Reovirus replication protein μ2 influences cell tropism by promoting particle assembly within viral inclusions

Journal of Virology

Volumn 86, Issue 20, 2012, Pages 10979-10987

  Ooms, Laura S ^a   Jerome, W Gray ^a   Dermody, Terence S ^a,b   Chappell, James D ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRO2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONFOCAL IMMUNOFLUORESCENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOFLUORESCENCE; LOW TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REOVIRUS; TEMPERATURE DEPENDENCE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRAL TROPISM; VIRION; VIRUS INCLUSION; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CELL LINE; DOGS; INCLUSION BODIES, VIRAL; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; PHENOTYPE; REOVIRIDAE; RNA, DOUBLE-STRANDED; RNA, VIRAL; TEMPERATURE; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS; VIRAL TROPISM; VIRUS ASSEMBLY; VIRUS REPLICATION;

MAMMALIA; ORTHOREOVIRUS; RNA VIRUSES;

EID: 84869039610     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01172-12     Document Type: Article

References (59)

1. Anderson N, Doane FW. 1966. An electron-microscope study of reovirus type 2 in L cells. J. Pathol. Bacteriol. 92:433-439.
2. Antczak JB, Joklik WK. 1992. Reovirus genome segment assortment into progeny genomes studied by the use of monoclonal antibodies directed against reovirus proteins. Virology 187:760-776.
3. Baer GS, Ebert DH, Chung CJ, Erickson AH, Dermody TS. 1999. Mutant cells selected during persistent reovirus infection do not express mature cathepsin L and do not support reovirus disassembly. J. Virol. 73:9532-9543.
4. Becker MM, et al. 2001. Reovirus μNS protein is required for nucleation of viral assembly complexes and formation of viral inclusions. J. Virol. 75:1459-1475.
5. Becker MM, Peters TR, Dermody TS. 2003. Reovirus σNS and μNS proteins form cytoplasmic inclusion structures in the absence of viral infection. J. Virol. 77:5948-5963.
6. Brentano L, Noah DL, Brown EG, Sherry B. 1998. The reovirus μ2, encoded by the M1 gene, is an RNA-binding protein. J. Virol. 72:8354-8357.
7. Broering TJ, et al. 2005. Carboxyl-proximal regions of reovirus nonstructural protein μNS necessary and sufficient for forming factory-like inclusions. J. Virol. 79:6194-6206.
8. Broering TJ, et al. 2004. Reovirus nonstructural protein μNS recruits viral core surface proteins and entering core particles to factory-like inclusions. J. Virol. 78:1882-1892.
9. Broering TJ, Parker JS, Joyce PL, Kim J, Nibert ML. 2002. Mammalian reovirus nonstructural proteinμNS forms large inclusions and colocalizes with reovirus microtubule-associated protein μ2 in transfected cells. J. Virol. 76:8285-8297.
10. Coombs KM. 1996. Identification and characterization of a doublestranded RNA-reovirus temperature-sensitive mutant defective in minor core protein μ2. J. Virol. 70:4237-4245.
11. Coombs KM. 2006. Reovirus structure and morphogenesis. Curr. Top. Microbiol. Immunol. 309:117-167.
12. Dales S. 1963. Association between the spindle apparatus and reovirus. Proc. Natl. Acad. Sci. U. S. A. 50:268-275.
13. Dales S, Gomatos P, Hsu KC. 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. Dermody TS, Parker J, Sherry B. Orthoreovirus. In Knipe DM, et al (ed), Fields virology, 6th ed, in press. Lippincott Williams & Wilkins, Philadelphia, PA.
15. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells
16. Ebert DH, Deussing J, Peters C, Dermody TS. 2002. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J. Biol. Chem. 277:24609-24617.16. Fields BN. 1971. Temperature-sensitive mutants of reovirus type 3 features of genetic recombination. Virology 46:142-148.
17. Gomatos PJ, Tamm I, Dales S, Franklin RM. 1962. Reovirus type 3: physical characteristics and interactions with L cells. Virology 17:441-454.
18. Hazelton PR, Coombs KM. 1995. The reovirus mutant tsA279 has temperature-sensitive lesions in the M2 and L2 genes: the M2 gene is associated with decreased viral protein production and blockade in transmembrane transport. Virology 207:46-58.
19. Ivanovic T, et al. 2011. Recruitment of cellular clathrin to viral factories and disruption of clathrin-dependent trafficking. Traffic 12:1179-1195.
20. Kaufer S, Coffey CM, Parker JS. 2012. The cellular chaperone Hsc70 is specifically recruited to reovirus viral factories independently of its chaperone function. J. Virol. 86:1079-1089.
21. Kim J, Parker JS, Murray KE, Nibert ML. 2004. Nucleoside and RNA triphosphatase activities of orthoreovirus transcriptase cofactor μ2. J. Biol. Chem. 279:4394-4403.
22. Kobayashi T, et al. 2007. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147-157.
23. Kobayashi T, Chappell JD, Danthi P, Dermody TS. 2006. Gene-specific inhibition of reovirus replication by RNA interference. J. Virol. 80:9053-9063.
24. Kobayashi T, Ooms LS, Chappell JD, Dermody TS. 2009. Identification of functional domains in reovirus replication proteins μNS and μ2. J. Virol. 83:2892-2906.
25. Kobayashi T, Ooms LS, Ikizler M, Chappell JD, Dermody TS. 2010. An improved reverse genetics system for mammalian orthoreoviruses. Virology 398:194-200.
26. Mbisa JL, Becker MM, Zou S, Dermody TS, Brown EG. 2000. Reovirus μ2 protein determines strain-specific differences in the rate of viral inclusion formation in L929 cells. Virology 272:16-26.
27. Miller CL, Broering TJ, Parker JS, Arnold MM, Nibert ML. 2003. Reovirus μNS protein localizes to inclusions through an association requiring the μNS amino terminus. J. Virol. 77:4566-4576.
28. Miller CL, et al. 2004. Increased ubiquitination and other covariant phenotypes attributed to a strain- and temperature-dependent defect of reovirus core protein μ2. J. Virol. 78:10291-10302.
29. Morgan EM, Zweerink HJ. 1975. Characterization of transcriptase and replicase particles isolated from reovirus infected cells. Virology 68:455-466.
30. Morgan EM, Zweerink HJ. 1974. Reovirus morphogenesis: core-like particles in cells infected at 39° with wild-type reovirus and temperaturesensitive mutants of groups B and G. Virology 59:556-565.
31. Noble S, Nibert ML. 1997. Core protein μ2 is a second determinant of nucleoside triphosphatase activities by reovirus cores. J. Virol. 71:7728-7735.
32. Nonoyama M, Millward S, Graham AF. 1974. Control of transcription of the reovirus genome. Nucleic Acids Res. 1:373-385.
33. Ooms LS, Kobayashi T, Dermody TS, Chappell JD. 2010. A post-entry step in the mammalian orthoreovirus replication cycle is a determinant of cell tropism. J. Biol. Chem. 285:41604-41613.
34. Parker JS, Broering TJ, Kim J, Higgins DE, Nibert ML. 2002. Reovirus core proteinm2determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J. Virol. 76:4483-4496.
35. Patton JT, Silvestri LS, Tortorici MA, Vasquez-Del Carpio R, Taraporewala ZF. 2006. Rotavirus genome replication and morphogenesis: role of the viroplasm. Curr. Top. Microbiol. Immunol. 309:169-187.
36. Reinisch KM, Nibert ML, Harrison SC. 2000. Structure of the reovirus core at 3.6 Å resolution. Nature 404:960-967.
37. Rhim JS, Jordan LE, Mayor HD. 1962. Cytochemical, fluorescentantibody and electron microscopic studies on the growth of reovirus (ECHO 10) in tissue culture. Virology 17:342-355.
38. Rhim JS, Smith KO, Melnick JL. 1961. Complete and coreless forms of reovirus (ECHO 10): ratio of number of virus particles to infective units in the one-step growth cycle. Virology 15:428-435.
39. Rodgers SE, et al. 1997. Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bcl-2. J. Virol. 71:2540-2546.
40. Schiff LA, Nibert ML, Tyler KL. 2007. Orthoreoviruses and their replication, p 1853-1915. In KnipeDMet al (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
41. Sharpe AH, Chen LB, Fields BN. 1982. The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120:399-411.
42. Shatkin AJ, LaFiandra AJ. 1972. Transcription by infectious subviral particles of reovirus. J. Virol. 10:698-706.
43. Silverstein SC, Dales S. 1968. The penetration of reovirus RNA and initiation of its genetic function in L-strain fibroblasts. J. Cell Biol. 36:197-230.
44. Silverstein SC, Schur PH. 1970. Immunofluorescent localization of double-stranded RNA in reovirus-infected cells. Virology 41:564-566.
45. Skehel JJ, Joklik WK. 1969. Studies on the in vitro transcription of reovirus RNA catalyzed by reovirus cores. Virology 39:822-831.
46. Spendlove RS, Lennette EH, Knight CO, Chin JN. 1963. Development of viral antigens and infectious virus on HeLa cells infected with reovirus. J. Immunol. 90:548-553.
47. Starnes MC, Joklik WK. 1993. Reovirus protein μ3 is a poly(C)-dependent poly(G) polymerase. Virology 193:356-366.
48. Stuart DI, Grimes JM. 2006. Structural studies on orbivirus proteins and particles. Curr. Top. Microbiol. Immunol. 309:221-244.
49. Sturzenbecker LJ, Nibert ML, Furlong DB, Fields BN. 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.
50. Tao Y, Farsetta DL, Nibert ML, Harrison SC. 2002. RNA synthesis in a cage-structural studies of reovirus polymerase μ3. Cell 111:733-745.
51. Virgin HW, Bassel-Duby IVR, Fields BN, Tyler KL. 1988. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J. Virol. 62:4594-4604.
52. Virgin HW, Tyler KL. 1991. Role of immune cells in protection against and control of reovirus infection in neonatal mice. J. Virol. 65:5157-5164.
53. Weibel ER. 1979. Stereological methods: practical methods for biological morphometry. Academic Press, London, United Kingdom.
54. Yin P, Cheang M, Coombs KM. 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.
55. Zarbl H, Millward S. 1983. The reovirus multiplication cycle, p 107-196. In Joklik WK (ed), The Reoviridae. Plenum Press, New York, NY.
56. Zhang X, Walker SB, Chipman PR, Nibert ML, Baker TS. 2003. Reovirus polymerase μ3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å. Nat. Struct. Biol. 10:1011-1018.
57. Zou S, Brown EG. 1996. Stable expression of the reovirus μ2 protein in mouse L cells complements the growth of a reovirus ts mutant with a defect in its M1 gene. Virology 217:42-48.
58. Zweerink HJ, Ito Y, Matsuhisa T. 1972. Synthesis of reovirus doublestranded RNA within virion-like particles. Virology 50:349-358.
59. Zweerink HJ, Morgan EM, Skyler JS. 1976. Reovirus morphogenesis: characterization of subviral particles in infected cells. Virology 73:442-453.