Apoptosis: Definition, mechanisms, and relevance to disease

American Journal of Medicine

Volumn 107, Issue 5, 1999, Pages 489-506

  Saikumar, Pothana ^a   Dong, Zheng ^a   Mikhailov, Valery ^a   Denton, Michael ^a   Weinberg, Joel M ^b   Venkatachalam, Manjeri A ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOKINE; PROTEIN BCL 2; TUMOR NECROSIS FACTOR RECEPTOR;

APOPTOSIS; AUTOIMMUNITY; CARCINOGENESIS; CELL DEATH; CONGENITAL MALFORMATION; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; ENZYME REGULATION; GRAFT REJECTION; HUMAN; LYMPHOPROLIFERATIVE DISEASE; NONHUMAN; OSTEOPOROSIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TERATOGENICITY; VIRUS REPLICATION;

EID: 0033230540     PISSN: 00029343     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9343(99)00259-4     Document Type: Article

References (192)

1. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis a basic biological phenomenon with wide-ranging implications in tissue kinetics . Br J Cancer. 26:1972;239-257.
2. Ellis H.M., Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell. 44:1986;817-829.
3. Ferlini C., De Angelis C., Biselli R., et al. Sequence of metabolic changes during X-ray-induced apoptosis. Exp Cell Res. 247:1999;160-167.
4. Papassotiropoulos A., Ludwig M., Naib-Majani W., Rao G.S. Induction of apoptosis and secondary necrosis in rat dorsal root ganglion cell cultures by oxidized low density lipoprotein. Neurosci Lett. 209:1996;33-36.
5. Wyllie A.H. Apoptosis an overview . Br Med Bull. 53:1997;451-465.
6. Saikumar P., Dong Z., Weinberg J.M., Venkatachalam M.A. Mechanisms of cell death in hypoxia/reoxygenation injury. Oncogene. 17:1998;3341-3349.
7. Loo D.T., Rillema J.R. Measurement of cell death. Meth Cell Biol. 57:1998;251-264.
8. McCarthy N.J., Evan G.I. Methods for detecting and quantifying apoptosis. Curr Top Dev Biol. 36:1998;259-278.
9. Charriaut-Marlangue C., Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 7:1995;61-64.
10. Dong Z., Saikumar P., Weinberg J.M., Venkatachalam M.A. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am J Pathol. 151:1997;1205-1213.
11. Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Meth. 184:1995;39-51.
12. Kashiwagi A., Hanada H., Yabuki M., et al. Thyroxine enhancement and the role of reactive oxygen species in tadpole tail apoptosis. Free Rad Biol Med. 26:1999;1001-1009.
13. O'Connor R. Survival factors and apoptosis. Adv Biochem Eng Biotechnol. 62:1998;137-166.
14. Gordon N. Apoptosis (programmed cell death) and other reasons for elimination of neurons and axons. Brain Dev. 17:1995;73-77.
15. Clarke P.G., Posada A., Primi M.P., Castagne V. Neuronal death in the central nervous system during development. Biomed Pharmacother. 52:1998;356-362.
16. Jacobson M.D., Weil M., Raff M.C. Programmed cell death in animal development. Cell. 88:1997;347-354.
17. Strange R., Friis R.R., Bemis L.T., Geske F.J. Programmed cell death during mammary gland involution. Meth Cell Biol. 46:1995;355-368.
18. Kokawa K., Shikone T., Nakano R. Apoptosis in the human uterine endometrium during the menstrual cycle. J Clin Endocrinol Metab. 81:1996;4144-4147.
19. Kerr J.F., Searle J. Deletion of cells by apoptosis during castration-induced involution of the rat prostate. Virchows Arch B Cell Pathol. 13:1973;87-102.
20. Weedon D., Searle J., Kerr J.F. Apoptosis. Its nature and implications for dermatopathology. Am J Dermatopathol. 1:1979;133-144.
21. Weil M., Raff M.C., Braga V.M. Caspase activation in the terminal differentiation of human epidermal keratinocytes. Curr Biol. 9:1999;361-364.
22. Sendo F., Tsuchida H., Takeda Y., et al. Regulation of neutrophil apoptosis - its biological significance in inflammation and the immune response. Hum Cell. 9:1996;215-222.
23. King L.B., Ashwell J.D. Thymocyte and T cell apoptosis is all death created equal? Thymus. 23:1994;209-230.
24. Geng Y.J. Regulation of programmed cell death or apoptosis in atherosclerosis. Heart Vessels. 12:(suppl):1997;76-80.
25. Rubin L.L. Neuronal cell death when, why and how . Br Med Bull. 53:1997;617-631.
26. Li Y., Powers C., Jiang N., Chopp M. Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat. J Neurol Sci. 156:1998;119-132.
27. Taimor G., Lorenz H., Hofstaetter B., et al. Induction of necrosis but not apoptosis after anoxia and reoxygenation in isolated adult cardiomyocytes of rat. Cardiovasc Res. 41:1999;147-156.
28. Nakano H., Kurihara K., Okamoto M., et al. Heat-induced apoptosis and p53 in cultured mammalian cells. Int J Radiat Biol. 71:1997;519-529.
29. Belka C., Marini P., Budach W., et al. Radiation-induced apoptosis in human lymphocytes and lymphoma cells critically relies on the up-regulation of CD95/Fas/APO-1 ligand. Radiat Res. 149:1998;588-595.
30. Boesen-de Cock J.G., Tepper A.D., de Vries E., et al. Common regulation of apoptosis signaling induced by CD95 and the DNA-damaging stimuli etoposide and gamma-radiation downstream from caspase-8 activation. J Biol Chem. 274:1999;14255-14261.
31. Weiss R.A. How does HIV cause AIDS? Science. 260:1993;1273-1279.
32. Kalams S.A., Walker B.D. The critical need for CD4 help in maintaining effective cytotoxic T lymphocyte responses. J Exp Med. 188:1998;2199-2204.
33. Arscott P.L., Baker J.R. Jr. Apoptosis and thyroiditis. Clin Immunol Immunopathol. 87:1998;207-217.
34. Stassi G., Todaro M., Bucchieri F., et al. Fas/Fas ligand-driven T cell apoptosis as a consequence of ineffective thyroid immunoprivilege in Hashimoto's thyroiditis. J Immunol. 162:1999;263-267.
35. Tsokos G.C., Liossis S.N. Immune cell signaling defects in lupus activation, anergy and death . Immunol Today. 20:1999;119-124.
36. Jenner P., Olanow C.W. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology. 47:(suppl 3):1996;S161-S170.
37. Jellinger K.A., Bancher C. Neuropathology of Alzheimer's disease a critical update . J Neural Transm. 54:(suppl):1998;77-95.
38. Erdem S., Mendell J.R., Sahenk Z. Fate of Schwann cells in CMT1A and HNPP evidence for apoptosis . J Neuropathol Exp Neurol. 57:1998;635-642.
39. Cory S., Strasser A., Jacks T., et al. Enhanced cell survival and tumorigenesis. Cold Spring Harb Symp Quant Biol. 59:1994;365-375.
40. Vaux D.L., Strasser A. The molecular biology of apoptosis. Proc Natl Acad Sci USA. 93:1996;2239-2244.
41. Yuan J. Evolutionary conservation of a genetic pathway of programmed cell death. J Cell Biochem. 60:1996;4-11.
42. Horvitz H.R., Shaham S., Hengartner M.O. The genetics of programmed cell death in the nematode Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 59:1994;377-385.
43. Spector M.S., Desnoyers S., Hoeppner D.J., Hengartner M.O. Interaction between the C. elegans cell-death regulators CED-9 and CED-4. Nature. 385:1997;653-656.
44. Wu D., Wallen H.D., Nunez G. Interaction and regulation of subcellular localization of CED-4 by CED-9. Science. 275:1997;1126-1129.
45. Seshagiri S., Miller L.K. Caenorhabditis elegans CED-4 stimulates CED-3 processing and CED-3-induced apoptosis. Curr Biol. 7:1997;455-460.
46. Chaudhary D., O'Rourke K., Chinnaiyan A.M., Dixit V.M. The death inhibitory molecules CED-9 and CED-4L use a common mechanism to inhibit the CED-3 death protease. J Biol Chem. 273:1998;17708-17712.
47. Ruoslahti E., Reed J.C. Anchorage dependence, integrins, and apoptosis. Cell. 77:1994;477-478.
48. Miyajima A., Ito Y., Kinoshita T. Cytokine signaling for proliferation, survival, and death in hematopoietic cells. Int J Hematol. 69:1999;137-146.
49. Gollapudi L., Oblinger M.M. Stable transfection of PC12 cells with estrogen receptor (ERalpha) protective effects of estrogen on cell survival after serum deprivation . J Neurosci Res. 56:1999;99-108.
50. Lee Y., Renaud R.A., Friedrich T.C., Gorski J. Estrogen causes cell death of estrogen receptor stably transfected cells via apoptosis. J Steroid Biochem Mol Biol. 67:1998;327-332.
51. Magnusson C., Vaux D.L. Signalling by CD95 and TNF receptors not only life and death . Immunol Cell Biol. 77:1999;41-46.
52. Wallach D., Boldin M., Goncharov T., et al. Exploring cell death mechanisms by analyzing signaling cascades of the TNF/NGF receptor family. Behring Inst Mitt. 97:1996;144-155.
53. Nagata S. Apoptosis by death factor. Cell. 88:1997;355-365.
54. French L.E., Tschopp J. Constitutive Fas ligand expression in several non-lymphoid mouse tissues implications for immune-protection and cell turnover . Behring Inst Mitt. 97:1996;156-160.
55. Nagata S. Human autoimmune lymphoproliferative syndrome, a defect in the apoptosis-inducing Fas receptor a lesson from the mouse model . J Hum Genet. 43:1998;2-8.
56. Boldin M.P., Varfolomeev E.E., Pancer Z., et al. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J Biol Chem. 270:1995;7795-7798.
57. Hofmann K., Tschopp J. The death domain motif found in Fas (Apo-1) and TNF receptor is present in proteins involved in apoptosis and axonal guidance. FEBS Lett. 371:1995;321-323.
58. Hsu H., Xiong J., Goeddel D.V. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell. 81:1995;495-504.
59. Chinnaiyan A.M., O'Rourke K., Tewari M., Dixit V.M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 81:1995;505-512.
60. Varfolomeev E.E., Boldin M.P., Goncharov T.M., Wallach D. A potential mechanism of "cross-talk" between the p55 tumor necrosis factor receptor and Fas/APO1 proteins binding to the death domains of the two receptors also bind to each other . J Exp Med. 183:1996;1271-1275.
61. Hsu H., Huang J., Shu H.B., et al. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity. 4:1996;387-396.
62. Offit P.A., Cunningham S.L., Dudzik K.I. Memory and distribution of virus-specific cytotoxic T lymphocytes (CTLs) and CTL precursors after rotavirus infection. J Virol. 65:1991;1318-1324.
63. Zajac A.J., Quinn D.G., Cohen P.L., Frelinger J.A. Fas-dependent CD4+ cytotoxic T-cell-mediated pathogenesis during virus infection. Proc Natl Acad Sci USA. 93:1996;14730-14735.
64. Miyashita T., Reed J.C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 80:1995;293-299.
65. Verheij M., van Blitterswijk W.J., Bartelink H. Radiation-induced apoptosis - the ceramide-SAPK signaling pathway and clinical aspects. Acta Oncol. 37:1998;575-581.
66. Miura M., Zhu H., Rotello R., et al. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 75:1993;653-660.
67. Alnemri E.S., Livingston D.J., Nicholson D.W., et al. Human ICE/CED-3 protease nomenclature. Letter. Cell. 87:1996;171.
68. Thornberry N.A., Rano T.A., Peterson E.P., et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem. 272:1997;17907-17911.
69. Thornberry N.A., Lazebnik Y. Caspases enemies within . Science. 281:1998;1312-1316.
70. Hofmann K., Bucher P., Tschopp J. The CARD domain a new apoptotic signalling motif . Trends Biochem Sci. 22:1997;155-156.
71. Kuida K., Lippke J.A., Ku G., et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 267:1995;2000-2003.
72. Li P., Allen H., Banerjee S., et al. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell. 80:1995;401-411.
73. Schielke G.P., Yang G.Y., Shivers B.D., Betz A.L. Reduced ischemic brain injury in interleukin-1 beta converting enzyme-deficient mice. J Cereb Blood Flow Metab. 18:1998;180-185.
74. Kuida K., Zheng T.S., Na S., et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature. 384:1996;368-372.
75. Janicke R.U., Sprengart M.L., Wati M.R., Porter A.G. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem. 273:1998;9357-9360.
76. Woo M., Hakem R., Soengas M.S., et al. Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev. 12:1998;806-819.
77. Varfolomeev E.E., Schuchmann M., Luria V., et al. Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity. 9:1998;267-276.
78. Yeh W.C., Pompa J.L., McCurrach M.E., et al. FADD essential for embryo development and signaling from some, but not all, inducers of apoptosis . Science. 279:1998;1954-1958.
79. Zhang J., Cado D., Chen A., et al. Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature. 392:1998;296-300.
80. Juo P., Kuo C.J., Yuan J., Blenis J. Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol. 8:1998;1001-1008.
81. Chaudhary P.M., Eby M.T., Jasmin A., Hood L. Activation of the c-Jun N-terminal kinase/stress-activated protein kinase pathway by overexpression of caspase-8 and its homologs. J Biol Chem. 274:1999;19211-19219.
82. Hakem R., Hakem A., Duncan G.S., et al. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell. 94:1998;339-352.
83. Kuida K., Haydar T.F., Kuan C.Y., et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 94:1998;325-337.
84. Sun X.M., MacFarlane M., Zhuang J., et al. Distinct caspase cascades are initiated in receptor-mediated and chemical-induced apoptosis. J Biol Chem. 274:1999;5053-5060.
85. Shaham S., Horvitz H.R. Developing Caenorhabditis elegans neurons may contain both cell-death protective and killer activities. Genes Dev. 10:1996;578-591.
86. Zou H., Henzel W.J., Liu X., et al. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 90:1997;405-413.
87. Yoshida H., Kong Y.Y., Yoshida R., et al. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 94:1998;739-750.
88. Cecconi F., Alvarez-Bolado G., Meyer B.I., et al. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 94:1998;727-737.
89. Srinivasula S.M., Ahmad M., Fernandes-Alnemri T., Alnemri E.S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell. 1:1998;949-957.
90. Duan H., Dixit V.M. RAIDD is a new 'death' adaptor molecule. Nature. 385:1997;86-89.
91. Medema J.P., Scaffidi C., Kischkel F.C., et al. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). Embo J. 16:1997;2794-2804.
92. Imai Y., Kimura T., Murakami A., et al. The CED-4-homologous protein FLASH is involved in Fas-mediated activation of caspase-8 during apoptosis. Nature. 398:1999;777-785.
93. Irmler M., Thome M., Hahne M., et al. Inhibition of death receptor signals by cellular FLIP. Nature. 388:1997;190-195.
94. Thome M., Schneider P., Hofmann K., et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 386:1997;517-521.
95. Ogasawara J, Watanabe-Fukunaga R, Adachi M, et al. Lethal effect of the anti-Fas antibody in mice. [Published erratum appears in Nature 1993;365:568.
96. Nature 1993;364:806-809.
97. Yang X., Chang H.Y., Baltimore D. Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. Science. 281:1998;1355-1357.
98. Reed J.C. Bcl-2 family proteins. Oncogene. 17:1998;3225-3236.
99. Zhong L.T., Sarafian T., Kane D.J., et al. bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci USA. 90:1993;4533-4537.
100. Memon S.A., Moreno M.B., Petrak D., Zacharchuk C.M. Bcl-2 blocks glucocorticoid- but not Fas- or activation-induced apoptosis in a T cell hybridoma. J Immunol. 155:1995;4644-4652.
101. Yang J., Liu X., Bhalla K., et al. Prevention of apoptosis by Bcl-2 release of cytochrome c from mitochondria blocked . Science. 275:1997;1129-1132.
102. Flomerfelt F.A., Miesfeld R.L. Recessive mutations in a common pathway block thymocyte apoptosis induced by multiple signals. J Cell Biol. 127:(pt 1):1994;1729-1742.
103. Saikumar P., Dong Z., Patel Y., et al. Role of hypoxia-induced Bax translocation and cytochrome c release in reoxygenation injury. Oncogene. 17:1998;3401-3415.
104. Greenlund L.J., Korsmeyer S.J., Johnson E.M. Jr. Role of BCL-2 in the survival and function of developing and mature sympathetic neurons. Neuron. 15:1995;649-661.
105. Strasser A., Harris A.W., Huang D.C., et al. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. Embo J. 14:1995;6136-6147.
106. Itoh N., Tsujimoto Y., Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J Immunol. 151:1993;621-627.
107. Adams J.M., Cory S. The Bcl-2 protein family arbiters of cell survival . Science. 281:1998;1322-1326.
108. Kelekar A., Thompson C.B. Bcl-2-family proteins the role of the BH3 domain in apoptosis . Trends Cell Biol. 8:1998;324-330.
109. Desagher S., Osen-Sand A., Nichols A., et al. Bid-induced conformational change of bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol. 144:1999;891-901.
110. Wang H.G., Pathan N., Ethell I.M., et al. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 284:1999;339-343.
111. Hsu Y.T., Youle R.J. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem. 273:1998;10777-10783.
112. Hsu Y.T., Wolter K.G., Youle R.J. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA. 94:1997;3668-3672.
113. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature. 399:1999;483-487.
114. Finucane D.M., Bossy-Wetzel E., Waterhouse N.J., et al. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem. 274:1999;2225-2233.
115. Bossy-Wetzel E., Newmeyer D.D., Green D.R. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. Embo J. 17:1998;37-49.
116. Eskes R., Antonsson B., Osen-Sand A., et al. Bax-induced cytochrome C release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2+ ions. J Cell Biol. 143:1998;217-224.
117. Priault M., Chaudhuri B., Clow A., et al. Investigation of bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur J Biochem. 260:1999;684-691.
118. 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. 96:1999;5492-5497.
119. Bradham C.A., Qian T., Streetz K., et al. The mitochondrial permeability transition is required for tumor necrosis factor alpha-mediated apoptosis and cytochrome c release. Mol Cell Biol. 18:1998;6353-6364.
120. Marzo I., Brenner C., Zamzami N., et al. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:1998;2027-2031.
121. Pastorino J.G., Chen S.T., Tafani M., et al. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J Biol Chem. 273:1998;7770-7775.
122. Beutner G., Ruck A., Riede B., et al. Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett. 396:1996;189-195.
123. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
124. Luo X., Budihardjo I., Zou H., et al. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
125. Gross A., Yin X.M., Wang K., et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem. 274:1999;1156-1163.
126. Wu D., Wallen H.D., Inohara N., Nunez G. Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J Biol Chem. 272:1997;21449-21454.
127. Chinnaiyan A.M., O'Rourke K., Lane B.R., Dixit V.M. Interaction of CED-4 with CED-3 and CED-9 a molecular framework for cell death . Science. 275:1997;1122-1126.
128. Hu Y., Benedict M.A., Wu D., et al. Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci USA. 95:1998;4386-4391.
129. Pan G., O'Rourke K., Dixit V.M. Caspase-9, Bcl-XL, and Apaf-1 form a ternary complex. J Biol Chem. 273:1998;5841-5845.
130. Cosulich S.C., Savory P.J., Clarke P.R. Bcl-2 regulates amplification of caspase activation by cytochrome c. Curr Biol. 9:1999;147-150.
131. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria a primary site for Bcl-2 regulation of apoptosis . Science. 275:1997;1132-1136.
132. Schendel S.L., Montal M., Reed J.C. Bcl-2 family proteins as ion-channels. Cell Death Differ. 5:1998;372-380.
133. Antonsson B., Conti F., Ciavatta A., et al. Inhibition of Bax channel-forming activity by Bcl-2. Science. 277:1997;370-372.
134. Schlesinger P.H., Gross A., Yin X.M., et al. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA. 94:1997;11357-11362.
135. Kuo T.H., Kim H.R., Zhu L., et al. Modulation of endoplasmic reticulum calcium pump by Bcl-2. Oncogene. 17:1998;1903-1910.
136. Lam M., Dubyak G., Chen L., et al. Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci USA. 91:1994;6569-6573.
137. Marin M.C., Fernandez A., Bick R.J., et al. Apoptosis suppression by bcl-2 is correlated with the regulation of nuclear and cytosolic Ca2+. Oncogene. 12:1996;2259-2266.
138. Otter I., Conus S., Ravn U., et al. The binding properties and biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli. J Biol Chem. 273:1998;6110-6120.
139. Patston P.A., Gettins P., Beechem J., Schapira M. Mechanism of serpin action evidence that C1 inhibitor functions as a suicide substrate . Biochemistry. 30:1991;8876-8882.
140. Deveraux Q.L., Roy N., Stennicke H.R., et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. Embo J. 17:1998;2215-2223.
141. Deveraux Q.L., Reed J.C. IAP family proteins - suppressors of apoptosis. Genes Dev. 13:1999;239-252.
142. Ambrosini G., Adida C., Altieri D.C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med. 3:1997;917-921.
143. Ambrosini G., Adida C., Sirugo G., Altieri D.C. Induction of apoptosis and inhibition of cell proliferation by survivin gene targeting. J Biol Chem. 273:1998;11177-11182.
144. Somerville M.J., Hunter A.G., Aubry H.L., et al. Clinical application of the molecular diagnosis of spinal muscular atrophy deletions of neuronal apoptosis inhibitor protein and survival motor neuron genes . Am J Med Genet. 69:1997;159-165.
145. Xu D.G., Crocker S.J., Doucet J.P., et al. Elevation of neuronal expression of NAIP reduces ischemic damage in the rat hippocampus. Nat Med. 3:1997;997-1004.
146. Simons M., Beinroth S., Gleichmann M., et al. Adenovirus-mediated gene transfer of inhibitors of apoptosis protein delays apoptosis in cerebellar granule neurons. J Neurochem. 72:1999;292-301.
147. Widmann C., Gibson S., Johnson G.L. Caspase-dependent cleavage of signaling proteins during apoptosis. A turn-off mechanism for anti-apoptotic signals. J Biol Chem. 273:1998;7141-7147.
148. Sanghavi D.M., Thelen M., Thornberry N.A., et al. Caspase-mediated proteolysis during apoptosis insights from apoptotic neutrophils . FEBS Lett. 422:1998;179-184.
149. Schwab B.L., Leist M., Knippers R., Nicotera P. Selective proteolysis of the nuclear replication factor MCM3 in apoptosis. Exp Cell Res. 238:1998;415-421.
150. Cheng E.H., Kirsch D.G., Clem R.J., et al. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1997;1966-1968.
151. French L.E., Hahne M., Viard I., et al. Fas and Fas ligand in embryos and adult mice ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover . J Cell Biol. 133:1996;335-343.
152. Kurrer M.O., Pakala S.V., Hanson H.L., Katz J.D. Beta cell apoptosis in T cell-mediated autoimmune diabetes. Proc Natl Acad Sci USA. 94:1997;213-218.
153. Chervonsky A.V., Wang Y., Wong F.S., et al. The role of Fas in autoimmune diabetes. Cell. 89:1997;17-24.
154. Zhang H.G., Su X., Liu D., et al. Induction of specific T cell tolerance by Fas ligand-expressing antigen-presenting cells. J Immunol. 162:1999;1423-1430.
155. Briscoe D.M., Alexander S.I., Lichtman A.H. Interactions between T lymphocytes and endothelial cells in allograft rejection. Curr Opin Immunol. 10:1998;525-531.
156. Cohen J.J. Apoptosis mechanisms of life and death in the immune system . J Allergy Clin Immunol. 103:1999;548-554.
157. Puck J.M., Sneller M.C. ALPS an autoimmune human lymphoproliferative syndrome associated with abnormal lymphocyte apoptosis . Semin Immunol. 9:(1):1997;77-84.
158. Sneller M.C., Wang J., Dale J.K., et al. Clinical, immunologic, and genetic features of an autoimmune lymphoproliferative syndrome associated with abnormal lymphocyte apoptosis. Blood. 89:1997;1341-1348.
159. Engel P., Francis D., Graem N. Expression of bcl-2 in fetal thymus, thymomas and thymic carcinomas. Association with p53 expression and review of the literature. Apmis. 106:1998;449-455.
160. Korsmeyer S.J. Bcl-2 a repressor of lymphocyte death . Immunol Today. 13:1992;285-288.
161. Schwartz D., Rotter V. p53-dependent cell cycle control response to genotoxic stress . Semin Cancer Biol. 8:1998;325-336.
162. Amundson S.A., Myers T.G., Fornace A.J. Jr. Roles for p53 in growth arrest and apoptosis putting on the brakes after genotoxic stress . Oncogene. 17:1998;3287-3299.
163. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell. 88:1997;323-331.
164. Soengas M.S., Alarcon R.M., Yoshida H., et al. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science. 284:1999;156-159.
165. Yin C., Knudson C.M., Korsmeyer S.J., Van Dyke T. Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature. 385:1997;637-640.
166. Evans S.C., Lozano G. The Li-Fraumeni syndrome an inherited susceptibility to cancer . Mol Med Today. 3:1997;390-395.
167. Strand S., Hofmann W.J., Hug H., et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells - a mechanism of immune evasion? Nat Med. 2:1996;1361-1366.
168. Hahne M., Rimoldi D., Schroter M., et al. Melanoma cell expression of Fas (Apo-1/CD95) ligand implications for tumor immune escape . Science. 274:1996;1363-1366.
169. O'Connell J., Bennett M.W., O'Sullivan G.C., et al. The Fas counterattack cancer as a site of immune privilege . Immunol Today. 20:1999;46-52.
170. O'Connell J., Bennett M.W., O'Sullivan G.C., et al. Fas ligand expression in primary colon adenocarcinomas evidence that the Fas counterattack is a prevalent mechanism of immune evasion in human colon cancer . J Pathol. 186:1998;240-246.
171. Chen J.J., Sun Y., Nabel G.J. Regulation of the proinflammatory effects of Fas ligand (CD95L). Science. 282:1998;1714-1717.
172. O'Connell J., Bennett M.W., O'Sullivan G.C., et al. The Fas counterattack a molecular mechanism of tumor immune privilege . Mol Med. 3:1997;294-300.
173. Tamura T., Aoyama N., Saya H., et al. Induction of Fas-mediated apoptosis in p53-transfected human colon carcinoma cells. Oncogene. 11:1995;1939-1946.
174. Hu S., Vincenz C., Ni J., et al. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1- and CD-95-induced apoptosis. J Biol Chem. 272:1997;17255-17257.
175. Krajcsi P., Dimitrov T., Hermiston T.W., et al. The adenovirus E3-14.7K protein and the E3-10.4K/14.5K complex of proteins, which independently inhibit tumor necrosis factor (TNF)-induced apoptosis, also independently inhibit TNF-induced release of arachidonic acid J Virol. 70:1996;4904-4913.
176. Shisler J., Yang C., Walter B., et al. The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J Virol. 71:1997;8299-8306.
177. Boyd J.M., Gallo G.J., Elangovan B., et al. 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. 11:1995;1921-1928.
178. Boulakia C.A., Chen G., Ng F.W., et al. Bcl-2 and adenovirus E1B 19 kDA protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose) polymerase. Oncogene. 12:1996;529-535.
179. Teodoro J.G., Branton P.E. Regulation of apoptosis by viral gene products. J Virol. 71:1997;1739-1746.
180. Martin M.E., Berk A.J. Adenovirus E1B 55K represses p53 activation in vitro. J Virol. 72:1998;3146-3154.
181. Kameda T., Mano H., Yuasa T., et al. Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts. J Exp Med. 186:1997;489-495.
182. Warner H.R. Aging and regulation of apoptosis. Curr Top Cell Regul. 35:1997;107-121.
183. Quigley H.A. Neuronal death in glaucoma. Prog Retin Eye Res. 18:1999;39-57.
184. Usami S., Takumi Y., Fujita S., et al. Cell death in the inner ear associated with aging is apoptosis? Brain Res. 747:1997;147-150.
185. Paradis E., Douillard H., Koutroumanis M., et al. Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulates bax expression in human neurons. J Neurosci. 16:1996;7533-7539.
186. Ona V.O., Li M., Vonsattel J.P., et al. Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature. 399:1999;263-267.
187. Rouquet N., Pages J.C., Molina T., et al. ICE inhibitor YVADcmk is a potent therapeutic agent against in vivo liver apoptosis. Curr Biol. 6:1996;1192-1195.
188. Giordano C., Stassi G., De Maria R., et al. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto's thyroiditis. Science. 275:1997;960-963.
189. Gougeon M.L., Ledru E., Lecoeur H., Garcia S. T cell apoptosis in HIV infection mechanisms and relevance for AIDS pathogenesis . Results Probl Cell Differ. 24:1998;233-248.
190. Brown J.M., Wouters B.G. Apoptosis, p53, and tumor cell sensitivity to anticancer agents. Cancer Res. 59:1999;1391-1399.
191. Haanen C., Vermes I. Apoptosis programmed cell death in fetal development . Europ J Obstet Gynecol Reproduct Biol. 64:1996;129-133.
192. Moley K.H., Chi M.M., Knudson C.M., et al. Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nature Med. 4:1998;1421-1424.