Structure of Mammalian Orthoreovirus Particles

  • M. L. Nibert
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 233/1)


An overview of the mammalian orthoreoviruses and comparisons with other double-stranded RNA (dsRNA) viruses are included to stimulate speculation about the evolution of these viruses and their structures.


dsRNA Segment Transcriptase Complex Reovirus Type Avian Reovirus Reoviridae Family 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Ahne W, Thomsen I, Winton J (1987) Isolation of a reovirus from the snake, Python regius. Arch Virol 94: 135–139Google Scholar
  2. Arnott S, Hukins DW, Dover SD (1972) Optimised parameters for RNA double-helices. Biochem Biophys Res Commun 48: 1392–1399PubMedCrossRefGoogle Scholar
  3. Bartlett JA, Joklik WK (1988) The sequence of the reovirus serotype 3 L3 genome segment which encodes the major core protein Al. Virology 167: 31–37PubMedCrossRefGoogle Scholar
  4. Bartlett NM, Gillies SC, Bullivant S. Bellamy AR (1974) Electron microscopy study of reovirus reaction cores. J Virol 14: 315–326PubMedGoogle Scholar
  5. Bassel-Duby R, Nibert ML, Homcy CJ, Fields BN, Sawutz DG (1987) Evidence that the al protein of reovirus serotype 3 is a multimer. J Virol 61: 1834–1841PubMedGoogle Scholar
  6. Bellamy AR, Nichols JL, Joklik WK (1972) Nucleotide sequences of reovirus oligonucleotides: evidence for abortive RNA synthesis during virus maturation. Nature (Lond) 238: 49–51CrossRefGoogle Scholar
  7. Bodkin DK, Nibert ML, Fields BN (1989) Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J Virol 63: 4676–4681PubMedGoogle Scholar
  8. Borsa J, Copps TP, Sargent MD, Long DG, Chapman JD (1973) New intermediate subviral particles in the in vitro uncoating of reovirus virions by chymotrypsin. J Virol 11: 552–564PubMedGoogle Scholar
  9. Bottcher B, Kiselev NA, Stel’Mashchuk VY, Perevozchikova NA, Borisov AV, Crowther RA (1997) Three-dimensional structure of infectious bursal disease virus determined by electron cryomicroscopy. J Virol 71: 325–330PubMedGoogle Scholar
  10. Bruenn JA (1991) Relationships among the positive strand and double-stranded RNA viruses as viewed through their RNA-dependent RNA polymerases. Nucleic Acids Res 19: 217–226PubMedCrossRefGoogle Scholar
  11. Burstin SJ, Spriggs DR, Fields BN (1982) Evidence for functional domains on the reovirus type 3 hemagglutinin. Virology 117: 146–155PubMedCrossRefGoogle Scholar
  12. Centonze VE, Ya C, Severson TF, Borisy GG, Nibert ML (1995) Visualization of individual reovirus particles by low-temperature, high-resolution scanning electron microscopy. J Struct Biol 115: 215–225PubMedCrossRefGoogle Scholar
  13. Chandran K, Nibert ML (1998) Protease cleavage of reovirus capsid protein gl/µ1C is blocked by alkyl sulfate detergents, fielding a new type of infectious subvirion particle. J Virol 72: 467–475PubMedGoogle Scholar
  14. Chappell JD, Goral MI, Rodgers SE, dePamphilis CW, Dennody 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: 750–756Google Scholar
  15. Cheng RH, Caston JR, Wang GJ, Gu F, Smith TJ, Baker TS, Bozarth RF, Trus BL, Cheng N, Wickner RB et al. (1994) Fungal virus capsids, cytoplasmic compartments for the replication of double-stranded RNA, formed as icosahedral shells of asymmetric Gag dimers. J Mol Biol 244: 255–258PubMedCrossRefGoogle Scholar
  16. Cleveland DR, Zarbl H, Millward S (1986) Reovirus guanylyltransferase is L2 gene product)2. J Virol 60: 307–311PubMedGoogle Scholar
  17. Coombs KM (1996) Identification and characterization of a double-stranded RNA-reovirus temperature-sensitive mutant defective in minor core protein p2. J. Virol 70: 4237–4245PubMedGoogle Scholar
  18. Coombs KM, Fields BN, Harrison SC (1990) Crystallization of the reovirus type 3 Dearing core. Crystal packing is determined by the X2 protein. J Mol Biol 215: 1–5PubMedCrossRefGoogle Scholar
  19. Danis C, Garzon S, Lemay G (1992) Further characterization of the ts453 mutant of mammalian orthoreovirus serotype 3 and nucleotide sequence of the mutated S4 gene. Virology 190: 494–498PubMedCrossRefGoogle Scholar
  20. Denzler KL, Jacobs BL (1994) Site-directed mutagenic analysis of reovirus a3 protein binding to dsRNA. Virology 204: 190–199PubMedCrossRefGoogle Scholar
  21. Dermody TS. Nibert ML, Bassel-Duby R, Fields BN (1990) A al region important for hemagglutination by serotype 3 reovirus strains. J Virol 64: 5173–5176PubMedGoogle Scholar
  22. 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 o2. J Virol 65: 5721–5731PubMedGoogle Scholar
  23. Drayna D, Fields BN (1982) Biochemical studies on the mechanism of chemical and physical inactivation of reovirus. J Gen Virol 63: 161–170PubMedCrossRefGoogle Scholar
  24. Dryden KA, Wang G, Yeager M, Nibert ML, Coombs KM, Furlong DB, Fields BN, Baker TS (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: 1023–1041PubMedCrossRefGoogle Scholar
  25. Duncan R (1996) The low pH-dependent entry of avian reovirus is accompanied by two specific cleavages of the major outer capsid protein 1.12C. Virology 219: 179–189CrossRefGoogle Scholar
  26. Duncan R, Home D, Cashdollar LW, Joklik WK, Lee PWK (1990) Identification of conserved domains in the cell attachment proteins of the three serotypes of reovirus. Virology 174: 399–409PubMedCrossRefGoogle Scholar
  27. Duncan R, Murphy FA, Mirkovic RR (1995) Characterization of a novel syncytium-inducing baboon reovirus. Virology 212: 752–756PubMedCrossRefGoogle Scholar
  28. Estes MK (1996) Rotaviruses and their replication. In: Fields BN, Knipe DM, Howley PM (eds) Fields virology, 3rd edn. Lippincott-Raven, Philadelphia, pp 1625–1656Google Scholar
  29. Farrell JA, Harvey JD, Bellamy AR (1974) Biophysical studies of reovirus type 3. I. The molecular weight of reovirus and reovirus cores. Virology 62: 145–153Google Scholar
  30. Fausnaugh J, Shatkin AJ (1990) Active site localization in a viral mRNA capping enzyme. J Biol Chem 265: 7669–7672PubMedGoogle Scholar
  31. Fraser RD, Furlong DB, Trus BL, Nibert ML, Fields BN, Steven AC (1990) Molecular structure of the cell-attachment protein of reovirus: correlation of computer-processed electron micrographs with sequence-based predictions. J Virol 64: 2990–3000PubMedGoogle Scholar
  32. Furlong DB, Nibert ML, Fields BN (1988) Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol 62: 246–256PubMedGoogle Scholar
  33. Goral MI, Mochow-Grundy M, Dermody TS (1996) Sequence diversity within the reovirus S3 gene: reoviruses evolve independently of host species, geographic locale, and date of isolation. Virology 216: 265–271PubMedCrossRefGoogle Scholar
  34. Granboulan N, Niveleau A (1967) Etude au microscope electronique du RNA de reovirus. J Microsc 6: 23–30Google Scholar
  35. Harvey JD, Farrell JA, Bellamy AR (1974) Biophysical studies of reovirus type 3. II. Properties of the hydrated particle. Virology 62: 154–160Google Scholar
  36. Harvey JD, Bellamy AR, Earnshaw WC, Schutt C (1981) Biophysical studies of reovirus type 3. IV. Low-angle x-ray diffraction studies. Virology 112: 240–249Google Scholar
  37. Hayes EC, Lee PWK, Miller SE, Joklik WK (1981) The interaction of a series of hybridoma IgGs with reovirus particles. Demonstration that the core protein k2. is exposed on the particle surface. Virology 108: 147–155PubMedCrossRefGoogle Scholar
  38. 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: 46–58PubMedCrossRefGoogle Scholar
  39. Hewat EA, Booth TF, Roy P (1994) Structure of correctly self-assembled bluetongue virus-like particles. J Struct Biol 112: 183–191PubMedCrossRefGoogle Scholar
  40. Hooper JW, Fields BN (1996) Role of the pl protein in reovirus stability and capacity to cause chromium release from host cells. J Virol 70: 459–467PubMedGoogle Scholar
  41. Huismans H, Joklik WK (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: 411–424PubMedCrossRefGoogle Scholar
  42. 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 µl. Virology 163: 591–602PubMedCrossRefGoogle Scholar
  43. Joklik WK (1972) Studies on the effect of chymotrypsin on reovirions. Virology 49: 700–801PubMedCrossRefGoogle Scholar
  44. Joklik WK (1983) The reovirus particle. In: Joklik WK (ed) The reoviridae. Plenum, New York, pp 9–78Google Scholar
  45. Kavenoff R, Talcove D, Mudd JA (1975) Genome-sized RNA from reovirus particles. Proc Natl Acad Sci USA 72: 4317–4321PubMedCrossRefGoogle Scholar
  46. Kedl R, Schmechel S, Schiff L (1995) Comparative sequence analysis of the reovirus S4 genes from 13 serotype 1 and serotype 3 field isolates. J Virol 69: 552–559PubMedGoogle Scholar
  47. Koonin EV (1992) Evolution of double-stranded RNA viruses: a case for polyphyletic origin from different groups of positive-stranded RNA viruses. Semin Virol 3: 327–340Google Scholar
  48. Koonin EV (1993) Computer-assisted identification of a putative methyltransferase domain in NS5 protein of fiaviviruses and X2 protein of reovirus. J Gen Virol 74: 733–740PubMedCrossRefGoogle Scholar
  49. Lawton JA, Estes MK, Prasad BV (1997) Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nature Struct Biol 4: 118–121PubMedCrossRefGoogle Scholar
  50. Lee PWK, Hayes EC, Joklik WK (1981) Protein al is the reovirus cell attachment protein. Virology 108: 156–163PubMedCrossRefGoogle Scholar
  51. Lemay G, Danis C (1994) Reovirus k1 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: 3261–3266PubMedCrossRefGoogle Scholar
  52. Leone G, Mah DC, Lee PWK (1991) The incorporation of reovirus cell attachment protein al into virions requires the N-terminal hydrophobic tail and the adjacent heptad repeat region. Virology 182: 346–350PubMedCrossRefGoogle Scholar
  53. Lepault J, Dubochet J, Baschong W, Kellenberger E (1987) Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J 6: 1507–1512PubMedGoogle Scholar
  54. Liu HJ, Giambrone JJ (1997) Amplification, cloning and sequencing of the crC-encoded gene of avian reovirus. J Virol Methods 63: 203–208PubMedCrossRefGoogle Scholar
  55. Lucia-Jandris P, Hooper JW, Fields BN (1993) Reovirus M2 gene is associated with chromium release from mouse L cells. J Virol 67: 5339–5345PubMedGoogle Scholar
  56. Luongo CL, Dryden KA, Farsetta DL, Margraf RL, Severson TF, Olson NH, Fields BN, Baker TS, Nibert ML (1997) Localization of a C-terminal region of 7,2 protein in reovirus cores. J Virol 71: 8035–8040PubMedGoogle Scholar
  57. Mao ZX, Joklik WK (1991) Isolation and enzymatic characterization of protein 7„2, the reovirus guanylyltransferase. Virology 185: 377–386PubMedCrossRefGoogle Scholar
  58. Metcalf P (1982) The symmetry of the reovirus outer shell. J Ultrastruct Res 78: 292–301PubMedCrossRefGoogle Scholar
  59. Metcalf P, Cyrklaff M, Adrian M (1991) The three-dimensional structure of reovirus obtained by cryoelectron microscopy. EMBO J 10: 3129–3136PubMedGoogle Scholar
  60. Miller JE, Samuel CE (1992) Proteolytic cleavage of the reovirus a3 protein results in enhanced double-stranded RNA-binding activity: identification of a repeated basic amino acid motif within the C-terminal binding region. J Virol 66: 5347–5356PubMedGoogle Scholar
  61. Morgan EM, Zweerink HJ (1974) Reovirus morphogenesis. Corelike particles in cells infected at 39° with wild-type reovirus and temperature-sensitive mutants of groups B and G. Virology 59: 556–565PubMedCrossRefGoogle Scholar
  62. Morgan EM, Zweerink HJ (1975) Characterization of transcriptase and replicase particles isolated from reovirus-infected cells. Virology 68: 455–466PubMedCrossRefGoogle Scholar
  63. Murphy FA (1996) Virus taxonomy. In: Fields BN, Knipe DM, Howley PM (eds) Fields virology, 3rd edn. Lippincott-Raven, Philadelphia, pp 15–57Google Scholar
  64. Ni Y, Ramig RF, Kemp MC (1993) Identification of proteins encoded by avian reoviruses and evidence for post-translational modification. Virology 193: 466–469PubMedCrossRefGoogle Scholar
  65. Nibert ML (1993) Structure and function of reovirus outer-capsid proteins as they relate to early steps in infection. PhD Thesis. Harvard University, Cambridge, MAGoogle Scholar
  66. Nibert ML, Fields BN (1992) A carboxy-terminal fragment of protein µl /µ1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66: 6408–6418PubMedGoogle Scholar
  67. Nibert ML, Dermody TS, Fields BN (1990) Structure of the reovirus cell-attachment protein: a model for the domain organization of al. J Virol 64: 2976–2989PubMedGoogle Scholar
  68. Nibert ML, Furlong DB, Fields BN (1991a) Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host. J Clin Invest 88: 727–734Google Scholar
  69. Nibert ML, Schiff LA, Fields BN (1991b) Mammalian reoviruses contain a myristoylated structural protein. J Virol 65: 1960–1967PubMedGoogle Scholar
  70. Noble S, Nibert ML (1997a) Characterization of an ATPase activity in reovirus cores and its genetic association with core-shell protein? l. J Virol 71:2182–2191Google Scholar
  71. Nibert ML, Chappell JD, Dermody TS (1995) Infectious subvirion particles of reovirus type 3 Dearing exhibit a loss in infectivity and contain a cleaved al protein. J Virol 69:5057–5067PubMedGoogle Scholar
  72. Noble S, Nibert ML (1997b) Core protein p2 is a second determinant of NTPase activities in reovirus cores. J Virol 71: 7728–7735PubMedGoogle Scholar
  73. Ozel M, Gelderblom H (1985) Capsid symmetry of viruses of the proposed birnavirus group. Arch Virol 84: 149–161PubMedCrossRefGoogle Scholar
  74. Powell KF, Harvey JD, Bellamy AR (1984) Reovirus RNA transcriptase: evidence for a conformational change during activation of the core particle. Virology 137: 1–8PubMedCrossRefGoogle Scholar
  75. 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 a3. Mol Cell Biol 8: 273–283PubMedGoogle Scholar
  76. Seliger LS, Zheng K, Shatkin AJ (1987) Complete nucleotide sequence of reovirus L2 gene and deduced amino acid sequence of viral mRNA guanylyltransferase. J Biol Chem 262: 16289–16293PubMedGoogle Scholar
  77. Shatkin AJ, Kozak M (1983) Biochemical aspects of reovirus transcription and translation. In: Joklik WK (ed) The reoviridae. Plenum, New York, pp 79–106Google Scholar
  78. Shaw AL, Rothnagel R, Chen D, Ramig RF, Chiu W, Prasad BVV (1993) Three-dimensional visualization of the rotavirus hemagglutinin structure. Cell 74: 693–701PubMedCrossRefGoogle Scholar
  79. Shaw AL, Samal SK, Subramanian K, Prasad BVV (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: 957–967PubMedCrossRefGoogle Scholar
  80. Shepard DA, Ehnstrom JG, Schiff LA (1995) Association of reovirus outer capsid proteins a3 and pl causes a conformational change that renders a3 protease sensitive. J Virol 69: 8180–8184PubMedGoogle Scholar
  81. Shepard DA, Ehnstrom JG, Skinner PJ, Schiff LA (1996) Mutations in the zinc-binding motif of the reovirus capsid protein a3 eliminate its ability to associate with capsid protein pl. J Virol 70: 2065–2068PubMedGoogle Scholar
  82. Smith RE, Zweerink HJ, Joklik WK (1969) Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39 (4): 791–810PubMedCrossRefGoogle Scholar
  83. Spencer SM, Sgro J-Y, Dryden KA, Baker TS, Nibert ML (1997) IRIS Explorer software for radial-depth cueing reovirus particles and other macromolecular structures determined by transmission cryoelectron microscopy and three-dimensional image reconstruction. J Struct Biol 120: 11–21PubMedCrossRefGoogle Scholar
  84. Spendlove RS, McClain ME, Lennette EH (1970) Enhancement of reovirus infectivity by extracellular removal or alteration of the virus capsid by proteolytic enzymes. J Gen Virol 8: 83–94PubMedCrossRefGoogle Scholar
  85. Starnes MC, Joklik WK (1993) Reovirus protein ?.3 is a poly(C)-dependent poly(G) polymerase. Virology 193: 356–366PubMedCrossRefGoogle Scholar
  86. Strong JE, Leone G, Duncan R, Sharma RK, Lee PWK (1991) Biochemical and biophysical characterization of the reovirus cell attachment protein al: evidence that it is a homotrimer. Virology 184: 23–32PubMedCrossRefGoogle Scholar
  87. 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: 2351–2361PubMedGoogle Scholar
  88. Tillotson L, Shatkin AJ (1992) Reovirus polypeptide a3 and N-terminal myristoylation of polypeptide pl are required for site-specific cleavage to µ1C in transfected cells. J Virol 66: 2180–2186PubMedGoogle Scholar
  89. Tosteson MT. Nibert ML, Fields BN (1993) Ion channels induced in lipid bilayers by subvirion particles of the nonenveloped mammalian reoviruses. Proc Natl Acad Sci USA 90: 10549–10552PubMedCrossRefGoogle Scholar
  90. Vieler E, Baumgartner W, Herbst W, Kohler G (1994) Characterization of a reovirus isolate from a rattle snake, Crotalus viridis, with neurological dysfunction. Arch Virol 138: 341–344Google Scholar
  91. Virgin HW IV, Mann MA, Fields BN, Tyler KL (1991) Monoclonal antibodies to reovirus reveal structure/function relationships between capsid proteins and genetics of susceptibility to antibody action. J Virol 65: 6772–6781PubMedGoogle Scholar
  92. Virgin HW IV, Mann MA, Tyler KL (1994) Protective antibodies inhibit reovirus internalization and uncoating by intracellular proteases. J Virol 68: 6719–6729PubMedGoogle Scholar
  93. Weiner HL, Fields BN (1977) Neutralization of reovirus: the gene responsible for the neutralization antigen. J Exp Med 146: 1305–1310PubMedCrossRefGoogle Scholar
  94. Wessner DR, Fields BN (1993) Isolation and genetic characterization of ethanol-resistant reovirus mutants. J Virol 67: 2442–2447PubMedGoogle Scholar
  95. White CK, Zweerink HJ (1976) Studies on the structure of reovirus cores: selective removal of polypeptide X2. Virology 70: 171–180PubMedCrossRefGoogle Scholar
  96. Wiener JR, Joklik WK (1989) The sequences of the reovirus serotype 1, 2, and 3 LI genome segments and analysis of the mode of divergence of the reovirus serotypes. Virology 169: 194–203Google Scholar
  97. Wiener JR, Bartlett JA, Joklik WK (1989) The sequences of reovirus serotype 3 genome segments MI and M3 encoding the minor protein p2 and the major nonstructural protein µNS, respectively. Virology 169: 293–304PubMedCrossRefGoogle Scholar
  98. Wilcox GE, Compans RW (1982) Cell fusion induced by Nelson Bay Virus. Virology 123: 312–322PubMedCrossRefGoogle Scholar
  99. Xu P, Miller SE, Joklik WK (1993) Generation of reovirus core-like particles in cells infected with hybrid vaccinia viruses that express genome segments LI, L2, L3, and S2. Virology 197: 726–731PubMedCrossRefGoogle Scholar
  100. Yamakawa M, Furuichi Y, Shatkin AJ (1982) Reovirus transcriptase and capping enzymes are active in intact virions. Virology 118: 157–168PubMedCrossRefGoogle Scholar
  101. Yeager M, Dryden KA, Olson NH, Greenberg HB, Baker TS (1990) Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J Cell Biol 110: 2133–2144PubMedCrossRefGoogle Scholar
  102. Yeager M, Weiner S, Coombs KM (1996) Transcriptionally active reovirus core particles visualized by electron cryo-microscopy and image reconstruction. Biophys J 70:A 116Google Scholar
  103. 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: 1223–1227PubMedGoogle Scholar
  104. Zweerink HJ, Morgan EM, Skyler JS (1976) Reovirus morphogenesis: characterization of subviral particles in infected cells. Virology 73: 442–453PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1998

Authors and Affiliations

  • M. L. Nibert
    • 1
    • 2
  1. 1.Institute for Molecular Virology, The Graduate SchoolUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of Biochemistry, College of Agricultural and Life SciencesUniversity of Wisconsin-MadisonMadisonUSA

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