Formation of the factory matrix is an important, though not a sufficient function of nonstructural protein μNS during reovirus infection

Virology

Volumn 375, Issue 2, 2008, Pages 412-423

  Arnold, Michelle M ^a,b   Murray, Kenneth E ^a   Nibert, Max L ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Inclusion body; Reoviridae; Silencing; siRNA; Viral factory; Viroplasm

Indexed keywords

MUTANT PROTEIN; PROTEIN MUNS; SMALL INTERFERING RNA; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; GENETIC COMPLEMENTATION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REOVIRUS; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; CELL LINE; INCLUSION BODIES; ORTHOREOVIRUS, MAMMALIAN; REOVIRIDAE INFECTIONS; VIRAL CORE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

MAMMALIAN ORTHOREOVIRUS; ORTHOREOVIRUS; REOVIRIDAE;

EID: 43249091496     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.02.024     Document Type: Article

References (52)

1. Ahmed R., Canning W.M., Kauffman R.S., Sharpe A.H., Hallum J.V., and Fields B.N. Role of the host cell in persistent viral infection: coevolution of L cells and reovirus during persistent infection. Cell 25 (1981) 325-332
2. Arias C.F., Dector M.A., Segovia L., Lopez T., Camacho M., Isa P., Espinosa R., and Lopez S. RNA silencing of rotavirus gene expression. Virus Res. 102 (2004) 43-51
3. Astell C., Silverstein S.C., Levin D.H., and Acs G. Regulation of the reovirus RNA transcriptase by a viral capsomere protein. Virology 48 (1972) 648-654
4. Attoui H., Fang Q., Mohd Jaafar F., Cantaloube J.F., Biagini P., de Micco P., and de Lamballerie X. Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae). J. Gen. Virol. 83 (2002) 1941-1951
5. Banerjee A.K., and Shatkin A.J. Transcription in vitro by reovirus-associated ribonucleic acid-dependent polymerase. J. Virol. 6 (1970) 1-11
6. Becker M.M., Peters T.R., and Dermody T.S. Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J. Virol. 77 (2003) 5948-5963
7. Broering T.J., McCutcheon A.M., Centonze V.E., and Nibert M.L. Reovirus nonstructural protein μNS binds to reovirus cores, but does not inhibit their transcription activity. J. Virol. 74 (2000) 5516-5524
8. Broering T.J., Parker J.S.L., Joyce P.L., Kim J., and Nibert M.L. Mammalian reovirus nonstructural protein μNS forms large inclusions and colocalizes with reovirus microtubule-associated protein μ2 in transfected cells. J. Virol. 76 (2002) 8285-8297
9. Broering T.J., Kim J., Miller C.L., Piggott C.D., Dinoso J.B., Nibert M.L., and Parker J.S.L. Reovirus nonstructural protein μNS recruits viral core surface proteins and entering core particles to factory-like inclusions. J. Virol. 78 (2004) 1882-1892
10. Broering T.J., Arnold M.M., Miller C.L., Hurt J.A., Joyce P.L., and Nibert M.L. Carboxyl-proximal regions of reovirus nonstructural protein μNS necessary and sufficient for forming factory-like inclusions. J. Virol. 79 (2005) 6194-6206
11. Buchholz U.J., Finke S., and Conzelmann K.K. Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73 (1999) 251-259
12. Campagna M., Eichwald C., Vascotto F., and Burrone O.R. RNA interference of rotavirus segment 11 mRNA reveals the essential role of NSP5 in the virus replicative cycle. J. Gen. Virol. 86 (2005) 1481-1487
13. Carvalho J., Arnold M.M., and Nibert M.L. Silencing and complementation of reovirus core protein μ2: functional correlations with μ2-microtubule association and differences between virus- and plasmid-derived μ2. Virology 364 (2007) 301-316
14. Chandran K., Walker S.B., Chen Y., Contreras C.M., Schiff L.A., Baker T.S., and Nibert M.L. In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3. J. Virol. 73 (1999) 3941-3950
15. Dales S. Association between the spindle apparatus and reovirus. Proc. Natl. Acad. Sci. U. S. A. 50 (1963) 268-275
16. Dales S., Gomatos P., and Hsu K.C. The uptake and development of reovirus in strain L cells followed with labelled viral ribonucleic acid and ferritin-antibody conjugates. Virology 25 (1965) 193-211
17. Drayna D., and Fields B.N. Activation and characterization of the reovirus transcriptase: genetic analysis. J. Virol. 41 (1982) 110-118
18. Fabbretti E., Afrikanova I., Vascotto F., and Burrone O.R. Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80 (1999) 333-339
19. Fields B.N., Raine C.S., and Baum S.G. Temperature-sensitive mutants of reovirus type 3: defects in viral maturation as studied by immunofluorescence and electron microscopy. Virology 43 (1971) 569-578
20. Gaillard Jr. R.K., and Joklik W.K. The relative translation efficiencies of reovirus messenger RNAs. Virology 147 (1985) 336-348
21. Gomatos P.J. RNA synthesis in reovirus-infected L929 mouse fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 58 (1967) 1798-1805
22. Jiang J., and Coombs K.M. Infectious entry of reovirus cores into mammalian cells enhanced by transfection. J. Virol. Methods 128 (2005) 88-92
23. Joklik W.K. Studies on the effect of chymotrypsin on reovirions. Virology 49 (1972) 700-715
24. Kobayashi T., Chappell J.D., Danthi P., and Dermody T.S. Gene-specific inhibition of reovirus replication by RNA interference. J. Virol. 80 (2006) 9053-9063
25. Lee P.W.K., Hayes E.C., and Joklik W.K. Characterization of anti-reovirus immunoglobulins secreted by cloned hybridoma cell lines. Virology 108 (1981) 134-146
26. Levin D.H., Acs G., and Silverstein S.C. Chain initiation by reovirus RNA transcriptase in vitro. Nature 227 (1970) 603-604
27. Lopez T., Rojas M., Ayala-Breton C., Lopez S., and Arias C.F. Reduced expression of the rotavirus NSP5 gene has a pleiotropic effect on virus replication. J. Gen. Virol. 86 (2005) 1609-1617
28. McCrae M.A., and Joklik W.K. The nature of the polypeptide encoded by each of the 10 double-stranded RNA segments of reovirus type 3. Virology 89 2 (1978) 578-593
29. McCutcheon A.M., Broering T.J., and Nibert M.L. Mammalian reovirus M3 gene sequences and conservation of coiled-coil motifs near the carboxyl terminus of the μNS protein. Virology 264 (1999) 16-24
30. Miller C.L., Broering T.J., Parker J.S.L., Arnold M.M., and Nibert M.L. Reovirus σNS protein localizes to inclusions through an association requiring the μNS amino-terminus. J. Virol. 77 (2003) 4566-4576
31. Miller C.L., Arnold M.M., Broering T.J., Eichwald C., Kim J., Dinoso J.D., and Nibert M.L. A cytoplasmic platform for easily visualizing protein-protein associations inside cells. Mol. Cell. Proteomics 6 (2007) 1027-1038
32. Murray K.E., and Nibert M.L. Guanidine hydrochloride inhibits mammalian orthoreovirus growth by reversibly blocking the synthesis of double-stranded RNA. J. Virol. 81 (2007) 4572-4584
33. Mustoe T.A., Ramig R.F., Sharpe A.H., and Fields B.N. Genetics of reovirus: identification of the dsRNA segments encoding the polypeptides of the mu and sigma size classes. Virology 89 (1978) 594-604
34. Nibert M.L., and Fields B.N. A carboxy-terminal fragment of protein μ1/μ1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J. Virol. 66 (1992) 6408-6418
35. Parker J.S.L., Broering T.J., Kim J., Higgins D.E., and Nibert M.L. Reovirus core protein μ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J. Virol. 76 (2002) 4483-4496
36. Petrie B.L., Greenberg H.L., Graham D.Y., and Estes M.K. Ultrastructural localization of rotavirus antigens using colloidal gold. Virus Res. 1 (1984) 133-152
37. Rhim J.S., Jordan L.E., and Mayor H.D. Cytochemical, fluorescent-antibody and electron microscopic studies on the growth of reovirus (ECHO 10) in tissue culture. Virology 17 (1962) 342-355
38. Schiff L.A., Nibert M.L., and Tyler K.L. Orthoreoviruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. 5th (2007), Lippincott Williams & Wilkins, Philadelphia 1853-1915
39. Sen A., Sen N., and Mackow E.R. The formation of viroplasm-like structures by the rotavirus NSP5 protein is calcium regulated and directed by a C-terminal helical domain. J. Virol. 81 (2007) 11758-11767
40. Sharpe A.H., Chen L.B., and Fields B.N. The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120 (1982) 399-411
41. Silvestri L.S., Taraporewala Z.F., and Patton J.T. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78 (2004) 7763-7774
42. Skehel J.J., and Joklik W.K. Studies on the in vitro transcription of reovirus RNA catalyzed by reovirus cores. Virology 39 (1969) 822-831
43. Spendlove R.S., Lennette E.H., and John A.C. The role of the mitotic apparatus in the intracellular location of reovirus antigen. J. Immunol. 90 (1963) 554-560
44. Su Y.P., Su B.S., Shien J.H., Liu H.J., and Lee L.H. The sequence and phylogenetic analysis of avian reovirus genome segments M1, M2, and M3 encoding the minor core protein μA, the major outer capsid protein μB, and the nonstructural protein μNS. J. Virol. Methods 133 (2006) 146-157
45. Taraporewala Z.F., Jiang X., Vasquez-Del Carpio R., Jayaram H., Prasad B.V.V., and Patton J.T. Structure-function analysis of rotavirus NSP2 octamer by using a novel complementation system. J. Virol. 80 (2006) 7984-7994
46. Tournier P., and Plissier M. The intracellular development of the reovirus studied with the electron microscope. Presse Med. 68 (1960) 683-688
47. Venter P.A., Krishna N.K., and Schneemann A. Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus. J. Virol. 79 (2005) 6239-6248
48. Virgin IV H.W., Bassel-Duby R., Fields B.N., and Tyler K.L. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62 (1988) 4594-4604
49. Wiener J.R., Bartlett J.A., and Joklik W.K. The sequences of reovirus serotype 3 genome segments M1 and M3 encoding the minor protein μ2 and the major nonstructural protein μNS, respectively. Virology 169 (1989) 293-304
50. Yamakawa M., Furuichi Y., and Shatkin A.J. Reovirus transcriptase and capping enzymes are active in intact virions. Virology 118 (1982) 157-168
51. Zarbl H.J., and Millward S. The reovirus multiplication cycle. In: Joklik W.K. (Ed). The Reoviridae (1983), Plenum Press, New York 107-196
52. Zhang Y., Guo D., Geng H., Liu M., Hu Q., Wang J., Tong G., Kong X., Liu N., and Liu C. Characterization of M-class genome segments of muscovy duck reovirus S14. Virus Res. 125 (2007) 42-53