Noncanonical functions of BCL-2 proteins in the nervous system

Advances in Experimental Medicine and Biology

Volumn 687, Issue , 2010, Pages 115-129

  Lamb, Heather M ^a   Hardwick, J Marie ^a  

^a Department of Molec Microb and Immunol ^*

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; GUANOSINE TRIPHOSPHATASE; KAINIC ACID; MITOFUSIN 2; NUCLEAR RECEPTOR NUR77; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; SUPEROXIDE DISMUTASE; VOLTAGE DEPENDENT ANION CHANNEL 2;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CATALYSIS; CELL DEATH; CELL PROTECTION; CHROMOSOME TRANSLOCATION; EMBRYO DEVELOPMENT; GENE INTERACTION; GENETIC VARIABILITY; HETEROZYGOSITY; HIPPOCAMPUS; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOLECULAR DYNAMICS; NERVOUS SYSTEM; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; SEIZURE; SEQUENCE HOMOLOGY; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; NEUROLOGIC DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SYNAPSE;

MUS;

ANIMALS; CELL DEATH; HUMANS; NERVOUS SYSTEM; NERVOUS SYSTEM DISEASES; NEURONS; PROTO-ONCOGENE PROTEINS C-BCL-2; SEIZURES; SYNAPSES;

EID: 77958121925     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-6706-0_7     Document Type: Article

References (140)

1. Tsujimoto Y, Cossman J, Jaffe E et al. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985; 228:1440-1443. (Pubitemid 15041322)
2. Ohno H, Fukuhara S, Takahashi R et al. C-yes and bcl-2 genes located on 18q21.3 in a follicular lymphoma cell line carrying a t(14;18) chromosomal translocation. Int J Cancer 1987; 39:785-788. (Pubitemid 17087883)
3. Graninger WB, Seto M, Boutain B et al. Expression of bcl-2 and bcl-2-ig fusion transcripts in normal and neoplastic cells. J Clin Invest 1987; 80:1512-1515. (Pubitemid 18027800)
4. Weiss LM, Warnke RA, Sklar J et al. Molecular analysis of the t(14;18) chromosomal translocation in malignant lymphomas. N Engl J Med 1987; 317:1185-1189. (Pubitemid 17150330)
5. Hengartner MO, Ellis RE, Horvitz HR. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 1992; 356:494-499.
6. Yuan J, Shaham S, Ledoux S et al. The c. Elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993; 75:641-652. (Pubitemid 23346363)
7. Vaux DL, Cory S, Adams JM. BCL-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize preb cells. Nature 1988; 335:440-442.
8. Henderson S, Huen D, Rowe M et al. Epstein-barr virus-coded bhrf1 protein, a viral homologue of bcl-2, protects human b-cells from programmed cell death. Proc Natl Acad Sci USA 1993; 90:8479-8483. (Pubitemid 23277692)
9. Adams JM, Cory S. The bcl-2 protein family: Arbiters of cell survival. Science 1998; 281:1322-1326. (Pubitemid 28406819)
10. Youle RJ, Strasser A. The bcl-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9:47-59.
11. Fletcher JI, Meusburger S, Hawkins CJ et al. Apoptosis is triggered when prosurvival bcl-2 proteins cannot restrain bax. Proc Natl Acad Sci USA 2008; 105:18081-18087.
12. Kuwana T, Mackey MR, Perkins G et al. Bid, bax and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 2002; 111:331-342. (Pubitemid 35341388)
13. Antonsson B, Montessuit S, Lauper S et al. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 2000; 345(Pt 2):271-278. (Pubitemid 30077167)
14. Budihardjo I, Oliver H, Lutter M et al. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 1999; 15:269-290. (Pubitemid 32250377)
15. Antonsson B, Conti F, Ciavatta A et al. Inhibition of bax channel-forming activity by bcl-2. Science 1997; 277:370-372. (Pubitemid 27450709)
16. Kvansakul M, Yang H, Fairlie WD et al. Vaccinia virus anti-apoptotic f1l is a novel bcl-2-like domain-swapped dimer that binds a highly selective subset of bh3-containing death ligands. Cell Death Differ 2008; 15:1564-1571.
17. Graham SC, Bahar MW, Cooray S et al. Vaccinia virus proteins a52 and b14 share a bcl-2-like fold but have evolved to inhibit nf-kappab rather than apoptosis. PLoS Pathog 2008; 4:e1000128.
18. Galindo KA, Lu WJ, Park JH et al. The bax/bak ortholog in drosophila, debcl, exerts limited control over programmed cell death. Development 2009; 136:275-283.
19. Bellows DS, Howell M, Pearson C et al. Epstein-barr virus balf1 is a bcl-2-like antagonist of the herpesvirus antiapoptotic bcl-2 proteins. J Virol 2002; 76:2469-2479. (Pubitemid 34150715)
20. Huang DC, Strasser A. Bh3-only proteins-essential initiators of apoptotic cell death. Cell 2000; 103:839-842.
21. Cheng EH, Wei MC, Weiler S et al. BCL-2, bcl-x(l) sequester bh3 domain-only molecules preventing bax- and bak-mediated mitochondrial apoptosis. Mol Cell 2001; 8:705-711. (Pubitemid 32946946)
22. Letai A, Bassik MC, Walensky LD et al. Distinct bh3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002; 2:183-192. (Pubitemid 41043974)
23. Billen LP, Kokoski CL, Lovell JF et al. Bcl-xl inhibits membrane permeabilization by competing with bax. PLoS Biol 2008; 6:e147.
24. Day CL, Smits C, Fan FC et al. Structure of the bh3 domains from the p53-inducible bh3-only proteins noxa and puma in complex with mcl-1. J Mol Biol 2008; 380:958-971.
25. Hinds MG, Smits C, Fredericks-Short R et al. Bim, bad and bmf: Intrinsically unstructured bh3-only proteins that undergo a localized conformational change upon binding to prosurvival bcl-2 targets. Cell Death Differ 2007; 14:128-136. (Pubitemid 44911900)
26. Oltersdorf T, Elmore SW, Shoemaker AR et al. An inhibitor of bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435:677-681. (Pubitemid 40825512)
27. Deng J, Carlson N, Takeyama K et al. Bh3 profiling identifies three distinct classes of apoptotic blocks to predict response to abt-737 and conventional chemotherapeutic agents. Cancer Cell 2007; 12:171-185. (Pubitemid 47199122)
28. Park CM, Bruncko M, Adickes J et al. Discovery of an orally bioavailable small molecule inhibitor of prosurvival b-cell lymphoma 2 proteins. J Med Chem 2008; 51:6902-6915.
29. Danial NN, Walensky LD, Zhang CY et al. Dual role of proapoptotic bad in insulin secretion and beta cell survival. Nat Med 2008; 14:144-153. (Pubitemid 351214557)
30. Gavathiotis E, Suzuki M, Davis ML et al. Bax activation is initiated at a novel interaction site. Nature 2008; 455:1076-1081.
31. Zhong Q, Gao W, Du F et al. Mule/arf-bp1, a bh3-only e3 ubiquitin ligase, catalyzes the polyubiquitination of mcl-1 and regulates apoptosis. Cell 2005; 121:1085-1095. (Pubitemid 40884398)
32. Oberstein A, Jeffrey PD, Shi Y. Crystal structure of the bcl-xl-beclin 1 peptide complex: Beclin 1 is a novel bh3-only protein. J Biol Chem 2007; 282:13123-13132. (Pubitemid 47100641)
33. Mihara M, Erster S, Zaika A et al. P53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11:577-590. (Pubitemid 36385115)
34. White C, Li C, Yang J et al. The endoplasmic reticulum gateway to apoptosis by bcl-x(l) modulation of the insp3r. Nat Cell Biol 2005; 7:1021-1028. (Pubitemid 41486277)
35. Puthalakath H, Villunger A, O'Reilly LA et al. Bmf: A proapoptotic bh3-only protein regulated by interaction with the myosin v actin motor complex, activated by anoikis. Science 2001; 293:1829-1832. (Pubitemid 32845780)
36. Pattingre S, Tassa A, Qu X et al. BCL-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell 2005; 122:927-939. (Pubitemid 41345209)
37. Delivani P, Adrain C, Taylor RC et al. Role for ced-9 and egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol Cell 2006; 21:761-773. (Pubitemid 43376127)
38. Guo JY, Yamada A, Kajino T et al. Aven-dependent activation of atm following DNA damage. Curr Biol 2008; 18:933-942.
39. Cheng EH, Levine B, Boise LH et al. Bax-independent inhibition of apoptosis by bcl-xl. Nature 1996; 379:554-556.
40. Cheng EH, Sheiko TV, Fisher JK et al. Vdac2 inhibits bak activation and mitochondrial apoptosis. Science 2003; 301:513-517. (Pubitemid 36900308)
41. Kim H, Rafiuddin-Shah M, Tu HC et al. Hierarchical regulation of mitochondrion-dependent apoptosis by bcl-2 subfamilies. Nat Cell Biol 2006; 8:1348-1358. (Pubitemid 44835109)
42. Hsu YT, Youle RJ. Nonionic detergents induce dimerization among members of the bcl-2 family. J Biol Chem 1997; 272:13829-13834. (Pubitemid 27224822)
43. Basanez G, Nechushtan A, Drozhinin O et al. Bax, but not bcl-xl, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad Sci USA 1999; 96:5492-5497. (Pubitemid 29234645)
44. Basanez G, Sharpe JC, Galanis J et al. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 2002; 277:49360-49365. (Pubitemid 36014367)
45. Kane DJ, Ord T, Anton R et al. Expression of bcl-2 inhibits necrotic neural cell death. J Neurosci Res 1995; 40:269-275.
46. Dickman MB, Park YK, Oltersdorf T et al. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA 2001; 98:6957-6962. (Pubitemid 32538324)
47. Krajewska M, Mai JK, Zapata JM et al. Dynamics of expression of apoptosis-regulatory proteins bid, bcl-2, bcl-x, bax and bak during development of murine nervous system. Cell Death Differ 2002; 9:145-157. (Pubitemid 34144774)
48. Krajewski S, Krajewska M, Shabaik A et al. Immunohistochemical determination of in vivo distribution of bax, a dominant inhibitor of bcl-2. Am J Pathol 1994; 145:1323-1336. (Pubitemid 24378488)
49. Krajewski S, Krajewska M, Shabaik A et al. Immunohistochemical analysis of in vivo patterns of bcl-x expression. Cancer Res 1994; 54:5501-5507. (Pubitemid 24346233)
50. Arbour N, Vanderluit JL, Le Grand JN et al. Mcl-1 is a key regulator of apoptosis during cns development and after DNA damage. J Neurosci 2008; 28:6068-6078.
51. O'Reilly LA, Print C, Hausmann G et al. Tissue expression and subcellular localization of the pro-survival molecule bcl-w. Cell Death Differ 2001; 8:486-494. (Pubitemid 32492769)
52. Uo T, Kinoshita Y, Morrison RS. Neurons exclusively express n-bak, a bh3 domain-only bak isoform that promotes neuronal apoptosis. J Biol Chem 2005; 280:9065-9073. (Pubitemid 40409600)
53. Fu NY, Sukumaran SK, Kerk SY et al. Baxbeta: A constitutively active human bax isoform that is under tight regulatory control by the proteasomal degradation mechanism. Mol Cell 2009; 33:15-29.
54. Lindsten T, Ross AJ, King A et al. 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. (Pubitemid 32045931)
55. Whitmore AV, Lindsten T, Raff MC et al. The proapoptotic proteins bax and bak are not involved in wallerian degeneration. Cell Death Differ 2003; 10:260-261. (Pubitemid 36553469)
56. Glebova NO, Ginty DD. Heterogeneous requirement of ngf for sympathetic target innervation in vivo. J Neurosci 2004; 24:743-751. (Pubitemid 38166500)
57. Liu QA, Shio H. Mitochondrial morphogenesis, dendrite development and synapse formation in cerebellum require both bcl-w and the glutamate receptor delta2. PLoS Genet 2008; 4:e1000097.
58. Murphy B, Dunleavy M, Shinoda S et al. BCL-2 protects hippocampus during experimental status epilepticus. Am J Pathol 2007; 171:1258-1268. (Pubitemid 47582899)
59. Veis DJ, Sorenson CM, Shutter JR et al. BCL-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys and hypopigmented hair. Cell 1993; 75:229-240. (Pubitemid 23320287)
60. Merry DE, Veis DJ, Hickey WF et al. BCL-2 protein expression is widespread in the developing nervous system and retained in the adult pns. Development 1994; 120:301-311.
61. Michaelidis TM, Sendtner M, Cooper JD et al. Inactivation of bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 1996; 17:75-89. (Pubitemid 26251593)
62. Motoyama N, Wang F, Roth KA et al. Massive cell death of immature hematopoietic cells and neurons in bcl-x-deficient mice. Science 1995; 267:1506-1510.
63. Zhang J, Chen YB, Hardwick JM et al. Magnetic resonance diffusion tensor microimaging reveals a role for bcl-x in brain development and homeostasis. J Neurosci 2005; 25:1881-1888. (Pubitemid 40292056)
64. Savitt JM, Jang SS, Mu W et al. Bcl-x is required for proper development of the mouse substantia nigra. J Neurosci 2005; 25:6721-6728. (Pubitemid 41023139)
65. Berman SB, Chen YB, Qi B et al. Bcl-xl increases mitochondrial fission, fusion and biomass in neurons. J Cell Biol 2009; 184:707-719.
66. Shindler KS, Latham CB, Roth KA. Bax deficiency prevents the increased cell death of immature neurons in bcl-x-deficient mice. J Neurosci 1997; 17:3112-3119. (Pubitemid 27175823)
67. Akhtar RS, Ness JM, Roth KA. BCL-2 family regulation of neuronal development and neurodegeneration. Biochim Biophys Acta 2004; 1644:189-203. (Pubitemid 38281275)
68. Roth KA, D'Sa C. Apoptosis and brain development. Ment Retard Dev Disabil Res Rev 2001; 7:261-266. (Pubitemid 33108264)
69. Akhtar RS, Geng Y, Klocke BJ et al. Bh3-only proapoptotic bcl-2 family members noxa and puma mediate neural precursor cell death. J Neurosci 2006; 26:7257-7264.
70. Geng Y, Akhtar RS, Shacka JJ et al. P53 transcription-dependent and -independent regulation of cerebellar neural precursor cell apoptosis. J Neuropathol Exp Neurol 2007; 66:66-74. (Pubitemid 46066790)
71. Akhtar RS, Klocke BJ, Strasser A et al. Loss of bh3-only protein bim inhibits apoptosis of hemopoietic cells in the fetal liver and male germ cells but not neuronal cells in bcl-x-deficient mice. J Histochem Cytochem 2008; 56:921-927.
72. Wagner KU, Claudio E, Rucker EB, 3rd et al. Conditional deletion of the bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 2000; 127:4949-4958.
73. Qi B, Hardwick JM. A bcl-xl timer sets platelet life span. Cell 2007; 128:1035-1036. (Pubitemid 46427881)
74. Mason KD, Carpinelli MR, Fletcher JI et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128:1173-1186. (Pubitemid 46427871)
75. Doonan F, Donovan M, Gomez-Vicente V et al. Bim expression indicates the pathway to retinal cell death in development and degeneration. J Neurosci 2007; 27:10887-10894. (Pubitemid 47535856)
76. Hetz C, Thielen P, Fisher J et al. The proapoptotic bcl-2 family member bim mediates motoneuron loss in a model of amyotrophic lateral sclerosis. Cell Death Differ 2007; 14:1386-1389. (Pubitemid 46965267)
77. McKernan DP, Cotter TG. A critical role for bim in retinal ganglion cell death. J Neurochem 2007; 102:922-930. (Pubitemid 47057287)
78. Bouillet P, Cory S, Zhang LC et al. Degenerative disorders caused by bcl-2 deficiency prevented by loss of its bh3-only antagonist bim. Dev Cell 2001; 1:645-653. (Pubitemid 33586117)
79. Lewis J, Wesselingh SL, Griffin DE et al. Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol 1996; 70:1828-1835. (Pubitemid 26062946)
80. Lewis J, Oyler GA, Ueno K et al. Inhibition of virus-induced neuronal apoptosis by bax. Nat Med 1999; 5:832-835. (Pubitemid 29318620)
81. Levine B, Huang Q, Isaacs JT et al. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 1993; 361:739-742. (Pubitemid 23070484)
82. Levine B, Goldman JE, Jiang HH et al. Bc1-2 protects mice against fatal alphavirus encephalitis. Proc Natl Acad Sci USA 1996; 93:4810-4815. (Pubitemid 26162833)
83. Irusta PM, Hardwick JM. Neuronal apoptosis pathways in sindbis virus encephalitis. Prog Mol Subcell Biol 2004; 36:71-93.
84. Cheng EH, Kirsch DG, Clem RJ et al. Conversion of bcl-2 to a bax-like death effector by caspases. Science 1997; 278:1966-1968. (Pubitemid 28013242)
85. Kirsch DG, Doseff A, Chau BN et al. Caspase-3-dependent cleavage of bcl-2 promotes release of cytochrome c. J Biol Chem 1999; 274:21155-21161.
86. Clem RJ, Cheng EH, Karp CL et al. Modulation of cell death by bcl-xl through caspase interaction. Proc Natl Acad Sci USA 1998; 95:554-559.
87. Grandgirard D, Studer E, Monney L et al. Alphaviruses induce apoptosis in bcl-2-overexpressing cells: Evidence for a caspase-mediated, proteolytic inactivation of bcl-2. EMBO J 1998; 17:1268-1278. (Pubitemid 28105506)
88. Basanez G, Zhang J, Chau BN et al. Pro-apoptotic cleavage products of bcl-xl form cytochrome c-conducting pores in pure lipid membranes. J Biol Chem 2001; 276:31083-31091.
89. Kelekar A, Thompson CB. BCL-2-family proteins: The role of the bh3 domain in apoptosis. Trends Cell Biol 1998; 8:324-330. (Pubitemid 28362590)
90. Seo SY, Chen YB, Ivanovska I et al. Bad is a pro-survival factor prior to activation of its pro-apoptotic function. J Biol Chem 2004; 279:42240-42249.
91. Condorelli F, Salomoni P, Cotteret S et al. Caspase cleavage enhances the apoptosis-inducing effects of bad. Mol Cell Biol 2001; 21:3025-3036. (Pubitemid 32298370)
92. Datta SR, Dudek H, Tao X et al. Akt phosphorylation of bad couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91:231-241. (Pubitemid 27456390)
93. Wood DE, Thomas A, Devi LA et al. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 1998; 17:1069-1078. (Pubitemid 28444591)
94. Chen D, Zhou Q. Caspase cleavage of bimel triggers a positive feedback amplification of apoptotic signaling. Proc Natl Acad Sci USA 2004; 101:1235-1240. (Pubitemid 38182672)
95. Gomez-Bougie P, Wuilleme-Toumi S, Menoret E et al. Noxa up-regulation and mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res 2007; 67:5418-5424. (Pubitemid 46997282)
96. Michels J, Johnson PW, Packham G. Mcl-1. Int J Biochem Cell Biol 2005; 37:267-271. (Pubitemid 39330187)
97. Michels J, O'Neill JW, Dallman CL et al. Mcl-1 is required for akata6 b-lymphoma cell survival and is converted to a cell death molecule by efficient caspase-mediated cleavage. Oncogene 2004; 23:4818-4827. (Pubitemid 38932154)
98. Li H, Zhu H, Xu CJ et al. Cleavage of bid by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis. Cell 1998; 94:491-501. (Pubitemid 28391865)
99. Gil-Parrado S, Fernandez-Montalvan A, Assfalg-Machleidt I et al. Ionomycin-activated calpain triggers apoptosis. A probable role for bcl-2 family members. J Biol Chem 2002; 277:27217-27226. (Pubitemid 34951738)
100. Qi B, Hardwick JM. BCL-2 turns deadly. Nat Chem Biol 2008; 4:722-723.
101. Kolluri SK, Zhu X, Zhou X et al. A short nur77-derived peptide converts bcl-2 from a protector to a killer. Cancer Cell 2008; 14:285-298.
102. Lin B, Kolluri SK, Lin F et al. Conversion of bcl-2 from protector to killer by interaction with nuclear orphan receptor nur77/tr3. Cell 2004; 116:527-540. (Pubitemid 38264430)
103. Luciano F, Krajewska M, Ortiz-Rubio P et al. Nur77 converts phenotype of bcl-b, an antiapoptotic protein expressed in plasma cells and myeloma. Blood 2007; 109:3849-3855. (Pubitemid 46641736)
104. Thompson J, Winoto A. During negative selection, nur77 family proteins translocate to mitochondria where they associate with bcl-2 and expose its proapoptotic bh3 domain. J Exp Med 2008; 205:1029-1036. (Pubitemid 351679679)
105. Hickman JA, Hardwick JM, Kaczmarek LK et al. Bcl-xl inhibitor abt-737 reveals a dual role for bcl-xl in synaptic transmission. J Neurophysiol 2008; 99:1515-1522. (Pubitemid 351413726)
106. Ubol S, Tucker PC, Griffin DE et al. Neurovirulent strains of alphavirus induce apoptosis in bcl-2-expressing cells: Role of a single amino acid change in the e2 glycoprotein. Proc Natl Acad Sci USA 1994; 91:5202-5206. (Pubitemid 24177821)
107. Levine B, Hardwick JM, Griffin DE. Persistence of alphaviruses in vertebrate hosts. Trends Microbiol 1994; 2:25-28. (Pubitemid 24043632)
108. Griffin DE, Hardwick JM. Perspective: Virus infections and the death of neurons. Trends Microbiol 1999; 7:155-160. (Pubitemid 29229901)
109. Griffin DE, Levine B, Ubol S et al. The effects of alphavirus infection on neurons. Ann Neurol 1994; 35 Suppl:S23-27. (Pubitemid 24153861)
110. Hardwick JM, Levine B. Sindbis virus vector system for functional analysis of apoptosis regulators. Methods Enzymol 2000; 322:492-508. (Pubitemid 30482081)
111. Fannjiang Y, Kim CH, Huganir RL et al. Bak alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev Cell 2003; 4:575-585. (Pubitemid 36437563)
112. Middleton G, Davies AM. Populations of ngf-dependent neurones differ in their requirement for bax to undergo apoptosis in the absence of ngf/trka signalling in vivo. Development 2001; 128:4715-4728. (Pubitemid 33138582)
113. Middleton G, Nunez G, Davies AM. Bax promotes neuronal survival and antagonises the survival effects of neurotrophic factors. Development 1996; 122:695-701.
114. Senoo-Matsuda N, Igaki T, Miura M. Bax-like protein drob-1 protects neurons from expanded polyglutamine-induced toxicity in drosophila. EMBO J 2005; 24:2700-2713. (Pubitemid 41076325)
115. Chew SK, Chen P, Link N et al. Genome-wide silencing in drosophila captures conserved apoptotic effectors. Nature 2009.
116. Sevrioukov EA, Burr J, Huang EW et al. Drosophila bcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 2007; 45:184-193. (Pubitemid 46676761)
117. Morrison RS, Wenzel HJ, Kinoshita Y et al. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 1996; 16:1337-1345.
118. Holcik M, Thompson CS, Yaraghi Z et al. The hippocampal neurons of neuronal apoptosis inhibitory protein 1 (naip1)-deleted mice display increased vulnerability to kainic acid-induced injury. Proc Natl Acad Sci USA 2000; 97:2286-2290. (Pubitemid 30134061)
119. Jonas EA, Hoit D, Hickman JA et al. Modulation of synaptic transmission by the bcl-2 family protein bcl-xl. J Neurosci 2003; 23:8423-8431. (Pubitemid 37129660)
120. Jonas EA, Hickman JA, Chachar M et al. Proapoptotic n-truncated bcl-xl protein activates endogenous mitochondrial channels in living synaptic terminals. Proc Natl Acad Sci USA 2004; 101:13590-13595. (Pubitemid 39238447)
121. Karbowski M, Norris KL, Cleland MM et al. Role of bax and bak in mitochondrial morphogenesis. Nature 2006; 443:658-662. (Pubitemid 44564703)
122. Jonas EA, Hickman JA, Hardwick JM et al. Exposure to hypoxia rapidly induces mitochondrial channel activity within a living synapse. J Biol Chem 2005; 280:4491-4497. (Pubitemid 40288615)
123. Jonas EA, Hardwick JM, Kaczmarek LK. Actions of bax on mitochondrial channel activity and on synaptic transmission. Antioxid Redox Signal 2005; 7:1092-1100. (Pubitemid 41232505)
124. Vander Heiden MG, Thompson CB. BCL-2 proteins: Regulators of apoptosis or of mitochondrial homeostasis? Nat Cell Biol 1999; 1:E209-216. (Pubitemid 129503663)
125. Vander Heiden MG, Li XX, Gottleib E et al. Bcl-xl promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J Biol Chem 2001; 276:19414-19419.
126. Vander Heiden MG, Chandel NS, Williamson EK et al. Bcl-xl regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997; 91:627-637. (Pubitemid 27513654)
127. Frank S. Dysregulation of mitochondrial fusion and fission: An emerging concept in neurodegeneration. Acta Neuropathol 2006; 111:93-100.
128. Detmer SA, Chan DC. Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 2007; 8:870-879. (Pubitemid 47622562)
129. Knott AB, Perkins G, Schwarzenbacher R et al. Mitochondrial fragmentation in neurodegeneration. Nat Rev Neurosci 2008; 9:505-518. (Pubitemid 351873464)
130. Jagasia R, Grote P, Westermann B et al. Drp-1-mediated mitochondrial fragmentation during egl-1-induced cell death in c. Elegans. Nature 2005; 433:754-760. (Pubitemid 40292985)
131. Li H, Chen Y, Jones AF et al. Bcl-xl induces drp1-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci USA 2008; 105:2169-2174. (Pubitemid 351439483)
132. Tan FJ, Husain M, Manlandro CM et al. Ced-9 and mitochondrial homeostasis in c. Elegans muscle. J Cell Sci 2008; 121:3373-3382.
133. Parone PA, James DI, Da Cruz S et al. Inhibiting the mitochondrial fission machinery does not prevent bax/bak-dependent apoptosis. Mol Cell Biol 2006; 26:7397-7408. (Pubitemid 44547692)
134. Breckenridge DG, Kang BH, Xue D. BCL-2 proteins egl-1 and ced-9 do not regulate mitochondrial fission or fusion in caenorhabditis elegans. Curr Biol 2009.
135. Berman SB, Pineda FJ, Hardwick JM. Mitochondrial fission and fusion dynamics: The long and short of it. Cell Death Differ 2008; 15:1147-1152. (Pubitemid 351850967)
136. Karbowski M, Youle RJ. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 2003; 10:870-880. (Pubitemid 36939697)
137. Sheridan C, Delivani P, Cullen SP et al. Bax- or bak-induced mitochondrial fission can be uncoupled from cytochrome c release. Mol Cell 2008; 31:570-585.
138. Twig G, Elorza A, Molina AJ et al. Fission and selective fusion govern segregation and elimination by autophagy. EMBO J 2008; 27:433-446. (Pubitemid 351161653)
139. Kowaltowski AJ, Cosso RG, Campos CB et al. Effect of bcl-2 overexpression on mitochondrial structure and function. J Biol Chem 2002; 277:42802-42807. (Pubitemid 35285655)
140. 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 2007; 3:374-376. (Pubitemid 46986348)