Mitochondrion-targeted apoptosis regulators of viral origin

Biochemical and Biophysical Research Communications

Volumn 304, Issue 3, 2003, Pages 575-581

  Boya, Patricia ^a   Roumier, Thomas ^a   Andreau, Karine ^a   Gonzalez Polo, Rosa Ana ^a   Zamzami, Naoufal ^a   Castedo, Maria ^a   Kroemer, Guido ^a  

^a CNRS   (France)

Author keywords

Apoptosis; Caspases; Cell death; Mitochondria

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; BENZODIAZEPINE RECEPTOR; CASPASE 3; CYCLOPHILIN; CYCLOPHILIN D; CYTOCHROME C; INHIBITOR OF APOPTOSIS PROTEIN; MATRIX METALLOPROTEINASE; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL PROTEIN K7; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RO 54864; RO 55864; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRUS PROTEIN; VOLTAGE GATED CHANNEL FORMING PROTEIN; VPR PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CYTOMEGALOVIRUS; EPSTEIN BARR VIRUS; HEPATITIS B VIRUS; HUMAN; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

CYTOMEGALOVIRUS; HEPATITIS B VIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 1;

EID: 0037427411     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(03)00630-2     Document Type: Article

References (67)

1. Ferri K.F., Kroemer G.K. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:2001;E255-E263.
2. Ravagnan L., Roumier T., Kroemer G. Mitochondria - the killer organelles and their weapons. J. Cell. Physiol. 192:2002;131-137.
3. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 6:2000;513-519.
4. Debatin K.M., Poncet D., Kroemer G. Chemotherapy: targeting the mitochondrial pathway. Oncogene. 21:2002;8786-8803.
5. Tschopp J., Thome M., Hofmann K., Meinl E. The fight of viruses against apoptosis. Curr. Opin. Genet. Dev. 8:1998;82-87.
6. Boya P., Roques B., Kroemer G. Bacterial and viral proteins regulating apoptosis at the mitochondrial level. EMBO J. 20:2001;4325-4331.
7. Martinou J.C., Green D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell. Biol. 2:2001;63-67.
8. Zamzami N., Kroemer G. Mitochondria in apoptosis. How Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2:2001;67-71.
9. Zamzami N., Kroemer G. Mitochondrial membrane permeabilization in apoptosis. The (w)hole story? Curr. Biol. 13:2003;R71-R73.
10. Wei M.C., Zong W.-X., Cheng E.H.-Y., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science. 292:2001;727-730.
11. Cheng E.H., Wei M.C., Weiler S., Flavell R.A., Mak T.W., Lindsten T., Korsmeyer S.J. BCL-2, BCL-XL sequester BH3 domain-only molecules preventing BAX and BAK-mediated mitochondrial apoptosis. Mol. Cell. 8:2001;705-711.
12. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson C.B. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15:2001;1481-1486.
13. McClintock D.S., Santore M.T., Lee V.Y., Brunelle J., Budinger G.R., Zong W.X., Thompson C.B., Hay N., Chandel N.S. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol. Cell Biol. 22:2002;94-104.
14. Griffiths G.J., Dubrez L., Morgan C.P., Jones N.A., Whitehouse J., Corfe B.M., Dive C., Hickman J.A. Cell damage-induced conformational changes of the pro-apoptotic protein bak in vivo precede the onset of apoptosis. J. Cell Biol. 144:1999;903-914.
15. Hsu Y.T., Wolter K.G., Youle R.J. Cytosol-to-membrane redistribution of Bax and Bcl-XL during apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;3668-3672.
16. Nechushtan A., Smith C.L., Lamensdorf I., Yoon S.H., Youle R.J. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol. 153:2001;1265-1276.
17. Saito M., Korsmeyer S.J., Schlesinger P.H. Bax-dependent transport of cytochrome c reconstituted in pure liposomes. Nat. Cell Biol. 2:2000;553-555.
18. Kuwana T., Mackey M.R., Perkins G.A., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, Bad, lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:2002;1-12.
19. Marzo I., Brenner C., Zamzami N., Jürgensmeier J., Susin S.A., Vieira H.L.A., Prévost M.-C., Xie Z., Matsuyama S., Reed J.C., Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:1998;2027-2031.
20. Eskes R.S., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:2000;929-935.
21. Grinberg M., Sarig R., Zaltsman V., Frumkin D., Grammatikakis N., Reuveny E., Gross A. tBID homooligomerizes in the mitochondrial membrane to induce apoptosis. J. Biol. Chem. 277:2002;12237-12245.
22. Schendel S.L., Azimov R., Pawloski K., Godzik A., Kagan B.L., Reed J.C. Ion channel activity of the BH3 only bcl-2 family member, BID. J. Biol. Chem. 274:1999;21932-21936.
23. Kudla G., Montessuit S., Eskes R., Berrier C., Martinou J.-C., Ghazi A., Antonsson B. The destabilization of lipid membrane induced by the C-terminal fragment of caspase 8-cleaved Bid is inhibited by the N-terminal fragment. J. Biol. Chem. 275:2000;22713-22718.
24. Zamzami N., El Hamel C., Muñoz C., Brenner C., Belzacq A.-S., Costantini P., Molle G., Kroemer G. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene. 19:2000;6342-6350.
25. Shimizu S., Tsujimoto Y. Proapoptic BH3-only Bcl-2 family members induce cytochrome c release, but not mitochondrial membrane potential loss, and do not directly modulate voltage-dependent anion channel activity. Proc. Natl. Acad. Sci. USA. 97:2000;577-582.
26. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell. 2:2002;55-67.
27. Letai A., Bassik M., Walensky L., Sorcinelli M., Weiler S., Korsmeyer S. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2:2002;183-192.
28. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3:1997;614-620.
29. Zoratti M., Szabò I. The mitochondrial permeability transition. Biochem. Biophys. Acta - Rev. Biomembranes. 1241:1995;139-176.
30. Woodfield K., Ruck A., Brdiczka D., Halestrap A.P. Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem. J. 336:1998;287-290.
31. Crompton M., Virji S., Ward J.M. Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem. 258:1998;729-735.
32. Ferri K.F., Jacotot E., Blanco J., Esté J.A., Zamzami A., Susin S.A., Brothers G., Reed J.C., Penninger J.M., Kroemer G. Apoptosis control in syncytia induced by the HIV-1-envelope glycoprotein complex. Role of mitochondria and caspases. J. Exp. Med. 192:2000;1081-1092.
33. Shimizu S., Matsuoka Y., Shinohara Y., Yoneda Y., Tsujimoto Y. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell Biol. 152:2001;237-250.
34. Madesh M., Hajnoczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155:2001;1003-1015.
35. Vander Heiden M.G., Chandel N.S., Li X.X., Schumacker P.T., Colombini M., Thompson C.B. Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc. Natl. Acad. Sci. USA. 97:2000;4666-4671.
36. Vander Heiden M.G., Li X.X., Gottleib E., Hill R.B., Thompson C.B., Colombini M. Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J. Biol. Chem. 276:2001;19414-19419.
37. Brenner C., Cadiou H., Vieira H.L.A., Zamzami N., Marzo I., Xie Z., Leber B., Andrews D., Duclohier H., Reed J.C., Kroemer G. Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene. 19:2000;329-336.
38. Crompton M. Mitochondrial intermembrane junctional complexes and their role in cell death. J. Physiol. 15:2000;11-21.
39. Vieira H.L., Belzacq A.-S., Haouzi D., Bernassola F., Cohen I., Jacotot E., Ferri K.F., Hamel E.H., Bartle L.M., Melino G., Brenner C., Goldmacher V., Kroemer G. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite and 4-hydroxynonenal. Oncogene. 20:2001;4305-4316.
40. Vieira H.L.A., Boya P., Cohen I., El Hamel C., Haouzi D., Druillenec S., Belzacq A.-S., Roques B., Brenner C., Kroemer G. Cell-permeable BH3 peptides overcome the cytoprotective effect of Bcl-2 and Bcl-XL. Oncogene. 21:2002;1963-1977.
41. Jacotot E., Ferri K.F., El Hamel C., Brenner C., Druillenec S., Hoebeke J., Rustin P., Métivier D., Lenoir C., Geuskens M., Vieira H.L.A., Loeffler M., Belzacq A.-S., Briand J.-P., Zamzami N., Edelman L., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 Vpr and Bcl-2. J. Exp. Med. 193:2001;509-520.
42. Belzacq A.S., Vieira H.L., Verrier F., Vandecasteele G., Cohen I., Prevost M.C., Petit P.X., Kahn A., Roques B., Rizzuto R., Brenner C., Kroemer G. Bcl-2 and Bax modulate adenine nucleotide translocase activity. Cancer Res. 63:2003;541-546.
43. Vander Heiden M.G., Thompson C.B. Bcl-2 proteins: inhibitors of apoptosis or regulators of mitochondrial homeostasis? Nat. Cell Biol. 1:1999;E209-E216.
44. Castedo M., Perfettini J.-L., Kroemer G. Mitochondrial apoptosis and the peripheral benzodiazepine receptor: A novel target for viral and pharmacological manipulation. J. Exp. Med. 196:2002;1121-1126.
45. Stoebner P.E., Carayon P., Casellas P., Portier M., Lavabre-Bertrand T., Cuq P., Cano J.P., Meynadier J., Meunier L. Transient protection by peripheral benzodiazepine receptors during the early events of ultraviolet light-induced apoptosis. Cell Death Differ. 8:2001;747-753.
46. Hirsch T., Decaudin D., Susin S.A., Marchetti P., Larochette N., Resche-Rigon M., Kroemer G. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp. Cell Res. 241:1998;426-434.
47. Decaudin D.M., Castedo M., Beurdeley-Thomas A., Nemati F., de Pinieux G., Caron A., Pouillart P., Wijdenes J., Rouillard D., Kroemer G., Poupon M.-F. Peripheral benzodiazepine receptor ligands reverse apoptosis resistance of cancer cells in vitro and in vivo. Cancer Res. 62:2002;1388-1393.
48. Lutter M., Fang M., Luo X., Nishijima M., Xie X.S., Wang X. Cardiolipin provides specificity for targeting tBid to mitochondria. Nat. Cell Biol. 2:2000;754-756.
49. Rahmani Z., Huh K.W., Lasher R., Siddiqui A. Hepatitis B virus X protein colocalizes to mitochondria with a human voltage-dependent anion channel, HVDAC3, alters its transmembrane potential. J. Virol. 74:2000;2840-2846.
50. Schuster R., Gerlich W.H., Schaefer S. Induction of apoptosis by the transactivating domains of the hepatitis B virus X gene leads to suppression of oncogenic transformation of primary rat embryo fibroblasts. Oncogene. 19:2000;1173-1180.
51. Goldmacher V.S., Bartle L.M., Skletskaya S., Dionne C.A., Kedersha N.L., Vater C.A., Han J.W., Lutz R.J., Watanabe S., McFarland E.D.C., Kieff E.D., Mocarski E.S., Chittenden T. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally related to Bcl-2. Proc. Natl. Acad. Sci. USA. 96:1999;12536-12541.
52. McCormick A.L., Smith V.L., Chow D., Mocarski E.S. Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J. Virol. 77:2003;631-641.
53. Hayajneh W.A., Colberg-Oley A.M., Skaleskaya A., Bartle L.M., Lesperance M.M., Contopoulos-Ionnidis D.G., Kedersha N.L., Goldmacher V.S. The sequence and antiapoptotic functional domains of the human cytomegalovirus UL37 exon 1 immediate early protein are conserved in multiple primary strains. Virology. 279:2001;233-240.
54. Schüler W., Wecker K., de Rocquigny H., Baudat Y., Sire J., Roques B.P. NMR structure of the (52-96) C-terminal domain of the HIV-1 regulatory protein Vpr: Molecular insights into its biological functions. J. Mol. Biol. 285:1999;2105-2117.
55. Jacotot E., Ravagnan L., Loeffler M., Ferri K.F., Vieira H.L.A., Zamzami N., Costantini P., Druillennec S., Hoebeke J., Brian J.P., Irinopoulos T., Daugas E., Susin S.A., Cointe D., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 191:2000;33-45.
56. Somasundaran M., Sharkey M., Brichacek B., Luzuriaga K., Emerman M., Sullivan J.L., Stevenson M. Evidence for a cytopathogenicity determinant in HIV-1 Vpr. Proc. Natl. Acad. Sci. USA. 99:2002;9503-9508.
57. Zhang L., Huang Y., Yuan H., Tuttleton S., Ho D.D. Genetic characterization of vif, vpr, vpu sequences from long-term survivors of human immunodeficiency virus type1 infection. Virology. 228:1997;340-349.
58. Muthumani K., Zhang D., Hwang D.S., Kudchodkar S., Dayes N.S., Desai B.M., Malik A.S., Yang J.S., Chattergoon M.A., Maguire H.C. Jr., Weiner D.B. Adenovirus encoding HIV-1 Vpr activates caspase 9 and induces apoptotic cell death in both p53 positive and negative human tumor cell lines. Oncogene. 21:2002;4613-4625.
59. Roumier T., Vieira H.L.A., Castedo M., Ferri K.F., Boya P., Andreau K., Druillenec S., Joza N., Penninger J.M., Roques B., Kroemer G. The C-terminal moiety of HIV-1 Vpr induces cell death via a caspase-independent mitochondrial pathway. Cell Death Differ. 9:2002;1212-1219.
60. Ciminale V., Zotti L., D'Agostini D.M., Ferro T., Casareto L., Franchini G., Bernardi P., ChiecoBianchi L. Mitochondrial targeting of the p13(II) protein coded by the x-II ORF of human T-cell leukemia/lymphotropic virus type I (HTLV-1). Oncogene. 18:1999;4505-4514.
61. D'Agostino D.M., Ranzato L., Arrigoni G., Cavallari I., Belleudi F., Torrisi M.R., Silic-Benussi M., Ferro T., Petronilli V., Marin O., Chieco-Bianchi L., Bernardi P., Ciminale V. Mitochondrial alterations induced by the p13II protein of human T-cell leukemia virus type 1. Critical role of arginine residues. J. Biol. Chem. 277:2002;34424-34433.
62. Chen W., Calvo P.A., Malide D., Gibbs J., Schubert U., Bacik I., Basta S., O'Neill R., Schickli J., Palese P., Henklein P., Bennink J.R., Yewdell J.W. A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7:2001;1306-1312.
63. Macen J.L., Graham K.A., Lee S.F., Schreiber M., Boshkov L.K., McFadden G. Expression of the myxoma virus tumor necrosis factor receptor homologue and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology. 218:1996;232-237.
64. Everett H., Barry M., Lee S.F., Sun X., Graham K., Stone J., Bleackley R.C., McFadden G. M11L: A novel mitochondria-localized protein of myxoma virus that blocks apoptosis of infected leukocytes. J. Exp. Med. 191:2000;1487-1498.
65. Everett H., Barry M., Sun X., Lee S.F., Frantz C., Berthiaume L.G., McFadden G., Bleackley R.C. The myxoma provirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J. Exp. Med. 196:2002;1127-1139.
66. Wang H.W., Sharp T.V., Koumi A., Koentges G., Boshoff C. Characterization of an anti-apoptotic glycoprotein encoded by Kaposi's sarcoma-associated herpesvirus which resembles a spliced variant of human survivin. EMBO J. 21:2002;2602-2615.
67. Feng P.J., Park J., Lee B.S., Lee S.H., Bram R.J., Jung J.U. Kaposi's sarcoma-associated herpesvirus mitochondrial K7 protein targets a cellular calcium-modulating cyclophilin ligand to modulate intracellular calcium concentration and inhibit apoptosis. J. Virol. 76:2002;11491-11504.