Regulators of apoptosis on the road to persistent alphavirus infection

Annual Review of Microbiology

Volumn 51, Issue , 1997, Pages 565-592

  Griffin, Diane E ^a   Hardwick, J Marie ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Apoptosis; Encephalitis; Virus; Virus persistence

Indexed keywords

PROTEIN BCL 2; TUMOR NECROSIS FACTOR RECEPTOR;

ALPHA VIRUS; APOPTOSIS; CELL DEATH; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA VIRUS INFECTION; SINDBIS VIRUS; VIRUS ENCEPHALITIS; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS VIRULENCE;

ALPHAVIRUS; ALPHAVIRUS INFECTIONS; ANIMALS; APOPTOSIS; CYSTEINE ENDOPEPTIDASES; ENCEPHALITIS, VIRAL; HUMANS; MICE; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, TUMOR NECROSIS FACTOR; SINDBIS VIRUS; VIRULENCE; VIRUS LATENCY; VIRUS REPLICATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

ALPHAVIRUS; ANIMALIA; RNA VIRUSES; SINDBIS VIRUS;

EID: 0030825748     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.micro.51.1.565     Document Type: Review

References (239)

1. Adamson DC, Dawson TM, Zink MC, Clements JE, Dawson VL. 1996. Neurovirulent simian immunodeficiency virus infection induces neuronal, endothelial, and glial apoptosis. Mol. Med. 2:417-28
2. Adamson DC, Wildemann B, Sasaki M, Glass JD, McArthur JC et al. 1996. Immunologic NO synthase: elevation in severe AIDS dementia and induction by HIV-1 gp41. Science 274:1917-21
3. Afonso CL, Neilan JG, Kutish GF, Rock DL. 1996. An african swine fever virus bcl-2 homolog, 5-HL, suppresses apoptotic cell death. J. Virol. 70:4858-63
4. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, et al. 1996. Human ICE/CED-3 protease nomenclature. Cell 87:171
5. Deleted in proof
6. Arends MJ, Morris RG, Wyllie AH. 1990. Apoptosis. The role of the endonuclease. Am. J. Pathol. 136:593-608
7. Baffy G, Miyashita T, Williamson JR, Reed JC. 1993. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced bcl-2 oncoprotein production. J. Biol. Chem. 268:6511-19
8. Beg AA, Baltimore D. 1996. An essential role for NF-kappaB in preventing TNF-induced cell death. Science 274:782-84
9. Bertin J, Mendrysa SM, LaCount DJ, Gaur S, Krebs JF, et al. 1996. Apoptotic suppression by baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like protease. J. Virol. 70:6251-59
10. Beyaert R, Vanhaesebroeck B, Declercq W, Vanlint J, Vandenabeele P, et al. 1995. Casein kinase-1 phosphorylates the p75 tumor necrosis factor receptor and negatively regulates tumor necrosis factor signaling for apoptosis. J. Biol. Chem. 270:23293-99
11. Birnbaum MJ, Clem RJ, Miller LK. 1994. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J. Virol. 68:2521-28
12. Bissonnette RP, Echeverri F, Mahboubi A, Green DR. 1992. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 359:552-54
13. Boise LH, Gonzalez-Garcia M, Postema CE, Ding LY, Lindsten T, et al. 1993. Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608
14. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1-and TNF receptor-induced cell death. Cell 85:803-15
15. Borden KLB, Boddy MN, Lally J, O'Reilly NJ, Martin S, et al. 1995. The solution structure of the RING finger domain from the acute promyelocytic leukaemia protooncoprotein PML. EMBO J. 14:1532-41
16. Boyd JM, Gallo GJ, Elangovan B, Houghton AB, Mastrom S, et al. 1995. Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11:1921-28
17. Brooks MA, Ali AN, Turner PC, Moyer RW. 1995. A rabbitpox virus serpin gene controls host range by inhibiting apoptosis in restrictive cells. J. Virol. 69:7688-98
18. Brun A, Rivas C, Esteban M, Escribano JM, Alonso C. 1996. African swine fever virus gene A179L, a viral homologue of bcl-2, protects cells from programmed cell death. Virology 225:227-30
19. Bump NJ, Hackett M, Hugunin M, Seshagiri S, Brady K, et al. 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-88
20. Caillet-Fauquet P, Perros M, Brandenburger A, Spegelaere P, Rommelaere J. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:2989-95
21. Casano FJ, Rolando AM, Mudgett JS, Molineaux SM. 1996. The structure and complete nucleotide sequence of the murine gene encoding interleukin-1 beta converting enzyme (ICE). Genomics 20:474-81
22. Cerretti DP, Kozlosky CJ, Mosley B, Nelson N, Vanness K, et al. 1992. Molecular cloning of the interleukin-1β converting enzyme. Science 256:97-100
23. Cheng EH, Levine B, Boise LH, Thompson CB, Hardwick JM. 1996. Bax-independent inhibition of apoptosis by Bcl-xL. Nature 379:554-56
24. Chen-Levy Z, Cleary ML. 1990. Membrane topology of the Bcl-2 protooncogenic protein demonstrated in vitro. J. Biol. Chem. 265:4929-33
25. Chen-Levy Z, Nourse J, Cleary ML. 1989. The bcl-2 candidate proto-oncogene product is a 24-kilodalton integral-membrane protein highly expressed in lymphoid cell lines and lymphomas carrying the t(14;18) translocation. Mol. Cell Biol. 9: 701-10
26. Chinnaiyan AM, O'Rourke K, Tewari M, Dixit VM. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81:505-12
27. Chinnaiyan AM, Orth K, O'Rourke K, Duan HJ, Poirier GG, Dixit VM. 1996. Molecular ordering of the cell death pathway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271:4573-76
28. Chinnaiyan AM, Tepper CG, Seidin MF, O'Rourke K, Kischfel FC, et al. 1996. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961-65
29. Chittenden T, Flemington C, Houghton AB, Ebb RG, Gallo GJ, et al. 1995. A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J. 14:5589-96
30. Chittenden T, Harrington EA, O'Connor R, Flemington C, Lutz RJ, et al. 1995. Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374:733-36
31. Cleary ML, Smith SD, Sklar J. 1986. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t( 14;18) translocation. Cell 47:19-28
32. Clem RJ, Fechheimer M, Miller LK. 1991. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254:1388-90
33. Clem RJ, Miller LK. 1993. Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J. Virol. 67:3730-38
34. Clem RJ, Miller LK. 1994. Control of programmed cell death by the baculovirus gene p35 and iap. Mol. Cell Biol. 14: 5212-22
35. Condreay LD, Brown DT. 1986. Exclusion of superinfecting homologous virus by Sindbis virus-infected Aedes albopictus (mosquito) cells. J. Virol. 58:81-86
36. Cowan WM, Fawcett JW, O'Leary DD, Stanfield BB. 1984. Regressive events in neurogenesis. Science 225:1258-65
37. Crook NE, Clem RJ, Miller LK. 1993. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67:2168-74
38. Darmon AJ, Nicholson DW, Bleackley RC. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme-B. Nature 377:446-48
39. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM, Snider WD, Korsmeyer SJ. 1996. Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-11
40. de Jong D, Prins FA, Mason DY, Reed JC, van Ommen GB, Kluin PM. 1994. Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells. Cancer Res. 54:256-60
41. Deng G, Podack ER. 1993. Suppression of apoptosis in a cytotoxic T-cell line by interleukin 2-mediated gene transcription and deregulated expression of the protooncogene bcl-2. Proc. Natl. Acad. Sci. USA 90:2189-93
42. 2+ pool depletion. Oncogene 12:2051-55
43. Driscoll M. 1992. Molecular genetics of cell death in the nematode Caenorhabditis elegans. J. Neurobiol. 23:1327-51
44. Duan H, Orth K, Chinnaiyan AM, Poirier GG, Froehlich CJ, et al. 1996. ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271:16720-24
45. Duckett CS, Nava VE, Gedrich RW, Clem RJ, Van Dogen JL et al. 1996. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J. 15:2685-94
46. Durant S, Homo F, Duval D. 1980. Calcium and A23187-induced cytolysis of mouse thymocytes. Biochem. Biophys. Res. Commun. 93:385-91
47. Duvall E, Wyllie AH. 1986. Death and the cell. Immunol. Today 7:115-19
48. Enari M, Talanian RV, Wong WW, Nagata S. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380:723-26
49. Esolen LM, Park SW, Hardwick JM, Griffin DE. 1995. Apoptosis as a cause of death in measles-virus-infected cells. J. Virol. 69:3955-58
50. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM Jr. 1994. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127:1717-27
51. Faucheu C, Diu A, Chan AWE, Blanchet AM, Miossec C, et al. 1995. A novel human protease similar to the interleukin-1β converting enzyme induces apoptosis in transfected cells. EMBO J. 14:1914-22
52. Freeman RS, Estus S, Johnson EM Jr. 1994. Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12:343-55
53. Frolov I, Schlesinger S. 1994. Comparison of the effects of Sindbis virus and Sindbis virus replicons on host cell protein synthesis and cytopathogenicity in BHK cells. J. Virol. 68:1721-27
54. Gagliardini V, Fernandez P-A, Lee RKK, Drexler HCA, Rotello RJ, et al. 1994. Prevention of vertebrate neuronal death by the crmA gene. Science 263:826-28
55. Gajewski TF, Thompson CB. 1996. Apoptosis meets signal transduction: elimination of a BAD influence. Cell 87:589-92
56. + concentrations and the regulation of protein synthesis in Sindbis virus-infected chick cells. Virology 96:108-20
57. Gibson L, Holmgreen SR, Huang DCS, Bernard O, Copeland NG et al. 1996. Bcl-w, a novel member of the bcl-2 family, promotes cell survival. Oncogene 13:665-75
58. Griffin DE. 1976. Role of the immune response in age-dependent resistance of mice to encephalitis due to Sindbis virus. J. Infect. Dis. 133:456-64
59. Griffin DE, Johnson RT. 1977. Role of the immune response in recovery from Sindbis virus encephalitis in mice. J. Immunol. 118:1070-75
60. Hahn CS, Lustig S, Strauss EG, Strauss JH. 1988. Western equine encephalitis virus is a recombinant virus. Proc. Natl. Acad. Sci. USA 85:5997-6001
61. Hammar SP, Monet NK. 1971. Tetrazolium salt and electron-microscopic studies of cellular degeneration and necrosis in the interdigital areas of the developing chick limb. J. Cell Sci. 8:229-51
62. Han J, Sabbatini P, Perez D, Rao L, Modha D, White E. 1996. The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10:461-77
63. Hanada M, Krajewski S, Tanaka S, Cazalshatem D, Spengler BA, et al. 1993. Regulation of Bcl-2 oncoprotein levels with differentiation of human neuroblastoma cells. Cancer Res. 53:4978-86
64. Hawkins CJ, Uren AG, Hacker G, Medcalf RL, Vaux DL. 1996. Inhibition of interleukin 1β-converting enzyme-mediated apoptosis of mammalian cells by baculovirus IAP. Proc. Natl. Acad. Sci. USA 93:13786-90
65. Hay BA, Wassarman DA, Rubin GM. 1995. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83:1253-62
66. Heller RA, Song K, Fan N, Chang DJ. 1992. The p70 tumor necrosis factor receptor mediates cytotoxicity. Cell 70:47-56
67. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, Rickinson A. 1993. 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 90:8479-83
68. Hengartner MO, Ellis RE, Horvitz HR. 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356:494-99
69. Hengartner MO, Horvitz HR. 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76:665-76
70. Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, Evans D. 1994. Apoptosis: a mechanism of cell killing by influenza A and B viruses. J. Virol. 68:3667-73
71. Hiramatsu N, Hayashi N, Katayama K, Mochizuki K, Kawanishi Y, et al. 1994. Immunohistochemical detection of Fas antigen in liver tissue of patients with chronic hepatitis C. Hepatoloxy 19:1354-59
72. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334-36
73. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-51
74. Hockenbery DM, Zutter M, Hickey W, Nahm M, Korsmeyer SJ. 1991. Bcl-2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc. Natl. Acad. Sci. USA 88:6961-65
75. Hsu H, Shu HB, Pan MG, Goeddel DV. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84:299-308
76. Hsu H, Xiong J, Goeddel DV. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-kB activation. Cell 81:495-504
77. Igarashi A, Koo R, Stollar V. 1977. Evolution and properties of Aedes albopictus cell cultures persistently infected with Sindbis virus. Virology 82:69-83
78. Inglot AD, Albin M, Chudzio T. 1973. Persistent infection of mouse cells with Sindbis virus: role of virulence of strains, auto-interfering particles and interferon. J. Gen. Virol. 20:105-10
79. Ishii HH, Gobe GC. 1993. Epstein-Barr virus infection is associated with increased apoptosis in untreated and phorbol ester-treated human Burkitt's lymphoma (AW-Ramos) cells. Biochem. Biophys. Res. Commun. 192:1415-23
80. Itoh N, Tsujimoto Y, Nagata S. 1993. Effect of bcl-2 on Fas antigen-mediated cell death. J. Immunol. 151:621-27
81. Itoh N, Yonehara S, Ishii A, Yonehara M, Mizushima S, et al. 1991. The polypeptide encoded by the cDNA for human cell surface antigen fas can mediate apoptosis. Cell 66:233-43
82. Jackson AC, Moench TR, Griffin DE. 1987. The pathogenesis of spinal cord involvement in the encephalomyelitis of mice caused by neuroadapted Sindbis virus infection. Lab. Invest. 56:418-23
83. Jackson AC, Moench TR, Trapp BD, Griffin DE. 1988. Basis of neurovirulence in Sindbis virus encephalomyelitis of mice. Lab. Invest. 58:503-9
84. Jackson M, Morrison KE, Al-Chalabi A, Bakker M, Leigh PN. 1996. Analysis of chromosome 5q13 genes in amyotrophic lateral sclerosis: homozygous NAIP deletion in a sporadic case. Ann. Neurol. 39:796-800
85. Jacobson MD, Burne JF, King MP, Miyashita T, Reed JC, Raff MC. 1993. Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361:365-69
86. Jacobson MD, Raff MC. 1995. Programmed cell death and bcl-2 protection in very low oxygen. Nature 374:814-16
87. Jelachich ML, Lipton HL. 1996. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J. Virol. 70:6856-61
88. Joe AK, Ferrari G, Jiang HH, Liang XH, Levine B. 1996. Dominant inhibitory ras delays Sindbis virus-induced apoptosis in neuronal cells. J. Virol. 70:7744-51
89. Johnson RT, McFarland HF, Levy SE. 1972. Age-dependent resistance to viral encephalitis: Studies of infections due to Sindbis virus in mice. J. Infect. Dis. 125:257-62
90. Kamada S, Shimono A, Shinto Y, Tsujimura T, Takahashi T, et al. 1995. Bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res. 55:354-59
91. Katsikis PD, Wunderlich ES, Smith CA, Herzenberg LA. 1995. Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J. Exp. Med. 181:2029-36
92. Kawanishi M. 1993. Epstein-Barr virus induces fragmentation of chromosomal DNA during lytic infection. J. Virol. 67:7654-58
93. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Can. 26:239-57
94. Kiefer MC, Brauer MJ, Powers VC, Wu JJ, Umansky SR, et al. 1995. Modulation of apoptosis by the widely distributed Bcl-2 homolgue Bak. Nature 374:736-39
95. Knudson CM, Tung KSK, Toutellotte WG, Brown GAJ, Korsmeyer SJ. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99
96. Kobayashi N, Hamamoto Y, Yamamoto N, Ishii A, Yonehara M, Yonehara S. 1990. Anti-fas monoclonal antibody is cytocidal to human immunodeficiency virus-infected cells without augmenting viral replication. Proc. Natl. Acad. Sci. USA 87:9620-24
97. Deleted in proof
98. Koyama AH. 1995. Induction of apoptotic DNA fragmentation by the infection of vesicular stomatitis virus. Virus Res. 37:285-90
99. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. 1993. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to bcl-2. Proc. Natl. Acad. Sci. USA 90: 3516-20
100. Krajewski S, Krajewsa M, Reed JC. 1996. Immunohistochemical analysis of in vivo patterns of Bak expression, a proapoptotic member of the Bcl-2 protein family. Cancer Res. 56:2849-55
101. Krajewski S, Krajewska M, Shabaik A, Wang HG, Irie S, et al. 1994. Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54:5501-7
102. Krajewski S, Tanaka S, Takayama S, Schibler MJ, Fenton W, Reed JC. 1993. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53:4701-14
103. Kumar S, Kinoshita M, Noda M, Copeland NG, Jenkins NA. 1994. Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegant cells death gene ced-3 and the mammalian IL-1β-converting enzyme. Genes Dev. 8:1613-26
104. 2+ fluxes. Proc. Natl. Acad. Sci. USA 91:6569-73
105. Laurent-Crawford AG, Krust B, Riviere Y, Desgranges C, Muller S, et al. 1993. Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res. Hum. Retroviruses 9:761-73
106. Levine B, Goldman JE, Jiang HH, Griffin DE, Hardwick JM. 1996. Bcl-2 protects mice against fatal alphavirus encephalitis. Proc. Natl. Acad. Sci. USA 93:4810-15
107. Levine B, Griffin DE. 1992. Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis. J. Virol. 66:6429-35
108. Levine B, Hardwick JM, Griffin DE. 1994. Persistence of alphaviruses in vertebrate hosts. Trends Microbiol. 2:25-28
109. Levine B, Hardwick JM, Trapp BD, Crawford TO, Bollinger RC, Griffin DE. 1991. Antibody-mediated clearance of alphavirus infection from neurons. Science 254:856-60
110. Levine B, Huang Q, Isaacs JT, Reed JC, Griffin DE, Hardwick JM. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739-42
111. Levine B, Jiang HH, Kleeman L, Yang G. 1996. Effect of E2 envelope glycoprotein cytoplasmic domain mutations on Sindbis virus pathogenesis. J. Virol. 70:1255-60
112. Lewis J, Wesselingh SL, Griffin DE, Hardwick JM. 1996. Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J. Virol. 70:1828-35
113. Lewis M, Tartaglia LA, Lee A, Bennett GL, Rice GC, et al. 1991. Cloning and expression of cDNAs for two distinct murine tumor necrosis factor receptors demonstrate one receptor is species specific. Proc. Natl. Acad. Sci. USA 88:2830-34
114. Lin K-I, Lee SH, Narayanan R, Baraban JM, Hardwick JM, Ratan RR. 1995. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappa B. J. Cell Biol. 131:1-14
115. Liston P, Roy N, Tamai K, Lefebvre C, Baird S et al. 1996. Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379:349-53
116. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-57
117. Loetscher H, Pan Y-CE, Lahm H-W, Gentz R, Brockhaus M, et al. 1990. Molecular cloning and expression of the human 55 kd tumor necrosis factor receptor. Cell 61:351-59
118. London E. 1992. Diptheria toxin: membrane interaction and membrane translocation. Biochim. Biophys. Acta 1113:25-51
119. Lopez S, Yao J-S, Kuhn RJ, Strauss EG, Strauss JH. 1994. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J. Virol. 68:1316-23
120. Lowe SW, Ruley HE. 1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:535-45
121. Lustig S, Halevy M, Ben-Nathan D, Akov Y. 1992. A novel variant of Sindbis virus is both neurovirulent and neuroinvasive in adult mice. J. Arch. Virol. 122:237-48
122. Lustig S, Jackson AC, Hahn CS, Griffin DE, Strauss EG, Strauss JH. 1988. The molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329-36
123. Marikainen P, Kyprianou N, Tucker RW, Isaacs JT. 1991. Programmed death of nonproliferating androgen-independent prostatic cancer cells. Cancer Res. 51: 4693-700
124. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM Jr. 1988. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106:829-44
125. McConkey DJ, Hartzell P, Nicotera P, Orrenius S. 1989. Calcium-activated DNA fragmentation kills immature thymocytes. FASEB J. 3:1843-49
126. McConkey DJ, Orrenius S. 1996. The role of calcium in the regulation of apoptosis. J. Leukocyte Biol. 59:775-83
127. Middleton G, Nunez G, Davies AM. 1996. Bax promotes neuronal survival and antagonises the survival effects of neurotrophic factors. Development 122:695-701
128. Miura M, Friedlander RM, Yuan JY. 1995. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl. Acad. Sci. USA 92:8318-22
129. Miura M, Zhu H, Rotello R, Hartwieg EA, Yuan JY. 1993. Induction of apoptosis in fibroblasts by IL-1-beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75:653-60
130. Moore LL, Bostick DA, Garry RF. 1988. Sindbis virus infection decreases intracellular pH: Alkaline medium inhibits processing of Sindbis virus polyproteins. Virology 166:1-9
131. Morey AL, Ferguson DJP, Fleming KA. 1993. Ultrastructural features of fetal erythroid precursors infected with parvovirus B19 in vitro: evidence of cell death by apoptosis. J. Pathol. 169:213-20
132. Motoyama N, Wang FP, Roth KA, Sawa H, Nakayama K, et al. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267:1506-10
133. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE et al. 1996. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381:335-41
134. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, et al. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-27
135. Nagata S, Golstein P. 1995. The fas death factor. Science 267:1449-56
136. Nakayama K, Nakayama K, Negishi I, Kuida K, Sawa H, Loh DY 1994. Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Natl Acad. Sci. USA 91:3700-4
137. Nakayama K, Nakayama K, Nakayama K, Negishi I, Kuida K, Shinkai Y. 1993. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 261:1584-88
138. Neilan JG, Lu Z, Afonso CL, Kutish GF, Sussman MD, Rock DL. 1993. An African swine fever virus gene with similarity to the proto-oncogene bcl-2 and the Epstein-Barr virus gene BHRF1. J. Virol. 67:4391-94
139. Nguyen M, Millar DG, Wee Yong V, Korsmeyer SJ, Shore GC. 1996. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. Am. J. Med. Sci. 268:25265-68
140. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37-43
141. Noteborn MHM, Todd D, Verschueren CAJ, Degauw HWFM, Curran WL, et al. 1994. A single chicken anemia virus protein induces apoptosis. J. Virol. 68:346-51
142. Nunez G, Clarke MF. 1994. The Bcl-2 family of proteins: regulators of cell death and survival. Trends Cell Biol. 4:399-406
143. Nunez G, Hockenbery D, McDonnell TJ, Sorensen CM, Korsmeyer SJ. 1991. Bcl-2 maintains B cell memory. Nature 353:71-73
144. Nunez G, London L, Hockenbery D, Alexander M, McKearn JP, Korsmeyer SJ. 1990. Deregulated bcl-2 gene expression selectively prolongs surrvival of growth factor-deprived hemopoietic cell lines. J. Immunol. 144:3602-10
145. Oehm A, Behrmann I, Falk W, Pawlita M, Maier G, et al. 1992. Purification and molecular cloning of the APO-1 cell surface antigen, a member of the tumor necrosis factor/nerve growth factor receptor superfamily. J. Biol. Chem. 267: 10709-15
146. Oltvai ZN, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-19
147. Osborne BA, Schwartz LM. 1994. Essential genes that regulate apoptosis. Trends Cell Biol. 4:394-98
148. Owen-Schaub LB, Yonehara S, Crump WL, Grimm EA. 1992. DNA fragmentation and cell death is selectively triggered in activated human lymphocytes by Fas antigen engagement. Cell. Immunol. 140:197-205
149. Peitsch MC, Georg H, Tschopp M, Tschopp J. 1994. The apoptosis endonucleases: cleaning up after cell death. Trends Cell Biol. 4:37-41
150. Peitsch MC, Polzar B, Stephan H, Crompton T, MacDonald HR, et al. 1993. Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J. 12:371-77
151. Pekosz A, Phillips J, Pleasure D, Merry D, Gonzalez-Scarano F. 1996. Induction of apoptosis by La Crosse virus infection and role of neuronal differentiation and human bcl-2 expression in its prevention. J. Virol. 70:5329-35
152. Peleg J. 1969. Inapparent persistent virus infection in continuously grown Aedesaegypti mosquito cells. J. Gen. Virol. 5:463-71
153. Prikhod'ko EA, Miller LK. 1996. Induction of apoptosis by baculovirus transactivator IE1. J. Virol. 70:7116-24
154. Qin XQ, Livingston DM, Kaelin WG Jr, Adams PD. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p-53 mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-22
155. Raff MC. 1992. Social controls on cell survival and cell death. Nature 356:397-400
156. Rao L, Debbas M, Sabbatini P, Hockenberry D, Korsmeyer S, White E. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the ElB 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-46
157. Ray CA, Black RA, Kronheim SR, Greenstreet TA, Sleath PR, et al. 1992. Viral inhibition of inflammation: Cowpox virus encodes an inhibitor of the interleukin-1-beta converting enzyme. Cell 69:597-604
158. Rice CM, Bell JR, Hunkapillar MW, Strauss EG, Strauss JH. 1982. Isolation and characterization of the hydrophobic COOH terminal domains of the Sindbis virus glycoproteins. J. Mol. Biol. 154: 355-78
159. Riedel B, Brown DT. 1977. Role of extracellular virus in the maintenance of the persistent infection induced in Aedes albopictus (mosquito) cells by Sindbis virus. J. Virol. 23:554-61
160. Riedel B, Brown DT. 1979. Novel antiviral activity found in the media of Sindbis virus persistently infected mosquito (Aedes albopictus) cell cultures. J. Virol. 29:51-60
161. Rosen A, Rosen-Casciola L, Ahearn J. 1995. Novel packages of viral and self-antigens are generated during apoptosis. J. Exp. Med. 181:1557-61
162. Rothe M, Pan MG, Henzel WJ, Ayres TM, Goeddel DV. 1995. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83:1243-52
163. Rothe M, Wong SC, Henzel WJ, Goeddel DV. 1994. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 78:681-92
164. Rothe M, Xiong J, Shu HB, Williamson K, Goddard A, Goeddel DV. 1996. I-TRAF is a novel TRAF-interacting protein that regulates TRAF-mediated signal transduction. Proc. Natl. Acad. Sci. USA 93:8241-46
165. Rouayrenc JF, Boise LH, Thompson CB, Privat A, Patey G. 1995. Presence of the long and the short forms of Bcl-X in several human and murine tissues. C. R. Acad Sci. 318:537-40
166. Roy N, Mahadevan MS, McLean M, Shutler G, Yaraghi Z, et al. 1995. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80:167-78
167. Russell DL, Dalrymple JM, Johnston RE. 1989. Sindbis virus mutations which coordinately affect glycoprotein processing, penetration, and virulence in mice. J. Virol. 63:1619-29
168. Savill J, Fadok V, Henson P, Haslett C. 1993. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14:131-36
169. Sawicki DL, Sawicki SG, Keranen S, Kaariainen L. 1981. Specific Sindbis virus-coded function for minus-strand RNA synthesis. J. Virol. 39:348-58
170. Schall TJ, Lewis M, Koller KJ, Lee A, Rice GC, et al. 1990. Molecular cloning and expression of a receptor for human tumor necrosis factor. Cell 61:361-70
171. Schnitzler P, Hug M, Handermann M, Janssen W, Koonin EV, et al. 1994. Identification of genes encoding zinc finger proteins, non-histone chromosomal HMG protein homologue, and a putative GTP phosphohydrolase in the genome of Chilo iridescent virus. Nucleic Acids Res. 22:158-66
172. Schoepp RJ, Johnston RE. 1993. Directed mutagenesis of a Sindbis virus pathogenesis site. Virology 193:149-59
173. Schulze-Osthoff K. 1994. The Fas/APO-1 receptor and its deadly ligand. Trends Cell Biol. 4:421-26
174. Deleted in proof
175. Sherman LA, Griffin DE. 1990. Pathogenesis of encephalitis induced in new-born mice by virulent and avirulent strains of Sindbis virus. J. Virol. 64:2041-46
176. Shimizu S, Eguchi Y, Kamiike W, Matsuda H, Tsujimoto Y. 1996. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene 12:2251-57
177. Shimizu S, Eguchi Y, Kamiike W, et al. 1996. Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13:21-29
178. Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H, Tsujimoto Y. 1995. Prevention of hypoxia-induced cell death by bcl-2 and bcl-xL. Nature 374:811-16
179. Shu HB, Takeuchi M, Goeddel DV. 1996. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc. Natl. Acad. Sci. USA 93:13973-78
180. L. J. Biol. Chem. 271:22764-72
181. Singh I, Helenius A. 1992. Role of ribosomes in Semliki Forest virus nucleocapsid uncoating. J. Virol. 66:7049-58
182. Smith CA, Davis T, Anderson D, Solam L, Beckmann MP, et al. 1990. A receptor of tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248:1019-23
183. Song HY, Rothe M, Goeddel DV. 1996. The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc. Natl. Acad. Sci. USA 93:6721-25
184. Stellar H. 1995. Mechanisms and genes of cellular suicide. Science 267:1445-49
185. Stevens TM. 1970. Arbovirus replication in mosquito cell lines (Singh) grown in monolayer or suspension culture. Proc. Soc. Exp. Biol. Med. 134:356-61
186. Strasser A, Harris AW, Cory S. 1991. Bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67:889-99
187. Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, et al. 1991. Enforced bcl-2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 88:8661-65
188. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication and evolution. Microbiol. Rev. 58:491-562
189. Takeuchi M, Rothe M, Goeddel DV. 1996. Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins. J. Biol. Chem. 271:19935-42
190. Takizawa T, Fukuda R, Miyawaki T, Ohashi K, Nakanishi Y. 1995. Activation of the apoptotic Fas antigen-encoding gene upon influenza virus infection involving spontaneously produced beta-interferon. Virology 209:288-96
191. Takizawa T, Matsukawa S, Higuchi Y, Nakamura S, Nakanishi Y, Fukuda R.
192. Tartaglia LA, Goeddel DV. 1992. Two TNF receptors. Immunol. Today 13:151-53
193. Tartaglia LA, Goeddel DV, Reynolds C, Figari IS, Weber RF, et al. 1993. Stimulation of human T-cell proliferation by specific activation of the 75-kDa tumor necrosis factor receptor. J. Immunol. 151:4637-41
194. Tartaglia LA, Weber RF, Figari IS, Reynolds C, Palladino MA Jr, Goeddel DV. 1991. The two different receptors for tumor necrosis factor mediate distinct cellular responses. Proc. Natl. Acad. Sci. USA 88:9292-96
195. Tewari M, Telford WG, Miller RA, Dixit VM. 1995. CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J. Biol. Chem. 270:22705-8
196. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, et al. 1992. A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356:768-74
197. Tollefson AE, Ryerse JS, Scaria A, Hermiston TW, Wold WSM. 1996. The E3-11.6-kDa adenovirus death protein (ADP) is required for efficient cell death: characterization of cells infected with adp mutants. Virology 220:152-62
198. Tolskaya EA, Romanova LI, Kolesnikova MS, Ivannikova TA, Smirnova EA, et al. 1995. Apoptosis-inducing and apoptosis-preventing function of poliovirus. J. Virol. 69:1181-89
199. Tortorella D, Sesardic D, Dawes CS, London E. 1995. Immunochemical analysis shows all three domains of diphtheria toxin penetrate across model membranes. J. Biol. Chem. 270:27446-52
200. Trauth BC, Klas C, Peters AMJ, Matzku S, Moller P, et al. 1989. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245:301-5
201. Tropea F, Troiano L, Monti D, Lovato E, Malorni W, et al. 1995. Sendai virus and herpes virus type 1 induce apoptosis in human peripheral blood mononuclear cells. Exp. Cell Res. 218:63-70
202. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. 1984. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226:1097-99
203. Tucker PC, Griffin DE. 1991. The mechanism of altered Sindbis virus neurovirulence associated with a single amino acid change in the E2 glycoprotein. J. Virol. 65:1551-57
204. Tucker PC, Griffin DE, Choi S, Bui N, Wesselingh S. 1996. Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis. J. Virol. 70:3972-77
205. Tucker PC, Strauss EG, Kuhn RJ, Strauss JH, Griffin DE. 1992. Viral determinants of age-dependent virulence of Sindbis virus for mice. J. Virol. 67:4605-10
206. Tucker PC, Strauss EG, Kuhn RJ, Strauss JH, Griffin DE. 1993. The age-dependent neurovirulence of Sindbis virus for mice is influenced by a single amino acid change at position 55 of the E2 glycoprotein. J. Virol. 67:4605-10
207. Tyler KL, Squier MKT, Rodgers SE, Schneider BE, Oberhaus SM, et al. 1995. Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein sigma-1. J. Virol. 69:6972-79
208. Ubol S, Griffin DE. 1991. Identification of a putative alphavirus receptor on mouse neural cells. J. Virol. 65:6913-21
209. Ubol S, Park S, Budihardjo I, Desnoyers S, Montrose MH et al. 1996. Temporal changes in chromatin, intracellular calcium, and poly (ADP-ribose) polymerase during Sindbis virus-induced apotosis of neuroblastoma cells. J. Virol. 70:2215-20
210. Ubol S, Tucker PC, Griffin DE, Hardwick JM. 1994. 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 91:5202-6
211. Ulug ET, Bose HR Jr. 1985. Effect of tunicamycin on the development of the cytopathic effect in Sindbis virus-infected avian fibroblasts. Virology 143:546-57
212. Uren AG, Pakusch M, Hawkins CJ, Puls KL, Vaux DL. 1996. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA 93:4974-78
213. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. 1996. Suppression of TNF-induced apoptosis by NF-kappaB. Science 274:787-89
214. Vandenabeele P, Declercq W, Beyaert R, Fiers W. 1995. Two tumour necrosis factor receptors: structure and function. Trends Cell Biol. 5:392-99
215. Vaux DL,Cory S, Adams JM. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-42
216. Vaux DL, Hacker G. 1995. Hypothesis: apoptosis caused by cytotoxins represents a defensive response that evolved to combat intracellular pathogens. Clin. Exp. Pharmacol. Physiol. 22:861-63
217. Vaux DL, Weissman IL, Kim SK. 1992. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258:1955-56
218. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75:229-40
219. Wada N, Matsumura M, Ohba Y, Kobayashi N, Takizawa T, Nakanishi Y. 1995. Transcription stimulation of the Fas-encoding gene by nuclear factor for interleukin-6 expression upon influenza virus infection. J. Biol. Chem. 270:18007-12
220. Waite MRF, Pfefferkorn ER. 1970. Phospholipid synthesis in Sindbis virus-infected cells. J. Virol. 6:637-43
221. Wang CY, Mayo MW, Baldwin AS Jr. 1996. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274:784-87
222. Wang H, Rapp UR, Reed JC. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87:629-38
223. Wang L, Miura M, Bergeron L, Zhu H, Yuan J. 1994. Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78:739-50
224. Wang S, Pittman RN. 1993. Altered protein binding to the octamer motif appears to be an early event in programmed neuronal cell death. Proc. Natl. Acad. Sci. USA 90:10385-89
225. Weiss B, Rosenthal R, Schlesinger S. 1980. Establishment and maintenance of persistent infection by Sindbis virus in BHK cells. J. Virol. 33:463-74
226. Wengler G. 1984. Identification of a transfer of viral core protein to cellular ribosomes during the early stages of alphavirus infection. Virology 134:435-42
227. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, et al. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500
228. White E. 1993. Regulation of apoptosis by the transforming genes of the DNA tumor virus adenovirus. Proc. Soc. Exp. Biol. Med. 204:30-39
229. White E, Sabbatini P, Debbas M, Wold WSM, Kusher DI, Gooding LR. 1992. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol. Cell. Biol. 12: 2570-80
230. White K, Tahaoglu E, Steller H. 1996. Cell killing by the Drosophila gene reaper. Science 271:805-7
231. Wu HY, Lozano G. 1994. NF-kappa-B activation of p53: a potential mechanism for suppressing cell growth in response to stress. J. Biol. Chem. 269:20067-74
232. Xue D, Shaham S, Horvitz HR. 1996. The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev. 10:1073-83
233. Yamada T, Yamaoka S, Goto T, Nakai M, Tsujimoto Y, Hatanaka M. 1994. The human T-cell leukemia virus type I tax protein induces apoptosis which is blocked by the bcl-2 protein. J. Virol. 68:3374-79
234. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ. 1995. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-91
235. Yin XM, Oltvai ZN, Korsmeyer SJ. 1994. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-23
236. Yuan JY, Horvitz HR. 1990. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev. Biol. 138:33-41
237. Yuan JY, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1-beta-converting enzyme. Cell 75:641-52
238. Zha H, Aime-Sempe C, Sato T, Reed JC. 1996. Proapoptotic proteins Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J. Biol. Chem. 271:7440-44
239. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87:619-28