Increased ubiquitination and other covariant phenotypes attributed to a strain- and temperature-dependent defect of reovirus core protein μ2

Journal of Virology

Volumn 78, Issue 19, 2004, Pages 10291-10302

  Miller, Cathy L ^a   Parker, John S L ^d   Dinoso, Jason B ^a   Piggott, Caroline D S ^a,b   Perron, Michel J ^a,c   Nibert, Max L ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD COLLEGE   (United States)

^c HARVARD UNIVERSITY   (United States)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; NOCODAZOLE; UBIQUITIN;

ALLELE; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL GROWTH; CONJUGATION; CONTROLLED STUDY; GENE LOCATION; GENE MAPPING; GENETIC CODE; GENETIC TRANSFECTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LABORATORY; MICROTUBULE; MORPHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; REOVIRUS; STAINING; TEMPERATURE DEPENDENCE; UBIQUITINATION; VIRUS CHARACTERIZATION; VIRUS CORE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS INFECTION; VIRUS ISOLATION; VIRUS STRAIN;

AMINO ACID SUBSTITUTION; GENES, VIRAL; INCLUSION BODIES, VIRAL; MICROTUBULES; NOCODAZOLE; ORTHOREOVIRUS; PHENOTYPE; PROTEIN FOLDING; REASSORTANT VIRUSES; RNA REPLICASE; TEMPERATURE; UBIQUITIN; VIRAL CORE PROTEINS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 4544281312     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.19.10291-10302.2004     Document Type: Article

References (52)

1. Becker, M. M., M. I. Goral, P. R. Hazelton, G. S. Baer, S. E. Rodgers, E. G. Brown, K. M. Coombs, and T. S. Dermody. 2001. Reovirus σNS protein is required for nucleation of viral assembly complexes and formation of viral inclusions. J. Virol. 75:1459-1475.
2. Becker, M. M., T. R. Peters, and T. S. Dermody. 2003. Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J. Virol. 77:5948-5963.
3. Bence, N. F., R. M. Sampat, and R. R. Kopito. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555.
4. Bodkin, D. K., and B. N. Fields. 1989. Growth and survival of reovirus in intestinal tissue: role of the L2 and S1 genes. J. Virol. 63:1188-1193.
5. Brentano, L., D. L. Noah, E. G. Brown, and B. Sherry. 1998. The reovirus protein μ2, encoded by the M1 gene, is an RNA-binding protein. J. Virol. 72:8354-8357.
6. Broering, T., A. McCutcheon, V. Centonze, and M. Nibert. 2000. Reovirus nonstructural protein μNS binds to reovirus cores but does not inhibit their transcription activity. J. Virol. 74:5516-5524.
7. Broering, T. J., J. Kim, C. L. Miller, C. D. S. Piggott, J. B. Dinoso, M. L. Nibert, and J. S. L. Parker. 2004. Reovirus nonstructural protein μNS recruits viral core surface proteins and entering core particles to factory-like inclusions. J. Virol. 78:1882-1892.
8. Broering, T. J., J. S. L. Parker, P. L. Joyce, J. Kim, and M. L. Nibert. 2002. Mammalian reovirus nonstructural protein μNS forms large inclusions and colocalizes with reovirus microtubule-associated protein μ2 in transfected cells. J. Virol. 76:8285-8297.
9. Brown, E. G., M. L. Nibert, and B. N. Fields. 1983. The L2 gene of reovirus serotype 3 controls the capacity to interfere, accumulate deletions, and establish persistent infection, p. 275-288. In R. W. Compans and D. H. L. Bishop (ed.), Double-stranded RNA viruses. Elsevier, New York, N.Y.
10. Coombs, K. M. 1996. Identification and characterization of a double-stranded RNA-reovirus temperature-sensitive mutant defective in minor core protein μ2. J. Virol. 70:4237-4245.
11. Coombs, K. M. 1998. Stoichiometry of reovirus structural proteins in virus, ISVP, and core particles. Virology 243:218-228.
12. Coombs, K. M., B. N. Fields, and S. C. Harrison. 1990. Crystallization of the reovirus type 3 Dearing core. Crystal packing is determined by the λ2 protein. J. Mol. Biol. 215:1-5.
13. Dales, S., P. Gomatos, and K. C. Hsu. 1965. The uptake and development of reovirus in strain L cells followed with labelled viral ribonucleic acid and ferritin-antibody conjugates. Virology 25:193-211.
14. Drayna, D., and B. N. Fields. 1982. Activation and characterization of the reovirus transcriptase: genetic analysis. J. Virol. 41:110-118.
15. Fujimuro, M., H. Sawada, and H. Yokosawa. 1994. Production and characterisation of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349:173-180.
16. Furlong, D. B., M. L. Nibert, and B. N. Fields. 1988. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 62:246-256.
17. Furman, M. H., and H. L. Ploegh. 2002. Lessons from viral manipulation of protein disposal pathways. J. Clin. Investig. 110:875-879.
18. m-C. Prog. Nucleic Acid Res. Mol. Biol. 19:3-20.
19. Garcia-Mata, R., Y. S. Gao, and E. Sztul. 2002. Hassles with taking out the garbage: aggravating aggresomes. Traffic 3:388-396.
20. Goldberg, A. L. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426:895-899.
21. Gomatos, P. J., I. Tamm, S. Dales, and R. M. Franklin. 1962. Reovirus type 3: physical characteristics and interactions with L cells. Virology 17:441-454.
22. Goral, M. I., M. Mochow-Grundy, and T. S. Dermody. 1996. Sequence diversity within the reovirus S3 gene: reoviruses evolve independently of host species, geographic locale, and date of isolation. Virology 216:265-271.
23. Haller, B. L., M. L. Barkon, G. P. Vogler, and H. W. Virgin IV. 1995. Genetic mapping of reovirus virulence and organ tropism in severe combined immunodeficient mice: organ-specific virulence genes. J. Virol. 49:357-364.
24. Hrdy, D. B., L. Rosen, and B. N. Fields. 1979. Polymorphism of the migration of double-stranded RNA genome segments of reovirus isolates from humans, cattle, and mice. J. Virol. 31:104-111.
25. Kim, J., J. S. L. Parker, K. E. Murray, and M. L. Nibert. 2004. Nucleoside and RNA triphosphatase activities of Orthoreovirus transcriptase cofactor μ2. J. Biol. Chem. 279:4394-4403.
26. Kopito, R. R. 2000. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10:524-530.
27. Leary, T. P., J. C. Erker, M. L. Chalmers, A. T. Cruz, J. D. Wetzel, S. M. Desai, I. K. Mushahwar, and T. S. Dermody. 2002. Detection of mammalian reovirus RNA by using reverse transcription-PCR: sequence diversity within the λ3-encoding L1 gene. J. Clin. Microbiol. 40:1368-1375.
28. Lee, D. H., and A. L. Goldberg. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397-403.
29. Matoba, Y., W. S. Colucci, B. N. Fields, and T. W. Smith. 1993. The reovirus M1 gene determines the relative capacity of growth of reovirus in cultured bovine aortic endothelial cells. J. Clin. Investig. 92:2883-2888.
30. Matoba, Y., B. Sherry, B. N. Fields, and T. W. Smith. 1991. Identification of the viral genes responsible for growth of strains of reovirus in cultured mouse heart cells. J. Clin. Investig. 87:1628-1633.
31. Mbisa, J. L., M. M. Becker, S. Zou, T. S. Dermody, and E. G. Brown. 2000. Reovirus μ2 protein determines strain-specific differences in the rate of viral inclusion formation in L929 cells. Virology 272:16-26.
32. Miller, C. L., T. J. Broering, J. S. L. Parker, M. M. Arnold, and M. L. Nibert. 2003. Reovirus σNS protein localizes to inclusions through an association requiring the μNS amino-terminus. J. Virol. 77:4566-4576.
33. Miller, C. L., and D. J. Pintel. 2001. The NS2 protein generated by the parvovirus minute virus of mice is degraded by the proteasome in a manner independent of ubiquitin chain elongation or activation. Virology 285:346-355.
34. Mustoe, T. A., R. F. Ramig, A. H. Sharpe, and B. N. Fields. 1978. Genetics of reovirus: identification of the ds RNA segments encoding the polypeptides of the μ and σ size classes. Virology 89:594-604.
35. Nibert, M. L., R. L. Margraf, and K. M. Coombs. 1996. Nonrandom segregation of parental alleles in reovirus reassortants. J. Virol. 70:7295-7300.
36. Nibert, M. L., and L. A. Schiff. 2001. Reoviruses and their replication, p. 1679-1728. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
37. Noble, S., and M. L. Nibert. 1997. Core protein μ2 is a second determinant of nucleoside triphosphatase activities by reovirus cores. J. Virol. 71:7728-7735.
38. Parker, J. S., T. J. Broering, J. Kim, D. E. Higgins, and M. L. Nibert. 2002. Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J. Virol. 76:4483-4496.
39. Pickart, C. M. 2004. Back to the future with ubiquitin. Cell 116:181-190.
40. Reinisch, K. M., M. L. Nibert, and S. C. Harrison. 2000. Structure of the reovirus core at 3.6 Å resolution. Nature 404:960-967.
41. Rhim, J. S., L. E. Jordan, and H. D. Mayor. 1962. Cytochemical, fluorescent-antibody and electron microscopic studies on the growth of reovirus (ECHO 10) in tissue culture. Virology 17:342-355.
42. Sharpe, A. H., L. B. Chen, and B. N. Fields. 1982. The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120:399-411.
43. Sherry, B., and B. N. Fields. 1989. The reovirus M1 gene, encoding a viral core protein, is associated with the myocarditic phenotype of a reovirus variant. J. Virol. 63:4850-4856.
44. Silverstein, S. C., and P. H. Schur. 1970. Immunofluorescent localization of double-stranded RNA in reovirus-infected cells. Virology 41:564-566.
45. Sturzenbecker, L. J., M. Nibert, D. Furlong, and B. N. Fields. 1987. Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J. Virol. 61:2351-2361.
46. Tao, Y., D. L. Farsetta, M. L. Nibert, and S. C. Harrison. 2002. RNA synthesis in a cage-structural studies of the reovirus polymerase λ3. Cell 111:733-745.
47. Touris-Otero, F., J. Martinez-Costas, V. N. Vakharia, and J. Benavente. 2004. Avian reovirus nonstructural protein μNS forms viroplasm-like inclusions and recruits protein σNS to these structures. Virology 319:94-106.
48. Tyler, K. L. 2001. Mammalian reoviruses, p. 1729-1748. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
49. Varshavsky, A. 2003. The N-end rule and regulation of apoptosis. Nat. Cell Biol. 5:373-376.
50. Yin, P., M. Cheang, and K. M. Coombs. 1996. The M1 gene is associated with differences in the temperature optimum of the transcriptase activity in reovirus core particles. J. Virol. 70:1223-1227.
51. Yin, P., N. D. Keirstead, T. J. Broering, M. M. Arnold, J. S. L. Parker, M. L. Nibert, and K. M. Coombs. Comparisons of the M1 genome segments and encoded μ2 proteins of different reovirus isolates. Virol. J. 1:6.
52. Zar, J. H. 1984. Biostatistical analysis, 2nd ed. Prentice Hall, Englewood Cliffs, N.J.