Encephalomyocarditis virus 2A protein is required for viral pathogenesis and inhibition of apoptosis

Journal of Virology

Volumn 85, Issue 20, 2011, Pages 10741-10754

  Carocci, M ^a   Cordonnier, N ^a   Huet, H ^a   Romey, A ^a   Relmy, A ^a   Gorna, K ^a   Blaise Boisseau, S ^a   Zientara, S ^a   Kassimi, L Bakkali ^a  

^a ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2A PROTEIN; CASPASE 3; COMPLEMENTARY DNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CLINICAL FEATURE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DEATH; ENCEPHALOMYOCARDITIS VIRUS; ENZYME ACTIVATION; FEMALE; GENE DELETION; HISTOPATHOLOGY; HOST RESISTANCE; IN VITRO STUDY; INHIBITION KINETICS; INOCULATION; MOLECULAR CLONING; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PATHOGENESIS; PICORNAVIRUS; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS ENCEPHALITIS; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; APOPTOSIS; CARDIOVIRUS INFECTIONS; CELL LINE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CRICETINAE; DISEASE MODELS, ANIMAL; ENCEPHALOMYOCARDITIS VIRUS; FEMALE; MICE; MICE, INBRED C57BL; MUTANT PROTEINS; RODENT DISEASES; SEQUENCE DELETION; SURVIVAL ANALYSIS; VIRAL PROTEINS; VIRULENCE FACTORS; VIRUS RELEASE; VIRUS REPLICATION;

ENCEPHALOMYOCARDITIS VIRUS; MUS; PICORNAVIRIDAE;

EID: 80054997211     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00394-11     Document Type: Article

References (56)

1. Agol, V. I., and A. P. Gmyl. 2010. Viral security proteins: counteracting host defences. Nat. Rev. Microbiol. 8:867-878.
2. Aminev, A. G., S. P. Amineva, and A. C. Palmenberg. 2003. Encephalomyocarditis viral protein 2A localizes to nucleoli and inhibits cap-dependent mRNA translation. Virus Res. 95:45-57.
3. Ano, Y., et al. 2010. Oxidative damage to neurons caused by the induction of microglial NADPH oxidase in encephalomyocarditis virus infection. Neurosci. Lett. 469:39-43.
4. Autret, A., et al. 2008. Early phosphatidylinositol 3-kinase/Akt pathway activation limits poliovirus-induced JNK-mediated cell death. J. Virol. 82: 3796-3802.
5. Bae, Y. S., and J. W. Yoon. 1993. Determination of diabetogenicity attributable to a single amino acid, Ala776, on the polyprotein of encephalomyocarditis virus. Diabetes 42:435-443.
6. Bedard, K. M., and B. L. Semler. 2004. Regulation of picornavirus gene expression. Microbes Infect. 6:702-713.
7. Beretta, L., Y. V. Svitkin, and N. Sonenberg. 1996. Rapamycin stimulates viral protein synthesis and augments the shutoff of host protein synthesis upon picornavirus infection. J. Virol. 70:8993-8996.
8. Breiman, A., et al. 2005. Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKepsilon. J. Virol. 79:3969-3978.
9. Brewer, L. A., et al. 2001. Porcine encephalomyocarditis virus persists in pig myocardium and infects human myocardial cells. J. Virol. 75:11621-11629.
10. Buenz, E. J., et al. 2009. Apoptosis of hippocampal pyramidal neurons is virus independent in a mouse model of acute neurovirulent picornavirus infection. Am. J. Pathol. 175:668-684.
11. Cerutis, D. R., R. H. Bruner, D. C. Thomas, and D. J. Giron. 1989. Tropism and histopathology of the D, B, K, andMMvariants of encephalomyocarditis virus. J. Med. Virol. 29:63-69.
12. Cui, T., S. Sankar, and A. G. Porter. 1993. Binding of encephalomyocarditis virus RNA polymerase to the 3'-noncoding region of the viral RNA is specific and requires the 3'-poly(A) tail. J. Biol. Chem. 268:26093-26098.
13. Denis, P., and F. Koenen. 2003. Molecular analysis of the capsid coding region of a virulent encephalomyocarditis virus isolate after serial cell passages and assessment of its virulence. Arch. Virol. 148:903-912.
14. Denis, P., et al. 2006. Genetic variability of encephalomyocarditis virus (EMCV) isolates. Vet. Microbiol. 113:1-12.
15. Edinger, A. L., and C. B. Thompson. 2004. Death by design: apoptosis, necrosis and autophagy. Curr. Opin. Cell Biol. 16:663-669.
16. Esfandiarei, M., et al. 2007. Coxsackievirus B3 activates nuclear factor kappa B transcription factor via a phosphatidylinositol-3 kinase/protein kinase Bdependent pathway to improve host cell viability. Cell. Microbiol. 9:2358-2371.
17. Fan, J., K. N. Son, S. Y. Arslan, Z. Liang, and H. L. Lipton. 2009. Theiler's murine encephalomyelitis virus leader protein is the only nonstructural protein tested that induces apoptosis when transfected into mammalian cells. J. Virol. 83:6546-6553.
18. Fultz, P. N., et al. 2001. In vivo attenuation of simian immunodeficiency virus by disruption of a tyrosine-dependent sorting signal in the envelope glycoprotein cytoplasmic tail. J. Virol. 75:278-291.
19. Galluzzi, L., et al. 2010. Viral strategies for the evasion of immunogenic cell death. J. Intern. Med. 267:526-542.
20. Groppo, R., B. A. Brown, and A. C. Palmenberg. 2011. Mutational analysis of the EMCV 2A protein identifies a nuclear localization signal and an eIF4E binding site. Virology 410:257-267.
21. Groppo, R., and A. C. Palmenberg. 2007. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 81:13067-13074.
22. Hahn, H., and A. C. Palmenberg. 2001. Deletion mapping of the encephalomyocarditis virus primary cleavage site. J. Virol. 75:7215-7218.
23. Hayden, M. S., and S. Ghosh. 2004. Signaling to NF-kappaB. Genes Dev. 18:2195-2224.
24. Jen, G., B. M. Detjen, and R. E. Thach. 1980. Shutoff of HeLa cell protein synthesis by encephalomyocarditis virus and poliovirus: a comparative study. J. Virol. 35:150-156.
25. Jones, P., et al. 2011. Encephalomyocarditis virus mortality in semi-wild bonobos (Pan panicus). J. Med. Primatol. 40:157-163.
26. Kanda, T., et al. 1999. Increased severity of viral myocarditis in mice lacking lymphocyte maturation. Int. J. Cardiol. 68:13-22.
27. Kassimi, L. B., A. Boutrouille, M. Gonzague, A. L. Mbanda, and C. Cruciere. 2002. Nucleotide sequence and construction of an infectious cDNA clone of an EMCV strain isolated from aborted swine fetus. Virus Res. 83:71-87.
28. Kim, H. S., W. T. Christianson, and H. S. Joo. 1989. Pathogenic properties of encephalomyocarditis virus isolates in swine fetuses. Arch. Virol. 109:51-57.
29. LaRue, R., et al. 2003. A wild-type porcine encephalomyocarditis virus containing a short poly(C) tract is pathogenic to mice, pigs, and cynomolgus macaques. J. Virol. 77:9136-9146.
30. Low, A., et al. 2007. Mutation in the glycosylated gag protein of murine leukemia virus results in reduced in vivo infectivity and a novel defect in viral budding or release. J. Virol. 81:3685-3692.
31. Lu, Q. 2005. Seamless cloning and gene fusion. Trends Biotechnol. 23:199-207.
32. Marcucci, K. T., Y. Martina, F. Harrison, C. A. Wilson, and D. R. Salomon. 2008. Functional hierarchy of two L domains in porcine endogenous retrovirus (PERV) that influence release and infectivity. Virology 375:637-645.
33. Medvedkina, O. A., I. V. Scarlat, N. O. Kalinina, and V. I. Agol. 1974. Virus-specific proteins associated with ribosomes of Krebs-II cells infected with encephalomyocarditis virus. FEBS Lett. 39:4-8.
34. Nakayama, Y., W. Su, A. Ohguchi, H. Nakayama, and K. Doi. 2004. Experimental encephalomyocarditis virus infection in pregnant mice. Exp. Mol. Pathol. 77:133-137.
35. Neznanov, N., et al. 2001. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface. J. Virol. 75:10409-10420.
36. Oberste, M. S., et al. 2009. Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg. Infect. Dis. 15:640-646.
37. Ohguchi, A., et al. 2006. Encepalomyocarditis virus-induced apoptosis and ultrastructural changes in the lacrimal and parotid glands of mice. Exp. Mol. Pathol. 80:201-207.
38. Okuwa, T., N. Taniura, M. Saito, T. Himeda, and Y. Ohara. 2010. Opposite effects of two nonstructural proteins of Theiler's murine encephalomyelitis virus regulates apoptotic cell death in BHK-21 cells. Microbiol. Immunol. 54:639-643.
39. Palmenberg, A. C., et al. 1984. The nucleotide and deduced amino acid sequences of the encephalomyocarditis viral polyprotein coding region. Nucleic Acids Res. 12:2969-2985.
40. Psalla, D., et al. 2006. Pathogenesis of experimental encephalomyocarditis: a histopathological, immunohistochemical and virological study in mice. J. Comp. Pathol. 135:142-145.
41. Romanova, L. I., et al. 2009. Antiapoptotic activity of the cardiovirus leader protein, a viral "security" protein. J. Virol. 83:7273-7284.
42. Roos, F. C., et al. 2010. Oncolytic targeting of renal cell carcinoma via encephalomyocarditis virus. EMBO Mol. Med. 2:275-288.
43. Salako, M. A., M. J. Carter, and G. E. Kass. 2006. Coxsackievirus protein 2BC blocks host cell apoptosis by inhibiting caspase-3. J. Biol. Chem. 281: 16296-16304.
44. Schwarz, E. M., et al. 1998. NF-kappaB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: a mechanism of resistance in p50 knockout mice. J. Virol. 72:5654-5660.
45. Sriram, S., D. J. Topham, S. K. Huang, and M. Rodriguez. 1989. Treatment of encephalomyocarditis virus-induced central nervous system demyelination with monoclonal anti-T-cell antibodies. J. Virol. 63:4242-4248.
46. Stellmann, C., and P. Bornarel. 1971. Calculation tables of D 50 titres of viral suspensions and their accuracy. Ann. Inst. Pasteur (Paris) 121:825-833.
47. Svitkin, Y. V., H. Hahn, A. C. Gingras, A. C. Palmenberg, and N. Sonenberg. 1998. Rapamycin and wortmannin enhance replication of a defective encephalomyocarditis virus. J. Virol. 72:5811-5819.
48. Takeda, M., K. Hirasawa, and K. Doi. 1991. Lesions in the central nervous system of DBA/2 mice infected with the D variant of encephalomyocarditis virus (EMC-D). J. Vet. Med. Sci. 53:1013-1017.
49. Takeda, M., S. Itagaki, and K. Doi. 1993. Biphasic disease of central nervous system induced in DBA/2 mice by the D variant of encephalomyocarditis virus (EMC-D). Int. J. Exp. Pathol. 74:493-499.
50. Takeda, M., et al. 1995. Distribution of viral RNA in the spinal cord of DBA/2 mice developing biphasic paralysis following infection with the D variant of encephalomyocarditis virus (EMC-D). Int. J. Exp. Pathol. 76:441-447.
51. Takeda, M., R. Ohtsuka, Y. Nakayama, and K. Doi. 2004. The role of CD4(+) T cells in biphasic hind limb paralysis induced by the D variant of encephalomyocarditis virus (EMC-D) in DBA/2 mice. Exp. Anim. 53:31-35.
52. Tanaka, N., et al. 1998. Type I interferons are essential mediators of apoptotic death in virally infected cells. Genes Cells 3:29-37.
53. Vanderplasschen, A., M. Hollinshead, and G. L. Smith. 1997. Antibodies against vaccinia virus do not neutralize extracellular enveloped virus but prevent virus release from infected cells and comet formation. J. Gen. Virol. 78(Pt. 8):2041-2048.
54. Vlemmas, J., et al. 2000. Immunohistochemical detection of encephalomyocarditis virus (EMCV) antigen in the heart of experimentally infected piglets. J. Comp. Pathol. 122:235-240.
55. Yeung, M. C., D. L. Chang, R. E. Camantigue, and A. S. Lau. 1999. Inhibitory role of the host apoptogenic gene PKR in the establishment of persistent infection by encephalomyocarditis virus in U937 cells. Proc. Natl. Acad. Sci. U. S. A. 96:11860-11865.
56. Yoon, J. W., and H. S. Jun. 2006. Viruses cause type 1 diabetes in animals. Ann. N. Y. Acad. Sci. 1079:138-146.