Carboxyl-proximal regions of reovirus nonstructural protein μNS necessary and sufficient for forming factory-like inclusions

Journal of Virology

Volumn 79, Issue 10, 2005, Pages 6194-6206

  Broering, Teresa J ^a,b,e   Arnold, Michelle M ^a,c   Miller, Cathy L ^a   Hurt, Jessica A ^a   Joyce, Patricia L ^b   Nibert, Max L ^a,c,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c HARVARD UNIVERSITY   (United States)

^d Massachusetts Biologic Laboratories   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; GREEN FLUORESCENT PROTEIN; HISTIDINE; PROTEIN MUNS; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INCLUSION; CONTROLLED STUDY; DIMERIZATION; GENE MUTATION; GENE REPLICATION; GENETIC TRANSFECTION; NONHUMAN; ORTHOREOVIRUS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REOVIRUS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CONSENSUS SEQUENCE; INCLUSION BODIES, VIRAL; MOLECULAR SEQUENCE DATA; REOVIRIDAE; SEQUENCE ALIGNMENT; VIRAL NONSTRUCTURAL PROTEINS; VIRUS ASSEMBLY;

AEQUOREA VICTORIA; AVES; MAMMALIA; REOVIRUS SP.; VICTORIA;

EID: 18144383857     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.10.6194-6206.2005     Document Type: Article

References (49)

1. Antczak, J. B., and W. K. Joklik. 1992. Reovirus genome segment assortment into progeny genomes studied by the use of monoclonal antibodies directed against reovirus proteins. Virology 187:760-776.
2. Attoui, H., Q. Fang, F. M. Jaafar, J. F. Cantaloube, P. Biagini, P. De Micco, and X. De Lamballerie. 2002. 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. 83:1941-1951.
3. 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.
4. 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.
5. 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.
6. Broering, T. J., J. Kim, C. L. Miller, C. D. 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.
7. 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.
8. Brookes, S. M., A. D. Hyatt, and B. T. Eaton. 1993. Characterization of virus inclusion bodies in bluetongue virus-infected cells. J. Gen. Virol. 74:525-530.
9. Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99:7877-7882.
10. Dales, S. 1963. Association between the spindle apparatus and reovirus. Proc. Natl. Acad. Sci. USA 50:268-275.
11. Dales, S., P. Gomatos, and K. C. Hsu. 1965. The uptake and development of reovirus in strain L cells followed with labeled viral ribonucleic acid and ferritin-antibody conjugates. Virology 25:193-211.
12. Eichwald, C., J. F. Rodriguez, and O. R. Burrone. 2004. Characterization of rotavirus NSP2/NSP5 interactions and the dynamics of viroplasm formation. J. Gen. Virol. 85:625-634.
13. Fields, B. N., C. S. Raine, and S. G. Baum. 1971. Temperature-sensitive mutants of reovirus type 3: defects in viral maturation as studied by immunofluorescence and electron microscopy. Virology 43:569-578.
14. 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.
15. Gillian, A. L., and M. L. Nibert. 1998. Amino terminus of reovirus nonstructural protein sigma NS is important for ssRNA binding and nucleoprotein complex formation. Virology 240:1-11.
16. Gillian, A. L., S. C. Schmechel, J. Livny, L. A. Schiff, and M. L. Nibert. 2000. Reovirus nonstructural protein σNS binds in multiple copies to single-stranded RNA and shares properties with single-stranded DNA binding proteins. J. Virol. 74:5939-5948.
17. Gomatos, P. J., O. Prakash, and N. M. Stamatos. 1981. Small reovirus particle composed solely of σNS with specificity for binding different nucleic acids. J. Virol. 39:115-124.
18. Hopfner, K. P., L. Craig, G. Moncalian, R. A. Zinkel, T. Usui, B. A. Owen, A. Karcher, B. Henderson, J. L. Bodmer, C. T. McMurray, J. P. Carney, J. H. Petrini, and J. A. Tainer. 2002. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562-566.
19. Huismans, H., and W. K. Joklik. 1976. Reovirus-coded polypeptides in infected cells: isolation of two native monomeric polypeptides with affinity for single-stranded and double-stranded RNA, respectively. Virology 70:411-424.
20. 2+ ion links the cytoplasmic tail of CD4 and the N-terminal region of Lck. J. Biol. Chem. 273:18729-18733.
21. Kim, P. W., Z. Y. Sun, S. C. Blacklow, G. Wagner, and M. J. Eck. 2003. A zinc clasp structure tethers Lck to T-cell coreceptors CD4 and CD8. Science 301:1725-1728.
22. Lee, P. W. K., E. C. Hayes, and W. K. Joklik. 1981. Characterization of anti-reovirus immunoglobulins secreted by cloned hybridoma cell lines. Virology 108:134-146.
23. Mayor, H. D. 1965. Studies on reovirus. 3. A labile, single-stranded ribonucleic acid associated with the late stages of infection. J. NCI. 35:919-925.
24. 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.
25. McCutcheon, A. M., T. J. Broering, and M. L. Nibert. 1999. Mammalian reovirus M3 gene sequences and conservation of coiled-coil motifs near the carboxyl terminus of the μNS protein. Virology 264:16-24.
26. 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.
27. Miller, D. J., M. D. Schwartz, and P. Ahlquist. 2001. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. J. Virol. 75:11664-11676.
28. Morgan, E. M., and H. J. Zweerink. 1975. Characterization of transcriptase and replicase particles isolated from reovirus-infected cells. Virology 68:455-466.
29. Moss, B. 2001. Poxviridae: the viruses and their replication, p. 2637-2671. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott Williams & Wilkins Co., Philadelphia, Pa.
30. 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.
31. Quimby, B. B., and A. H. Corbett. 2001. Nuclear transport mechanisms. Cell. Mol. Life Sci. 58:1766-1773.
32. Restrepo-Hartwig, M. A., and P. Ahlquist. 1996. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J. Virol. 70:8908-8916.
33. 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.
34. Richardson, M. A., and Y. Furuichi. 1985. Synthesis in Escherichia coli of the reovirus nonstructural protein σNS. J. Virol. 56:527-533.
35. Roizman, B., and A. E. Sears. 2001. Herpes simplex viruses and their replication, p. 2231-2295. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott Williams & Wilkins Co., Philadelphia, Pa.
36. Schwartz, M., J. Chen, M. Janda, M. Sullivan, J. den Boon, and P. Ahlquist. 2002. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9:505-514.
37. 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.
38. Silverstein, S. C., and S. Dales. 1968. The penetration of reovirus RNA and initiation of its genetic function in L-strain fibroblasts. J. Cell Biol. 36:197-230.
39. Silverstein, S. C., and P. H. Schur. 1970. Immunofluorescent localization of double-stranded RNA in reovirus-infected cells. Virology 41:564-566.
40. Silvestri, L. S., Z. F. Taraporewala, and J. T. Patton. 2004. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78:7763-7774.
41. Spendlove, R. S., E. H. Lennette, J. N. Chin, and C. O. Knight. 1964. Effect of antimitotic agents on intracellular reovirus antigen. Cancer Res. 24:1826-1833.
42. Stamatos, N. M., and P. J. Gomatos. 1982. Binding to selected regions of reovirus mRNAs by a nonstructural reovirus protein. Proc. Natl. Acad. Sci. USA 79:3457-3461.
43. Theron, J., H. Huismans, and L. H. Nel. 1996. Site-specific mutations in the NS2 protein of epizootic haemorrhagic disease virus markedly affect the formation of cytoplasmic inclusion bodies. Arch. Virol. 141:1143-1151.
44. Touris-Otero, F., M. Cortez-San Martin, J. Martinez-Costas, and J. Benavente. 2004. Avian reovirus morphogenesis occurs within viral factories and begins with the selective recruitment of σNS and λA to μNS inclusions. J. Mol. Biol. 341:361-374.
45. 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.
46. Wiener, J. R., J. A. Bartlett, and W. K. Joklik. 1989. The sequences of reovirus serotype 3 genome segments M1 and M3 encoding the minor protein μ2 and the major nonstructural protein μNS, respectively. Virology 169:293-304.
47. Wilson, I. A., H. L. Niman, R. A. Houghten, A. R. Cherenson, M. L. Connolly, and R. A. Lerner. 1984. The structure of an antigenic determinant in a protein. Cell 37:767-778.
48. Wolf, E., P. S. Kim, and B. Berger. 1997. MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci. 6:1179-1189.
49. Zweerink, H. J., M. J. McDowell, and W. K. Joklik. 1971. Essential and nonessential noncapsid reovirus proteins. Virology 45:716-723.