Avian reovirus: Structure and biology

Virus Research

Volumn 123, Issue 2, 2007, Pages 105-119

  Benavente, Javier ^a   Martínez Costas, Jose ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Avian reovirus; Cell cell fusion; RNA virus; Virus morphogenesis; Virus replication; Virus structure; Virus host interactions

Indexed keywords

HYBRID PROTEIN; INTERFERON; MU B PROTEIN; MU NS PROTEIN; PROTEIN LAMBDA A; PROTEIN LAMBDA B; PROTEIN LAMBDA C; PROTEIN MU A; PROTEIN P10; PROTEIN P17; PROTEIN SIGMA A; PROTEIN SIGMA B; PROTEIN SIGMA C; PROTEIN SIGMA NS; UNCLASSIFIED DRUG; VIRUS PROTEIN;

APOPTOSIS; AVIAN REOVIRUS; CELL FUSION; CELL MEMBRANE PERMEABILITY; CISTRON; GENE EXPRESSION; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; REOVIRUS; REVIEW; RNA TRANSLATION; S1 GENE; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS MORPHOGENESIS; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; CELL PHYSIOLOGY; CELLS; GENOME, VIRAL; MOLECULAR WEIGHT; ORTHOREOVIRUS, AVIAN; REOVIRIDAE INFECTIONS; VIRAL PROTEINS; VIRION; VIRUS REPLICATION;

AVES; AVIAN ORTHOREOVIRUS; MAMMALIA; ORTHOREOVIRUS; RNA VIRUSES;

EID: 33846001004     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2006.09.005     Document Type: Review

References (90)

1. Attoui H., Billoir F., Biagini P., de Micco P., and de Lamballerie X. Complete sequence determination and genetic analysis of Banna virus and Kadipiro virus. Proposal for assignment to a new genus (Seadornavirus) within the family Reoviridae. J. Gen. Virol. 81 (2000) 1507-1515
2. Barton E.S., Forrest J.C., Connolly J.L., Chappell J.D., Liu Y., Schnell F.J., Nusrat A., Parkos C.A., and Dermody T.S. Junction adhesion molecule is a receptor for reovirus. Cell 104 (2001) 441-451
3. Benavente J., and Shatkin A.J. Avian reovirus mRNAs are nonfunctional in infected mouse L cells: translational basis for virus host-range restriction. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 4257-4261
4. Bodelon G., Labrada L., Martínez-Costas J., and Benavente J. The avian reovirus genome segment S1 is a functionally tricistronic gene that expresses one structural and two nonstructural proteins in infected cells. Virology 290 (2001) 181-191
5. Bodelon G., Labrada L., Martínez-Costas J., and Benavente J. Modification of late membrane permeability in avian reovirus-infected cells. Viroporin activity of the S1-encoded nonstructural p10 protein. J. Biol. Chem. 277 (2002) 17789-17796
6. Breun L.A., Broering T.J., McCutcheon A.M., Harrison S.J., Luongo C.L., and nibert M.L. Mammalian reovirus L2 gene and lambda2 core spike protein sequences and whole-genome comparisons of reovirus type 1 Lang, type 2 Jones, and type 3 Dearing. Virology 287 (2001) 333-348
7. Carrasco L. Entry of animal viruses and macromolecules into cells. FEBS Lett. 350 (1994) 151-154
8. Carrasco L. Modification of membrane permeability by animal viruses. Adv. Virus Res. 45 (1995) 61-112
9. Clemens M. PKR-a protein kinase regulated by double-stranded RNA. Int. J. Biochem. Cell Biol. 29 (1997) 945-949
10. Costas C., Martínez-Costas J., Bodelón G., and Benavente J. The second open reading frame of the avian reovirus S1 gene encodes a transcription-dependent and CRM1-independent nucleocytoplasmic shuttling protein. J. Virol. 79 (2005) 2141-2150
11. Duncan R. The low pH-dependent entry of avian reovirus is accompanied by two specific cleavages of the major outer capsid protein μ2C. Virology 219 (1996) 179-189
12. Duncan R., Chen Z., Walsh S., and Wu S. Avian reovirus-induced syncytium formation is independent of infectious progeny virus production and enhances the rate, but is not essential, for virus-induced cytopathology and virus egress. Virology 224 (1996) 453-464
13. Duncan R., Corcoran J., Shou J., and Stoltz D. Reptilian reovirus: a new fusogenic Orthoreovirus species. Virology 319 (2004) 131-140
14. Duncan R., and Sullivan K. Characterization of two avian reoviruses that exhibit strain-specific quantitative differences in their syncytium-inducing and pathogenic capabilities. Virology 250 (1998) 263-272
15. Dryden K.A., Wang G., Yeager M., Nibert M.L., Coombs K.M., Furlong D.B., Fields B.N., and Baker T.S. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J. Cell Biol. 122 (1993) 1023-1041
16. Ellis M.N., Eidson C.S., Brown J., and Kleven S.H. Studies of interferon induction and interferon sensitivity of avian reoviruses. Avian Dis. 27 (1983) 927-936
17. Ernst H., and Shatkin A.J. Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 48-52
18. 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
19. Gonzalez M.E., and Carrasco L. Viroporins. FEBS Lett. 552 (2003) 28-34
20. González-López C., Martínez-Costas J., Esteban M., and Benavente J. Evidence that avian reovirus σA protein is an inhibitor of the double-stranded RNA-dependent protein kinase. J. Gen. Virol. 84 (2003) 1629-1639
21. Goodbourn S., Didcock L., and Randall R.E. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81 (2000) 2341-2364
22. Grande A., and Benavente J. Optimal conditions for the growth, purification and storage of the avian reovirus S1133. J. Virol. Methods 85 (2000) 43-54
23. Grande A., Costas C., and Benavente J. Subunit composition and conformational stability of the oligomeric form of the avian reovirus cell-attachment protein σC. J. Gen. Virol. 83 (2002) 131-139
24. Grande A., Rodriguez E., Costas C., Everitt E., and Benavente J. Oligomerization and cell-binding properties of the avian reovirus cell-attachment protein sigmaC. Virology 274 (2000) 367-377
25. Guardado Calvo P., Fox G.C., Hermo Parrado X.L., Llamas-Saiz A.L., Costas C., Martínez-Costas J., Benavente J., and van Raaij M.J. Structure of the carboxy-terminal receptor-binding domain of avian reovirus fibre sigmaC. J. Mol. Biol. 354 (2005) 137-149
26. Haller O., Kochs G., and Weber F. The interferon response circuit: Induction and suppression by pathogenic viruses. Virology 344 (2006) 119-130
27. Hsiao J., Martínez-Costas J., Benavente J., and Vakharia V.N. Cloning, expression, and characterization of avian reovirus guanylyltransferase. Virology 296 (2002) 288-299
28. Jackson R.J., and Kaminski A. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1 (1995) 985-1000
29. Jones R.C. Avian reovirus infections. Rev. Sci. Tech. 19 (2000) 614-625
30. Kant A., Balk F., Born L., van Roozelaar D., Heijmans J., Gielkins A., and ter Huurne A. Classification of Dutch and German avian reoviruses by sequencing the σC protein. Vet. Res. 34 (2003) 203-212
31. Kielian M., and Jungerwirth S. Mechanisms of enveloped virus entry into cells. Mol. Biol. Med. 7 (1990) 17-31
32. Kozak M. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266 (1991) 19867-19870
33. Kozak M. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299 (2002) 1-34
34. Labrada L., Bodelon G., Vinuela J., and Benavente J. Avian reoviruses cause apoptosis in cultured cells: viral uncoating but not viral gene expression is required for apoptosis induction. J. Virol. 76 (2002) 7932-7941
35. Lau R.Y., van Alstyne D., Berckmans R., and Graham A.F. Synthesis of reovirus-specific polypeptides in cells pretreated with cycloheximide. J. Virol. 16 (1975) 470-478
36. Liemann S., Chandran K., Baker T.S., Nibert M.L., and Harrison S.C. Structure of the reovirus membrane-penetration, μ1, in a complex with its protector protein, σ3. Cell 108 (2002) 283-295
37. Liu H.-J., Lin P.-Y., Lee J.-W., and Shih W.-L. Retardation of cell growth by avian reovirus p17 through activation of p53 pathway. Biochem. Biophys. Res. Commun. 336 (2005) 709-715
38. Lupiani B., Subramanian K., and Samal S.K. Aquareoviruses. Annu. Rev. Fish Dis. 5 (1995) 175-208
39. Mallo M., Martínez-Costas J., and Benavente J. Avian reovirus S1133 can replicate in mouse L cells: effect of pH and cell attachment status on viral infection. J. Virol. 65 (1991) 5499-5505
40. Marsh M., and Helenius A. Virus entry into animal cells. Adv. Virus Res. 36 (1989) 107-151
41. Martínez-Costas J., Grande A., Varela R., García-Martínez C., and Benavente J. Protein architecture of avian reovirus S1133 and identification of the cell attachment protein. J. Virol. 71 (1997) 59-64
42. Martínez-Costas J., Gónzalez-López C., Vakharia V.N., and Benavente J. Possible involvement of the double-stranded RNA-binding core protein sigmaA in the resistance of avian reovirus to interferon. J. Virol. 74 (2000) 1124-1131
43. Martínez-Costas J., Varela R., and Benavente J. Endogenous enzymatic activities of the avian reovirus S1133: identification of the viral capping enzyme. Virology 206 (1995) 1017-1026
44. Mertens P. The dsRNA viruses. Virus Res. 101 (2004) 3-13
45. Metcalf P., Cyrclaff M., and Adrian M. The 3-dimensional structure of reovirus obtained by cryoelectron microscopy. EMBO J. 10 (1991) 3129-3136
46. Nason E.L., Samal S.K., and Prasad B.V.V. Trypsin-induced structural transformation in aquareovirus. J. Virol. 74 (2000) 6546-6555
47. 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
48. Nibert M.L., and Schiff L.A. Reoviruses and their replication. In: Knipe D.M., and Hooley P.M. (Eds). Fields Virology. fourth ed. (2001), Lippincott Willams & Wilkins, Philadelphia, PA 1679-1728
49. Nonoyama M., Millward S., and Graham A.F. Control of transcription of the reovirus genome. Nucleic Acids Res. 1 (1974) 373-385
50. Odegard A.L., Chandran K., Liemann S., Harrison S.C., and Nibert M.L. Disulfide bonding among μ1 trimers in mammalian reovirus outer capsid: a late and reversible step in virion morphogenesis. J. Virol. 77 (2003) 5389-5400
51. Olland A.M., Jane-Valbuena J., Schiff L.A., Nibert M.L., and Harrison S.C. Structure of the reovirus outer capsid and dsRNA-binding protein sigma3 at 1.8 Å resolution. EMBO J. 20 (2001) 979-989
52. Olson N.O. In: Hofstad M.S. (Ed). Disease of Poultry (1978), Ames, Iowa
53. 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
54. Rebouillat D., and Hovanessian A.G. The human 2′,5′-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J. Interferon Cytokine Res. 19 (1999) 295-308
55. Reinisch K.M., Nibert M.L., and Harrison S.C. Structure of the reovirus core at 3.6 Å resolution. Nature 404 (2000) 960-967
56. 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
57. Robertson M.D., and Wilcox G.E. Avian reovirus. Vet. Bull. 56 (1986) 759-766
58. Rosenberger J.K., Sterner F.J., Botts S., Lee K.P., and Margolin A. In vitro and in vivo characterization of avian reoviruses. I. Pathogenicity and antigenic relatedness of several avian reovirus isolates. Avian Dis. 33 (1989) 535-544
59. Ryabova L.A., and Hohn T. Ribosome shunting in the cauliflower mosaic virus 35S RNA leader is a special case of reinitiation of translation functioning in plant and animal systems. Genes Dev. 14 (2000) 817-829
60. Salsman J., Top D., Boutilier J., and Duncan R. Extensive syncytium formation by the reovirus FAST proteins triggers apoptosis-induced membrane instability. J. Virol. 79 (2005) 8090-8100
61. Schnitzer T.J. Protein coding assignment of the S genes of the avian reovirus S1133. Virology 141 (1985) 167-170
62. Schnitzer T.J., Ramos T., and Gouvea V. Avian reovirus polypeptides: analysis of intracellular virus-specified products, virions, top component, and cores. J. Virol. 43 (1982) 1006-1014
63. Sen G.C. Viruses and interferons. Ann. Rev. Microbiol. 55 (2001) 255-281
64. Shapouri M.R., Arella M., and Silim A. Evidence for the multimeric nature and cell binding ability of avian reovirus sigma 3 protein. J. Gen. Virol. 77 (1996) 1203-1210
65. Shapouri M.R., Kane M., Letarte M., Bergeron J., Arella M., and Silim A. Cloning, sequencing and expression of the S1 gene of avian reovirus. J. Gen. Virol. 76 (1995) 1515-1520
66. Shatkin A.J., and LaFiandra A.J. Transcription by infectious subviral particles of reoviruses. Proc. Natl. Acad. Sci. U.S.A. 10 (1972) 698-706
67. Shih W.L., Hsu H.W., Liao M.H., Lee L.H., and Liu H.J. Avian reovirus σC protein induces apoptosis in cultured cells. Virology 321 (2004) 65-74
68. Shmulevitz M., Corcoran J., Salsean J., and Duncan R. Cell-cell fusion induced by the avian reovirus membrana fusion protein is regulated by protein degradation. J. Virol. 78 (2004) 5996-6004
69. Shmulevitz M., and Duncan R. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO J. 19 (2000) 902-912
70. Shmulevitz M., Salsman J., and Duncan R. Palmytoylation, membrane-proximal basic residues, and transmembrane glycine residues in the reovirus p10 protein are essential for syncytium formation. J. Virol. 77 (2003) 9769-9779
71. Shmulevitz M., Yameen Z., Dawe S., Shou J., O'Hara D., Holmes I., and Duncan R. Sequential partially overlapping gene arrangement in the tricistronic S1 genome segments of avian reovirus and Nelson Bay reovirus: implications for translation initiation. J. Virol. 76 (2002) 609-618
72. Silverstein S.C., and Schur P.H. Immunofluorescent localization of double-stranded RNA in reovirus-infected cells. Virology 41 (1970) 564-566
73. Spandidos D.A., and Graham A.F. Physical and chemical characterization of an avian reovirus. J. Virol. 19 (1976) 968-976
74. Spandidos D.A., and Graham A.F. Nonpermissive infection of L cells by avian reovirus: restricted transcription of the viral genome. J. Virol. 19 (1976) 977-984
75. Sturzenbecker L.J., Nibert M., Furlong D., and Fields B.N. Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J. Virol. 61 (1987) 2351-2361
76. Tourís-Otero F., Cortez-San Martín M., Martínez-Costas J., and Benavente J. Avian reovirus morphogenesis occurs within viral factories and begins with the selective recruitment of σNS and λA to μNS inclusions. J. Mol. Biol. 341 (2004) 361-374
77. Tourís-Otero F., Martínez-Costas J., Vakharia V.N., and Benavente J. Avian reovirus nonstructural protein μNS forms viroplasm-like inclusions and recruits σNS to these structures. Virology 319 (2004) 94-106
78. Tourís-Otero F., Martínez-Costas J., Vakharia V.N., and Benavente J. Characterization of the nucleic acid-binding activity of the avian reovirus nonstructural protein σNS. J. Gen. Virol. 86 (2005) 1159-1169
79. van der Heide L. The history of avian reovirus. Avian Dis. 44 (2000) 638-641
80. Varela R., and Benavente J. Protein coding assignment of avian reovirus strain S1133. J. Virol. 68 (1994) 6775-6777
81. Varela R., Martínez-Costas J., Mallo M., and Benavente J. Intracellular posttranslational modifications of S1133 avian reovirus proteins. J. Virol. 70 (1996) 2974-2981
82. Wiebe M.E., and Joklik W.K. The mechanism of inhibition of reovirus replication by interferon. Virology 66 (1975) 229-240
83. Xu W., Patrick M.K., Hazelton P.R., and Coombs K.M. Avian reovirus temperature-sensitive mutant tsA12 has a lesion in major core protein σA and is defective in assembly. J. Virol. 78 (2004) 11142-11151
84. Yin H.S., and Lee L.H. Identification and characterization of RNA-binding activities of avian reovirus non-structural protein σNS. J. Gen. Virol. 79 (1998) 1411-1413
85. Yin H.S., Shien J.H., and Lee L.H. Synthesis in Escherichia coli of avian reovirus core protein σA and its dsRNA-binding activity. Virology 266 (2000) 33-41
86. Yin H.S., Su Y.P., and Lee L.H. Evidence of nucleotidyl phosphatase activity associated with core protein sigma A of avian reovirus S1133. Virology 293 (2002) 379-385
87. Yin P., Keirstead N.D., Broering T.J., Arnold M.M., Parker J.S., Nibert M.L., and Coombs K.M. Comparisons of the M1 genome segments and encoded mu2 proteins of different reovirus isolates. Virol. J. 1 (2004) 6
88. Zhang X., Tang J., Walker S.B., O'Hara D., Nibert M.L., Duncan R., and Baker T.S. Structure of avian Orthoreovirus virion by electron cryomicroscopy and image reconstruction. Virology 343 (2005) 25-35
89. Zhang X., Walker S.B., Chipman P.R., Nibert M.L., and Baker T.S. Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å. Nat. Struct. Biol. 10 (2003) 1011-1018
90. Zweerink H.J., and Joklik W.K. Studies on the intracellular synthesis of reovirus-specific proteins. Virology 41 (1970) 501-518