1887

Abstract

The salivary gland hypertrophy virus (GpSGHV) is a dsDNA virus with rod-shaped, enveloped virions. Its 190 kb genome contains 160 putative protein-coding ORFs. Here, the structural components, protein composition and associated aspects of GpSGHV morphogenesis and cytopathology were investigated. Four morphologically distinct structures: the nucleocapsid, tegument, envelope and helical surface projections, were observed in purified GpSGHV virions by electron microscopy. Nucleocapsids were present in virogenic stroma within the nuclei of infected salivary gland cells, whereas enveloped virions were located in the cytoplasm. The cytoplasm of infected cells appeared disordered and the plasma membranes disintegrated. Treatment of virions with 1 % NP-40 efficiently partitioned the virions into envelope and nucleocapsid fractions. The fractions were separated by SDS-PAGE followed by in-gel trypsin digestion and analysis of the tryptic peptides by liquid chromatography coupled to electrospray and tandem mass spectrometry. Using the MaxQuant program with Andromeda as a database search engine, a total of 45 viral proteins were identified. Of these, ten and 15 were associated with the envelope and the nucleocapsid fractions, respectively, whilst 20 were detected in both fractions, most likely representing tegument proteins. In addition, 51 host-derived proteins were identified in the proteome of the virus particle, 13 of which were verified to be incorporated into the mature virion using a proteinase K protection assay. This study provides important information about GpSGHV biology and suggests options for the development of future anti-GpSGHV strategies by interfering with virus–host interactions.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.047423-0
2013-01-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/1/193.html?itemId=/content/journal/jgv/10.1099/vir.0.047423-0&mimeType=html&fmt=ahah

References

  1. Abd-Alla A. , Bossin H. , Cousserans F. , Parker A. , Bergoin M. , Robinson A. . ( 2007; ). Development of a non-destructive PCR method for detection of the salivary gland hypertrophy virus (SGHV) in tsetse flies. . J Virol Methods 139:, 143–149. [CrossRef] [PubMed]
    [Google Scholar]
  2. Abd-Alla A. M. M. , Vlak J. M. , Bergoin M. , Maruniak J. E. , Parker A. G. , Burand J. P. , Jehle J. A. , Boucias D. G. . Hytrosavirus Study Group of the ICTV ( 2009; ). Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. . Arch Virol 154:, 909–918. [CrossRef] [PubMed]
    [Google Scholar]
  3. Abd-Alla A. M. M. , Boucias D. G. , Bergoin M. . ( 2010a; ). Hytrosaviruses: structure and genomic properties. . In Insect Virology, pp. 103–121. Edited by Asgari S. , Johnson K. N. . . Norfolk:: Caister Academic Press;.
    [Google Scholar]
  4. Abd-Alla A. M. M. , Kariithi H. M. , Parker A. G. , Robinson A. S. , Kiflom M. , Bergoin M. , Vreysen M. J. B. . ( 2010b; ). Dynamics of the salivary gland hypertrophy virus in laboratory colonies of Glossina pallidipes (Diptera: Glossinidae). . Virus Res 150:, 103–110. [CrossRef] [PubMed]
    [Google Scholar]
  5. Abd-Alla A. M. M. , Parker A. G. , Vreysen M. J. B. , Bergoin M. . ( 2011; ). Tsetse salivary gland hypertrophy virus: hope or hindrance for tsetse control?. PLoS Negl Trop Dis 5:, e1220. [CrossRef] [PubMed]
    [Google Scholar]
  6. Afonso C. L. , Tulman E. R. , Lu Z. , Zsak L. , Kutish G. F. , Rock D. L. . ( 2000; ). The genome of fowlpox virus. . J Virol 74:, 3815–3831. [CrossRef] [PubMed]
    [Google Scholar]
  7. Alroy I. , Yarden Y. . ( 1997; ). The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. . FEBS Lett 410:, 83–86. [CrossRef] [PubMed]
    [Google Scholar]
  8. Amargier A. , Lyon J. P. , Vago C. , Meynadier G. , Veyrunes J. C. . ( 1979; ). Mise en evidence et purification d’un virus dans la proliferation monstrueuse glandulaire d’insectes. Etude sur Merodon equestris F. (Diptere,(Diptere: Syrphidae). . C R Acad Sci D 289:, 481–484 (in French).
    [Google Scholar]
  9. Asković S. , Baumann R. . ( 1997; ). Activation domain requirements for disruption of Epstein–Barr virus latency by ZEBRA. . J Virol 71:, 6547–6554.[PubMed]
    [Google Scholar]
  10. Attardi L. D. , Tjian R. . ( 1993; ). Drosophila tissue-specific transcription factor NTF-1 contains a novel isoleucine-rich activation motif. . Genes Dev 7: (7B), 1341–1353. [CrossRef] [PubMed]
    [Google Scholar]
  11. Bai M. , Harfe B. , Freimuth P. . ( 1993; ). Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. . J Virol 67:, 5198–5205.[PubMed]
    [Google Scholar]
  12. Belin M. T. , Boulanger P. . ( 1993; ). Involvement of cellular adhesion sequences in the attachment of adenovirus to the HeLa cell surface. . J Gen Virol 74:, 1485–1497. [CrossRef] [PubMed]
    [Google Scholar]
  13. Biggin M. D. , Bickel S. , Benson M. , Pirrotta V. , Tjian R. . ( 1988; ). Zeste encodes a sequence-specific transcription factor that activates the Ultrabithorax promoter in vitro. . Cell 53:, 713–722. [CrossRef] [PubMed]
    [Google Scholar]
  14. Blackwell J. L. , Brinton M. A. . ( 1997; ). Translation elongation factor-1α interacts with the 3′ stem-loop region of West Nile virus genomic RNA. . J Virol 71:, 6433–6444.[PubMed]
    [Google Scholar]
  15. Boucias D. G. , Deng F. , Hu Z. , Garcia-Maruniak A. , Lietze V. U. . ( 2012; ). Analysis of the structural proteins from the Musca domestica hytrosavirus with an emphasis on the major envelope protein. . J Invertebr Pathol (in press).[PubMed]
    [Google Scholar]
  16. Cantin R. , Méthot S. , Tremblay M. J. . ( 2005; ). Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. . J Virol 79:, 6577–6587. [CrossRef] [PubMed]
    [Google Scholar]
  17. Cartwright B. , Smale C. J. , Brown F. . ( 1969; ). Surface structure of vesicular stomatitis virus. . J Gen Virol 5:, 1–10. [CrossRef] [PubMed]
    [Google Scholar]
  18. Chazal N. , Gerlier D. . ( 2003; ). Virus entry, assembly, budding, and membrane rafts. . Microbiol Mol Biol Rev 67:, 226–237. [CrossRef] [PubMed]
    [Google Scholar]
  19. Chen Y. H. , MacGregor J. P. , Goldstein D. A. , Hall M. R. . ( 1979; ). Histone modifications in simian virus 40 and in nucleoprotein complexes containing supercoiled viral DNA. . J Virol 30:, 218–224.[PubMed]
    [Google Scholar]
  20. Cimarelli A. , Luban J. . ( 1999; ). Translation elongation factor 1-α interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. . J Virol 73:, 5388–5401.[PubMed]
    [Google Scholar]
  21. Coler R. R. , Boucias D. G. , Frank J. H. , Maruniak J. E. , Garcia-Canedo A. , Pendland J. C. . ( 1993; ). Characterization and description of a virus causing salivary gland hyperplasia in the housefly, Musca domestica . . Med Vet Entomol 7:, 275–282. [CrossRef] [PubMed]
    [Google Scholar]
  22. Conesa A. , Götz S. , García-Gómez J. M. , Terol J. , Talón M. , Robles M. . ( 2005; ). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. . Bioinformatics 21:, 3674–3676. [CrossRef] [PubMed]
    [Google Scholar]
  23. Cox J. , Mann M. . ( 2008; ). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. . Nat Biotechnol 26:, 1367–1372. [CrossRef] [PubMed]
    [Google Scholar]
  24. Cox J. , Mann M. . ( 2011; ). Quantitative, high-resolution proteomics for data-driven systems biology. . Annu Rev Biochem 80:, 273–299. [CrossRef] [PubMed]
    [Google Scholar]
  25. Cox J. , Neuhauser N. , Michalski A. , Scheltema R. A. , Olsen J. V. , Mann M. . ( 2011; ). Andromeda: a peptide search engine integrated into the MaxQuant environment. . J Proteome Res 10:, 1794–1805. [CrossRef] [PubMed]
    [Google Scholar]
  26. De Giuli C. , Kawai S. , Dales S. , Hanafusa H. . ( 1975; ). Absence of surface projections of some noninfectious forms of RSV. . Virology 66:, 253–260. [CrossRef] [PubMed]
    [Google Scholar]
  27. Dolnik O. , Volchkova V. , Garten W. , Carbonnelle C. , Becker S. , Kahnt J. , Ströher U. , Klenk H. D. , Volchkov V. . ( 2004; ). Ectodomain shedding of the glycoprotein GP of Ebola virus. . EMBO J 23:, 2175–2184. [CrossRef] [PubMed]
    [Google Scholar]
  28. Forterre P. , Filee J. , Myllykallio H. . ( 2004; ). Origin and evolution of DNA and DNA replication machineries. . In The Genetic Code and the Origin of Life, pp. 145–168. Edited by de Pouplana L. R. . . New York:: Kluwer Academic/Plenum Publishers;. [CrossRef]
    [Google Scholar]
  29. Fraser M. J. . ( 1986; ). Ultrastructural observations of virion maturation in Autographa californica nuclear polyhedrosis virus infected Spodoptera frugiperda cells. . J Ultrastruct Mol Struct Res 95:, 189–195. [CrossRef]
    [Google Scholar]
  30. Garcia-Maruniak A. , Abd-Alla A. M. M. , Salem T. Z. , Parker A. G. , Lietze V. U. , van Oers M. M. , Maruniak J. E. , Kim W. , Burand J. P. . & other authors ( 2009; ). Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. . J Gen Virol 90:, 334–346. [CrossRef] [PubMed]
    [Google Scholar]
  31. Gorbalenya A. E. , Koonin E. V. . ( 1989; ). Viral proteins containing the purine NTP-binding sequence pattern. . Nucleic Acids Res 17:, 8413–8438. [CrossRef] [PubMed]
    [Google Scholar]
  32. Görlich D. , Kutay U. . ( 1999; ). Transport between the cell nucleus and the cytoplasm. . Annu Rev Cell Dev Biol 15:, 607–660.[PubMed] [CrossRef]
    [Google Scholar]
  33. Groves A. K. , Cotter M. A. , Subramanian C. , Robertson E. S. . ( 2001; ). The latency-associated nuclear antigen encoded by Kaposi’s sarcoma-associated herpesvirus activates two major essential Epstein–Barr virus latent promoters. . J Virol 75:, 9446–9457. [CrossRef] [PubMed]
    [Google Scholar]
  34. Gurer C. , Cimarelli A. , Luban J. . ( 2002; ). Specific incorporation of heat shock protein 70 family members into primate lentiviral virions. . J Virol 76:, 4666–4670. [CrossRef] [PubMed]
    [Google Scholar]
  35. Gwack Y. , Byun H. , Hwang S. , Lim C. , Choe J. . ( 2001; ). CREB-binding protein and histone deacetylase regulate the transcriptional activity of Kaposi’s sarcoma-associated herpesvirus open reading frame 50. . J Virol 75:, 1909–1917. [CrossRef] [PubMed]
    [Google Scholar]
  36. Hakim M. , Fass D. . ( 2009; ). Dimer interface migration in a viral sulfhydryl oxidase. . J Mol Biol 391:, 758–768. [CrossRef] [PubMed]
    [Google Scholar]
  37. Hakim M. , Mandelbaum A. , Fass D. . ( 2011; ). Structure of a baculovirus sulfhydryl oxidase, a highly divergent member of the Erv flavoenzyme family. . J Virol 85:, 9406–9413. [CrossRef] [PubMed]
    [Google Scholar]
  38. Hiramatsu Y. , Uno F. , Yoshida M. , Hatano Y. , Nii S. . ( 1999; ). Poxvirus virions: their surface ultrastructure and interaction with the surface membrane of host cells. . J Electron Microsc (Tokyo) 48:, 937–946. [CrossRef] [PubMed]
    [Google Scholar]
  39. Hsu C. H. , Kingsbury D. W. . ( 1985; ). Constitutively phosphorylated residues in the NS protein of vesicular stomatitis virus. . J Biol Chem 260:, 8990–8995.[PubMed]
    [Google Scholar]
  40. Hsu C. H. , Morgan E. M. , Kingsbury D. W. . ( 1982; ). Site-specific phosphorylation regulates the transcriptive activity of vesicular stomatitis virus NS protein. . J Virol 43:, 104–112.[PubMed]
    [Google Scholar]
  41. Iyer L. M. , Leipe D. D. , Koonin E. V. , Aravind L. . ( 2004; ). Evolutionary history and higher order classification of AAA+ ATPases. . J Struct Biol 146:, 11–31. [CrossRef] [PubMed]
    [Google Scholar]
  42. Jaenson T. G. T. . ( 1978; ). Virus-like rods associated with salivary gland hyperplasia in tsetse, Glossina pallidipes . . Trans R Soc Trop Med Hyg 72:, 234–238. [CrossRef] [PubMed]
    [Google Scholar]
  43. James J. A. , Escalante C. R. , Yoon-Robarts M. , Edwards T. A. , Linden R. M. , Aggarwal A. K. . ( 2003; ). Crystal structure of the SF3 helicase from adeno-associated virus type 2. . Structure 11:, 1025–1035. [CrossRef] [PubMed]
    [Google Scholar]
  44. Jehle J. A. , Blissard G. W. , Bonning B. C. , Cory J. S. , Herniou E. A. , Rohrmann G. F. , Theilmann D. A. , Thiem S. M. , Vlak J. M. . ( 2006; ). On the classification and nomenclature of baculoviruses: a proposal for revision. . Arch Virol 151:, 1257–1266. [CrossRef] [PubMed]
    [Google Scholar]
  45. Johnson D. C. , Baines J. D. . ( 2011; ). Herpesviruses remodel host membranes for virus egress. . Nat Rev Microbiol 9:, 382–394. [CrossRef] [PubMed]
    [Google Scholar]
  46. Kalejta R. F. . ( 2008; ). Tegument proteins of human cytomegalovirus. . Microbiol Mol Biol Rev 72:, 249–265. [CrossRef] [PubMed]
    [Google Scholar]
  47. Kariithi H. M. , İnce İ. A. , Boeren S. , Vervoort J. , Bergoin M. , van Oers M. M. , Abd-Alla A. M. , Vlak J. M. . ( 2010; ). Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. . J Gen Virol 91:, 3065–3074. [CrossRef] [PubMed]
    [Google Scholar]
  48. Kariithi H. M. , İnce İ. A. , Boeren S. , Abd-Alla A. M. M. , Parker A. G. , Aksoy S. , Vlak J. M. , van Oers M. M. . ( 2011; ). The salivary secretome of the tsetse fly Glossina pallidipes (Diptera: Glossinidae) infected by salivary gland hypertrophy virus. . PLoS Negl Trop Dis 5:, e1371. [CrossRef] [PubMed]
    [Google Scholar]
  49. Kariithi H. M. , van Lent J. , van Oers M. M. , Abd-Alla A. M. , Vlak J. M. . ( 2012; ). Proteomic footprints of a member of Glossinavirus (Hytrosaviridae): an expeditious approach to virus control strategies in tsetse factories. . J Invertebr Pathol (in press).[PubMed]
    [Google Scholar]
  50. Kay B. K. , Williamson M. P. , Sudol M. . ( 2000; ). The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. . FASEB J 14:, 231–241.[PubMed]
    [Google Scholar]
  51. Kingsford L. , Emerson S. U. . ( 1980; ). Transcriptional activities of different phosphorylated species of NS protein purified from vesicular stomatitis virions and cytoplasm of infected cells. . J Virol 33:, 1097–1105.[PubMed]
    [Google Scholar]
  52. Kremer J. R. , Mastronarde D. N. , McIntosh J. R. . ( 1996; ). Computer visualization of three-dimensional image data using IMOD. . J Struct Biol 116:, 71–76. [CrossRef] [PubMed]
    [Google Scholar]
  53. Kuo M. H. , Allis C. D. . ( 1998; ). Roles of histone acetyltransferases and deacetylases in gene regulation. . Bioessays 20:, 615–626. [CrossRef] [PubMed]
    [Google Scholar]
  54. Kuzio J. , Jaques R. , Faulkner P. . ( 1989; ). Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. . Virology 173:, 759–763. [CrossRef] [PubMed]
    [Google Scholar]
  55. Labeit S. , Kolmerer B. . ( 1995; ). The complete primary structure of human nebulin and its correlation to muscle structure. . J Mol Biol 248:, 308–315. [CrossRef] [PubMed]
    [Google Scholar]
  56. Lackmann M. , Ueckermann C. , Engelmann K. , Koch G. . ( 1987; ). Properties of poliovirus associated protein kinase. . Arch Virol 95:, 1–16. [CrossRef] [PubMed]
    [Google Scholar]
  57. Lieberman P. M. . ( 2006; ). Chromatin regulation of virus infection. . Trends Microbiol 14:, 132–140. [CrossRef] [PubMed]
    [Google Scholar]
  58. Lietze V. U. , Geden C. J. , Blackburn P. , Boucias D. G. . ( 2007; ). Effects of salivary gland hypertrophy virus on the reproductive behavior of the housefly, Musca domestica . . Appl Environ Microbiol 73:, 6811–6818. [CrossRef] [PubMed]
    [Google Scholar]
  59. Lietze V. U. , Abd-Alla A. M. , Boucias D. G. . ( 2011a; ). Two hytrosaviruses, MdSGHV and GpSGHV, induce distinct cytopathologies in their respective host insects. . J Invertebr Pathol 107:, 161–163. [CrossRef] [PubMed]
    [Google Scholar]
  60. Lietze V.-U. , Abd-Alla A. M. M. , Vreysen M. J. B. , Geden C. J. , Boucias D. G. . ( 2011b; ). Salivary gland hypertrophy viruses: a novel group of insect pathogenic viruses. . Annu Rev Entomol 56:, 63–80. [CrossRef] [PubMed]
    [Google Scholar]
  61. Lietze V. U. , Geden C. J. , Doyle M. A. , Boucias D. G. . ( 2012; ). Disease dynamics and persistence of Musca domestica salivary gland hypertrophy virus infections in laboratory house fly (Musca domestica) populations. . Appl Environ Microbiol 78:, 311–317. [CrossRef] [PubMed]
    [Google Scholar]
  62. Luo L. , Zeng L. . ( 2010; ). A new rod-shaped virus from parasitic wasp Diachasmimorpha longicaudata (Hymenoptera: Braconidae). . J Invertebr Pathol 103:, 165–169. [CrossRef] [PubMed]
    [Google Scholar]
  63. Mastronarde D. N. . ( 2005; ). Automated electron microscope tomography using robust prediction of specimen movements. . J Struct Biol 152:, 36–51. [CrossRef] [PubMed]
    [Google Scholar]
  64. McGeoch D. J. , Barnett B. C. , MacLean C. A. . ( 1993; ). Emerging functions of alphaherpesvirus genes. . Semin Virol 4:, 125–134. [CrossRef]
    [Google Scholar]
  65. Moerdyk-Schauwecker M. , Hwang S. I. , Grdzelishvili V. Z. . ( 2009; ). Analysis of virion associated host proteins in vesicular stomatitis virus using a proteomics approach. . Virol J 6:, 166. [CrossRef] [PubMed]
    [Google Scholar]
  66. Mujawar Z. , Rose H. , Morrow M. P. , Pushkarsky T. , Dubrovsky L. , Mukhamedova N. , Fu Y. , Dart A. , Orenstein J. M. . & other authors ( 2006; ). Human immunodeficiency virus impairs reverse cholesterol transport from macrophages. . PLoS Biol 4:, e365. [CrossRef] [PubMed]
    [Google Scholar]
  67. Nermut M. V. , Wallengren K. , Pager J. . ( 1999; ). Localization of actin in Moloney murine leukemia virus by immunoelectron microscopy. . Virology 260:, 23–34. [CrossRef] [PubMed]
    [Google Scholar]
  68. Nicewonger J. , Suck G. , Bloch D. , Swaminathan S. . ( 2004; ). Epstein–Barr virus (EBV) SM protein induces and recruits cellular Sp110b to stabilize mRNAs and enhance EBV lytic gene expression. . J Virol 78:, 9412–9422. [CrossRef] [PubMed]
    [Google Scholar]
  69. Odindo M. O. , Payne C. C. , Crook N. E. , Jarrett P. . ( 1986; ). Properties of a novel DNA virus from the tsetse fly, Glossina pallidipes . . J Gen Virol 67:, 527–536. [CrossRef] [PubMed]
    [Google Scholar]
  70. Ott D. E. . ( 1997; ). Cellular proteins in HIV virions. . Rev Med Virol 7:, 167–180. [CrossRef] [PubMed]
    [Google Scholar]
  71. Ott D. E. . ( 2002; ). Potential roles of cellular proteins in HIV-1. . Rev Med Virol 12:, 359–374. [CrossRef] [PubMed]
    [Google Scholar]
  72. Ott D. E. , Coren L. V. , Kane B. P. , Busch L. K. , Johnson D. G. , Sowder R. C. II , Chertova E. N. , Arthur L. O. , Henderson L. E. . ( 1996; ). Cytoskeletal proteins inside human immunodeficiency virus type 1 virions. . J Virol 70:, 7734–7743.[PubMed]
    [Google Scholar]
  73. Ott D. E. , Coren L. V. , Chertova E. N. , Gagliardi T. D. , Schubert U. . ( 2000a; ). Ubiquitination of HIV-1 and MuLV Gag. . Virology 278:, 111–121. [CrossRef] [PubMed]
    [Google Scholar]
  74. Ott D. E. , Coren L. V. , Johnson D. G. , Kane B. P. , Sowder R. C. II , Kim Y. D. , Fisher R. J. , Zhou X. Z. , Lu K. P. , Henderson L. E. . ( 2000b; ). Actin-binding cellular proteins inside human immunodeficiency virus type 1. . Virology 266:, 42–51. [CrossRef] [PubMed]
    [Google Scholar]
  75. Peng K. , van Oers M. M. , Hu Z. , van Lent J. W. , Vlak J. M. . ( 2010; ). Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. . J Virol 84:, 9497–9504. [CrossRef] [PubMed]
    [Google Scholar]
  76. Robbins J. , Dilwortht S. M. , Laskey R. A. , Dingwall C. . ( 1991; ). Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. . Cell 64:, 615–623. [CrossRef] [PubMed]
    [Google Scholar]
  77. Roivainen M. , Hyypiä T. , Piirainen L. , Kalkkinen N. , Stanway G. , Hovi T. . ( 1991; ). RGD-dependent entry of coxsackievirus A9 into host cells and its bypass after cleavage of VP1 protein by intestinal proteases. . J Virol 65:, 4735–4740.[PubMed]
    [Google Scholar]
  78. Ruoslahti E. . ( 1996; ). RGD and other recognition sequences for integrins. . Annu Rev Cell Dev Biol 12:, 697–715. [CrossRef] [PubMed]
    [Google Scholar]
  79. Scheidtmann K. H. , Hardung M. , Echle B. , Walter G. . ( 1984; ). DNA-binding activity of simian virus 40 large T antigen correlates with a distinct phosphorylation state. . J Virol 50:, 1–12.[PubMed]
    [Google Scholar]
  80. Sen A. , Todaro G. J. . ( 1977; ). The genome-associated, specific RNA binding proteins of avian and mammalian type C viruses. . Cell 10:, 91–99. [CrossRef] [PubMed]
    [Google Scholar]
  81. Sen A. , Sherr C. J. , Todaro G. J. . ( 1977; ). Phosphorylation of murine type C viral p12 proteins regulates their extent of binding to the homologous viral RNA. . Cell 10:, 487–496. [CrossRef] [PubMed]
    [Google Scholar]
  82. Senkevich T. G. , Weisberg A. S. , Moss B. . ( 2000a; ). Vaccinia virus E10R protein is associated with the membranes of intracellular mature virions and has a role in morphogenesis. . Virology 278:, 244–252. [CrossRef] [PubMed]
    [Google Scholar]
  83. Senkevich T. G. , White C. L. , Koonin E. V. , Moss B. . ( 2000b; ). A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation. . Proc Natl Acad Sci U S A 97:, 12068–12073. [CrossRef] [PubMed]
    [Google Scholar]
  84. Shayakhmetov D. M. , Eberly A. M. , Li Z. Y. , Lieber A. . ( 2005; ). Deletion of penton RGD motifs affects the efficiency of both the internalization and the endosome escape of viral particles containing adenovirus serotype 5 or 35 fiber knobs. . J Virol 79:, 1053–1061. [CrossRef] [PubMed]
    [Google Scholar]
  85. Shenk T. E. , Stinski M. F. . (eds) ( 2008; ). Human Cytomegalovirus. Berlin:: Springer-Verlag;. [CrossRef]
    [Google Scholar]
  86. Sitbon E. , Pietrokovski S. . ( 2003; ). New types of conserved sequence domains in DNA-binding regions of homing endonucleases. . Trends Biochem Sci 28:, 473–477. [CrossRef] [PubMed]
    [Google Scholar]
  87. Slack J. , Arif B. M. . ( 2006; ). The baculoviruses occlusion-derived virus: virion structure and function. . Adv Virus Res 69:, 99–165. [CrossRef] [PubMed]
    [Google Scholar]
  88. Sparks W. O. , Rohlfing A. , Bonning B. C. . ( 2011; ). A peptide with similarity to baculovirus ODV-E66 binds the gut epithelium of Heliothis virescens and impedes infection with Autographa californica multiple nucleopolyhedrovirus. . J Gen Virol 92:, 1051–1060. [CrossRef] [PubMed]
    [Google Scholar]
  89. Tandon R. , Mocarski E. S. . ( 2011; ). Cytomegalovirus pUL96 is critical for the stability of pp150-associated nucleocapsids. . J Virol 85:, 7129–7141. [CrossRef] [PubMed]
    [Google Scholar]
  90. Varnum S. M. , Streblow D. N. , Monroe M. E. , Smith P. , Auberry K. J. , Pasa-Tolic L. , Wang D. , Camp D. G. II , Rodland K. . & other authors ( 2004; ). Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. . J Virol 78:, 10960–10966. [CrossRef] [PubMed]
    [Google Scholar]
  91. Wang M. Q. , Kim W. , Gao G. , Torrey T. A. , Morse H. C. III , De Camilli P. , Goff S. P. . ( 2003; ). Endophilins interact with Moloney murine leukemia virus Gag and modulate virion production. . J Biol 3:, 4. [CrossRef] [PubMed]
    [Google Scholar]
  92. Witt D. J. , Naeve C. W. , Summers D. F. . ( 1981; ). Phosphorylation of vesicular stomatitis virus proteins as a possible contributing factor in virion uncoating. . J Gen Virol 56:, 383–391. [CrossRef] [PubMed]
    [Google Scholar]
  93. Xie X. , Xu L. , Yang F. . ( 2006; ). Proteomic analysis of the major envelope and nucleocapsid proteins of white spot syndrome virus. . J Virol 80:, 10615–10623. [CrossRef] [PubMed]
    [Google Scholar]
  94. Young J. C. , MacKinnon E. A. , Faulkner P. . ( 1993; ). The architecture of the virogenic stroma in isolated nuclei of Spodoptera frugiperda cells in vitro infected by Autographa californica nuclear polyhedrosis virus. . J Struct Biol 110:, 141–153. [CrossRef]
    [Google Scholar]
  95. Zhu F. X. , Cusano T. , Yuan Y. . ( 1999; ). Identification of the immediate-early transcripts of Kaposi’s sarcoma-associated herpesvirus. . J Virol 73:, 5556–5567.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.047423-0
Loading
/content/journal/jgv/10.1099/vir.0.047423-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error