Reoviruses I pp 167-183 | Cite as

Reovirus Capsid Proteins σ3 and µ1: Interactions That Influence Viral Entry, Assembly, and Translational Control

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


Mammalian reoviruses are prototypical members of the Reoviridae family. Characteristics shared by members of this family include a segmented dsRNA genome and a nonenveloped particle consisting of two or three concentric proteinaceous capsids. The ten genome segments of mammalian reoviruses together encode only 11 unique proteins. These proteins execute the reovirus replication program in a variety of cell types within diverse animal hosts.


Capsid Protein Reovirus Infection Subviral Particle Reovirus Type Mammalian Reovirus 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amano Y, Katagiri S, Ishida N, Watanabe Y (1971) Spontaneous degradation of reovirus capsid into subunits. J Virol 8 (5): 805–808PubMedGoogle Scholar
  2. Amerongen HM, Wilson GA, Fields BN, Neutra MR (1994) Proteolytic processing of reovirus is required for adherence to intestinal M cells. J Virol 68 (12): 8428–8432PubMedGoogle Scholar
  3. 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 (2): 760–776PubMedCrossRefGoogle Scholar
  4. Banerjee AK, Shatkin AJ (1970) Transcription in vitro by reovirus-associated ribonucleic acid-dependent polymerase. J Virol 6 (1): 1–11PubMedCrossRefGoogle Scholar
  5. Bass DM, Bodkin D, Dambrauskas R, Trier JS, Fields BN, Wolf JL (1990) Intraluminal proteolytic activation plays an important role in replication of type 1 reovirus in the intestines of neonatal mice. J Virol 64 (4): 1830–1833PubMedGoogle Scholar
  6. Beattie EK, Denzler L, Tartaglia J, Perkus ME, Paoletti E, Jacobs BL (1995) Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J Virol 69 (1): 499–505PubMedGoogle Scholar
  7. Belli BA, Samuel CE (1993) Biosynthesis of reovirus-specified polypeptides: identification of regions of the bicistronic reovirus Sl mRNA that affect the efficiency of translation in animal cells. Virology 193 (1): 16–27PubMedCrossRefGoogle Scholar
  8. Bodkin DK, Nibert ML, Fields BN (1989) Proteolytic digestion of reovirus in the intestinal lumens of neonatal mice. J Virol 63 (1 1): 4676–4681PubMedGoogle Scholar
  9. Borsa J, Graham AF (1968) Reovirus: RNA polymerase activity in purified virions. Biochem Biophys Res Commun 33 (6): 895–901PubMedCrossRefGoogle Scholar
  10. 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 (4): 552–564PubMedGoogle Scholar
  11. Borsa J, Morash BD, Sargent MD, Copps TP, Lievaart PA, Szekely JG (1979) Two modes of entry of reovirus particles into L cells. J Gen Virol 45 (1): 161–170PubMedCrossRefGoogle Scholar
  12. Borsa J, Sargent MD, Lievaart PA, Copps TP (1981) Reovirus: evidence for a second step in the intracellular uncoating and transcriptase activation process. Virology I11 (1): 191–200CrossRefGoogle Scholar
  13. Chang CT, Zweerink HJ (1971) Fate of parental reovirus in infected cell. Virology 46 (3): 544–555PubMedCrossRefGoogle Scholar
  14. Cross RK, Fields BN (1976) Reovirus-specific polypeptides: analysis using discontinuous gel electrophoresis. J Virol 19 (1): 162–173PubMedGoogle Scholar
  15. 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
  16. Denzler KL, Jacobs BL (1994) Site-directed mutagenic analysis of reovirus sigma 3 protein binding to dsRNA. Virology 204 (1): 190–199PubMedCrossRefGoogle Scholar
  17. Dermody TS, Nibert ML, Wetzel JD, Tong X, Fields BN (1993) Cells and viruses with mutations affecting viral entry are selected during persistent infections of L cells with mammalian reoviruses. J Virol 76: 2055–2063Google Scholar
  18. Drayna D, Fields BN (1982a) Biochemical studies on the mechanism of chemical and physical inactivation of reovirus. J Gen Virol 63 (1): 161–170PubMedCrossRefGoogle Scholar
  19. Drayna D, Fields BN (1982b) Genetic studies on the mechanism of chemical and physical inactivation of reovirus. J Gen Virol 63: 149–160PubMedCrossRefGoogle Scholar
  20. 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 (5): 1023–1041PubMedCrossRefGoogle Scholar
  21. Feduchi E, Esteban M, Carrasco L (1988) Reovirus type 3 synthesizes proteins in interferon-treated HeLa cells without reversing the antiviral state. Virology 164: 420–426PubMedCrossRefGoogle Scholar
  22. Fields BN, Raine CS, Baum SG (1971) Temperature-sensitive mutants of reovirus type 3: defects in viral maturation as studied by immunofluorescence and electron microscopy. Virology 43: 569–578PubMedCrossRefGoogle Scholar
  23. 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
  24. Giantini M, Shatkin AJ (1989) Stimulation of chloramphenicol acetyltransferase mRNA translation by reovirus capsid polypeptide sigma 3 in cotransfected COS cells. J Virol 63 (6): 2415–2421PubMedGoogle Scholar
  25. Gomatos PJ, Tamm I (1963) Macromolecular synthesis in reovirus-infected L cells. Biochim Biophys Acta 72: 651–653PubMedCrossRefGoogle Scholar
  26. Gomatos PJ, Tamm I, Dales S, Franklin RM (1962) Reovirus type 3: physical characteristics and interactions with L cells. Virology 17: 441–454PubMedCrossRefGoogle Scholar
  27. 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 (1): 46–58PubMedCrossRefGoogle Scholar
  28. Henry GL, McConnack SJ, Thomis DC, Samuel CE (1994) Mechanism of interferon action. Translational control and the RNA-dependent protein kinase (PKR): antagonists of PKR enhance the translational activity of mRNAs that include a 161 nucleotide region from reovirus SI mRNA. J Biol Regul Homeost Agents 8 (1): 15–24PubMedGoogle Scholar
  29. Hooper JW, Fields BN (I 996a) Monoclonal antibodies to reovirus sigma 1 and mu 1 proteins inhibit chromium release from mouse L cells. J Virol 70(1):672–677Google Scholar
  30. Hooper JW, Fields BN (1996b) Role of the mu 1 protein in reovirus stability and capacity to cause chromium release from host cells. J Virol 70 (1): 459–467PubMedGoogle Scholar
  31. Hovanessian AG (1991) Interferon-induced and double-stranded RNA-activated enzymes: a specific protein kinase and 2’,5’-oligoadenylate synthetases. J Interferon Res I1 (4): 199–205CrossRefGoogle Scholar
  32. 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 (2): 411–424PubMedCrossRefGoogle Scholar
  33. Imani F, Jacobs BL (1988) Inhibitory activity for the interferon-induced protein kinase is associated with the reovirus serotype 1 sigma 3 protein. Proc Nati Acad Sci USA 85 (21): 7887–7891CrossRefGoogle Scholar
  34. Jayasuriya AKU (1991) Molecular characterization of the reovirus M2 gene. Microbiology and molecular genetics. Thesis, Harvard UniversityGoogle Scholar
  35. Jeffrey IW, Kadereit S, Meurs EF, Metzger T, Bachmann M, Schwemmte M, Hovanessian AG, Clemens MJ (1995) Nuclear localization of the interferon-inducible protein kinase PKR in human cells and transfected mouse cells. Exp Cell Res 218 (1): 17–27PubMedCrossRefGoogle Scholar
  36. Jimenez-Garcia LF, Green SR, Matthews MB, Spector DL (1993) Organization of the double-stranded RNA-activated protein kinase DAI and virus-associated VA RNAI in adenovirus-2-infected HeLa cells. J Cell Sci 106: 11–22PubMedGoogle Scholar
  37. Joklik WK (1972) Studies on the effect of chymotrypsin on reovirions. Virology 49: 700–801PubMedCrossRefGoogle Scholar
  38. 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 (1): 552–559PubMedGoogle Scholar
  39. Lau RY, Van Alstyne D, Berckmans R, Graham AF (1975) Synthesis of reovirus-specific polypeptides in cells pretreated with cycloheximide. J Virol 16 (3): 470–478PubMedGoogle Scholar
  40. Lee PWK, Hayes EC, Joklik WK (1981b) Characterization of anti-reovirus immunoglobulins secreted by cloned hybridoma cell lines. Virology 108: 134–146PubMedCrossRefGoogle Scholar
  41. Lee W, Hayes EC, Joklik WK (1981a) Protein sigma 1 is the reovirus cell attachment protein. Virology 108 (1): 156–163PubMedCrossRefGoogle Scholar
  42. Lemieux R, Zarbl H, Millward S (1984) mRNA discrimination in extracts from uninfected and reovirusinfected L-cells. J Virol 51(1):215–222PubMedGoogle Scholar
  43. Lloyd RM, Shatkin AJ (1992) Translational stimulation by reovirus polypeptide sigma 3: substitution for VAI RNA and inhibition of phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J Virol 66 (12): 6878–6884PubMedGoogle Scholar
  44. Lucia-Jandris P, Hooper JW, Fields BN (1993) Reovirus M2 gene is associated with chromium release from mouse L cells. J Virol 67 (9): 5339–5345PubMedGoogle Scholar
  45. Luftig RB, Kilham SS, Hay AJ, Zweerink HJ, Joklik WK (1972) An ultrastructural study of virions and cores of reovirus type 3. Virology 48 (1): 170–181PubMedCrossRefGoogle Scholar
  46. Mabrouk T, Lemay G (1994a) Mutations in a CCHC zinc-binding motif of the reovirus sigma 3 protein decrease its intracellular stability. J Virol 68 (8): 5287–5290PubMedGoogle Scholar
  47. Mabrouk T, Lemay G (1946) The sequence similarity of reovirus sigma 3 protein to picornaviral proteases is unrelated to its role in mu 1 viral protein cleavage. Virology 202(2):615–620CrossRefGoogle Scholar
  48. Mabrouk T, Danis C, Lemay G (1995) Two basic motifs of reovirus sigma 3 protein are involved in double-stranded RNA binding. Biochem Cell Biol 73 (3/4): 137–145PubMedCrossRefGoogle Scholar
  49. Maratos-Flier E, Goodman MJ, Murray AH, Kahn CR (1986) Ammonium inhibits processing and cytotoxicity of reovirus, a nonenveloped virus. J Clin Invest 78 (4): 1003–1007PubMedCrossRefGoogle Scholar
  50. Mayor HD, Jamison RM, Jordan LE, Mitchell MV (1965) Reoviruses. II. Structure and composition of the virion. J Bacteriol 89: 1548–1556PubMedGoogle Scholar
  51. Metcalf P (1982) The symmetry of the reovirus outer shell. J Ultrastruct Res 78: 292–301PubMedCrossRefGoogle Scholar
  52. Miller JE, Samuel CE (1992) Proteolytic cleavage of the reovirus sigma 3 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 (9): 5347–5356PubMedGoogle Scholar
  53. Morgan EM, Zweerink HJ (1974) Reovirus morphogenesis: core-like particles in cells infected at 39 with wild-type reovirus and temperature-sensitive mutants of groups B and G. Virology 59:556–565 Morgan EM, Zweerink HJ (1975) Characterization of transcriptase and replicase particles isolated fromreovirus-infected cells. Virology 68 (2): 455–466CrossRefGoogle Scholar
  54. Morin MJ, Warner A, Fields BN (1994) A pathway for entry of reoviruses into the host through M cells of the respiratory tract. J Exp Med 180(4): 1523–1. 527CrossRefGoogle Scholar
  55. Neutra MR, Frey A, Kraehenbuhl J-P (1996) Epithelial M cells: gateways for mucosal infection and immunization. Cell 86: 345–348PubMedCrossRefGoogle Scholar
  56. Nibert ML, Fields BN (1992) A carboxy-terminal fragment of protein mu I/mu IC is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J Virol 66 (11): 6408–6418PubMedGoogle Scholar
  57. Nibert ML, Schiff LA, Fields BN (1991) Mammalian reoviruses contain a myristoylated structural protein. J Virol 65: 1960–1967PubMedGoogle Scholar
  58. Nibert ML, Chappell JD, Dermody TS (1995) Infectious subvirion particles of reovirus type 3 Dearing exhibit a loss in infectivity and contain a cleaved sigma 1 protein. J Virol 69 (8): 5057–5067PubMedGoogle Scholar
  59. Nibert ML, Schiff L, Fields BN (1996) Reoviruses and their replication. In: Fields BN, Knipe DM, Howley Fields PM (eds) Virology. Lippincott-Raven, PhiladelphiaGoogle Scholar
  60. Nonoyama M, Millward S, Graham AF (1974) Control of transcription of the reovirus genome. Nucleic Acids Res 1: 373–385PubMedCrossRefGoogle Scholar
  61. Pett DM, Vanaman TC, Joklik WK (1973) Studies on the amino and carboxyl terminal amino acid sequences of reovirus capsid polypeptides. Virology 52 (1): 174–186PubMedCrossRefGoogle Scholar
  62. 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: 428–435PubMedCrossRefGoogle Scholar
  63. Rubin DH, Weiner DB, Dworkin C, Greene MI, Maul GG, Williams WV (1992) Receptor utilization by reovirus type 3: distinct binding sites on thymoma and fibroblast cell lines result in differential compartmentalization of virions. Microb Pathog 12: 351–365PubMedCrossRefGoogle Scholar
  64. Sabin AB (1959) Reoviruses. Science 130: 1387–1389Google Scholar
  65. Samuel CE, Brody MS (1990) Biosynthesis of reovirus-specified polypeptides: 2-aminopurine increases the efficiency of translation of reovirus s mRNA but not s4 mRNA in transfected cells. Virology 176 (1): 106 - l13PubMedCrossRefGoogle Scholar
  66. Schiff LA, Nibert ML, Co MS, Brown EG, Fields BN (1988) Distinct binding sites for zinc and doublestranded RNA in the reovirus outer capsid protein sigma 3. Mol Cell Biol 8 (1): 273–283PubMedGoogle Scholar
  67. Schmechel S, Chute M, Skinner P, Anderson R, Schiff L (in press) Preferential translation of reovirus mRNA by a sigma3-dependent mechanism. Virology 232:62–73Google Scholar
  68. Sharpe AH, Fields BN (1982) Reovirus inhibition of cellular RNA and protein synthesis: role of the S4 gene. Virology 122 (2): 381–391PubMedCrossRefGoogle Scholar
  69. Shatkin AJ, LaFiandra AJ (1972) Transcription by infectious subviral particles of reovirus. J Virol 10 (4): 698–706PubMedGoogle Scholar
  70. Shepard DA, Ehnstrom JG, Skinner PJ, Schiff LA (1996) Mutations in the zinc-binding motif of the reovirus capsid protein sigma3 eliminate its ability to associate with capsid protein muI. J Virol 70 (3): 2065–2068PubMedGoogle Scholar
  71. Silverstein SC, Dales S (1968) The penetration of reovirus RNA and initiation of its genetic function in L-strain fibroblasts. J Cell Biol 36: 197–230CrossRefGoogle Scholar
  72. Silverstein SC, Astell C, Levin DH, Schonberg M, Acs G (1972) The mechanisms of reovirus uncoating and gene activation in vivo. Virology 47: 797–806PubMedCrossRefGoogle Scholar
  73. Skup D, Millward S (1980b) Reovirus-induced modification of cap-dependent translation in infected L cells. Proc Natl Acad Sci USA 77 (1): 152–156PubMedCrossRefGoogle Scholar
  74. 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
  75. Spandidos DA, Krystal G, Graham AF (1976) Regulated transcription of the genomes of defective virions and temperature-sensitive mutants of reovirus. J Virol 18: 7–19PubMedGoogle Scholar
  76. 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
  77. 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
  78. Wallis C, Smith KO, Melnick JL (1964) Reovirus activation by heating and inactivation by cooling in MgCL solution. Virology 22: 608–619PubMedCrossRefGoogle Scholar
  79. Ward RL, Shatkin AJ (1972) Association of reovirus mRNA with viral proteins: a possible mechanism for linking the genome segments. Arch Biochem Biophys 152: 378–384PubMedCrossRefGoogle Scholar
  80. Ward R, Banerjee AK, LaFiandra A, Shatkin AJ (1972) Reovirus-specific ribonucleic acid from polysomes of infected L cells. J Virol 9 (1): 61–69PubMedGoogle Scholar
  81. Watanabe Y, Millward S, Graham AF (1968) Regulation of transcription of the reovirus genome. J Mol Biol 36: 107–123PubMedCrossRefGoogle Scholar
  82. Weiner HL, Ramig RF, Mustoe TA, Fields BN (1978) Identification of the gene coding for the hemagglutinin of reovirus. Virology 86: 581–584PubMedCrossRefGoogle Scholar
  83. Wessner DR, Fields BN (1993) Isolation and genetic characterization of ethanol-resistant reovirus mutants. J Virol 67: 2442–2447PubMedGoogle Scholar
  84. White CK, Zweerink HJ (1976) Studies on the structure of reovirus cores: selective removal of polypeptide lambda 2. Virology 70 (1): 171–180PubMedCrossRefGoogle Scholar
  85. Yue Z, Shatkin AJ (1996) Regulated, stable expression and nuclear presence of reovirus double-stranded RNA-binding protein s3 in HeLa cells. J Virol 70 (6): 3497–3501PubMedGoogle Scholar
  86. Zarbl H, Skup D, Millward S (1980) Reovirus progeny subviral particles synthesize uncapped mRNA. J Virol 34 (2): 497–505PubMedGoogle Scholar
  87. Zweerink HJ (1974) Multiple forms of ss-dsRNA polymerase activity in reovirus-infected cells. Nature (Lond) 247: 313–315CrossRefGoogle Scholar
  88. Zweerink HJ, Joklik WK (1970) Studies on the intracellular synthesis of reovirus-specified proteins. Virology 41 (3): 501–518PubMedCrossRefGoogle Scholar
  89. Zweerink HJ, Ito Y, Matsuhisa T (1972) Synthesis of reovirus double-stranded RNA within virionlike particles. Virology 50 (2): 349–358PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1998

Authors and Affiliations

  • L. A. Schiff
    • 1
  1. 1.Department of MicrobiologyUniversity of MinnesotaMinneapolisUSA

Personalised recommendations