1887

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Volume 100, Issue 2

Proteomic analysis of the Heliothis virescens ascovirus 3i (HvAV-3i) virion Free

Abstract

Ascoviruses are enveloped, circular, double-stranded DNA viruses that can effectively control the appetite of lepidopteran larvae, thereby reducing the consequent damage and economic losses to crops. In this study, the virion of a sequenced Heliothis virescens ascovirus 3i (HvAV-3i) strain was used to perform proteomic analysis using both in-gel and in-solution digestion. A total of 81 viral proteins, of which 67 were associated with the virions, were identified in the proteome of HvAV-3i virions. Among these proteins, 23 with annotated functions were associated with DNA/RNA metabolism/transcription, virion assembly, sugar and lipid metabolism, signalling, cellular homoeostasis and cell lysis. Twenty-one viral membrane proteins were also identified. Some of the minor ‘virion’ proteins identified may be non-virion contaminants of viral proteins synthesized during replication, identified by more recent and highly sensitive methods. The extensive identification of the ascoviral proteome will establish a foundation for further investigation of ascoviral replication and infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Heliothis virescens ascovirus 3i , HvAV-3i , proteomics and virion-associated viral proteins
© 2019 The Authors
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2018-12-12
2023-03-22
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References

  1. Stasiak K, Renault S, Federici BA, Bigot Y. Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J Insect Physiol 2005; 51:103–115 [View Article][PubMed]
     [Google Scholar]
  2. Li SJ, Hopkins RJ, Zhao YP, Zhang YX, Hu J et al. Imperfection works: Survival, transmission and persistence in the system of Heliothis virescens ascovirus 3h (HvAV-3h), Microplitis similis and Spodoptera exigua. Sci Rep 2016; 6:21296 [View Article][PubMed]
     [Google Scholar]
  3. Hamm JJ, Styer EL, Federici BA. Comparison of field-collected ascovirus isolates by DNA hybridization, host range, and histopathology. J Invertebr Pathol 1998; 72:138–146 [View Article][PubMed]
     [Google Scholar]
  4. Asgari S, Bideshi DK, Bigot Y, Federici BA, Cheng XW et al. ICTV Virus Taxonomy Profile: Ascoviridae . J Gen Virol 2017; 98:4–5 [View Article][PubMed]
     [Google Scholar]
  5. Federici BA. Enveloped double-stranded DNA insect virus with novel structure and cytopathology. Proc Natl Acad Sci USA 1983; 80:7664–7668 [View Article][PubMed]
     [Google Scholar]
  6. Huang GH, Garretson TA, Cheng XH, Holztrager MS, Li SJ et al. Phylogenetic position and replication kinetics of Heliothis virescens ascovirus 3h (HvAV-3h) isolated from Spodoptera exigua . PLoS One 2012; 7:e40225 [View Article][PubMed]
     [Google Scholar]
  7. Li SJ, Wang X, Zhou ZS, Zhu J, Hu J et al. A comparison of growth and development of three major agricultural insect pests infected with Heliothis virescens ascovirus 3h (HvAV-3h). PLoS One 2013; 8:e85704 [View Article][PubMed]
     [Google Scholar]
  8. Huang GH, Hou DH, Wang M, Cheng XW, Hu Z. Genome analysis of Heliothis virescens ascovirus 3h isolated from China. Virol Sin 2017; 32:147–154 [View Article][PubMed]
     [Google Scholar]
  9. Liu YY, Xian WF, Xue J, Wei YL, Cheng XW et al. Complete Genome Sequence of a Renamed Isolate, Trichoplusia ni Ascovirus 6b, from the United States. Genome Announc 2018; 6:e0014818 [View Article][PubMed]
     [Google Scholar]
  10. Arai E, Ishii K, Ishii H, Sagawa S, Makiyama N et al. An ascovirus isolated from Spodoptera litura (Noctuidae: Lepidoptera) transmitted by the generalist endoparasitoid Meteorus pulchricornis (Braconidae: Hymenoptera). J Gen Virol 2018; 99:574–584 [View Article][PubMed]
     [Google Scholar]
  11. Cui L, Cheng X, Li L, Li J. Identification of Trichoplusia ni ascovirus 2c virion structural proteins. J Gen Virol 2007; 88:2194–2197 [View Article][PubMed]
     [Google Scholar]
  12. Tan Y, Bideshi DK, Johnson JJ, Bigot Y, Federici BA. Proteomic analysis of the Spodoptera frugiperda ascovirus 1a virion reveals 21 proteins. J Gen Virol 2009; 90:359–365 [View Article][PubMed]
     [Google Scholar]
  13. Song W, Lin Q, Joshi SB, Lim TK, Hew CL. Proteomic studies of the Singapore grouper iridovirus. Mol Cell Proteomics 2006; 5:256–264 [View Article][PubMed]
     [Google Scholar]
  14. Ince IA, Boeren SA, van Oers MM, Vervoort JJ, Vlak JM. Proteomic analysis of Chilo iridescent virus. Virology 2010; 405:253–258 [View Article][PubMed]
     [Google Scholar]
  15. Chen ZS, Hou DH, Cheng XW, Wang X, Huang GH. Genomic analysis of a novel isolate Heliothis virescens ascovirus 3i (HvAV-3i) and identification of ascoviral repeat ORFs (aros). Arch Virol 2018; 163:2849–2853 [View Article][PubMed]
     [Google Scholar]
  16. Federici BA, Vlak JM, Hamm JJ. Comparative study of virion structure, protein composition and genomic DNA of three ascovirus isolates. J Gen Virol 1990; 71:1661–1668 [View Article][PubMed]
     [Google Scholar]
  17. Yu JL, Guo L. Quantitative proteomic analysis of Salmonella enterica serovar Typhimurium under PhoP/PhoQ activation conditions. J Proteome Res 2011; 10:2992–3002 [View Article][PubMed]
     [Google Scholar]
  18. Hou D, Chen X, Zhang L-K. Proteomic analysis of Mamestra brassicae nucleopolyhedrovirus progeny virions from two different hosts. PLoS One 2016; 11:e0153365 [View Article]
     [Google Scholar]
  19. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH et al. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 2007; 6:1638–1655 [View Article][PubMed]
     [Google Scholar]
  20. van Oers MM, Vlak JM. Baculovirus genomics. Curr Drug Targets 2007; 8:1051–1068 [View Article][PubMed]
     [Google Scholar]
  21. Zhao K, Cui L. Molecular characterization of the major virion protein gene from the Trichoplusia ni ascovirus. Virus Genes 2003; 27:93–102 [View Article][PubMed]
     [Google Scholar]
  22. Kuang W, Zhang H, Wang M, Zhou NY, Deng F et al. Three conserved regions in baculovirus sulfhydryl oxidase P33 are critical for enzymatic activity and function. J Virol 2017; 91:e0115817 [View Article][PubMed]
     [Google Scholar]
  23. Wang F, Bi X, Chen LM, Hew CL. ORF018R, a highly abundant virion protein from Singapore grouper iridovirus, is involved in serine/threonine phosphorylation and virion assembly. J Gen Virol 2008; 89:1169–1178 [View Article][PubMed]
     [Google Scholar]
  24. Jacob T, van den Broeke C, Favoreel HW. Viral serine/threonine protein kinases. J Virol 2011; 85:1158–1173 [View Article][PubMed]
     [Google Scholar]
  25. Hardwick JM. Apoptosis in viral pathogenesis. Cell Death Differ 2001; 8:109–110 [View Article][PubMed]
     [Google Scholar]
  26. Bideshi DK, Tan Y, Bigot Y, Federici BA. A viral caspase contributes to modified apoptosis for virus transmission. Genes Dev 2005; 19:1416–1421 [View Article][PubMed]
     [Google Scholar]
  27. Zaghloul H, Hice R, Arensburger P, Federici BA. Transcriptome analysis of the Spodoptera frugiperda ascovirus in vivo provides insights into how its apoptosis inhibitors and caspase promote increased synthesis of viral vesicles and virion progeny. J Virol 2017; 91:e0087417 [View Article][PubMed]
     [Google Scholar]
  28. Piégu B, Asgari S, Bideshi D, Federici BA, Bigot Y. Evolutionary relationships of iridoviruses and divergence of ascoviruses from invertebrate iridoviruses in the superfamily Megavirales. Mol Phylogenet Evol 2015; 84:44–52 [View Article][PubMed]
     [Google Scholar]
  29. Liu F, Putnam A, Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proceedings of the National Academy of Sciences 2008; 105:20209–20214 [View Article]
     [Google Scholar]
  30. Jessberger R. The many functions of SMC proteins in chromosome dynamics. Nat Rev Mol Cell Biol 2002; 3:767–778 [View Article][PubMed]
     [Google Scholar]
  31. Martenot C, Travaillé E, Lethuillier O, Lelong C, Houssin M. Genome exploration of six variants of the Ostreid Herpesvirus 1 and characterization of large deletion in OsHV-1μVar specimens. Virus Res 2013; 178:462–470 [View Article][PubMed]
     [Google Scholar]
  32. 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]
  33. Ince IA, Westenberg M, Vlak JM, Demirbağ Z, Nalçacioğlu R et al. Open reading frame 193R of Chilo iridescent virus encodes a functional inhibitor of apoptosis (IAP). Virology 2008; 376:124–131 [View Article][PubMed]
     [Google Scholar]
  34. Deveraux QL, Reed JC. IAP family proteins-suppressors of apoptosis. Genes Dev 1999; 13:239–252 [View Article][PubMed]
     [Google Scholar]
  35. Zhang L, Villa NY, Mcfadden G. Interplay between poxviruses and the cellular ubiquitin/ubiquitin-like pathways. FEBS Lett 2009; 583:607–614 [View Article][PubMed]
     [Google Scholar]
  36. Federici BA, Bideshi DK, Tan Y, Spears T, Bigot Y. Ascoviruses: superb manipulators of apoptosis for viral replication and transmission. Curr Top Microbiol Immunol 2009; 328:171–196[PubMed]
     [Google Scholar]
  37. Shindou H, Shimizu T. Acyl-CoA:lysophospholipid acyltransferases. J Biol Chem 2009; 284:1–5 [View Article][PubMed]
     [Google Scholar]
  38. Shindou H, Hishikawa D, Harayama T, Yuki K, Shimizu T. Recent progress on acyl CoA: lysophospholipid acyltransferase research. J Lipid Res 2009; 50 Suppl:S46–S51 [View Article][PubMed]
     [Google Scholar]
  39. Tehlivets O, Scheuringer K, Kohlwein SD. Fatty acid synthesis and elongation in yeast. Biochimica et Biophysica Acta 2007; 1771:255–270
     [Google Scholar]
  40. Jakobsson A, Westerberg R, Jacobsson A. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 2006; 45:237–249 [View Article][PubMed]
     [Google Scholar]
  41. Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW et al. Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes. Virology 1997; 238:243–253 [View Article][PubMed]
     [Google Scholar]
  42. Vesper SJ, Vesper MJ. Possible role of fungal hemolysins in sick building syndrome. Adv Appl Microbiol 2004; 55:191–213 [View Article][PubMed]
     [Google Scholar]
  43. Berne S, Lah L, Sepcić K. Aegerolysins: structure, function, and putative biological role. Protein Sci 2009; 18:NA–706 [View Article][PubMed]
     [Google Scholar]
  44. Gentschev I, Dietrich G, Goebel W. The E. coli alpha-hemolysin secretion system and its use in vaccine development. Trends Microbiol 2002; 10:39–45 [View Article][PubMed]
     [Google Scholar]
  45. Kattenhorn LM, Mills R, Wagner M, Lomsadze A, Makeev V et al. Identification of proteins associated with murine cytomegalovirus virions. J Virol 2004; 78:11187–11197 [View Article][PubMed]
     [Google Scholar]
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Proteomic analysis of the Heliothis virescens ascovirus 3i (HvAV-3i) virion
J. Gen. Virol. 100, 301 (2019); https://doi.org/10.1099/jgv.0.001197
/content/journal/jgv/10.1099/jgv.0.001197
/content/journal/jgv/10.1099/jgv.0.001197
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