Sequence Analysis of the Genome of Piscine Orthoreovirus (PRV) Associated with Heart and Skeletal Muscle Inflammation (HSMI) in Atlantic Salmon (Salmo salar)

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Markussen, Turhan ^a   Dahle, Maria K ^a   Tengs, Torstein ^a   Løvoll, Marie ^a   Finstad, Øystein W ^c   Wiik Nielsen, Christer R ^a   Grove, Søren ^a   Lauksund, Silje ^b   Robertsen, Børre ^b   Rimstad, Espen ^c  

^a NORWEGIAN VETERINARY INSTITUTE   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; M CLASS PROTEIN; PROLINE; PROTEIN 124 AA (P13); PROTEIN 71 AA (P8); PROTEIN 98 AA (P11); PROTEIN LAMBDA 1; PROTEIN MU 1; PROTEIN SIGMA 1; PROTEIN SIGMA 2; PROTEIN SIGMA 3; SIALIC ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ARTICLE; ATLANTIC SALMON; CELL INCLUSION; CELL INTERACTION; CELLULAR DISTRIBUTION; CISTRON; ENDOSOME; GENOME; GOLGI COMPLEX; GRASS CARP REOVIRUS; HEART AND SKELETAL MUSCLE INFLAMMATION; HUMAN; HUMAN CELL; INFLAMMATION; L CLASS GENE; M CLASS GENE; MEMBRANE PERMEABILITY; MYOCARDITIS; MYRISTYLATION; NONHUMAN; ORTHOREOVIRUS; PISCINE ORTHOREOVIRUS; PREDICTION; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; S CLASS GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRAIN DIFFERENCE; VIRION; VIRUS GENE; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; GENOME, VIRAL; HEART; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; ORTHOREOVIRUS; REOVIRIDAE; SALMO SALAR; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84880813000     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070075     Document Type: Article

References (150)

1. Palacios G, Løvoll M, Tengs T, Hornig M, Hutchison S, et al. (2010) Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS One 5: e11487.
2. Kongtorp RT, Taksdal T, Lyngøy A, (2004) Pathology of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar. Dis Aquat Organ 59: 217-224.
3. Mikalsen AB, Haugland Ø, Rode M, Solbakk IT, Evensen Ø, (2012) Atlantic salmon reovirus infection causes a CD8 T cell myocarditis in Atlantic salmon (Salmo salar L.). PLoS One 7: e37269.
4. Løvoll M, Wiik-Nielsen J, Grove S, Wiik-Nielsen CR, Kristoffersen AB, et al. (2010) A novel totivirus and piscine reovirus (PRV) in Atlantic salmon (Salmo salar) with cardiomyopathy syndrome (CMS). Virol J 7: 309.
5. Attoui H, Fang Q, Mohd JF, Cantaloube JF, Biagini P, et al. (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.
6. Duncan R, (1999) Extensive sequence divergence and phylogenetic relationships between the fusogenic and nonfusogenic orthoreoviruses: a species proposal. Virology 260: 316-328.
7. Thalmann CM, Cummins DM, Yu M, Lunt R, Pritchard LI, et al. (2010) Broome virus, a new fusogenic Orthoreovirus species isolated from an Australian fruit bat. Virology 402: 26-40.
8. Weiner HL, Drayna D, Averill DR Jr, Fields BN, (1977) Molecular basis of reovirus virulence: role of the S1 gene. Proc Natl Acad Sci U S A 74: 5744-5748.
9. Weiner HL, Powers ML, Fields BN, (1980) Absolute linkage of virulence and central nervous system cell tropism of reoviruses to viral hemagglutinin. J Infect Dis 141: 609-616.
10. Lee PW, Hayes EC, Joklik WK, (1981) Protein sigma 1 is the reovirus cell attachment protein. Virology 108: 156-163.
11. Tyler KL, Mann MA, Fields BN, Virgin HW, (1993) Protective anti-reovirus monoclonal antibodies and their effects on viral pathogenesis. J Virol 67: 3446-3453.
12. Silverstein SC, Astell C, Levin DH, Schonberg M, Acs G, (1972) The mechanisms of reovirus uncoating and gene activation in vivo. Virology 47: 797-806.
13. Chang CT, Zweerink HJ, (1971) Fate of parental reovirus in infected cell. Virology 46: 544-555.
14. Lucia-Jandris P, Hooper JW, Fields BN, (1993) Reovirus M2 gene is associated with chromium release from mouse L cells. J Virol 67: 5339-5345.
15. Chandran K, Walker SB, Chen Y, Contreras CM, Schiff LA, et al. (1999) In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins mu1 and sigma3. J Virol 73: 3941-3950.
16. Sturzenbecker LJ, Nibert M, Furlong D, 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.
17. Chandran K, Farsetta DL, Nibert ML, (2002) Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption. J Virol 76: 9920-9933.
18. Chandran K, Nibert ML, (2003) Animal cell invasion by a large nonenveloped virus: reovirus delivers the goods. Trends Microbiol 11: 374-382.
19. Guglielmi KM, Johnson EM, Stehle T, Dermody TS, (2006) Attachment and cell entry of mammalian orthoreovirus. Curr Top Microbiol Immunol 309: 1-38.
20. Furuichi Y, Muthukrishnan S, Tomasz J, Shatkin AJ, (1976) Mechanism of formation of reovirus mRNA 5′-terminal blocked and methylated sequence, m7GpppGmpC. J Biol Chem 251: 5043-5053.
21. Bisaillon M, Bergeron J, Lemay G, (1997) Characterization of the nucleoside triphosphate phosphohydrolase and helicase activities of the reovirus lambda1 protein. J Biol Chem 272: 18298-18303.
22. Bisaillon M, Lemay G, (1997) Characterization of the reovirus lambda1 protein RNA 5′-triphosphatase activity. J Biol Chem 272: 29954-29957.
23. Noble S, Nibert ML, (1997) Characterization of an ATPase activity in reovirus cores and its genetic association with core-shell protein lambda1. J Virol 71: 2182-2191.
24. Cleveland DR, Zarbl H, Millward S, (1986) Reovirus guanylyltransferase is L2 gene product lambda 2. J Virol 60: 307-311.
25. Wiener JR, Joklik WK, (1989) The sequences of the reovirus serotype 1, 2, and 3 L1 genome segments and analysis of the mode of divergence of the reovirus serotypes. Virology 169: 194-203.
26. Furuichi Y, Morgan M, Muthukrishnan S, Shatkin AJ, (1975) Reovirus messenger RNA contains a methylated, blocked 5′-terminal structure: m7G(5′)ppp(5′)GmpCp-. Proc Natl Acad Sci U S A 72: 362-366.
27. Fausnaugh J, Shatkin AJ, (1990) Active site localization in a viral mRNA capping enzyme. J Biol Chem 265: 7669-7672.
28. Mao ZX, Joklik WK, (1991) Isolation and enzymatic characterization of protein lambda 2, the reovirus guanylyltransferase. Virology 185: 377-386.
29. Martinez-Costas J, Varela R, Benavente J, (1995) Endogenous enzymatic activities of the avian reovirus S1133: identification of the viral capping enzyme. Virology 206: 1017-1026.
30. Schiff LA, Nibert ML, Tyler KL (2007) Orthoreoviruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al., editors. Fields Virology. 5 ed: Lippincott Williams & Wilkins, Philadelphia, PA. 1853-1915.
31. Mohd JF, Goodwin AE, Belhouchet M, Merry G, Fang Q, et al. (2008) Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses. Virology 373: 310-321.
32. Chapell JD, Goral MI, Rodgers SE, dePamphilis CW, Dermody TS, (1994) Sequence diversity within the reovirus S2 gene: reovirus genes reassort in nature, and their termini are predicted to form a panhandle motif. J Virol 68: 750-756.
33. Li JK, Keene JD, Scheible PP, Joklik WK, (1980) Nature of the 3′-terminal sequences of the plus and minus strands of the S1 gene of reovirus serotypes 1, 2 and 3. Virology 105: 41-51.
34. Zou S, Brown EG, (1992) Identification of sequence elements containing signals for replication and encapsidation of the reovirus M1 genome segment. Virology 186: 377-388.
35. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
36. Tao Y, Farsetta DL, Nibert ML, Harrison SC, (2002) RNA synthesis in a cage-structural studies of reovirus polymerase lambda3. Cell 111: 733-745.
37. Bisaillon M, Lemay G, (1999) Computational sequence analysis of mammalian reovirus proteins. Virus Genes 18: 13-37.
38. Xu W, Coombs KM, (2008) Avian reovirus L2 genome segment sequences and predicted structure/function of the encoded RNA-dependent RNA polymerase protein. Virol J 5: 153.
39. Bruenn JA, (2003) A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res 31: 1821-1829.
40. O'Reilly EK, Kao CC, (1998) Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 252: 287-303.
41. Kamer G, Argos P, (1984) Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res 12: 7269-7282.
42. Poch O, Sauvaget I, Delarue M, Tordo N, (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8: 3867-3874.
43. Morozov SY, (1989) A possible relationship of reovirus putative RNA polymerase to polymerases of positive-strand RNA viruses. Nucleic Acids Res 17: 5394.
44. Hsiao J, Martinez-Costas J, Benavente J, Vakharia VN, (2002) Cloning, expression, and characterization of avian reovirus guanylyltransferase. Virology 296: 288-299.
45. Luongo CL, Contreras CM, Farsetta DL, Nibert ML, (1998) Binding site for S-adenosyl-L-methionine in a central region of mammalian reovirus lambda2 protein. Evidence for activities in mRNA cap methylation. J Biol Chem 273: 23773-23780.
46. Luongo CL, Reinisch KM, Harrison SC, Nibert ML, (2000) Identification of the guanylyltransferase region and active site in reovirus mRNA capping protein lambda2. J Biol Chem 275: 2804-2810.
47. Qiu T, Luongo CL, (2003) Identification of two histidines necessary for reovirus mRNA guanylyltransferase activity. Virology 316: 313-324.
48. Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, et al. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res 38: W563-W568.
49. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202.
50. Varela R, Benavente J, (1994) Protein coding assignment of avian reovirus strain S1133. J Virol 68: 6775-6777.
51. Bartlett JA, Joklik WK, (1988) The sequence of the reovirus serotype 3 L3 genome segment which encodes the major core protein lambda 1. Virology 167: 31-37.
52. Fang Q, Attoui H, Cantaloube JF, Biagini P, Zhu Z, et al. (2000) Sequence of genome segments 1, 2, and 3 of the grass carp reovirus (Genus Aquareovirus, family Reoviridae). Biochem Biophys Res Commun 274: 762-766.
53. Kim J, Tao Y, Reinisch KM, Harrison SC, Nibert ML, (2004) Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein-protein interfaces. Virus Res 101: 15-28.
54. Reinisch KM, Nibert ML, Harrison SC, (2000) Structure of the reovirus core at 3.6 A resolution. Nature 404: 960-967.
55. Bisaillon M, Lemay G, (1997) Molecular dissection of the reovirus lambda1 protein nucleic acids binding site. Virus Res 51: 231-237.
56. Harrison SJ, Farsetta DL, Kim J, Noble S, Broering TJ, et al. (1999) Mammalian reovirus L3 gene sequences and evidence for a distinct amino-terminal region of the lambda1 protein. Virology 258: 54-64.
57. Lemay G, Danis C, (1994) Reovirus lambda 1 protein: affinity for double-stranded nucleic acids by a small amino-terminal region of the protein independent from the zinc finger motif. J Gen Virol 75: 3261-3266.
58. Xu W, Coombs KM, (2009) Conserved structure/function of the orthoreovirus major core proteins. Virus Res 144: 44-57.
59. Wang L, Brown SJ, (2006) BindN: a web-based tool for efficient prediction of DNA and RNA binding sites in amino acid sequences. Nucleic Acids Res 34: W243-W248.
60. Coombs KM, (1998) Stoichiometry of reovirus structural proteins in virus, ISVP, and core particles. Virology 243: 218-228.
61. Brentano L, Noah DL, Brown EG, Sherry B, (1998) The reovirus protein mu2, encoded by the M1 gene, is an RNA-binding protein. J Virol 72: 8354-8357.
62. Noble S, Nibert ML, (1997) Core protein mu2 is a second determinant of nucleoside triphosphatase activities by reovirus cores. J Virol 71: 7728-7735.
63. Kim J, Parker JS, Murray KE, Nibert ML, (2004) Nucleoside and RNA triphosphatase activities of orthoreovirus transcriptase cofactor mu2. J Biol Chem 279: 4394-4403.
64. Su YP, Shien JH, Liu HJ, Yin HS, Lee LH, (2007) Avian reovirus core protein muA expressed in Escherichia coli possesses both NTPase and RTPase activities. J Gen Virol 88: 1797-1805.
65. Kobayashi T, Ooms LS, Chappell JD, Dermody TS, (2009) Identification of functional domains in reovirus replication proteins muNS and mu2. J Virol 83: 2892-2906.
66. Parker JS, Broering TJ, Kim J, Higgins DE, Nibert ML, (2002) Reovirus core protein mu2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J Virol 76: 4483-4496.
67. Yin P, Keirstead ND, Broering TJ, Arnold MM, Parker JS, et al. (2004) Comparisons of the M1 genome segments and encoded mu2 proteins of different reovirus isolates. Virol J 1: 6.
68. Touris-Otero F, Cortez-San MM, Martinez-Costas J, Benavente J, (2004) Avian reovirus morphogenesis occurs within viral factories and begins with the selective recruitment of sigmaNS and lambdaA to microNS inclusions. J Mol Biol 341: 361-374.
69. Irvin SC, Zurney J, Ooms LS, Chappell JD, Dermody TS, et al. (2012) A single-amino-acid polymorphism in reovirus protein mu2 determines repression of interferon signaling and modulates myocarditis. J Virol 86: 2302-2311.
70. Jayasuriya AK, Nibert ML, Fields BN, (1988) Complete nucleotide sequence of the M2 gene segment of reovirus type 3 dearing and analysis of its protein product mu 1. Virology 163: 591-602.
71. Wiener JR, Joklik WK, (1988) Evolution of reovirus genes: a comparison of serotype 1, 2, and 3 M2 genome segments, which encode the major structural capsid protein mu 1C. Virology 163: 603-613.
72. Tillotson L, Shatkin AJ, (1992) Reovirus polypeptide sigma 3 and N-terminal myristoylation of polypeptide mu 1 are required for site-specific cleavage to mu 1C in transfected cells. J Virol 66: 2180-2186.
73. Varela R, Martinez-Costas J, Mallo M, Benavente J, (1996) Intracellular posttranslational modifications of S1133 avian reovirus proteins. J Virol 70: 2974-2981.
74. Odegard AL, Chandran K, Zhang X, Parker JS, Baker TS, et al. (2004) Putative autocleavage of outer capsid protein micro1, allowing release of myristoylated peptide micro1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78: 8732-8745.
75. Nibert ML, Odegard AL, Agosto MA, Chandran K, Schiff LA, (2005) Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J Mol Biol 345: 461-474.
76. McCrae MA, Joklik WK, (1978) The nature of the polypeptide encoded by each of the 10 double-stranded RNA segments of reovirus type 3. Virology 89: 578-593.
77. Mustoe TA, Ramig RF, Sharpe AH, Fields BN, (1978) Genetics of reovirus: identification of the ds RNA segments encoding the polypeptides of the mu and sigma size classes. Virology 89: 594-604.
78. Noad L, Shou J, Coombs KM, Duncan R, (2006) Sequences of avian reovirus M1, M2 and M3 genes and predicted structure/function of the encoded mu proteins. Virus Res 116: 45-57.
79. Ivanovic T, Boulant S, Ehrlich M, Demidenko AA, Arnold MM, et al. (2011) Recruitment of cellular clathrin to viral factories and disruption of clathrin-dependent trafficking. Traffic 12: 1179-1195.
80. Mora M, Partin K, Bhatia M, Partin J, Carter C, (1987) Association of reovirus proteins with the structural matrix of infected cells. Virology 159: 265-277.
81. Broering TJ, Kim J, Miller CL, Piggott CD, Dinoso JB, et al. (2004) Reovirus nonstructural protein mu NS recruits viral core surface proteins and entering core particles to factory-like inclusions. J Virol 78: 1882-1892.
82. Broering TJ, McCutcheon AM, Centonze VE, Nibert ML, (2000) Reovirus nonstructural protein muNS binds to core particles but does not inhibit their transcription and capping activities. J Virol 74: 5516-5524.
83. Broering TJ, Parker JS, Joyce PL, Kim J, Nibert ML, (2002) Mammalian reovirus nonstructural protein microNS forms large inclusions and colocalizes with reovirus microtubule-associated protein micro2 in transfected cells. J Virol 76: 8285-8297.
84. Miller CL, Arnold MM, Broering TJ, Hastings CE, Nibert ML, (2010) Localization of mammalian orthoreovirus proteins to cytoplasmic factory-like structures via nonoverlapping regions of microNS. J Virol 84: 867-882.
85. Miller CL, Broering TJ, Parker JS, Arnold MM, Nibert ML, (2003) Reovirus sigma NS protein localizes to inclusions through an association requiring the mu NS amino terminus. J Virol 77: 4566-4576.
86. Brandariz-Nunez A, Menaya-Vargas R, Benavente J, Martinez-Costas J, (2010) Avian reovirus microNS protein forms homo-oligomeric inclusions in a microtubule-independent fashion, which involves specific regions of its C-terminal domain. J Virol 84: 4289-4301.
87. Touris-Otero F, Martinez-Costas J, Vakharia VN, Benavente J, (2004) Avian reovirus nonstructural protein microNS forms viroplasm-like inclusions and recruits protein sigmaNS to these structures. Virology 319: 94-106.
88. McCutcheon AM, Broering TJ, Nibert ML, (1999) Mammalian reovirus M3 gene sequences and conservation of coiled-coil motifs near the carboxyl terminus of the microNS protein. Virology 264: 16-24.
89. Cai L, Sun X, Shao L, Fang Q, (2011) Functional investigation of grass carp reovirus nonstructural protein NS80. Virol J 8: 168.
90. Broering TJ, Arnold MM, Miller CL, Hurt JA, Joyce PL, et al. (2005) Carboxyl-proximal regions of reovirus nonstructural protein muNS necessary and sufficient for forming factory-like inclusions. J Virol 79: 6194-6206.
91. Wiener JR, Bartlett JA, Joklik WK, (1989) The sequences of reovirus serotype 3 genome segments M1 and M3 encoding the minor protein mu 2 and the major nonstructural protein mu NS, respectively. Virology 169: 293-304.
92. Busch LK, Rodriguez-Grille J, Casal JI, Martinez-Costas J, Benavente J, (2011) Avian and mammalian reoviruses use different molecular mechanisms to synthesize their {micro}NS isoforms. J Gen Virol 92: 2566-2574.
93. Kozak M, (1991) An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 115: 887-903.
94. Schnitzer TJ, Ramos T, Gouvea V, (1982) Avian reovirus polypeptides: analysis of intracellular virus-specified products, virions, top component, and cores. J Virol 43: 1006-1014.
95. Yin HS, Shieh HK, Lee LH, (1997) Characterization of the double-stranded RNA genome segment S3 of avian reovirus. J Virol Methods 67: 93-101.
96. Key T, Read J, Nibert ML, Duncan R, (2013) Piscine Reovirus Encodes a Cytotoxic, Nonfusogenic, Integral Membrane Protein and Previously Unrecognized Virion Outer-Capsid Proteins. J Gen Virol 94: 1039-50.
97. Schiff LA, Nibert ML, Co MS, Brown EG, Fields BN, (1988) Distinct binding sites for zinc and double-stranded RNA in the reovirus outer capsid protein sigma 3. Mol Cell Biol 8: 273-283.
98. Martinez-Costas J, Grande A, Varela R, Garcia-Martinez C, Benavente J, (1997) Protein architecture of avian reovirus S1133 and identification of the cell attachment protein. J Virol 71: 59-64.
99. Cheng L, Fang Q, Shah S, Atanasov IC, Zhou ZH, (2008) Subnanometer-resolution structures of the grass carp reovirus core and virion. J Mol Biol 382: 213-222.
100. Guardado-Calvo P, Vazquez-Iglesias L, Martinez-Costas J, Llamas-Saiz AL, Schoehn G, et al. (2008) Crystal structure of the avian reovirus inner capsid protein sigmaA. J Virol 82: 11208-11216.
101. Yin HS, Shien JH, Lee LH, (2000) Synthesis in Escherichia coli of avian reovirus core protein varsigmaA and its dsRNA-binding activity. Virology 266: 33-41.
102. Dermody TS, Schiff LA, Nibert ML, Coombs KM, Fields BN, (1991) The S2 gene nucleotide sequences of prototype strains of the three reovirus serotypes: characterization of reovirus core protein sigma 2. J Virol 65: 5721-5731.
103. Richardson MA, Furuichi Y, (1983) Nucleotide sequence of reovirus genome segment S3, encoding non-structural protein sigma NS. Nucleic Acids Res 11: 6399-6408.
104. Gillian AL, Nibert ML, (1998) Amino terminus of reovirus nonstructural protein sigma NS is important for ssRNA binding and nucleoprotein complex formation. Virology 240: 1-11.
105. la Cour T, Kiemer L, Molgaard A, Gupta R, Skriver K, et al. (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 17: 527-536.
106. Weiner HL, Ault KA, Fields BN, (1980) Interaction of reovirus with cell surface receptors. I. Murine and human lymphocytes have a receptor for the hemagglutinin of reovirus type 3. J Immunol 124: 2143-2148.
107. Ernst H, Shatkin AJ, (1985) Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc Natl Acad Sci U S A 82: 48-52.
108. Bodelon G, Labrada L, Martinez-Costas J, Benavente J, (2001) The avian reovirus genome segment S1 is a functionally tricistronic gene that expresses one structural and two nonstructural proteins in infected cells. Virology 290: 181-191.
109. Grande A, Costas C, Benavente J, (2002) Subunit composition and conformational stability of the oligomeric form of the avian reovirus cell-attachment protein sigmaC. J Gen Virol 83: 131-139.
110. Shaw AL, Samal SK, Subramanian K, Prasad BV, (1996) The structure of aquareovirus shows how the different geometries of the two layers of the capsid are reconciled to provide symmetrical interactions and stabilization. Structure 4: 957-967.
111. Fraser RD, Furlong DB, Trus BL, Nibert ML, Fields BN, et al. (1990) Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J Virol 64: 2990-3000.
112. Nibert ML, Dermody TS, Fields BN, (1990) Structure of the reovirus cell-attachment protein: a model for the domain organization of sigma 1. J Virol 64: 2976-2989.
113. Shapouri MR, Kane M, Letarte M, Bergeron J, Arella M, et al. (1995) Cloning, sequencing and expression of the S1 gene of avian reovirus. J Gen Virol 76: 1515-1520.
114. Strong JE, Leone G, Duncan R, Sharma RK, Lee PW, (1991) Biochemical and biophysical characterization of the reovirus cell attachment protein sigma 1: evidence that it is a homotrimer. Virology 184: 23-32.
115. Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, et al. (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104: 441-451.
116. Dryden KA, Wang G, Yeager M, Nibert ML, Coombs KM, et al. (1993) 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: 1023-1041.
117. Chappell JD, Duong JL, Wright BW, Dermody TS, (2000) Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J Virol 74: 8472-8479.
118. Chappell JD, Prota AE, Dermody TS, Stehle T, (2002) Crystal structure of reovirus attachment protein sigma1 reveals evolutionary relationship to adenovirus fiber. EMBO J 21: 1-11.
119. Campbell JA, Schelling P, Wetzel JD, Johnson EM, Forrest JC, et al. (2005) Junctional adhesion molecule a serves as a receptor for prototype and field-isolate strains of mammalian reovirus. J Virol 79: 7967-7978.
120. Gentsch JR, Pacitti AF, (1985) Effect of neuraminidase treatment of cells and effect of soluble glycoproteins on type 3 reovirus attachment to murine L cells. J Virol 56: 356-364.
121. Paul RW, Choi AH, Lee PW, (1989) The alpha-anomeric form of sialic acid is the minimal receptor determinant recognized by reovirus. Virology 172: 382-385.
122. Dermody TS, Nibert ML, Bassel-Duby R, Fields BN, (1990) A sigma 1 region important for hemagglutination by serotype 3 reovirus strains. J Virol 64: 5173-5176.
123. Chappell JD, Gunn VL, Wetzel JD, Baer GS, Dermody TS, (1997) Mutations in type 3 reovirus that determine binding to sialic acid are contained in the fibrous tail domain of viral attachment protein sigma1. J Virol 71: 1834-1841.
124. Reiter DM, Frierson JM, Halvorson EE, Kobayashi T, Dermody TS, et al. (2011) Crystal structure of reovirus attachment protein sigma1 in complex with sialylated oligosaccharides. PLoS Pathog 7: e1002166.
125. Racine T, Hurst T, Barry C, Shou J, Kibenge F, et al. (2009) Aquareovirus effects syncytiogenesis by using a novel member of the FAST protein family translated from a noncanonical translation start site. J Virol 83: 5951-5955.
126. Guo H, Sun X, Yan L, Shao L, Fang Q, (2013) The NS16 protein of aquareovirus-C is a fusion-associated small transmembrane (FAST) protein, and its activity can be enhanced by the nonstructural protein NS26. Virus Res 171: 129-137.
127. Shmulevitz M, Duncan R, (2000) A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO J 19: 902-912.
128. Ke F, He LB, Pei C, Zhang QY, (2011) Turbot reovirus (SMReV) genome encoding a FAST protein with a non-AUG start site. BMC Genomics 12: 323.
129. Dawe S, Duncan R, (2002) The S4 genome segment of baboon reovirus is bicistronic and encodes a novel fusion-associated small transmembrane protein. J Virol 76: 2131-2140.
130. Corcoran JA, Duncan R, (2004) Reptilian reovirus utilizes a small type III protein with an external myristylated amino terminus to mediate cell-cell fusion. J Virol 78: 4342-4351.
131. Boutilier J, Duncan R, (2011) The reovirus fusion-associated small transmembrane (FAST) proteins: virus-encoded cellular fusogens. Curr Top Membr 68: 107-140.
132. Touris-Otero F, Martinez-Costas J, Vakharia VN, Benavente J, (2005) Characterization of the nucleic acid-binding activity of the avian reovirus non-structural protein sigma NS. J Gen Virol 86: 1159-1169.
133. Zurney J, Kobayashi T, Holm GH, Dermody TS, Sherry B, (2009) Reovirus mu2 protein inhibits interferon signaling through a novel mechanism involving nuclear accumulation of interferon regulatory factor 9. J Virol 83: 2178-2187.
134. Gonzalez-Lopez C, Martinez-Costas J, Esteban M, Benavente J, (2003) Evidence that avian reovirus sigmaA protein is an inhibitor of the double-stranded RNA-dependent protein kinase. J Gen Virol 84: 1629-1639.
135. Martinez-Costas J, Gonzalez-Lopez C, Vakharia VN, Benavente J, (2000) Possible involvement of the double-stranded RNA-binding core protein sigmaA in the resistance of avian reovirus to interferon. J Virol 74: 1124-1131.
136. Sherry B, (2009) Rotavirus and reovirus modulation of the interferon response. J Interferon Cytokine Res 29: 559-567.
137. Imani F, Jacobs BL, (1988) Inhibitory activity for the interferon-induced protein kinase is associated with the reovirus serotype 1 sigma 3 protein. Proc Natl Acad Sci U S A 85: 7887-7891.
138. Lauksund S, Svingerud T, Bergan V, Robertsen B, (2009) Atlantic salmon IPS-1 mediates induction of IFNa1 and activation of NF-kappaB and localizes to mitochondria. Dev Comp Immunol 33: 1196-1204.
139. Bergan V, Steinsvik S, Xu H, Kileng Ø, Robertsen B, (2006) Promoters of type I interferon genes from Atlantic salmon contain two main regulatory regions. FEBS J 273: 3893-3906.
140. Boehme KW, Frierson JM, Konopka JL, Kobayashi T, Dermody TS, (2011) The reovirus sigma1s protein is a determinant of hematogenous but not neural virus dissemination in mice. J Virol 85: 11781-11790.
141. Boehme KW, Guglielmi KM, Dermody TS, (2009) Reovirus nonstructural protein sigma1s is required for establishment of viremia and systemic dissemination. Proc Natl Acad Sci U S A 106: 19986-19991.
142. Hoyt CC, Richardson-Burns SM, Goody RJ, Robinson BA, Debiasi RL, et al. (2005) Nonstructural protein sigma1s is a determinant of reovirus virulence and influences the kinetics and severity of apoptosis induction in the heart and central nervous system. J Virol 79: 2743-2753.
143. Poggioli GJ, Keefer C, Connolly JL, Dermody TS, Tyler KL, (2000) Reovirus-induced G(2)/M cell cycle arrest requires sigma1s and occurs in the absence of apoptosis. J Virol 74: 9562-9570.
144. Chulu JL, Huang WR, Wang L, Shih WL, Liu HJ, (2010) Avian reovirus nonstructural protein p17-induced G(2)/M cell cycle arrest and host cellular protein translation shutoff involve activation of p53-dependent pathways. J Virol 84: 7683-7694.
145. Costas C, Martinez-Costas J, Bodelon G, Benavente J, (2005) The second open reading frame of the avian reovirus S1 gene encodes a transcription-dependent and CRM1-independent nucleocytoplasmic shuttling protein. J Virol 79: 2141-2150.
146. John KR, George MR, Richards RH, Frerichs GN, (2001) Characteristics of a new reovirus isolated from epizootic ulcerative syndrome infected snakehead fish. Dis Aquat Organ 46: 83-92.
147. Wolf E, Kim PS, Berger B, (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci 6: 1179-1189.
148. Lupas A, Van DM, Stock J, (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
149. Kyte J, Doolittle RF, (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
150. Ren J, Wen L, Gao X, Jin C, Xue Y, et al. (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 21: 639-644.