The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore

Journal of Experimental Medicine

Volumn 196, Issue 9, 2002, Pages 1127-1139

  Everett, Helen ^a   Barry, Michele ^a   Sun, Xuejun ^a   Lee, Siow Fong ^b   Frantz, Christine ^a   Berthiaume, Luc G ^a   McFadden, Grant ^c   Chris Bleackley, R ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA HOSPITAL   (Canada)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Apoptosis; Mitochondria; PK11195; Poxviridae; Protoporphyrin IX

Indexed keywords

CYTOCHROME C; ISOQUINOLINE DERIVATIVE; M11L PROTEIN; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; PROTEIN BCL 2; PROTOPORPHYRIN; STAUROSPORINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRUS PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CROSS LINKING; DRUG PROTEIN BINDING; ENERGY TRANSFER; FLUORESCENCE; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MYXOMA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS VIRULENCE;

ANIMALS; APOPTOSIS; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; ION CHANNELS; JURKAT CELLS; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYXOMA VIRUS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTOPORPHYRINS; RECEPTORS, GABA-A; RECOMBINANT FUSION PROTEINS; VIRAL PROTEINS;

EID: 0037020864     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20011247     Document Type: Article

References (66)

1. Zimmermann, K.C., C. Bonzon, and D.R. Green. 2001. The machinery of programmed cell death. Pharmacol. Ther. 92:57-70.
2. Hay, S.W., and G. Kannourakis. 2002. A time to kill: Viral manipulation of the cell death program. J. Gen. Virol. 83: 1547-1564.
3. Roulston, A., R.C. Marcellus, and P.E. Branton. 1999. Viruses and apoptosis. Annu. Rev. Microbiol. 53:577-628.
4. Nash, P., J. Barrett, J.-X. Cao, S. Hota-Mitchell, A. Lalani, H. Everett, X.-M. Xu, J. Robichaud, S. Hnatiuk, C. Ainslie, et al. 1999. Immunomodulation by viruses: The myxoma virus story, Immunol. Rev. 168:103-120.
5. Macen, J.L., K.A. Graham, S.F. Lee, M. Schreiber, L.K. Boshkov, and G. McFadden. 1996. Expression of the myxoma virus tumor necrosis factor receptor homologue (T2) and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology. 218:232-237.
6. Everett, H., M. Barry, S.-F. Lee, X. Sun, K. Graham, J. Stone, R.C. Bleackley, and G. McFadden. 2000. M11L: A novel mitochondria-localized protein of myxoma virus that blocks apoptosis of infected leukocytes. J. Exp. Med. 191: 1487-1498.
7. Opgenorth, A., K. Graham, N. Nation, D. Strayer, and G. McFadden. 1992. Deletion analysis of two tandemly arranged virulence genes in myxoma virus, M11L and myxoma growth factor. J. Virol. 66:4720-4731.
8. Bernardi, P., V. Petronilli, F. Di Lisa, and M. Forte. 2001. A mitochondrial perspective on cell death. Trends Biochem. Sci. 26:112-117.
9. Ferri, K.F., and G. Kroemer. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:E255-E263.
10. Wang, X. 2001. The expanding role of mitochondria in apoptosis. Genes Dev. 15:2922-2933.
11. Parone, P.A., D. James, and J.-C. Martinou. 2002. Mitochondria: Regulating the inevitable. Biochimie. 84:105-111.
12. Crompton, M. 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:233-249.
13. Gross, A., J.M. McDonnell, and S.J. Korsmeyer. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899-1911.
14. Harris, M.H., and C.B. Thompson. 2000. The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 7:1182-1191.
15. Everett, H., and G. McFadden. 2001. Viruses and apoptosis: Meddling with mitochondria. Virology. 288:1-7.
16. Boya, P., B. Roques, and G. Kroemer. 2001. Viral and bacterial proteins regulating apoptosis at the mitochondrial level. EMBO J. 20:4325-4331.
17. Goldmacher, V.S., L.M. Bartle, A. Skaletskaya, C.A. Dionne, N.L. Kedersha, C.A. Vater, J.-W. Han, R.J. Lutz, S. Watanabe, E.D. Cahir McFarland, et al. 1999. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. USA. 96: 12536-12541.
18. Jacotot, E., L. Ravagnan, M. Loeffler, K.F. Ferri, H.L.A. Vieira, N. Zamzami, P. Costantini, S. Druillennec, J. Hoebeke, J.P. Briand, et al. 2000. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 191:33-45.
19. Jacotot, E., K.F. Ferri, C. El Hamel, C. Brenner, S. Druillennec, J. Hoebeke, P. Rustin, D. Metivier, C. Lenoir, M. Geuskens, et al. 2001. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2. J. Exp. Med. 193: 509-519.
20. Rahmani, Z., K.-W. Huh, R. Lasher, and A. Siddiqui. 2000. Hepatitis B virus X protein colocalizes to mitochondria with a human voltage-dependent anion channel, HVDAC3, and alters its transmembrane potential. J. Virol. 74:2840-2846.
21. Casellas, P., S. Galiegue, and A.S. Basile. 2002. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem. Int. 40:475-486.
22. Gavish, M., I. Bachman, R. Shoukrun, Y. Katz, L. Veenman, G. Weisinger, and A. Weizman. 1999. Enigma of the peripheral benzodiazepine receptor. Pharmacol. Rev. 51:629-650.
23. McEnery, M.W., A.M. Snowman, R.R. Trifiletti, and S.H. Snyder. 1992. Isolation of the mitochondrial benzodiazepine receptor: Association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc. Natl. Acad. Sci. USA. 89:3170-3174.
24. Culty, M., H. Li, N. Boujrad, H. Amri, B. Vidic, J.M. Bernassau, J.L. Reversat, and V. Papadopoulos. 1999. In vitro studies on the role of the peripheral-type benzodiazepine receptor in steroidogenesis. J. Steroid Biochem. Mol. Biol. 69: 123-130.
25. Kroemer, G., and J.C. Reed. 2000. Mitochondrial control of cell death. Nat. Med. 6:513-519.
26. Papadopoulos, V., N. Boujrad, M.D. Ikonomovic, P. Ferrara, and B. Vidic. 1994. Topography of the Leydig cell mitochondrial peripheral-type benzodiazepine receptor. Mol. Cell. Endocrinol. 104:R5-R9.
27. Braestrup, C., and R.F. Squires. 1977. Specific benzodiazepine receptors in rat brain characterized by high-affinity [3H]diazepam binding. Proc. Natl. Acad. Sci. USA. 74:3805-3809.
28. Carayon, P., M. Portier, D. Dussossoy, A. Bord, G. Petitpretre, X. Canat, G. Le Fur, and P. Casellas. 1996. Involvement of peripheral benzodiazepine receptors in the protection of hematopoietic cells against oxygen radical damage. Blood. 87:3170-3178.
29. Dussossoy, D., P. Carayon, D. Feraut, S. Belugou, T. Combes, X. Canat, H. Vidal, and P. Casellas. 1996. Development of a monoclonal antibody to immuno-cytochemical analysis of the cellular localization of the peripheral benzodiazepine receptor. Cytometry. 24:39-48.
30. Verma, A., and S.H. Snyder. 1988. Characterization of porphyrin interactions with peripheral type benzodiazepine receptors. Mol. Pharmacol. 34:800-805.
31. Torres, S.R., T.S. Frode, G.M. Nardi, N. Vita, R. Reeb, P. Ferrara, R.M. Ribeiro-do-Valle, and R.C. Farges. 2000. Anti-inflammatory effects of peripheral benzodiazepine receptor ligands in two mouse models of inflammation. Eur. J. Pharmacol. 408:199-211.
32. Klegeris, A., E.G. McGeer, and P.L. McGeer. 2000. Inhibitory action of 1-(2-chlorophenyl-N-methyl-N- (1-methylpropyl)-3-isoquinolinecarboxamide (PK11195) on some mononuclear phagocyte functions. Biochem. Pharmacol. 59: 1305-1314.
33. Stoebner, P.-E., P. Carayon, P. Casellas, M. Portier, T. Lavabre-Bertrand, P. Cuq, J.-P. Cano, J. Meynadier, and L. Meunier. 2001. Transient protection by peripheral benzodiazepine receptors during the early events of ultraviolet light-induced apoptosis. Cell Death Differ. 8:747-753.
34. Johnston, C., W. Jiang, T. Chu, and B. Levine. 2001. Identification of genes involved in the host response to neuroviru neurovir-ulent alphavirus infection. J. Virol. 75:10431-10445.
35. Marchetti, P., T. Hirsch, N. Zamzami, M. Castedo, D. Decaudin, S.A. Susin, B. Masse, and G. Kroemer. 1996. Mitochondrial permeability transition triggers lymphocyte apoptosis. J. Immunol. 157:4830-4836.
36. Fischer, R., M. Schmitt, J.G. Bode, and D. Haussinger. 2001. Expression of the peripheral-type benzodiazepine receptor and apoptosis induction in hepatic stellate cells. Gastroenterology. 120:1212-1226.
37. Fennel, D.A., M. Corbo, A. Pallaska, and F.E. Cotter. 2001. Bcl-2 resistant mitochondrial toxicity mediated by the isoquinoline carbozamide PK11195 involves de novo generation of reactive oxygen species. Br. J. Cancer. 84:1397-1404.
38. Maaser, K., M. Hopfner, A. Jansen, G. Weisinger, M. Gavish, A.P. Kozikowski, A. Weizman, P. Carayon, E.O. Reicken, M. Zeitz, and H. Scherubi. 2001. Specific ligands of the peripheral benzodiazepine receptor induce apoptosis and cell cycle arrest in human colorectal cancer cells. Br. J. Cancer. 85:1771-1780.
39. Chelli, B., A. Falleni, F. Salvetti, V. Gremigni, A. Lucacchini, and C. Martini. 2001. Peripheral-type benzodiazepine receptor ligands: Mitochondrial permeability transition induction in rat cardiac tissue. Biochem. Pharmacol. 61:695-705.
40. Pastorino, J.G., G. Simbula, E. Gilfor, J.B. Hoek, and J.L. Farber. 1994. Protoporphyrin IX, an endogenous ligand of the peripheral benzodiazepine receptor, potentiates induction of the mitochondrial permeability transition and the killing of cultured hepatocytes by rotenone. J. Biol. Chem. 269:31041-31046.
41. Pastorino, J.G., G. Simbula, K. Yamamoto, P.A. Glascott, R.J. Rothman, and J.L. Farber. 1996. The cytotoxicity of tumor necrosis factor depends on induction of the mitochondrial permeability transition. J. Biol. Chem. 271:29792-29798.
42. Bono, F., I. Lamarche, V. Prabonnaud, G. Le Fur, and J.M. Herbert. 1999. Peripheral benzodiazepine receptor agonists exhibit potent and apoptotic activities. Biochem. Biophys. Res. Commun. 265:457-461.
43. Hirsch, T., D. Decaudin, S.A. Susin, P. Marchetti, N. Larochette, M. Resche-Rignon, and G. Kroemer. 1998. PK11195, a ligand of the mitochondrial benzodiazepine receptor, facilitates the induction of apoptosis and reverses Bcl-2-mediated cytoprotection. Exp. Cell Res. 241:426-434.
44. Ravagnan, L., I. Marzo, P. Constantini, S.A. Susin, N. Zamzami, P.X. Petit, F. Hirsch, M. Goulbern, M.-F. Poupon, L. Miccoli, et al. 1999. Londamine triggers apoptosis via a direct, Bcl-2-inhibited effect on the mitochondrial permeability transition pore. Ontogene. 18:2537-2546.
45. Larochette, N., D. Decaudin, E. Jacotot, C. Brenner, I. Marzo, S.A. Susin, N. Zamzami, Z. Xie, J. Reed, and G. Kroemer. 1999. Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp. Cell Res. 249:413-421.
46. Tanimoto, Y., Y. Onishi, Y. Sato, and H. Kizaki. 1999. Benzodiazepine receptor agonists modulate thymocyte apoptosis through reduction of the mitochondrial transmembrane transmembrane potential. Jpn. J. Pharmacol. 79:177-183.
47. Lilge, L., M. Portnoy, and B.C. Wilson. 2000. Apoptosis induced in vivo by photodynamic therapy in normal brain and intracranial tumor tissue. Br. J. Cancer. 83:1110-1117.
48. Noodt, B.B., K. Berg, T. Stokke, Q. Peng, and J.M. Nesland. 1996. Apoptosis and necrosis induced with light and 5-aminolaevulinic acid-derived protoporphyrin IX. Br. J. Cancer. 74:22-29.
49. Graham, K.A., A. Opgenorth, C. Upton, and G. McFadden. 1992. Myxoma virus M11L ORF encodes a protein for which cell surface localization is critical for manifestation of viral virulence. Virology. 191:112-124.
50. Kozikowski, A.P., M. Kotoula, D. Ma, N. Boujrad, W. Tuckmantel, and V. Papadopoulos. 1997. Synthesis and biology of a 7-Nitro-2,1,3-benzoxadiazol-4-yl derivative of 2-Phenylindole-3-acetamide: A fluorescent probe for the peripheral-type benzodiazepine receptor. J. Med. Chem. 40: 2435-2439.
51. Bastiaens, P.I., I.V. Majoul, P.J. Verveer, H.D. Soling, and T.M. Jovin. 1996. Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15:4246-4253.
52. Dickinson, M.E., G. Bearman, S. Tilie, R. Lansford, and S.E. Fraser. 2001. Multi-spectral imaging and linear unmixing add a whole new dimension to laser scanning fluorescence microscopy. Biotechniques. 31:1272-1278.
53. Farkas, D.L., M. Wei, P. Febbroriello, J.H. Carson, and L.M. Loew. 1989. Simultaneous imaging of cell and mitochondrial membrane potential. Biophys. J. 56:1053-1069.
54. Stryer, L. 1978. Fluorescence energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47:819-846.
55. Förster, T. 1948. Intermolecular energy migration and fluorescence. Ann. Physiol. 2:55-75.
56. Bastiaens, P.I., and A. Squire. 1999. Fluorescence lifetime imaging microscopy: Spatial resolution of biochemical processes in the cell. Trends Cell Biol. 9:48-52.
57. Xia, Z., and Y. Liu. 2001. Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes. Biophys. J. 81:2395-2402.
58. Mossman, K., C. Upton, and G. McFadden. 1995. The myxoma virus soluble interferon-γ receptor homolog, M-T7, inhibits interferon-γ in a species specific manner. J. Biol. Chem. 270:3031-3038.
59. r 18,000 subunit of the peripheral-type benzodiazepine receptor exhibits both benzodiazepine and isoquinoline carboxamide binding sites in the absence of the voltage-dependent anion channel or of the adenine nucleotide carrier. J. Biol. Chem. 272:28102-28106.
60. Nguyen, M., D.G. Millar, V.W. Youg, S.J. Korsmeyer, and G.C. Shore. 1993. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J. Biol. Chem. 268:25265-25268.
61. Nguyen, M., P.E. Branton, P.A. Walton, Z.N. Oltvai, S.J. Korsmeyer, and G.C. Shore. 1994. Role of the membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J. Biol. Chem. 269:16521-16524.
62. Tanaka, S., K. Saito, and J.C. Reed. 1993. Structure-function analysis of the bcl-2 oncoprotein. J. Biol. Chem. 268:10920-10926.
63. Zhu, W., A. Cowie, G.W. Wasfy, L.Z. Penn, B. Leber, and D.W. Andrews. 1996. Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J. 15:4130-4141.
64. Froesch, B.A., C. Aime-Sempe, B. Leber, D. Andrews, and J.C. Reed. 1999. Inhibition of p53 transcriptional activity by Bcl-2 requires its membrane-anchoring domain. J. Biol. Chem. 274:6469-6475.
65. Bellows, D.S., B.N. Chau, P. Lee, Y. Lazebnik, W.H. Bums, and J.M. Hardwick. 2000. Antiapoptotic herpesvirus Bcl-2 homologs escape caspase-mediated conversion to proapoptotic proteins. J. Virol. 74:5024-5031.
66. Savill, J. 1997. Apoptosis in the resolution of inflammation. J. Leukoc. Biol. 61:375-380.