1887

Abstract

Nudiviruses are arthropod-specific large double-stranded circular DNA viruses, related to baculoviruses, which replicate in the nucleus of the cells they infect. To date, six fully sequenced nudiviral genomes are available in databases, and the protein profile from nudivirus particles was mainly characterized by PAGE. However, only a few direct matches have been completed between genomic and proteomic data, with the exception of the major occlusion body protein from nudivirus and four nucleocapsid proteins from nudivirus-2. The function of predicted nudiviral proteins is still inferred from what is known from baculoviruses or endogenous nudiviruses (i.e. bracoviruses). nudivirus (ToNV) is the causative agent of crane fly nucleopolyhedrosis. Along with nudivirus, ToNV is the second fully sequenced nudivirus to be described as forming occlusion bodies. The protein profile revealed by Coomassie-stained SDS-PAGE is very similar to those observed for other nudiviruses, with five major protein bands of about 75, 48, 35, 25 and 12 kDa. Proteomic analysis, using on-line nanoflow liquid chromatography in tandem with high-resolution mass spectrometry, revealed that ToNV occlusion bodies are composed of 52 viral proteins, the most abundant of which are the functional homologue of baculovirus polyhedrin/granulin and the homologues of three nudivirus-2 predicted proteins: the two virion structural proteins 34K (Hz2V052, the baculovirus capsid protein VP39 homologue) and 11K (Hz2V025), and the hypothetical protein Hz2V079, a newly identified nudivirus core gene product.

Keyword(s): nudivirus and proteome
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2017-02-01
2024-10-05
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References

  1. Huger AM, Krieg A. Baculoviridae. Nonoccluded baculoviruses. In Adams JR, Bonami J-R. (editors) Atlas of Invertebrate Viruses Boca Raton, FL: CRC Press; 1991 pp. 287–319
    [Google Scholar]
  2. Wang Y, Bininda-Emond ORP, Jehle JA. Nudivirus genomics and phylogeny. In Garcia ML, Romanowski V. (editors) Viral Genomes - Molecular Structure, Diversity, Gene Expression Mechanisms and Host-Virus Interactions 2012 pp. 33–52 www.intechopen.com/books/viral-genomesmolecular-structure-diversit y-gene-expression-mechanisms-and-host-virusinteractions/nudivirus-genomics-and-phylogeny
    [Google Scholar]
  3. Jehle JA, Abd-Alla AMM, Wang Y. Phylogeny and evolution of Hytrosaviridae. J Invertebr Pathol 2013; 112:S62–S67 [View Article]
    [Google Scholar]
  4. Bézier A, Thézé J, Gavory F, Gaillard J, Poulain J et al. The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family. J Virol 2015; 89:3008–3025 [View Article][PubMed]
    [Google Scholar]
  5. Gauthier L, Cornman S, Hartmann U, Cousserans F, Evans JD et al. The Apis mellifera filamentous virus genome. Viruses 2015; 7:3798–3815 [View Article][PubMed]
    [Google Scholar]
  6. Jehle JA, Burand J, Herniou EA, Harrison R, Arif B et al. Creation of a new family Nudiviridae including two new genera and three species. Taxonomy proposals; 2013 http://talk.ictvonline.org/files/proposals/taxonomy_proposals_invertebrate1/m/inv 04/4770.aspx
  7. Granados RR, Nguyen T, Cato B. An insect cell line persistently infected with a baculovirus-like particle. Intervirology 1978; 10:309–317 [View Article][PubMed]
    [Google Scholar]
  8. Cheng CH, Liu SM, Chow TY, Hsiao YY, Wang DP et al. Analysis of the complete genome sequence of the Hz-1 virus suggests that it is related to members of the Baculoviridae. J Virol 2002; 76:9024–9034 [View Article][PubMed]
    [Google Scholar]
  9. Raina AK, Adams JR, Lupiani B, Lynn DE, Kim W et al. Further characterization of the gonad-specific virus of corn eatworm, Helicoverpa zea. J Invertebr Pathol 2000; 76:6–12 [View Article]
    [Google Scholar]
  10. Burand JP, Rallis CP. In vivo dose-response of insects to Hz-2V infection. Virol J 2004; 1:15 [View Article][PubMed]
    [Google Scholar]
  11. Burand JP, Kim W, Afonso CL, Tulman ER, Kutish GF et al. Analysis of the genome of the sexually transmitted insect virus Helicoverpa zea nudivirus 2. Viruses 2012; 4:28–61 [View Article][PubMed]
    [Google Scholar]
  12. Unckless RL. A DNA virus of Drosophila. PLoS One 2011; 6:e26564 [View Article][PubMed]
    [Google Scholar]
  13. Smith KM, Xeros N. An unusual virus disease of a dipterous larva. Nature 1954; 173:866–867[PubMed] [CrossRef]
    [Google Scholar]
  14. Bergoin M, Guelpa B. Dissolution des inclusions du virus de la polyhedrose nucléaire du diptère Tipula paludosa MEIG. Etude ultrastructurale du virion. Arch Virol 1977; 53:243–254 [View Article]
    [Google Scholar]
  15. Huger AM. A new virus disease of crickets (Orthoptera: Gryllidae) causing macronucleosis of fatbody. J Inverteb Pathol 1985; 45:108–111 [View Article]
    [Google Scholar]
  16. Wang Y, Kleespies RG, Huger AM, Jehle JA. The genome of Gryllus bimaculatus nudivirus indicates an ancient diversification of baculovirus-related nonoccluded nudiviruses of insects. J Virol 2007; 81:5395–5406 [View Article][PubMed]
    [Google Scholar]
  17. Huger AM. A virus disease of the Indian rhinoceros beetle, Oryctes rhinoceros (Linnaeus), caused by a new type of insect virus, Rhabdionvirus oryctes gen. n., sp. n. J Invertebr Pathol 1966; 8:38–51 [View Article][PubMed]
    [Google Scholar]
  18. Payne CC. The isolation and characterization of a virus from Oryctes rhinoceros. J Gen Virol 1974; 25:105–116 [View Article][PubMed]
    [Google Scholar]
  19. Payne CC, Compson D, De Looze SM. Properties of the nucleocapsids of a virus isolated from Oryctes rhinoceros. Virology 1977; 77:269–280[PubMed] [CrossRef]
    [Google Scholar]
  20. Wang Y, Van Oers MM, Crawford AM, Vlak JM, Jehle JA. Genomic analysis of Oryctes rhinoceros virus reveals genetic relatedness to Heliothis zea virus 1. Arch Virol 2007; 152:519–531 [View Article][PubMed]
    [Google Scholar]
  21. Mari J, Bonami JR, Poulos B, Lightner D. Preliminary characterization and partial cloning of the genome of a baculovirus from: Penaeus monodon (PmSMPV = MBV). Dis Aquat Organ 1993; 16:207–215 [View Article]
    [Google Scholar]
  22. Yang YT, Lee DY, Wang Y, Hu JM, Li WH et al. The genome and occlusion bodies of marine Penaeus monodon nudivirus (PmNV, also known as MBV and PemoNPV) suggest that it should be assigned to a new nudivirus genus that is distinct from the terrestrial nudiviruses. BMC Genomics 2014; 15:628 [View Article][PubMed]
    [Google Scholar]
  23. Bonami JR, Bruce LD, Poulos BT, Mari J, Lightner DV. Partial characterization and cloning of the genome of PvSNPV (= BP-type virus) pathogenic for Penaeus vannamei. Dis Aquat Organ 1995; 23:59–66 [View Article]
    [Google Scholar]
  24. Stentiford GD, Bateman K, Feist SW. Pathology and ultrastructure of an intranuclear bacilliform virus (IBV) infecting brown shrimp Crangon crangon (Decapoda: Crangonidae). Dis Aquat Organ 2004; 58:89–97 [View Article][PubMed]
    [Google Scholar]
  25. Burand JP. Nudiviruses. In Miller LK, Ball LA. (editors) The Insect Viruses New York and London, FL: Plenum Press; 1998 pp. 69–90 [CrossRef]
    [Google Scholar]
  26. Lin CL, Lee JC, Chen SS, Wood HA, Li ML et al. Persistent Hz-1 virus infection in insect cells: evidence for insertion of viral DNA into host chromosomes and viral infection in a latent status. J Virol 1999; 73:128–139[PubMed]
    [Google Scholar]
  27. Bézier A, Annaheim M, Herbinière J, Wetterwald C, Gyapay G et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 2009; 323:926–930 [View Article][PubMed]
    [Google Scholar]
  28. Thézé J, Bézier A, Periquet G, Drezen JM, Herniou EA. Paleozoic origin of insect large dsDNA viruses. Proc Natl Acad Sci USA 2011; 108:15931–15935 [View Article][PubMed]
    [Google Scholar]
  29. Pichon A, Bézier A, Urbach S, Aury JM, Jouan V et al. Recurrent DNA virus domestication leading to different parasite virulence strategies. Sci Adv 2015; 1:e1501150 [View Article][PubMed]
    [Google Scholar]
  30. Cheng RL, Xi Y, Lou YH, Wang Z, Xu JY et al. Brown planthopper nudivirus DNA integrated in its host genome. J Virol 2014; 88:5310–5318 [View Article][PubMed]
    [Google Scholar]
  31. Chaivisuthangkura P, Tawilert C, Tejangkura T, Rukpratanporn S, Longyant S et al. Molecular isolation and characterization of a novel occlusion body protein gene from Penaeus monodon nucleopolyhedrovirus. Virology 2008; 381:261–267 [View Article][PubMed]
    [Google Scholar]
  32. Bonami JR, Aubert H, Mari J, Poulos BT, Lightner DV. The polyhedra of the occluded baculoviruses of marine decapod crustacea: a unique structure, crystal organization, and proposed model. J Struct Biol 1997; 120:134–145 [View Article][PubMed]
    [Google Scholar]
  33. Couch JA. Free and occluded virus, similar to Baculovirus, in hepatopancreas of pink shrimp. Nature 1974; 247:229–231 [CrossRef]
    [Google Scholar]
  34. Wang Y, Bininda-Emonds OR, van Oers MM, Vlak JM, Jehle JA. The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes 2011; 42:444–456 [View Article][PubMed]
    [Google Scholar]
  35. Burand JP, Stiles B, Wood HA. Structural and intracellular proteins of the nonoccluded baculovirus Hz-1. J Virol 1983; 46:137–142[PubMed]
    [Google Scholar]
  36. Crawford AM, Sheehan C. Replication of Oryctes baculovirus in cell culture: viral morphogenesis, infectivity and protein synthesis. J Gen Virol 1985; 66:529–539 [CrossRef]
    [Google Scholar]
  37. Kim W. Characterization of genome and structural proteins of the sexually transmitted insect virus, Hz-2V. Doctoral dissertations. Paper AAI3379978 2009
  38. Rohrmann GF. Baculovirus Molecular Biology, 3rd ed. Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information; 2013 www.ncbi.nlm.nih.gov/books/NBK114593/
    [Google Scholar]
  39. Nadala ECB, Tapay LM, Loh PC. Characterization of a non-occluded baculovirus-like agent pathogenic to penaeid shrimp. Dis Aquat Organ 1998; 33:221–229 [View Article]
    [Google Scholar]
  40. Braunagel SC, Russell WK, Rosas-Acosta G, Russell DH, Summers MD. Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci USA 2003; 100:9797–9802 [View Article][PubMed]
    [Google Scholar]
  41. Deng F, Wang R, Fang M, Jiang Y, Xu X et al. Proteomics analysis of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus identified two new occlusion-derived virus-associated proteins, HA44 and HA100. J Virol 2007; 81:9377–9385 [View Article][PubMed]
    [Google Scholar]
  42. Perera O, Green TB, Stevens SM, White S, Becnel JJ. Proteins associated with Culex nigripalpus nucleopolyhedrovirus occluded virions. J Virol 2007; 81:4585–4590 [View Article][PubMed]
    [Google Scholar]
  43. Wang R, Deng F, Hou D, Zhao Y, Guo L et al. Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 2010; 84:7233–7242 [View Article][PubMed]
    [Google Scholar]
  44. Wang XF, Zhang BQ, Xu HJ, Cui YJ, Xu YP et al. ODV-associated proteins of the Pieris rapae granulovirus. J Proteome Res 2011; 10:2817–2827 [View Article][PubMed]
    [Google Scholar]
  45. Hou D, Zhang L, Deng F, Fang W, Wang R et al. Comparative proteomics reveal fundamental structural and functional differences between the two progeny phenotypes of a baculovirus. J Virol 2013; 87:829–839 [View Article][PubMed]
    [Google Scholar]
  46. Kariithi HM, Ince IA, Boeren S, Vervoort J, Bergoin M et al. Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. J Gen Virol 2010; 91:3065–3074 [View Article][PubMed]
    [Google Scholar]
  47. Cottrell JS. Protein identification using MS/MS data. J Proteomics 2011; 74:1842–1851 [View Article][PubMed]
    [Google Scholar]
  48. Ishihama Y. Proteomic LC-MS systems using nanoscale liquid chromatography with tandem mass spectrometry. J Chromatogr A 2005; 1067:73–83[PubMed] [CrossRef]
    [Google Scholar]
  49. Rieux L, Sneekes E-J, Swart R. Nano LC: principles, evolution, and state-of-the-art of the technique. LCGC NA 2011; 29:926–934 www.chromatographyonline.com/lcgc/Column%3A+Innovations+in+HPLC/Nano-LC-Principles-Evolution-and-State-of-the-Art-/Article Standard/Article/detail/745381
    [Google Scholar]
  50. Garcia-Maruniak A, Maruniak JE, Farmerie W, Boucias DG. Sequence analysis of a non-classified, non-occluded DNA virus that causes salivary gland hypertrophy of Musca domestica, MdSGHV. Virology 2008; 377:184–196 [View Article][PubMed]
    [Google Scholar]
  51. Lu H. Characterization of a novel baculovirus, gonad-specific virus, GSV. Thesis dissertation. Department of Microbiology, University of Massachusetts, Amherst, MA 1997
    [Google Scholar]
  52. Liu X, Chen K, Cai K, Yao Q. Determination of protein composition and host-derived proteins of Bombyx mori nucleopolyhedrovirus by 2-dimensional electrophoresis and mass spectrometry. Intervirology 2008; 51:369–376 [View Article][PubMed]
    [Google Scholar]
  53. Xu F, Ince IA, Boeren S, Vlak JM, Van Oers MM. Protein composition of the occlusion derived virus of Chrysodeixis chalcites nucleopolyhedrovirus. Virus Res 2011; 158:1–7 [View Article][PubMed]
    [Google Scholar]
  54. Braconi CT, Ardisson-Araújo DM, Paes Leme AF, Oliveira JV, Pauletti BA et al. Proteomic analyses of baculovirus Anticarsia gemmatalis multiple nucleopolyhedrovirus budded and occluded virus. J Gen Virol 2014; 95:980–989 [View Article][PubMed]
    [Google Scholar]
  55. Zhang X, Liang Z, Yin X, Shao X. Proteomic analysis of the occlusion-derived virus of Clostera anachoreta granulovirus. J Gen Virol 2015; 96:2394–2404 [View Article][PubMed]
    [Google Scholar]
  56. Van Oers MM, Vlak JM. Baculovirus genomics. Curr Drug Targets 2007; 8:1051–1068 [View Article][PubMed]
    [Google Scholar]
  57. Slack J, Arif BM. The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 2007; 69:99–165 [View Article][PubMed]
    [Google Scholar]
  58. Abd-Alla AM, Kariithi HM, Cousserans F, Parker NJ, Ince IA et al. Comprehensive annotation of Glossina pallidipes salivary gland hypertrophy virus from ethiopian tsetse flies: a proteogenomics approach. J Gen Virol 2016; 97:1010–1031 [View Article][PubMed]
    [Google Scholar]
  59. Wetterwald C, Roth T, Kaeslin M, Annaheim M, Wespi G et al. Identification of bracovirus particle proteins and analysis of their transcript levels at the stage of virion formation. J Gen Virol 2010; 91:2610–2619 [View Article][PubMed]
    [Google Scholar]
  60. Burke GR, Thomas SA, Eum JH, Strand MR. Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors. PLoS Pathog 2013; 9:e1003348 [View Article][PubMed]
    [Google Scholar]
  61. Meynardier G, Ricou G, Bergoin M. Virose à corps d’inclusion chez Tipula paludosa (Diptera) en France. Re Pathol Vég Entomo Agric Fr 1964; 43:113–118
    [Google Scholar]
  62. Grainge I, Jayaram M. The integrase family of recombinase: organization and function of the active site. Mol Microbiol 1999; 33:449–456 [View Article][PubMed]
    [Google Scholar]
  63. Liu Y, Kao HI, Bambara RA. Flap endonuclease 1: a central component of DNA metabolism. Annu Rev Biochem 2004; 73:589–615 [View Article][PubMed]
    [Google Scholar]
  64. Balakrishnan L, Bambara RA. Flap endonuclease 1. Annu Rev Biochem 2013; 82:119–138 [View Article][PubMed]
    [Google Scholar]
  65. Vanarsdall AL, Okano K, Rohrmann GF. Characterization of a baculovirus with a deletion of vlf-1. Virology 2004; 326:191–201 [View Article][PubMed]
    [Google Scholar]
  66. Li Y, Wang J, Deng R, Zhang Q, Yang K et al. Vlf-1 deletion brought AcMNPV to defect in nucleocapsid formation. Virus Genes 2005; 31:275–284 [View Article][PubMed]
    [Google Scholar]
  67. Vanarsdall AL, Okano K, Rohrmann GF. Characterization of the role of very late expression factor 1 in baculovirus capsid structure and DNA processing. J Virol 2006; 80:1724–1733 [View Article][PubMed]
    [Google Scholar]
  68. Peng K, Van Oers MM, Hu Z, Van Lent JW, Vlak JM. Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. J Virol 2010; 84:9497–9504 [View Article][PubMed]
    [Google Scholar]
  69. Peng K, Van Lent JW, Boeren S, Fang M, Theilmann DA et al. Characterization of novel components of the baculovirus per os infectivity factor complex. J Virol 2012; 86:4981–4988 [View Article][PubMed]
    [Google Scholar]
  70. Zhu S, Wang W, Wang Y, Yuan M, Yang K. The baculovirus core gene ac83 is required for nucleocapsid assembly and per os infectivity of Autographa californica nucleopolyhedrovirus. J Virol 2013; 87:10573–10586 [View Article][PubMed]
    [Google Scholar]
  71. Tweeten KA, Bulla LA, Consigli RA. Characterization of an extremely basic protein derived from granulosis virus nucleocapsids. J Virol 1980; 33:866–876[PubMed]
    [Google Scholar]
  72. Searle BC. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 2010; 10:1265–1269 [View Article][PubMed]
    [Google Scholar]
  73. Lundgren DH, Hwang SI, Wu L, Han DK. Role of spectral counting in quantitative proteomics. Expert Rev Proteomics 2010; 7:39–53 [View Article][PubMed]
    [Google Scholar]
  74. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005; 4:1265–1272 [View Article][PubMed]
    [Google Scholar]
  75. Pearson MN, Russell RL, Rohrmann GF, Beaudreau GS. P39, a major baculovirus structural protein: immunocytochemical characterization and genetic location. Virology 1988; 167:407–413 [View Article][PubMed]
    [Google Scholar]
  76. Thiem SM, Miller LK. Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol 1989; 63:2008–2018[PubMed]
    [Google Scholar]
  77. Faulkner P, Kuzio J, Williams GV, Wilson JA. Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo. J Gen Virol 1997; 78:3091–3100 [View Article][PubMed]
    [Google Scholar]
  78. Braunagel SC, Summers MD. Molecular biology of the baculovirus occlusion-derived virus envelope. Curr Drug Targets 2007; 8:1084–1095[PubMed] [CrossRef]
    [Google Scholar]
  79. Kikhno I, Gutiérrez S, Croizier L, Croizier G, Ferber ML. Characterization of pif, a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol 2002; 83:3013–3022 [View Article][PubMed]
    [Google Scholar]
  80. Ott DE. Potential roles of cellular proteins in HIV-1. Rev Med Virol 2002; 12:359–374 [View Article][PubMed]
    [Google Scholar]
  81. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P. Cellular proteins in influenza virus particles. PLoS Pathog 2008; 4:e1000085 [View Article][PubMed]
    [Google Scholar]
  82. Lanier LM, Volkman LE. Actin binding and nucleation by Autographa california M nucleopolyhedrovirus. Virology 1998; 243:167–177 [View Article][PubMed]
    [Google Scholar]
  83. Saphire ACS, Gallay PA, Bark SJ. Proteomic analysis of human immunodeficiency virus using liquid chromatography/tandem mass spectrometry effectively distinguishes specific incorporated host proteins. J Proteome Res 2005; 5:530–538 [CrossRef]
    [Google Scholar]
  84. Segura MM, Garnier A, Di Falco MR, Whissell G, Meneses-Acosta A et al. Identification of host proteins associated with retroviral vector particles by proteomic analysis of highly purified vector preparations. J Virol 2008; 82:1107–1117 [View Article][PubMed]
    [Google Scholar]
  85. Ohkawa T, Volkman LE, Welch MD. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J Cell Biol 2010; 190:187–195 [View Article][PubMed]
    [Google Scholar]
  86. Volkman LE. Baculovirus infectivity and the actin cytoskeleton. Curr Drug Targets 2007; 8:1075–1083 [View Article][PubMed]
    [Google Scholar]
  87. Marek M, Merten OW, Galibert L, Vlak JM, Van Oers MM. Baculovirus VP80 protein and the F-actin cytoskeleton interact and connect the viral replication factory with the nuclear periphery. J Virol 2011; 85:5350–5362 [View Article][PubMed]
    [Google Scholar]
  88. Bannister JV, Bannister WH, Rotilio G. Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem 1987; 22:111–180 [View Article][PubMed]
    [Google Scholar]
  89. Thézé J, Takatsuka J, Nakai M, Arif B, Herniou EA. Gene acquisition convergence between entomopoxviruses and baculoviruses. Viruses 2015; 7:1960–1974 [View Article][PubMed]
    [Google Scholar]
  90. Almazán F, Tscharke DC, Smith GL. The vaccinia virus superoxide dismutase-like protein (A45R) is a virion component that is nonessential for virus replication. J Virol 2001; 75:7018–7029 [View Article][PubMed]
    [Google Scholar]
  91. Chung CS, Chen CH, Ho MY, Huang CY, Liao CL et al. Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J Virol 2006; 80:2127–2140 [View Article][PubMed]
    [Google Scholar]
  92. Lartigue A, Burlat B, Coutard B, Chaspoul F, Claverie JM et al. The megavirus chilensis Cu,Zn-superoxide dismutase: the first viral structure of a typical cellular copper chaperone-independent hyperstable dimeric enzyme. J Virol 2015; 89:824–832 [View Article][PubMed]
    [Google Scholar]
  93. Thézé J, Takatsuka J, Li Z, Gallais J, Doucet D et al. New insights into the evolution of Entomopoxvirinae from the complete genome sequences of four entomopoxviruses infecting Adoxophyes honmai, Choristoneura biennis, Choristoneura rosaceana, and Mythimna separata. J Virol 2013; 87:7992–8003 [View Article][PubMed]
    [Google Scholar]
  94. Tomalski MD, Eldridge R, Miller LK. A baculovirus homolog of a Cu/Zn superoxide dismutase gene. Virology 1991; 184:149–161 [View Article][PubMed]
    [Google Scholar]
  95. Teoh ML, Walasek PJ, Evans DH. Leporipoxvirus Cu,Zn-superoxide dismutase (SOD) homologs are catalytically inert decoy proteins that bind copper chaperone for SOD. J Biol Chem 2003; 278:33175–33184 [View Article][PubMed]
    [Google Scholar]
  96. Krecic AM, Swanson MS. hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 1999; 11:363–371 [View Article][PubMed]
    [Google Scholar]
  97. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 2002; 3:195–205 [View Article][PubMed]
    [Google Scholar]
  98. Gattoni R, Mahé D, Mähl P, Fischer N, Mattei MG et al. The human hnRNP-M proteins: structure and relation with early heat shock-induced splicing arrest and chromosome mapping. Nucleic Acids Res 1996; 24:2535–2542 [View Article][PubMed]
    [Google Scholar]
  99. Jorba N, Juarez S, Torreira E, Gastaminza P, Zamarreño N et al. Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 2008; 8:2077–2088 [View Article][PubMed]
    [Google Scholar]
  100. Dechtawewat T, Songprakhon P, Limjindaporn T, Puttikhunt C, Kasinrerk W et al. Role of human heterogeneous nuclear ribonucleoprotein C1/C2 in dengue virus replication. Virol J 2015; 6:12–14
    [Google Scholar]
  101. Jagdeo JM, Dufour A, Fung G, Luo H, Kleifeld O et al. Heterogeneous nuclear ribonucleoprotein M facilitates enterovirus infection. J Virol 2015; 89:7064–7078 [View Article][PubMed]
    [Google Scholar]
  102. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685[PubMed] [CrossRef]
    [Google Scholar]
  103. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002; 74:5383–5392 [View Article][PubMed]
    [Google Scholar]
  104. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003; 75:4646–4658 [View Article][PubMed]
    [Google Scholar]
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