Skip to main content
SpringerLink
Log in

Early Steps in Avian Reovirus Morphogenesis

  • Chapter
Reoviruses: Entry, Assembly and Morphogenesis

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 309))

Abstract

Avian reoviruses are important pathogens that may cause considerable economic losses in poultry farming. Their genome expresses at least eight structural and four nonstructural proteins, three of them encoded by the S1 gene. These viruses enter cells by receptor-mediated endocytosis, and acidification of virus-containing endosomes is necessary for the virus to uncoat and release transcriptionally active cores into the cytosol. Avian reoviruses replicate within cytoplasmic inclusions of globular morphology, termed viral factories, which are not microtubule-associated, and which are formed by the nonstructural protein µNS. This protein also mediates the association of some viral proteins (but not of others) with inclusions, suggesting that the recruitment of viral proteins into avian reovirus factories has specificity. Avian reovirus morphogenesis is a complex and temporally controlled process that takes place exclusively within viral factories of infected cells. Core assembly takes place within the first 30 min after the synthesis of their protein components, and fully formed cores are then coated by outer-capsid polypeptides over the next 30 min to generate mature infectious reovirions. Based on data from avian reovirus studies and on results reported for other members of the Reoviridae family, we present a model for avian reovirus gene expression and morphogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bodelon G, Labrada L, Martínez-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

    Article  PubMed  CAS  Google Scholar 

  • Broering TJ, Parker JSL, Joyce PL, Kim J, Nibert ML (2002) Mammalian reovirus nonstructural protein µNS forms large inclusions and colocalizes with reovirus microtubule-associated protein µ2 in transfected cells. J Virol 76:8285–8297

    Article  PubMed  CAS  Google Scholar 

  • Broering TJ, Kim J, Miller CL, Piggot CDS, Dinoso JB, Nibert ML, Parker JSL (2004) Reovirus nonstructural protein µNS recruits viral core surface proteins and entering core particles to factory-like inclusions. J Virol 78:1882–1892

    Article  PubMed  CAS  Google Scholar 

  • Chandran K, Zhang X, Olson NH, Walker SB, Chappell JD, Dermody TS, Baker TS, Nibert ML (2001) Complete in vitroassemblyof the reovirusouter capsidproduces highly infectious particles suitable for genetic studies of the receptor-binding protein. J Virol 75:5335–5342

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Ramig RF (1993a) Rescue of infectivity by in vitro transcapsidation of rotavirus single-shelled particles. Virology 192:422–429

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Ramig RF (1993b) Rescue of infectivity by sequential in vitro transcapsidation of rotavirus core particles with inner capsid and outer capsid proteins. Virology 194:743–751

    Article  PubMed  CAS  Google Scholar 

  • Dryden KA, Farsetta DL, Wang GJ, Keegan JM, Fields BN, Baker TS, Nibert ML (1998) Internal structures containing transcriptase-related proteins in top component particles of mammalian orthorevirus. Virology 225:33–46

    Article  Google Scholar 

  • Duncan R (1996) The lowpH-dependent entry of avian reovirus is accompanied by two specific cleavages of the major outer capsid protein µ2C. Virology 219:179–189

    Article  CAS  Google Scholar 

  • Duncan R (1999) Extensive sequence divergence and phylogenetic relationships between the fusogenic and nonfusogenic orthoreoviruses: a species proposal. Virology 260:316–328

    Article  PubMed  CAS  Google Scholar 

  • Fabbretti E, Afrikanova I, Vascotto F, Burrone OR (1999) Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J Gen Virol 80:333–339

    PubMed  CAS  Google Scholar 

  • 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 43:569–578

    Article  PubMed  CAS  Google Scholar 

  • Gillian AL, Nibert ML (1998) Amino terminus of reovirus nonstructural protein σNS is important for ssRNA binding and nucleoprotein complex formation. Virology 240:1–11

    Article  PubMed  CAS  Google Scholar 

  • Glass SE, Naqi SA, Hall CF, Kerr KM (1973) Isolation and characterization of a virus associated with arthritis of chickens. Avian Dis 17:415–424

    Article  PubMed  CAS  Google Scholar 

  • Grande A, Costas C, Benavente J (2002) Subunit composition and conformational stability of the oligomeric form of the avian reovirus cell-attachment protein σC. J Gen Virol 83:131–139

    PubMed  CAS  Google Scholar 

  • Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Zientara S, Mertens PPC, Stuart DI (1998) The atomic structure of the bluetongue virus core. Nature 395:470–478

    Article  PubMed  CAS  Google Scholar 

  • Jones RC (2000) Avian reovirus infections. Rev Sci Tech 19:614–625

    PubMed  CAS  Google Scholar 

  • Kant A, Balk F, Born L, van Roozelaar D, Heijmans J, Gielkins A, ter Huurne A (2003) Classification of Dutch and German avian reoviruses by sequencing the σC protein. Vet Res 34:203–212

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Zhang X, Centonze VE, Bowman VD, Noble S, Baker TS, Nibert ML (2002) The hydrophilic amino-terminal arm of reovirus core shell protein λ1 is dispensable for particle assembly. J Virol 76:12211–12222

    Article  PubMed  CAS  Google Scholar 

  • Labbé M, Charpilienne A, Crawford SE, Estes MK, Cohen J (1991) Expression of rotavirus VP2 produces empty corelike particles. J Virol 65:2946–2952

    PubMed  Google Scholar 

  • Labrada L, Bodelon G, Vinuela J, Benavente J (2002) Avian reoviruses cause apoptosis in cultured cells: viral uncoating but not viral gene expression is required for apoptosis induction. J Virol 76:7932–7941

    Article  PubMed  CAS  Google Scholar 

  • Loudon PT, Roy P (1992) Interaction of nucleic acids with core-like and subcore-like particles of bluetongue virus. Virology 191:231–236

    Article  PubMed  CAS  Google Scholar 

  • Martínez-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

    Article  PubMed  Google Scholar 

  • Martínez-Costas J, Grande A, Varela R, García-Martínez C, Benavente J (1997) Protein architecture of avian reovirus S1133 and identification of the cell attachment protein. J Virol 71:59–64

    PubMed  Google Scholar 

  • Mertens, P (2004) The dsRNA viruses. Virus Res 101:3–13

    Article  PubMed  CAS  Google Scholar 

  • Miller CL, Broering TJ, Parker JSL, Arnold MM, Nibert ML (2003) Reovirus σNS protein localizes to inclusions through an association requiring the µNS amino terminus. J Virol 77:4566–4576

    Article  PubMed  CAS  Google Scholar 

  • Mora M, Partin K, Bhatia M, Partin J, Carter C (1987) Association of avian reovirus proteins with the structural matrix of infected cells. Virology 159:265–277

    Article  PubMed  CAS  Google Scholar 

  • Nibert ML, Schiff LA (2001) Reoviruses and their replication. In:Knipe DM, Hooley PM (eds) Fields virology. Lippincott Willams & Wilkins, Philadelphia, pp. 1679–1728

    Google Scholar 

  • Parker JSL, Broering TJ, Kim J, Higgins DE, Nibert ML (2002) Reovirus core protein µ2 determines the filamentous morphology of viral inclusion bodies by interacting with and stabilizing microtubules. J Virol 76:4483–4496

    Article  PubMed  CAS  Google Scholar 

  • Reinisch KM, Nibert ML, Harrison SC (2000) Structure of the reovirus core at 3.6 Å resolution. Nature 404:960–967

    Article  PubMed  CAS  Google Scholar 

  • Rhim JS, Jordan LE, Mayor HD (1962) Cytochemical, fluorescent-antibody and electron microscopic studies on the growth of reovirus (ECHO 10) in tissue culture. Virology 17:342–355

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Shapouri MR, Arella M, Silim A (1996) Evidence for the multimeric nature and cell binding ability of avian reovirus sigma 3 protein. J Gen Virol 77:1203–1210

    Article  PubMed  CAS  Google Scholar 

  • Shmulevitz M, Salsman J, Duncan R (2003) Palmytoylation, membrane-proximal basic residues, and transmembrane glycine residues in the reovirus p10 protein are essential for syncytium formation. J Virol 77:9769–9779

    Article  PubMed  CAS  Google Scholar 

  • Silverstein SC, Schur PH (1970) Immunofluorescent localization of double-stranded RNA in reovirus-infected cells. Virology 41:564–566

    Article  PubMed  CAS  Google Scholar 

  • Silvestri LS, Taraporewala ZF, Patton JT (2004) Rotavirus replication: plus-sense templates for double-stranded RNA synthesis aremade in viroplasms. JVirol 78:7763–7774

    Article  CAS  Google Scholar 

  • Spandidos DA, Graham AF (1976) Physical and chemical characterization of an avian reovirus. J Virol 19:968–976

    PubMed  CAS  Google Scholar 

  • Thomas CP, Booth TF, Roy P (1990) Synthesis of bluetongue virus-encoded phospho-protein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J Gen Virol 71:2073–2083

    PubMed  CAS  Google Scholar 

  • Tourís-Otero F, Cortez-San Martín M, Martínez-Costas J, Benavente J (2004a) Avian reovirusmorphogenesis occurswithin viral factories and beginswith the selective recruitment of σNS and λA to µNS inclusions. J Mol Biol 341:361–374

    Article  PubMed  CAS  Google Scholar 

  • Tourís-Otero F, Martínez-Costas J, Vakharia VN, Benavente J (2004b) Avian reovirus nonstructural protein µNS forms viroplasm-like inclusions and recruits σNS to these structures. Virology 319:94–106

    Article  PubMed  CAS  Google Scholar 

  • Tourís-Otero F, Martínez-Costas J, Vakharia VN, Benavente J (2005) Characterization of the nucleic acid-binding activity of the avian reovirus nonstructural protein σNS. J Gen Virol 86:1159–1169

    Article  PubMed  CAS  Google Scholar 

  • Van der Heide L (2000) The history of avian reovirus. Avian Dis 44:638–641

    Article  PubMed  Google Scholar 

  • Varela R, Benavente J (1994) Protein coding assignment of avian reovirus strain S1133. J Virol 68:6775–6777

    PubMed  CAS  Google Scholar 

  • Varela R, Martínez-Costas J, Mallo M, Benavente J (1996) Intracellular posttranslational modifications of S1133 avian reovirus proteins. J Virol 70:2974–2981

    PubMed  CAS  Google Scholar 

  • Xu P, Miller SE, Joklik WK (1993) Generation of reovirus core-like particles in cells infected with hybrid vaccinia viruses that express genome segments L1, L2, L3, and S2. Virology 197:726–731

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Patrick MK, Hazelton PR, Coombs KM (2004) Avian reovirus temperature-sensitive mutant tsA12 has a lesion in major core protein σA and is defective in assembly. J Virol 78:11142–11151

    Article  PubMed  CAS  Google Scholar 

  • Yin HS, Lee LH (1998) Identification and characterization of RNA-binding activities of avian reovirus non-structural protein σNS. J Gen Virol 79:1411–1413

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Bioquímica y Biología Molecular, Universidad de Santiago de Compostela, 15782, Santiago de Compostela, Spain

    J. Benavente & J. Martínez-Costas

Authors
  1. J. Benavente
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Martínez-Costas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Martínez-Costas .

Editor information

Editors and Affiliations

  1. Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, UK

    Polly Roy M.Sc., Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Benavente, J., Martínez-Costas, J. (2006). Early Steps in Avian Reovirus Morphogenesis. In: Roy, P. (eds) Reoviruses: Entry, Assembly and Morphogenesis. Current Topics in Microbiology and Immunology, vol 309. Springer, Berlin, Heidelberg . https://doi.org/10.1007/3-540-30773-7_3

Download citation

Publish with us

Policies and ethics

Search

Navigation