Viral control of mitochondrial apoptosis

PLoS Pathogens

Volumn 4, Issue 5, 2008, Pages

  Galluzzi, Lorenzo ^a,b,c   Brenner, Catherine ^d   Morselli, Eugenia ^a,b,c   Touat, Zahia ^d   Kroemer, Guido ^a,b,c  

^a Institut Gustave Roussy   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; PROTEIN BCL 2; VIRUS PROTEIN;

APOPTOSIS; ENZYME REGULATION; EVOLUTION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; INFLAMMATION; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; REVIEW; VIRUS INFECTION; ANIMAL; METABOLISM; PATHOGENICITY; PATHOLOGY; PERMEABILITY; PHYSIOLOGY; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS;

ANIMALS; APOPTOSIS; HOST-PATHOGEN INTERACTIONS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PERMEABILITY; PROTO-ONCOGENE PROTEINS C-BCL-2; VIRAL PHYSIOLOGY; VIRAL PROTEINS; VIRUS DISEASES; VIRUSES;

EID: 44949151607     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000018     Document Type: Review

References (100)

1. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163.
2. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, et al. (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014.
3. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, et al. (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284:339-343.
4. De Maria R, Lenti L, Malisan F, d'Agostino F, Tomassini B, et al. (1997) Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science 277: 1652-1655.
5. Ricci JE, Munoz-Pinedo C, Fitzgerald P, Bailly-Maitre B, Perkins GA, et al. (2004) Disruption of mitochondrial function during apoptosis ismediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117: 773-786.
6. Demaurex N, Distelhorst C (2003) Cell biology. Apoptosis - the calcium connection. Science 300: 65-67.
7. Boya P, Roumier T, Andreau K, Gonzalez-Polo RA, Zamzami N, et al. (2003) Mitochondrion-targeted apoptosis regulators of viral origin. Biochem Biophys Res Commun 304: 575-581.
8. Castedo M, Perfettini JL, Andreau K, Roumier T, Piacentini M, et al. (2003) Mitochondrial apoptosis induced by the HIV-1 envelope. Ann N Y Acad Sci 1010: 19-28.
9. Galluzzi L, Larochette N, Zamzami N, Kroemer G (2006) Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25: 4812-4830.
10. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
11. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, et al. (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342.
12. Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487.
13. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, et al. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
14. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, et al. (1998) The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med 187: 1261-1271.
15. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17: 393-403.
16. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, et al. (2003) p53-and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302: 1036-1038.
17. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, et al. (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300: 135-139.
18. Letai A (2005) Pharmacological manipulation of Bcl-2 family members to control cell death. J Clin Invest 115: 2648-2655.
19. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, et al. (2004) The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427: 461-465.
20. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, et al. (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434: 652-658.
21. Galluzzi L, Kroemer G (2007) Mitochondrial apoptosis without VDAC. Nat Cell Biol 9: 487-489.
22. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, et al. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031.
23. Gougeon ML (2003) Apoptosis as an HIV strategy to escape immune attack. Nat Rev Immunol 3: 392-404.
24. Jacotot E, Ferri KF, El Hamel C, Brenner C, Druillennec S, et al. (2001) Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J Exp Med 193: 509-519.
25. Kim CM, Koike K, Saito I, Miyamura T, Jay G (1991) HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351: 317-320.
26. Yoshida M (2001) Multiple viral strategies of HTLV-1 for dysregulation of cell growth control. Annu Rev Immunol 19: 475-496.
27. D'Agostino DM, Silic-Benussi M, Hiraragi H, Lairmore MD, Ciminale V (2005) The human T-cell leukemia virus type 1 p13II protein: effects on mitochondrial function and cell growth. Cell Death Differ 12 Suppl 1: 905-915.
28. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, et al. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7: 1306-1312.
29. Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW (2003) The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function. J Virol 77: 7214-7224.
30. Doorbar J, Ely S, Sterling J, McLean C, Crawford L (1991) Specific interaction between HPV-16 E1-E4 and cytokeratins results in collapse of the epithelial cell intermediate filament network. Nature 352: 824-827.
31. Ferri KF, Jacotot E, Blanco J, Este JA, Zamzami N, et al. (2000) Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex: role of mitochondria and caspases. J Exp Med 192: 1081-1092.
32. Castedo M, Ferri KF, Blanco J, Roumier T, Larochette N, et al. (2001) Human immunodeficiency virus 1 envelope glycoprotein complex-induced apoptosis involves mammalian target of rapamycin/FKBP12-rapamycin-associated protein-mediated p53 phosphorylation. J Exp Med 194: 1097-1110.
33. Perfettini JL, Roumier T, Castedo M, Larochette N, Boya P, et al. (2004) NF-kappaB and p53 are the dominant apoptosis-inducing transcription factors elicited by the HIV-1 envelope. J Exp Med 199: 629-640.
34. Li CJ, Friedman DJ, Wang C, Metelev V, Pardee AB (1995) Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 268: 429-431.
35. Chen D, Wang M, Zhou S, Zhou Q (2002) HIV-1 Tat targets microtubules to induce apoptosis, a process promoted by the pro-apoptotic Bcl-2 relative Bim. Embo J 21: 6801-6810.
36. Nie Z, Phenix BN, Lum JJ, Alam A, Lynch DH, et al. (2002) HIV-1 protease processes procaspase 8 to cause mitochondrial release of cytochrome c, caspase cleavage and nuclear fragmentation. Cell Death Differ 9: 1172-1184.
37. White E, Sabbatini P, Debbas M, Wold WS, Kusher DI, et al. (1992) The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol Cell Biol 12: 2570-2580.
38. Rao L, Debbas M, Sabbatini P, Hockenbery D, Korsmeyer S, et al. (1992) The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc Natl Acad Sci U S A 89: 7742-7746.
39. White E, Cipriani R, Sabbatini P, Denton A (1991) Adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of E1A proteins. J Virol 65: 2968-2978.
40. Shimazu T, Degenhardt K, Nur EKA, Zhang J, Yoshida T, et al. (2007) NBK/ BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Genes Dev 21: 929-941.
41. Hart LS, Ornelles D, Koumenis C (2007) The adenoviral E4orf6 protein induces atypical apoptosis in response to DNA damage. J Biol Chem 282: 6061-6067.
42. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63: 1129-1136.
43. Munger K, Werness BA, Dyson N, Phelps WC, Harlow E, et al. (1989) Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. Embo J 8: 4099-4105.
44. Gaddy DF, Lyles DS (2005) Vesicular stomatitis viruses expressing wild-type or mutant M proteins activate apoptosis through distinct pathways. J Virol 79: 4170-4179.
45. Medigeshi GR, Lancaster AM, Hirsch AJ, Briese T, Lipkin WI, et al. (2007) West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81: 10849-10860.
46. Tan YX, Tan TH, Lee MJ, Tham PY, Gunalan V, et al. (2007) Induction of apoptosis by the severe acute respiratory syndrome coronavirus 7a protein is dependent on its interaction with the Bcl-XL protein. J Virol 81: 6346-6355.
47. Cuconati A, White E (2002) Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev 16: 2465-2478.
48. Huang DC, Cory S, Strasser A (1997) Bcl-2, Bcl-XL and adenovirus protein E1B19kD are functionally equivalent in their ability to inhibit cell death. Oncogene 14: 405-414.
49. Han J, Sabbatini P, Perez D, Rao L, Modha D, et al. (1996) The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev 10: 461-477.
50. Farrow SN, White JH, Martinou I, Raven T, Pun KT, et al. (1995) Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K. Nature 374: 731-733.
51. Chiou SK, Tseng CC, Rao L, White E (1994) Functional complementation of the adenovirus E1B 19-kilodalton protein with Bcl-2 in the inhibition of apoptosis in infected cells. J Virol 68: 6553-6566.
52. Goldmacher VS, Bartle LM, Skaletskaya A, Dionne CA, Kedersha NL, et al. (1999) A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc Natl Acad Sci U S A 96: 12536-12541.
53. Arnoult D, Bartle LM, Skaletskaya A, Poncet D, Zamzami N, et al. (2004) Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc Natl Acad Sci U S A 101: 7988-7993.
54. Poncet D, Pauleau AL, Szabadkai G, Vozza A, Scholz SR, et al. (2006) Cytopathic effects of the cytomegalovirus-encoded apoptosis inhibitory protein vMIA. J Cell Biol 174: 985-996.
55. 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.
56. Wasilenko ST, Stewart TL, Meyers AF, Barry M (2003) Vaccinia virus encodes a previously uncharacterized mitochondrial-associated inhibitor of apoptosis. Proc Natl Acad Sci U S A 100: 14345-14350.
57. Wasilenko ST, Banadyga L, Bond D, Barry M (2005) The vaccinia virus F1L protein interacts with the proapoptotic protein Bak and inhibits Bak activation. J Virol 79: 14031-14043.
58. Everett H, Barry M, Sun X, Lee SF, Frantz C, et al. (2002) The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J Exp Med 196: 1127-1139.
59. Su J, Wang G, Barrett JW, Irvine TS, Gao X, et al. (2006) Myxoma virus M11L blocks apoptosis through inhibition of conformational activation of Bax at the mitochondria. J Virol 80: 1140-1151.
60. Douglas AE, Corbett KD, Berger JM, McFadden G, Handel TM (2007) Structure of M11L: A myxoma virus structural homolog of the apoptosis inhibitor, Bcl-2. Protein Sci 16: 695-703.
61. Kvansakul M, van Delft MF, Lee EF, Gulbis JM, Fairlie WD, et al. (2007) A structural viral mimic of prosurvival Bcl-2: a pivotal role for sequestering proapoptotic Bax and Bak. Mol Cell 25: 933-942.
62. Cooray S, Bahar MW, Abrescia NG, McVey CE, Bartlett NW, et al. (2007) Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J Gen Virol 88: 1656-1666.
63. Banadyga L, Gerig J, Stewart T, Barry M (2007) Fowlpox virus encodes a Bcl-2 homologue that protects cells from apoptotic death through interaction with the proapoptotic protein Bak. J Virol 81: 11032-11045.
64. Westphal D, Ledgerwood EC, Hibma MH, Fleming SB, Whelan EM, et al. (2007) A novel Bcl-2-like inhibitor of apoptosis is encoded by the parapoxvirus ORF virus. J Virol 81: 7178-7188.
65. Marshall WL, Yim C, Gustafson E, Graf T, Sage DR, et al. (1999) Epstein-Barr virus encodes a novel homolog of the bcl-2 oncogene that inhibits apoptosis and associates with Bax and Bak. J Virol 73: 5181-5185.
66. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, et al. (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 U S A 90: 8479-8483.
67. Bellows DS, Howell M, Pearson C, Hazlewood SA, Hardwick JM (2002) Epstein-Barr virus BALF1 is a BCL-2-like antagonist of the herpesvirus antiapoptotic BCL-2 proteins. J Virol 76: 2469-2479.
68. Lee MA, Yates JL (1992) BHRF1 of Epstein-Barr virus, which is homologous to human proto-oncogene bcl2, is not essential for transformation of B cells or for virus replication in vitro. J Virol 66: 1899-1906.
69. Hickish T, Robertson D, Clarke P, Hill M, di Stefano F, et al. (1994) Ultrastructural localization of BHRF1: an Epstein-Barr virus gene product which has homology with bcl-2. Cancer Res 54: 2808-2811.
70. Tarodi B, Subramanian T, Chinnadurai G (1994) Epstein-Barr virus BHRF1 protein protects against cell death induced by DNA-damaging agents and heterologous viral infection. Virology 201: 404-407.
71. Cheng EH, Nicholas J, Bellows DS, Hayward GS, Guo HG, et al. (1997) A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc Natl Acad Sci U S A 94: 690-694.
72. Nava VE, Cheng EH, Veliuona M, Zou S, Clem RJ, et al. (1997) Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncogene. J Virol 71: 4118-4122.
73. Huang Q, Petros AM, Virgin HW, Fesik SW, Olejniczak ET (2002) Solution structure of a Bcl-2 homolog from Kaposi sarcoma virus. Proc Natl Acad Sci U S A 99: 3428-3433.
74. Gangappa S, van Dyk LF, Jewett TJ, Speck SH, Virgin HWt (2002) Identification of the in vivo role of a viral bcl-2. J Exp Med 195: 931-940.
75. Bellows DS, Chau BN, Lee P, Lazebnik Y, Burns WH, et al. (2000) Antiapoptotic herpesvirus Bcl-2 homologs escape caspase-mediated conversion to proapoptotic proteins. J Virol 74: 5024-5031.
76. Wang HW, Sharp TV, Koumi A, Koentges G, Boshoff C (2002) Characterization of an anti-apoptotic glycoprotein encoded by Kaposi's sarcomaassociated herpesvirus which resembles a spliced variant of human survivin. Embo J 21: 2602-2615.
77. 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: 227-230.
78. Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, et al. (2001) A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci U S A 98: 7829-7834.
79. Reeves MB, Davies AA, McSharry BP, Wilkinson GW, Sinclair JH (2007) Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316: 1345-1348.
80. Matsuda G, Nakajima K, Kawaguchi Y, Yamanashi Y, Hirai K (2003) Epstein-Barr virus (EBV) nuclear antigen leader protein (EBNA-LP) forms complexes with a cellular anti-apoptosis protein Bcl-2 or its EBV counterpart BHRF1 through HS1-associated protein X-1. Microbiol Immunol 47: 91-99.
81. Erdtmann L, Franck N, Lerat H, Le Seyec J, Gilot D, et al. (2003) The hepatitis C virus NS2 protein is an inhibitor of CIDE-B-induced apoptosis. J Biol Chem 278: 18256-18264.
82. Lee SH, Kim YK, Kim CS, Seol SK, Kim J, et al. (2005) E2 of hepatitis C virus inhibits apoptosis. J Immunol 175: 8226-8235.
83. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, et al. (1997) Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517-521.
84. Brinkmann MM, Pietrek M, Dittrich-Breiholz O, Kracht M, Schulz TF (2007) Modulation of host gene expression by the K15 protein of Kaposi's sarcoma-associated herpesvirus. J Virol 81: 42-58.
85. Guasparri I, Keller SA, Cesarman E (2004) KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993-1003.
86. Sun Q, Matta H, Chaudhary PM (2003) The human herpes virus 8-encoded viral FLICE inhibitory protein protects against growth factor withdrawal-induced apoptosis via NF-kappa B activation. Blood 101: 1956-1961.
87. Chin YR, Horwitz MS (2005) Mechanism for removal of tumor necrosis factor receptor 1 from the cell surface by the adenovirus RIDalpha/beta complex. J Virol 79: 13606-13617.
88. Elsing A, Burgert HG (1998) The adenovirus E3/10.4K-14.5K proteins down-modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc Natl Acad Sci U S A 95: 10072-10077.
89. Clem RJ, Fechheimer M, Miller LK (1991) Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388-1390.
90. Clem RJ, Miller LK (1994) Control of programmed cell death by the baculovirus genes p35 and iap. Mol Cell Biol 14: 5212-5222.
91. Sugimoto A, Friesen PD, Rothman JH (1994) Baculovirus p35 prevents developmentally programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans. Embo J 13: 2023-2028.
92. Xue D, Horvitz HR (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377: 248-251.
93. Crook NE, Clem RJ, Miller LK (1993) An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 67: 2168-2174.
94. 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 U S A 93: 4974-4978.
95. Hay BA, Wassarman DA, Rubin GM (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83: 1253-1262.
96. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, et al. (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. Embo J 17: 2215-2223.
97. Rodriguez CI, Nogal ML, Carrascosa AL, Salas ML, Fresno M, et al. (2002) African swine fever virus IAP-like protein induces the activation of nuclear factor kappa B. J Virol 76: 3936-3942.
98. Stauber RH, Mann W, Knauer SK (2007) Nuclear and cytoplasmic survivin: molecular mechanism, prognostic, and therapeutic potential. Cancer Res 67:5999-6002.
99. Feng P, Liang C, Shin YC, E X, Zhang W, et al. (2007) A novel inhibitory mechanism of mitochondrion-dependent apoptosis by a herpesviral protein. PLoS Pathog 3: e174. doi:10.1371/journal.ppat.0030174.
100. Maxwell KL, Frappier L (2007) Viral proteomics. Microbiol Mol Biol Rev 71: 398-411.