2:647-656.
14. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J. Cell Sci. 2009, 122:437-441.
15. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
16. Lindsten T., Ross A.J., King A., Zong W.X., Rathmell J.C., Shiels H.A., Ulrich E., Waymire K.G., Mahar P., Frauwirth K., Chen Y., Wei M., Eng V.M., Adelman D.M., Simon M.C., Ma A., Golden J.A., Evan G., Korsmeyer S.J., MacGregor G.R., Thompson C.B. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 2000, 6:1389-1399.
17. Ow Y.P., Green D.R., Hao Z., Mak T.W. Cytochrome c: functions beyond respiration. Nat. Rev. Mol. Cell Biol. 2008, 9:532-542.
18. Kim H., Rafiuddin-Shah M., Tu H.C., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat. Cell Biol. 2006, 8:1348-1358.
19. Kuwana T., Bouchier-Hayes L., Chipuk J.E., Bonzon C., Sullivan B.A., Green D.R., Newmeyer D.D. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 2005, 17:525-535.
20. Letai A., Bassik M.C., Walensky L.D., Sorcinelli M.D., Weiler S., Korsmeyer S.J. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002, 2:183-192.
21. Willis S.N., Fletcher J.I., Kaufmann T., van Delft M.F., Chen L., Czabotar P.E., Ierino H., Lee E.F., Fairlie W.D., Bouillet P., Strasser A., Kluck R.M., Adams J.M., Huang D.C. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007, 315:856-859.
22. Merino D., Giam M., Hughes P.D., Siggs O.M., Heger K., O'Reilly L.A., Adams J.M., Strasser A., Lee E.F., Fairlie W.D., Bouillet P. The role of BH3-only protein Bim extends beyond inhibiting Bcl-2-like prosurvival proteins. J. Cell Biol. 2009, 186:355-362.
23. Labi V., Erlacher M., Kiessling S., Villunger A. BH3-only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ. 2006, 13:1325-1338.
24. Kutuk O., Letai A. Regulation of Bcl-2 family proteins by posttranslational modifications. Curr. Mol. Med. 2008, 8:102-118.
25. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
26. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
27. Hetz C., Glimcher L.H. Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol. Cell 2009, 35:551-561.
28. Hetz C.A. ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid. Redox Signal. 2007, 9:2345-2355.
29. Hetz C., Glimcher L. The daily job of night killers: alternative roles of the BCL-2 family in organelle physiology. Trends Cell Biol. 2008, 18:38-44.
30. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K., Kaufman R.J. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 2002, 16:452-466.
31. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415:92-96.
32. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107:881-891.
33. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 2003, 23:7448-7459.
34. Hetz C., Glimcher L.H. The UPRosome and XBP-1: mastering secretory cell function. Curr. Immunol. Rev. 2008, 4:1-10.
35. Hollien J., Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006, 313:104-107.
36. Han D., Lerner A.G., Vande Walle L., Upton J.P., Xu W., Hagen A., Backes B.J., Oakes S.A., Papa F.R. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009, 138:562-575.
37. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
38. Nishitoh H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., Hori S., Kakizuka A., Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 2002, 16:1345-1355.
39. Nguyen D.T., Kebache S., Fazel A., Wong H.N., Jenna S., Emadali A., Lee E.H., Bergeron J.J., Kaufman R.J., Larose L., Chevet E. Nck-dependent activation of extracellular signal-regulated kinase-1 and regulation of cell survival during endoplasmic reticulum stress. Mol. Biol. Cell 2004, 15:4248-4260.
40. Gu F., Nguyen D.T., Stuible M., Dube N., Tremblay M.L., Chevet E. Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J. Biol. Chem. 2004, 279:49689-49693.
41. Hu P., Han Z., Couvillon A.D., Kaufman R.J., Exton J.H. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol. Cell. Biol. 2006, 26:3071-3084.
42. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T., Tohyama M. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 2001, 276:13935-13940.
43. Hetz C., Bernasconi P., Fisher J., Lee A.H., Bassik M.C., Antonsson B., Brandt G.S., Iwakoshi N.N., Schinzel A., Glimcher L.H., Korsmeyer S.J. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 2006, 312:572-576.
44. Lin J.H., Li H., Zhang Y., Ron D., Walter P. Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE 2009, 4:e4170.
45. Lin J.H., Li H., Yasumura D., Cohen H.R., Zhang C., Panning B., Shokat K.M., Lavail M.M., Walter P. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007, 318:944-949.
46. Bailly-Maitre B., Belgardt B.F., Jordan S.D., Coornaert B., von Freyend M.J., Kleinridders A., Mauer J., Cuddy M., Kress C.L., Willmes D., Essig M., Hampel B., Protzer U., Reed J.C., Bruning J.C. Hepatic Bax inhibitor-1 inhibits IRE1alpha and protects from obesity-associated insulin resistance and glucose intolerance. J. Biol. Chem. 2010, 285:6198-6207.
47. Lee G.H., Kim H.K., Chae S.W., Kim D.S., Ha K.C., Cuddy M., Kress C., Reed J.C., Kim H.R., Chae H.J. Bax inhibitor-1 regulates endoplasmic reticulum stress-associated reactive oxygen species and heme oxygenase-1 expression. J. Biol. Chem. 2007, 282:21618-21628.
48. Bailly-Maitre B., Fondevila C., Kaldas F., Droin N., Luciano F., Ricci J.E., Croxton R., Krajewska M., Zapata J.M., Kupiec-Weglinski J.W., Farmer D., Reed J.C. Cytoprotective gene bi-1 is required for intrinsic protection from endoplasmic reticulum stress and ischemia-reperfusion injury. Proc. Natl Acad. Sci. USA 2006, 103:2809-2814.
49. Lisbona F., Rojas-Rivera D., Thielen P., Zamorano S., Todd D., Martinon F., Glavic A., Kress C., Lin J.H., Walter P., Reed J.C., Glimcher L.H., Hetz C. BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol. Cell 2009, 33:679-691.
50. Huckelhoven R. BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 2004, 9:299-307.
51. Reimers K., Choi C.Y., Bucan V., Vogt P.M. The Bax Inhibitor-1 (BI-1) family in apoptosis and tumorigenesis. Curr. Mol. Med. 2008, 8:148-156.
52. Hu L., Smith T.F., Goldberger G. LFG: a candidate apoptosis regulatory gene family. Apoptosis 2009, 14:1255-1265.
53. Xu Q., Reed J.C. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell 1998, 1:337-346.
54. Klee M., Pallauf K., Alcala S., Fleischer A., Pimentel-Muinos F.X. Mitochondrial apoptosis induced by BH3-only molecules in the exclusive presence of endoplasmic reticular Bak. EMBO J. 2009, 28:1757-1768.
55. Luo D., He Y., Zhang H., Yu L., Chen H., Xu Z., Tang S., Urano F., Min W. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. J. Biol. Chem. 2008, 283:11905-11912.
56. Gonzalez T.N., Walter P. Ire1p: a kinase and site-specific endoribonuclease. Meth. Mol. Biol. 2001, 160:25-36.
57. Y. Qiu, T. Mao, Y. Zhang, M. Shao, J. You, Q. Ding, Y. Chen, D. Wu, D. Xie, X. Lin, X. Gao, R.J. Kaufman, W. Li, Y. Liu, A crucial role for RACK1 in the regulation of glucose-stimulated IRE1alpha activation in pancreatic beta cells, Sci. Signal. 3 (2010) ra7.
58. A.D. Sanjeev Gupta, Shane Deegan, Fernanda Lisbona, Claudio Hetz and Afshin Samali., HSP72 protects cells from ER stress-induced apoptosis via enhancement of IRE1-XBP1 signalling through a physical interaction, Plos Biology 8 (2010) e1000410.
59. Lisbona F., Hetz C. Turning off the unfolded protein response: an interplay between the apoptosis machinery and ER stress signaling. Cell Cycle 2009, 8:1643-1644.
60. Mauro C., Crescenzi E., De Mattia R., Pacifico F., Mellone S., Salzano S., de Luca C., D'Adamio L., Palumbo G., Formisano S., Vito P., Leonardi A. Central role of the scaffold protein tumor necrosis factor receptor-associated factor 2 in regulating endoplasmic reticulum stress-induced apoptosis. J. Biol. Chem. 2006, 281:2631-2638.
61. Matsuzawa A., Nishitoh H., Tobiume K., Takeda K., Ichijo H. Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: advanced findings from ASK1 knockout mice. Antioxid. Redox Signal. 2002, 4:415-425.
62. P.I. Merksamer, F.R. Papa, The UPR and cell fate at a glance, J. Cell Sci. 123 1003-1006.
63. Heath-Engel H.M., Chang N.C., Shore G.C. The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene 2008, 27:6419-6433.
64. Szegezdi E., Duffy A., O'Mahoney M.E., Logue S.E., Mylotte L.A., O'Brien T., Samali A. ER stress contributes to ischemia-induced cardiomyocyte apoptosis. Biochem. Biophys. Res. Commun. 2006, 349:1406-1411.
65. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005, 115:2656-2664.
66. Reed J.C. Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell Death Differ. 2006, 13:1378-1386.
67. Reimertz C., Kogel D., Rami A., Chittenden T., Prehn J.H. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J. Cell Biol. 2003, 162:587-597.
68. Nickson P., Toth A., Erhardt P. PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress. Cardiovasc. Res. 2007, 73:48-56.
69. Li J., Lee B., Lee A.S. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 2006, 281:7260-7270.
70. Cazanave S.C., Elmi N.A., Akazawa Y., Bronk S.F., Mott J.L., Gores G.J. CHOP and AP-1 cooperatively mediate PUMA expression during lipoapoptosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G236-G243.
71. Armstrong J.L., Flockhart R., Veal G.J., Lovat P.E., Redfern C.P. Regulation of endoplasmic reticulum stress-induced cell death by ATF4 in neuroectodermal tumor cells. J. Biol. Chem. 2010, 285:6091-6100.
72. Futami T., Miyagishi M., Taira K. Identification of a network involved in thapsigargin-induced apoptosis using a library of small interfering RNA expression vectors. J. Biol. Chem. 2005, 280:826-831.
73. Jiang C.C., Lucas K., Avery-Kiejda K.A., Wade M., deBock C.E., Thorne R.F., Allen J., Hersey P., Zhang X.D. Up-regulation of Mcl-1 is critical for survival of human melanoma cells upon endoplasmic reticulum stress. Cancer Res. 2008, 68:6708-6717.
74. Wang Q., Mora-Jensen H., Weniger M.A., Perez-Galan P., Wolford C., Hai T., Ron D., Chen W., Trenkle W., Wiestner A., Ye Y. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc. Natl Acad. Sci. USA 2009, 106:2200-2205.
75. Germain M., Mathai J.P., Shore G.C. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 2002, 277:18053-18060.
76. Mathai J.P., Germain M., Shore G.C. BH3-only BIK regulates BAX, BAK-dependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J. Biol. Chem. 2005, 280:23829-23836.
77. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., Hughes P.D., Michalak E.M., McKimm-Breschkin J., Motoyama N., Gotoh T., Akira S., Bouillet P., Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
78. Fu H.Y., Okada K., Liao Y., Tsukamoto O., Isomura T., Asai M., Sawada T., Okuda K., Asano Y., Sanada S., Asanuma H., Asakura M., Takashima S., Komuro I., Kitakaze M., Minamino T. Ablation of C/EBP homologous protein attenuates endoplasmic reticulum-mediated apoptosis and cardiac dysfunction induced by pressure overload. Circulation 2010, 122:361-369.
79. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 2001, 7:1165-1176.
80. Tamaki N., Hatano E., Taura K., Tada M., Kodama Y., Nitta T., Iwaisako K., Seo S., Nakajima A., Ikai I., Uemoto S. CHOP deficiency attenuates cholestasis-induced liver fibrosis by reduction of hepatocyte injury. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G498-G505.
81. Fleischer A., Rebollo A., Ayllon V. BH3-only proteins: the lords of death. Arch. Immunol. Ther. Exp. (Warsz) 2003, 51:9-17.
82. Morishima N., Nakanishi K., Tsuchiya K., Shibata T., Seiwa E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J. Biol. Chem. 2004, 279:50375-50381.
83. Elyaman W., Terro F., Suen K.C., Yardin C., Chang R.C., Hugon J. BAD and Bcl-2 regulation are early events linking neuronal endoplasmic reticulum stress to mitochondria-mediated apoptosis. Brain Res. Mol. Brain Res. 2002, 109:233-238.
84. Upton J.P., Austgen K., Nishino M., Coakley K.M., Hagen A., Han D., Papa F.R., Oakes S.A. Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol. Cell. Biol. 2008, 28:3943-3951.
85. Zong W.X., Li C., Hatzivassiliou G., Lindsten T., Yu Q.C., Yuan J., Thompson C.B. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 2003, 162:59-69.
86. Wang X., Olberding K.E., White C., Li C. Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ. 2010, 68:1-10.
87. Hetz C., Vitte P.A., Bombrun A., Rostovtseva T.K., Montessuit S., Hiver A., Schwarz M.K., Church D.J., Korsmeyer S.J., Martinou J.C., Antonsson B. Bax channel inhibitors prevent mitochondrion-mediated apoptosis and protect neurons in a model of global brain ischemia. J. Biol. Chem. 2005, 280:42960-42970.
88. Oakes S.A., Lin S.S., Bassik M.C. The control of endoplasmic reticulum-initiated apoptosis by the BCL-2 family of proteins. Curr. Mol. Med. 2006, 6:99-109.
89. Breckenridge D.G., Germain M., Mathai J.P., Nguyen M., Shore G.C. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22:8608-8618.
90. Pinton P., Rizzuto R. Bcl-2 and Ca2+ homeostasis in the endoplasmic reticulum. Cell Death Differ. 2006, 13:1409-1418.
91. Scorrano L., Oakes S.A., Opferman J.T., Cheng E.H., Sorcinelli M.D., Pozzan T., Korsmeyer S.J. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 2003, 300:135-139.
92. Bassik M.C., Scorrano L., Oakes S.A., Pozzan T., Korsmeyer S.J. Phosphorylation of BCL-2 regulates ER Ca2+ homeostasis and apoptosis. EMBO J. 2004, 23:1207-1216.
93. Oakes S.A., Opferman J.T., Pozzan T., Korsmeyer S.J., Scorrano L. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem. Pharmacol. 2003, 66:1335-1340.
94. Lam M., Dubyak G., Chen L., Nunez G., Miesfeld R.L., Distelhorst C.W. Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc. Natl Acad. Sci. USA 1994, 91:6569-6573.
95. Distelhorst C.W., Lam M., McCormick T.S. Bcl-2 inhibits hydrogen peroxide-induced ER Ca2+ pool depletion. Oncogene 1996, 12:2051-2055.
96. Pinton P., Ferrari D., Magalhaes P., Schulze-Osthoff K., Di Virgilio F., Pozzan T., Rizzuto R. Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J. Cell Biol. 2000, 148:857-862.
97. Foyouzi-Youssefi R., Arnaudeau S., Borner C., Kelley W.L., Tschopp J., Lew D.P., Demaurex N., Krause K.H. Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 2000, 97:5723-5728.
98. Pinton P., Ferrari D., Rapizzi E., Di Virgilio F., Pozzan T., Rizzuto R. The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J. 2001, 20:2690-2701.
99. H.M. Ni, C.J. Baty, N. Li, W.X. Ding, W. Gao, M. Li, X. Chen, J. Ma, G.K. Michalopoulos, X.M. Yin, Bid agonist regulates murine hepatocyte proliferation by controlling endoplasmic reticulum calcium homeostasis, Hepatology 52 (2010) 338-348.
100. Chae H.J., Kim H.R., Xu C., Bailly-Maitre B., Krajewska M., Krajewski S., Banares S., Cui J., Digicaylioglu M., Ke N., Kitada S., Monosov E., Thomas M., Kress C.L., Babendure J.R., Tsien R.Y., Lipton S.A., Reed J.C. BI-1 regulates an apoptosis pathway linked to endoplasmic reticulum stress. Mol. Cell 2004, 15:355-366.
101. Westphalen B.C., Wessig J., Leypoldt F., Arnold S., Methner A. BI-1 protects cells from oxygen glucose deprivation by reducing the calcium content of the endoplasmic reticulum. Cell Death Differ. 2005, 12:304-306.
102. Xu C., Xu W., Palmer A.E., Reed J.C. BI-1 regulates endoplasmic reticulum Ca2+ homeostasis downstream of Bcl-2 family proteins. J. Biol. Chem. 2008, 283:11477-11484.
103. de Mattia F., Gubser C., van Dommelen M.M., Visch H.J., Distelmaier F., Postigo A., Luyten T., Parys J.B., de Smedt H., Smith G.L., Willems P.H., van Kuppeveld F.J. Human Golgi antiapoptotic protein modulates intracellular calcium fluxes. Mol. Biol. Cell 2009, 20:3638-3645.
104. Ahn T., Yun C.H., Kim H.R., Chae H.J. Cardiolipin, phosphatidylserine, and BH4 domain of Bcl-2 family regulate Ca2+/H+ antiporter activity of human Bax inhibitor-1. Cell Calcium 2010, 47:387-396.
105. Kim H.R., Lee G.H., Ha K.C., Ahn T., Moon J.Y., Lee B.J., Cho S.G., Kim S., Seo Y.R., Shin Y.J., Chae S.W., Reed J.C., Chae H.J. Bax Inhibitor-1 Is a pH-dependent regulator of Ca2+ channel activity in the endoplasmic reticulum. J. Biol. Chem. 2008, 283:15946-15955.
106. Oakes S.A., Scorrano L., Opferman J.T., Bassik M.C., Nishino M., Pozzan T., Korsmeyer S.J. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 2005, 102:105-110.
107. Chen R., Valencia I., Zhong F., McColl K.S., Roderick H.L., Bootman M.D., Berridge M.J., Conway S.J., Holmes A.B., Mignery G.A., Velez P., Distelhorst C.W. Bcl-2 functionally interacts with inositol 1, 4, 5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1, 4, 5-trisphosphate. J. Cell Biol. 2004, 166:193-203.
108. White C., Li C., Yang J., Petrenko N.B., Madesh M., Thompson C.B., Foskett J.K. The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat. Cell Biol. 2005, 7:1021-1028.
109. Vanderheyden V., Devogelaere B., Missiaen L., De Smedt H., Bultynck G., Parys J.B. Regulation of inositol 1, 4, 5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation. Biochim. Biophys. Acta 2009, 1793:959-970.
110. Rong Y.P., Barr P., Yee V.C., Distelhorst C.W. Targeting Bcl-2 based on the interaction of its BH4 domain with the inositol 1, 4, 5-trisphosphate receptor. Biochim. Biophys. Acta 2009, 1793:971-978.
111. Rong Y.P., Aromolaran A.S., Bultynck G., Zhong F., Li X., McColl K., Matsuyama S., Herlitze S., Roderick H.L., Bootman M.D., Mignery G.A., Parys J.B., De Smedt H., Distelhorst C.W. Targeting Bcl-2-IP3 receptor interaction to reverse Bcl-2's inhibition of apoptotic calcium signals. Mol. Cell 2008, 31:255-265.
112. Rizzuto R., Marchi S., Bonora M., Aguiari P., Bononi A., De Stefani D., Giorgi C., Leo S., Rimessi A., Siviero R., Zecchini E., Pinton P. Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochim. Biophys. Acta 2009, 1787:1342-1351.
113. Lin S.S., Bassik M.C., Suh H., Nishino M., Arroyo J.D., Hahn W.C., Korsmeyer S.J., Roberts T.M. PP2A regulates BCL-2 phosphorylation and proteasome-mediated degradation at the endoplasmic reticulum. J. Biol. Chem. 2006, 281:23003-23012.
114. Dremina E.S., Sharov V.S., Kumar K., Zaidi A., Michaelis E.K., Schoneich C. Anti-apoptotic protein Bcl-2 interacts with and destabilizes the sarcoplasmic/endoplasmic reticulum Ca2+-ATPase (SERCA). Biochem. J. 2004, 383:361-370.
115. Dremina E.S., Sharov V.S., Schoneich C. Displacement of SERCA from SR lipid caveolae-related domains by Bcl-2: a possible mechanism for SERCA inactivation. Biochemistry 2006, 45:175-184.
116. Kuo T.H., Kim H.R., Zhu L., Yu Y., Lin H.M., Tsang W. Modulation of endoplasmic reticulum calcium pump by Bcl-2. Oncogene 1998, 17:1903-1910.
117. Tsujimoto Y., Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 2007, 12:835-840.
118. Zhivotovsky B., Galluzzi L., Kepp O., Kroemer G. Adenine nucleotide translocase: a component of the phylogenetically conserved cell death machinery. Cell Death Differ. 2009, 16:1419-1425.
119. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 2005, 120:159-162.
120. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
121. Xie Z., Klionsky D.J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 2007, 9:1102-1109.
122. Cuervo A.M. Autophagy: in sickness and in health. Trends Cell Biol. 2004, 14:70-77.
123. Aita V.M., Liang X.H., Murty V.V., Pincus D.L., Yu W., Cayanis E., Kalachikov S., Gilliam T.C., Levine B. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 1999, 59:59-65.
124. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676.
125. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., Rosen J., Eskelinen E.L., Mizushima N., Ohsumi Y., Cattoretti G., Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 2003, 112:1809-1820.
126. Yue Z., Jin S., Yang C., Levine A.J., Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl Acad. Sci. USA 2003, 100:15077-15082.
127. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
128. Ciechomska I.A., Goemans G.C., Skepper J.N., Tolkovsky A.M. Bcl-2 complexed with Beclin-1 maintains full anti-apoptotic function. Oncogene 2009, 28:2128-2141.
129. Maiuri M.C., Le Toumelin G., Criollo A., Rain J.C., Gautier F., Juin P., Tasdemir E., Pierron G., Troulinaki K., Tavernarakis N., Hickman J.A., Geneste O., Kroemer G. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 2007, 26:2527-2539.
130. Maiuri M.C., Criollo A., Tasdemir E., Vicencio J.M., Tajeddine N., Hickman J.A., Geneste O., Kroemer G. BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X(L). Autophagy 2007, 3:374-376.
131. Papandreou I., Lim A.L., Laderoute K., Denko N.C. Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L. Cell Death Differ. 2008, 15:1572-1581.
132. Daido S., Kanzawa T., Yamamoto A., Takeuchi H., Kondo Y., Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 2004, 64:4286-4293.
133. S. Ghavami, M. Eshragi, S.R. Ande, W.J. Chazin, T. Klonisch, A.J. Halayko, K.D. McNeill, M. Hashemi, C. Kerkhoff, M. Los, S100A8/A9 induces autophagy and apoptosis via ROS-mediated cross-talk between mitochondria and lysosomes that involves BNIP3, Cell Res. 20 (2010) 314-331.
134. Mazure N.M., Pouyssegur J. Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia. Autophagy 2009, 5:868-869.
135. Bellot G., Garcia-Medina R., Gounon P., Chiche J., Roux D., Pouyssegur J., Mazure N.M. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 2009, 29:2570-2581.
136. Band M., Joel A., Hernandez A., Avivi A. Hypoxia-induced BNIP3 expression and mitophagy: in vivo comparison of the rat and the hypoxia-tolerant mole rat. Spalax ehrenbergi. FASEB J. 2009, 23:2327-2335.
137. Wei Y., Pattingre S., Sinha S., Bassik M., Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 2008, 30:678-688.
138. Criollo A., Vicencio J.M., Tasdemir E., Maiuri M.C., Lavandero S., Kroemer G. The inositol trisphosphate receptor in the control of autophagy. Autophagy 2007, 3:350-353.
139. Criollo A., Maiuri M.C., Tasdemir E., Vitale I., Fiebig A.A., Andrews D., Molgo J., Diaz J., Lavandero S., Harper F., Pierron G., di Stefano D., Rizzuto R., Szabadkai G., Kroemer G. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ. 2007, 14:1029-1039.
140. Hoyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., Bianchi K., Fehrenbacher N., Elling F., Rizzuto R., Mathiasen I.S., Jaattela M. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 2007, 25:193-205.
141. Hoyer-Hansen M., Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007, 14:1576-1582.
142. Kouroku Y., Fujita E., Tanida I., Ueno T., Isoai A., Kumagai H., Ogawa S., Kaufman R.J., Kominami E., Momoi T. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007, 14:230-239.
143. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback J.A., Urano F., Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 2006, 26:9220-9231.
144. Yorimitsu T., Nair U., Yang Z., Klionsky D.J. Endoplasmic reticulum stress triggers autophagy. J. Biol. Chem. 2006, 281:30299-30304.
145. Bernales S., McDonald K.L., Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 2006, 4:e423.
146. Ding W.X., Ni H.M., Gao W., Hou Y.F., Melan M.A., Chen X., Stolz D.B., Shao Z.M., Yin X.M. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J. Biol. Chem. 2007, 282:4702-4710.
147. Ding W.X., Ni H.M., Gao W., Yoshimori T., Stolz D.B., Ron D., Yin X.M. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 2007, 171:513-524.
148. T. Rzymski, M. Milani, L. Pike, F. Buffa, H.R. Mellor, L. Winchester, I. Pires, E. Hammond, I. Ragoussis, A.L. Harris, Regulation of autophagy by ATF4 in response to severe hypoxia, Oncogene 29 (2010) 4424-4435.
149. K.M. Rouschop, T. van den Beucken, L. Dubois, H. Niessen, J. Bussink, K. Savelkouls, T. Keulers, H. Mujcic, W. Landuyt, J.W. Voncken, P. Lambin, A.J. van der Kogel, M. Koritzinsky, B.G. Wouters, The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5, J. Clin. Invest. 120 (2010) 127-141.
150. Klee M., Pimentel-Muinos F.X. Bcl-X(L) specifically activates Bak to induce swelling and restructuring of the endoplasmic reticulum. J. Cell Biol. 2005, 168:723-734.
151. Karbowski M., Norris K.L., Cleland M.M., Jeong S.Y., Youle R.J. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006, 443:658-662.
152. Nakajima K., Hirose H., Taniguchi M., Kurashina H., Arasaki K., Nagahama M., Tani K., Yamamoto A., Tagaya M. Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion. EMBO J. 2004, 23:3216-3226.
153. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
154. Hayashi T., Rizzuto R., Hajnoczky G., Su T.P. MAM: more than just a housekeeper. Trends Cell Biol. 2009, 19:81-88.
155. T. Simmen, E.M. Lynes, K. Gesson, G. Thomas, Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM), Biochim. Biophys. Acta 1798 (2010) 1465-1473.
156. Schuler M., Green D.R. Transcription, apoptosis and p53: catch-22. Trends Genet. 2005, 21:182-187.
157. Zinkel S., Gross A., Yang E. BCL2 family in DNA damage and cell cycle control. Cell Death Differ. 2006, 13:1351-1359.
158. Kamer I., Sarig R., Zaltsman Y., Niv H., Oberkovitz G., Regev L., Haimovich G., Lerenthal Y., Marcellus R.C., Gross A. Proapoptotic BID is an ATM effector in the DNA-damage response. Cell 2005, 122:593-603.
159. Zinkel S.S., Hurov K.E., Ong C., Abtahi F.M., Gross A., Korsmeyer S.J. A role for proapoptotic BID in the DNA-damage response. Cell 2005, 122:579-591.
160. Bruey J.M., Bruey-Sedano N., Luciano F., Zhai D., Balpai R., Xu C., Kress C.L., Bailly-Maitre B., Li X., Osterman A., Matsuzawa S., Terskikh A.V., Faustin B., Reed J.C. Bcl-2 and Bcl-XL regulate proinflammatory caspase-1 activation by interaction with NALP1. Cell 2007, 129:45-56.
161. Danial N.N., Gramm C.F., Scorrano L., Zhang C.Y., Krauss S., Ranger A.M., Datta S.R., Greenberg M.E., Licklider L.J., Lowell B.B., Gygi S.P., Korsmeyer S.J. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 2003, 424:952-956.
162. Danial N.N., Walensky L.D., Zhang C.Y., Choi C.S., Fisher J.K., Molina A.J., Datta S.R., Pitter K.L., Bird G.H., Wikstrom J.D., Deeney J.T., Robertson K., Morash J., Kulkarni A., Neschen S., Kim S., Greenberg M.E., Corkey B.E., Shirihai O.S., Shulman G.I., Lowell B.B., Korsmeyer S.J. Dual role of proapoptotic BAD in insulin secretion and beta cell survival. Nat. Med. 2008, 14:144-153.
163. Kim H., Tu H.C., Ren D., Takeuchi O., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Stepwise activation of BAX and BAK by tBID. BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 2009, 36:487-499.
164. Wang H.Q., Takahashi R. Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. Antioxid. Redox Signal. 2007, 9:553-561.
165. Ghribi O. The role of the endoplasmic reticulum in the accumulation of beta-amyloid peptide in Alzheimer's disease. Curr. Mol. Med. 2006, 6:119-133.
166. Hetz C.A., Soto C. Stressing out the ER: a role of the unfolded protein response in prion-related disorders. Curr. Mol. Med. 2006, 6:37-43.
167. Nassif M., Matus S., Castillo K., Hetz C. Amyotrophic lateral sclerosis pathogenesis: a journey through the secretory pathway. Antioxid Redox Signal 2010, 13:1955-1989.
168. R. Vidal, B. Caballero, A. Couve, C. Hetz, Converging pathways in the occurrence of endoplasmic reticulum (ER) stress in Huntington's disease., Curr. Mol. Med. 11 (2011).
169. Garcia-Martinez J.M., Perez-Navarro E., Xifro X., Canals J.M., Diaz-Hernandez M., Trioulier Y., Brouillet E., Lucas J.J., Alberch J. BH3-only proteins Bid and Bim(EL) are differentially involved in neuronal dysfunction in mouse models of Huntington's disease. J. Neurosci. Res. 2007, 85:2756-2769.
170. Leon R., Bhagavatula N., Ulukpo O., McCollum M., Wei J. BimEL as a possible molecular link between proteasome dysfunction and cell death induced by mutant huntingtin. Eur. J. Neurosci. 2010, 31:1915-1925.
171. Hetz C., Thielen P., Fisher J., Pasinelli P., Brown R.H., Korsmeyer S., Glimcher L. The proapoptotic BCL-2 family member BIM mediates motoneuron loss in a model of amyotrophic lateral sclerosis. Cell Death Differ. 2007, 14:1386-1389.
172. Kieran D., Woods I., Villunger A., Strasser A., Prehn J.H. Deletion of the BH3-only protein puma protects motoneurons from ER stress-induced apoptosis and delays motoneuron loss in ALS mice. Proc. Natl Acad. Sci. USA 2007, 104:20606-20611.
173. Ness J.M., Harvey C.A., Strasser A., Bouillet P., Klocke B.J., Roth K.A. Selective involvement of BH3-only Bcl-2 family members Bim and Bad in neonatal hypoxia-ischemia. Brain Res. 2006, 1099:150-159.
174. Kuroki K., Virard I., Concannon C.G., Engel T., Woods I., Taki W., Plesnila N., Henshall D.C., Prehn J.H. Effects of transient focal cerebral ischemia in mice deficient in puma. Neurosci. Lett. 2009, 451:237-240.
175. Concannon C.G., Ward M.W., Bonner H.P., Kuroki K., Tuffy L.P., Bonner C.T., Woods I., Engel T., Henshall D.C., Prehn J.H. NMDA receptor-mediated excitotoxic neuronal apoptosis in vitro and in vivo occurs in an ER stress and PUMA independent manner. J. Neurochem. 2008, 105:891-903.
176. Oltersdorf T., Elmore S.W., Shoemaker A.R., Armstrong R.C., Augeri D.J., Belli B.A., Bruncko M., Deckwerth T.L., Dinges J., Hajduk P.J., Joseph M.K., Kitada S., Korsmeyer S.J., Kunzer A.R., Letai A., Li C., Mitten M.J., Nettesheim D.G., Ng S., Nimmer P.M., O'Connor J.M., Oleksijew A., Petros A.M., Reed J.C., Shen W., Tahir S.K., Thompson C.B., Tomaselli K.J., Wang B., Wendt M.D., Zhang H., Fesik S.W., Rosenberg S.H. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435:677-681.
177. Nguyen M., Marcellus R.C., Roulston A., Watson M., Serfass L., Murthy Madiraju S.R., Goulet D., Viallet J., Belec L., Billot X., Acoca S., Purisima E., Wiegmans A., Cluse L., Johnstone R.W., Beauparlant P., Shore G.C. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc. Natl Acad. Sci. USA 2007, 104:19512-19517.
178. Walensky L.D., Kung A.L., Escher I., Malia T.J., Barbuto S., Wright R.D., Wagner G., Verdine G.L., Korsmeyer S.J. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 2004, 305:1466-1470.
179. Walensky L.D., Pitter K., Morash J., Oh K.J., Barbuto S., Fisher J., Smith E., Verdine G.L., Korsmeyer S.J. A stapled BID BH3 helix directly binds and activates BAX. Mol. Cell 2006, 24:199-210.
180. Letai A. Pharmacological manipulation of Bcl-2 family members to control cell death. J. Clin. Invest. 2005, 115:2648-2655.