Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis

Journal of Virology

Volumn 77, Issue 1, 2003, Pages 631-641

  McCormick, A Louise ^a   Smith, Vanessa L ^a   Chow, Dar ^a   Mocarski, Edward S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; DNA DAMAGE; FIBROBLAST; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; IMMEDIATE EARLY GENE; IMMUNE RESPONSE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; NATURAL KILLER CELL; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELLS, CULTURED; CYTOMEGALOVIRUS; HUMANS; IMMEDIATE-EARLY PROTEINS; MICE; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; VIRAL PROTEINS;

EID: 0037213306     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.1.631-641.2003     Document Type: Article

References (49)

1. Abbate, J., J.C. Lacayo, M. Prichard, G. Pari, and M. A. McVoy. 2001. Bifunctional protein conferring enhanced green fluorescence and puromycin resistance. BioTechniques 31:336-340.
2. Barber, G. N. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8:113-126.
3. Belzacq, A. S., C. El Hamel, H. L. Vieira, I. Cohen, D. Haouzi, D. Metivier, P. Marchetti, C. Brenner, and G. Kraemer. 2001. Adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437. Oncogene 20:7579-7587.
4. Borst, E. M., G. Hahn, U. H. Kaszinowski, and M. Messerle. 1999. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: A new approach for construction of HCMV mutants. J. Virol. 73:8320-8329.
5. Boya, P., B. Roques, and G. Kroemer. 2001. New EMBO members' review: Vital and bacterial proteins regulating apoptosis at the mitochondrial level. EMBO J. 20:4325-4331.
6. Brenner, C., H. Cadiou, H. L. Vieira, N. Zamzami, I. Marzo, Z. Xie, B. Leber, D. Andrews, H. Duclohier, J. C. Reed, and G. Kroemer. 2000. Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene 19:329-336.
7. Browne, E. P., B. Wing, D. Coleman, and T. Shenk. 2001. Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: Viral block to the accumulation of antiviral mRNAs. J. Virol. 75:12319-12330.
8. Colberg-Poley, A. M., M. B. Patel, D. P. Erezo, and J. E. Slater. 2000. Human cytomegalovirus UL37 immediate-early regulatory proteins traffic through the secretory apparatus and to mitochondria. J. Gen. Virol. 81:1779-1789.
9. Collier, N. C., M. P. Sheetz, and M. J. Schlesinger. 1993. Concomitant changes in mitochondria and intermediate filaments during heat shock and recovery of chicken embryo fibroblasts. J. Cell Biochem. 52:297-307.
10. Collins, T. J., M. J. Berridge, P. Lipp, and M. D. Bootman. 2002. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21:1616-1627.
11. Condreay, J. P., S. M. Witherspoon, W. C. Clay, and T. A. Kost. 1999. Transient and stable gene expression in mammalian cells transduced with a recombinant baculovirus vector. Proc. Natl. Acad. Sci. USA 96:127-132.
12. Cuconati, A., K. Degenhardt, R. Sundararajan, A. Anschel, and E. White. 2002. Bak and Bax function to limit adenovirus replication through apoptosis induction. J. Virol. 76:4547-4558.
13. De Vos, K., V. Goossens, E. Boone, D. Vercammen, K. Vancompernolle, P. Vandenabeele, G. Haegeman, W. Fiers, and J. Grooten. 1998. The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J. Biol. Chem. 273:9673-9680.
14. Edwards, K. M., J. E. Davis, K. A. Browne, V. R. Sutton, and J. A. Trapani. 1999. Anti-viral strategies of cytotoxic T lymphocytes are manifested through a variety of granule-bound pathways of apoptosis induction. Immunol. Cell Biol. 77:76-89.
15. Elmore, S. P., T. Qian, S. F. Grissom, and J. J. Lemasters. 2001. The mitochondrial permeability transition initiates autophagy in rat hepalocytes. FASEB J. 15:2286-2287.
16. Frank, S., B. Gaume, E. S. Belgmann-Leitner, W. W. Leitner, E. G. Robert, F. Catez, C. L. Smith, and R. J. Youle. 2001. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1:515-525.
17. Furukawa, T., S. Sakuma, and S. A. Plotkin. 1976. Human cytomegalovirus infection of WI-38 cells stimulates mitochondrial DNA synthesis. Nature 262:414-416.
18. Gilkerson, R. W., D. H. Margineantu, R. A. Capaldi, and J. M. Selker. 2000. Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett. 474:1-4
19. Goldmacher, V. S. 2002. vMIA, a viral inhibitor of apoptosis targeting mitochondria. Biochimie 84:177-185.
20. Goldmacher, V. S., L. M. Bartle, A. Skaletskaya, C. A. Dionne, N. L. Kedersha, C. A. Vater, J. Han, R. J. Lutz, S. Watanabe, E. D. McFarland, E. D. Kieff, E. S. Mocarski, and T. Chittenden. 1999. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. USA 96:12536-12541.
21. Greaves, R. F., J. M. Brown, J. Vieira, and E. S. Mocarski. 1995. Selectable insertion and deletion mutagenesis of the human cytomegalovirus genome using the Escherichia coli guanosine phosphoribosyl transferase (gpt) gene. J. Gen. Virol. 76:2151-2160.
22. Hayajneh, W. A., A. M. Colberg-Poley, A. Skalelskaya, L. M. Bartle, M. M. Lesperance, D. G. Contopoulos-Ioannidis, N. L. Kedersha, and V. S. Goldmacher. 2001. The sequence and antiapoptotic functional domains of the human cytomegalovirus UL37 exon 1 immediate early protein are conserved in multiple primary strains. Virology 279:233-240.
23. Hayajneh, W. A., D. G. Cantopoulos-Ioannidis, M. M. Lesperance, A. M. Venegas, and A. M. Collberg-Poley. 2001. The carboxyl terminus of the human cytomegalovirus UL37 immediate-early glycoprotein is conserved in primary strains and is important for transactivation. J. Gen. Virol. 82:1569-1579.
24. Jan, G., A. S. Belzacq, D. Haouzi, A. Rouault, D. Metivier, G. Kroemer, and C. Brenner. 2002. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ. 9:179-188.
25. Klionsky, D. J., and S. D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721.
26. Landini, M. P., and M. Rugolo. 1984. Increased accumulation of a lipophilic cation (tetraphenylphosphonium) in human embryo fibroblasts after infection with cytomegalovirus. J. Gen. Virol. 65:2269-2272.
27. Li, H., H. Zhu, C. J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501.
28. 1 phase of the cell cycle. J. Virol. 73:676-683.
29. Misaka, T., T. Miyashita, and Y. Kubo. 2002. Primary structure of a dynamin-related mouse mitochondrial GTPase and its distribution in brain, subcellular localization, and effect on mitochondrial morphology. J. Biol. Chem. 277:15834-15842.
30. Mocarski, E. S., Jr., and C. T. Courcelle. 2001. Cytomegaloviruses and their replication., p. 2629-2673. In D. M. Knipe, P. M. Howley, D. E. Griffin, et al. (ed.), Fields Virology. Lippincott Williams & Wilkins, Philadelphia, Pa.
31. Murata, T., F. Goshima, T. Daikoku, K. Inagaki-Ohara, H. Takakuwa, K. Kato, and Y. Nishiyama. 2000. Mitochondrial distribution and function in herpes simplex virus-infected cells. J. Gen. Virol. 81:401-06.
32. Murphy, E. A., D. N. Streblow, J. A. Nelson, and M. F. Stinski. 2000. The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells. J. Virol. 74:7108-7118.
33. Nechusbtan, A., C. L. Smith, I. Lamensdorf, S. H. Yoon, and R. J. Youle. 2001. Bax and Bak coalesce into mitochondria-associated clusters during apoptosis. J. Cell Biol. 153:1265-1276.
34. Nishiyama, Y., and T. Murata. 2002. Anti-apoptotic protein kinase of herpes simplex virus. Trends Microbiol. 10:105-107.
35. Patterson, C. E., and T. Shenk. 1999. Human cytomegalovirus UL36 protein is dispensable for viral replication in cultured cells. J. Virol. 73:7126-7131.
36. Penfold, M. E., and E. S. Mocarski. 1997. Formation of cytomegalovirus DNA replication compartments defined by localization of viral proteins and DNA synthesis. Virology 239:46-61.
37. Simmen, K. A., J. Singh, B. G. Luukkonen, M. Lopper, A. Bittner, N. E. Miller, M. R. Jackson, T. Compton, and K. Fruh. 2001. Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc. Natl. Acad. Sci. USA 98:7140-7145.
38. Skaletskaya, A., L. M. Bartle, T. Chittenden, A. L. McCormick, E. S. Mocarski, and V. S. Goldmacher. 2001. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. USA 98:7829-7834.
39. Spector, D., R. Goldman, and L. Leinwand (ed.). 1998. Cells: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
40. Tanaka, K., J. P. Zou, K. Takeda, V. J. Ferrans, G. R. Sandford, T. M. Johnson, T. Finkel, and S. E. Epstein. 1999. Effects of human cytomegalovirus immediate-early proteins on p53-mediated apoptosis in coronary artery smooth muscle cells. Circulation 99:1656-1659.
41. Tanaka, Y., Y. Kanai, Y. Okada, S. Nonaka, S. Takeda, A. Harada, and N. Hirokawa. 1998. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93:1147-1158.
42. Tolkovsky, A. M., L Xue, G. C. Fletcher, and V. Borutaite. 2002. Mitochondrial disappearance from cells: A clue to the role of autophagy in programmed cell death and disease? Biochimie 84:233-240.
43. Vieira, H. L., A. S. Belzacq, D. Haouzi, F. Bernassola, I. Cohen, E. Jacotot, K. F. Ferri, C. El Hamel, L. M. Bartle, G. Melino, C. Brenner, V. Goldmachar, and G. Kroemer. 2001. The adenine nucleotide translocator: A target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20:4305-4316.
44. Wallach, D., E. E. Varfolomeev, N. L. Malinin, Y. V. Goitsev, A. V. Kovalenko, and M. P. Boldin. 1999. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol. 17:331-367.
45. White, E. 2001. Regulation of the cell cycle and apoptosis by the oncogenes of adenovirus. Oncogene 20:7836-7846.
46. Yaffe, M. P. 1999. The machinery of mitochondrial inheritance and behavior. Science 283:1493-1497.
47. Yu, Y., and J. C. Alwine. 2002. Human cytomegalovirus major immediateearly proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylillosilide 3′-OH kinase pathway and the cellular kinase Akt. J. Virol. 76:3731-3738.
48. Zhou, G., V. Galvan, G. Campadelli-Fiume, and B. Roizman. 2000. Glycoprotein D or J delivered in trans blocks apoptosis in SK-N-SH cells induced by a herpes simplex virus 1 mutant lacking intact genes expressing both glycoproteins. J. Virol. 74:11782-11791.
49. Zhu, H., Y. Shen, and T. Shenk. 1995. Human cytomegalovirus IE1 and IE2 proteins block apoplosis. J. Virol. 69:7960-7970.