Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 106, Issue 1

Transcriptional dynamics during Heliothis zea nudivirus 1 infection in an ovarian cell line from Open Access

Abstract

Nudiviruses (family ) are double-stranded DNA viruses that infect various insects and crustaceans. Among them, Heliothis zea nudivirus 1 (HzNV-1) represents the rare case of a lepidopteran nudivirus inducing a sexual pathology. Studies about molecular pathological dynamics of HzNV-1 or other nudiviruses are scarce. Hence, this study aims to provide a transcriptomic profile of HzNV-1 in an ovary-derived cell line of (HZ-AM1), during early (3, 6 and 9 h post-infection) and advanced (12 and 24 h post-infection) stages of infection. Total RNA was extracted from both virus- and mock-infected cells, and RNA-seq analysis was performed to examine both virus and host transcriptional dynamics. Hierarchical clustering was used to categorize viral genes, while differential gene expression analysis was utilized to pinpoint host genes that are significantly affected by the infection. Hierarchical clustering classified the 154 HzNV-1 genes into four temporal phases, with early phases mainly involving transcription and replication genes and later phases including genes for virion assembly. In addition, a novel viral promoter motif was identified in the upstream region of early-expressed genes. Host gene analysis revealed significant upregulation of heat shock protein genes and downregulation of histone genes. The identification of temporal patterns in viral gene expression enhances the molecular understanding of nudivirus pathology, while the identified differentially expressed host genes highlight the key pathways most hijacked by HzNV-1 infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): differential expression , Helicoverpa zea , immune response , Nudiviridae , ovarian cells and RNA-seq
Funding
This study was supported by the:
  • H2020 Marie Skłodowska-Curie Actions (Award 859850)
    • Principle Award Recipient: M. van OersMonique
© 2025 Wageningen University
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.002066
2025-01-13
2025-01-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/106/1/jgv002066.html?itemId=/content/journal/jgv/10.1099/jgv.0.002066&mimeType=html&fmt=ahah

References

  1. Guinet B, Leobold M, Herniou EA, Bloin P, Burlet N et al. A novel and diverse family of filamentous DNA viruses associated with parasitic wasps. Virus Evol 2024; 10:veae022 [View Article] [PubMed]
     [Google Scholar]
  2. Petersen JM, Bézier A, Drezen J-M, van Oers MM. The naked truth: an updated review on nudiviruses and their relationship to bracoviruses and baculoviruses. J Invertebr Pathol 2022; 189:107718 [View Article] [PubMed]
     [Google Scholar]
  3. 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]
  4. Huger AM. A new virus disease of crickets (Orthoptera: Gryllidae) causing macronucleosis of fatbody. J Invertebr Pathol 1985; 45:108–111 [View Article]
     [Google Scholar]
  5. Burand JP, Rallis CP, Tan W. Horizontal transmission of Hz-2V by virus infected Helicoverpa zea moths. J Invertebr Pathol 2004; 85:128–131 [View Article] [PubMed]
     [Google Scholar]
  6. Rallis CP, Burand JP. Pathology and ultrastructure of Hz-2V infection in the agonadal female corn earworm, Helicoverpa zea. J Invertebr Pathol 2002; 81:33–44 [View Article] [PubMed]
     [Google Scholar]
  7. Harrison RL, Herniou EA, Bézier A, Jehle JA, Burand JP et al. ICTV virus taxonomy profile: Nudiviridae. J Gen Virol 2020; 101:3–4 [View Article]
     [Google Scholar]
  8. Raina AK, Adams JR, Lupiani B, Lynn DE, Kim W et al. Further characterization of the gonad-specific virus of corn earworm, Helicoverpa zea. J Invertebr Pathol 2000; 76:6–12 [View Article]
     [Google Scholar]
  9. 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]
  10. Kelly DC, Lescott T, Ayres MD, Carey D, Coutts A et al. Induction of a nonoccluded baculovirus persistently infecting Heliothis zea cells by Heliothis armigera and Trichoplusia ni nuclear polyhedrosis viruses. Virol 1981; 112:174–189 [View Article] [PubMed]
     [Google Scholar]
  11. Granados RR, Lawler KA. In vivo pathway of Autographa californica baculovirus invasion and infection. Virol 1981; 108:297–308 [View Article] [PubMed]
     [Google Scholar]
  12. Ralston AL, Huang YS, Kawanishi CY. Cell culture studies with the IMC-Hz-1 nonoccluded virus. Virol 1981; 115:33–44 [View Article] [PubMed]
     [Google Scholar]
  13. Etebari K, Parry R, Beltran MJB, Furlong MJ. Genomic structural and transcriptional variation of Oryctes rhinoceros nudivirus (OrNV) in coconut rhinoceros beetle. Microbiol 20202020.05.27.119867 [View Article]
     [Google Scholar]
  14. Etebari K, Gharuka M, Asgari S, Furlong MJ. Diverse host immune responses of different geographical populations of the coconut rhinoceros beetle to Oryctes rhinoceros nudivirus (OrNV) infection. Microbiol Spectr 2021; 9:e0068621 [View Article] [PubMed]
     [Google Scholar]
  15. Etebari K, Parry R, Beltran MJB, Furlong MJ. Transcription profile and genomic variations of Oryctes rhinoceros nudivirus in coconut rhinoceros beetles. J Virol 2020; 94:e01097-20 [View Article] [PubMed]
     [Google Scholar]
  16. Bezier A, Annaheim M, Herbiniere J, Wetterwald C, Gyapay G et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 2009; 323:926–930 [View Article]
     [Google Scholar]
  17. Bézier A, Louis F, Jancek S, Periquet G, Thézé J et al. Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata : insights into the evolutionary dynamics of bracoviruses. Phil Trans R Soc B 2013; 368:20130047 [View Article]
     [Google Scholar]
  18. 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]
     [Google Scholar]
  19. Burke GR, Strand MR. Deep sequencing identifies viral and wasp genes with potential roles in replication of microplitis demolitor bracovirus. J Virol 2012; 86:3293–3306 [View Article]
     [Google Scholar]
  20. Cerqueira de Araujo A, Leobold M, Bézier A, Musset K, Uzbekov R et al. Conserved viral transcription plays a key role in virus-like particle production of the parasitoid wasp Venturia canescens. J Virol 2022; 96:e0052422 [View Article] [PubMed]
     [Google Scholar]
  21. Gauthier J, Boulain H, van Vugt JJFA, Baudry L, Persyn E et al. Author Correction: chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization. Commun Biol 2021; 4:1–15 [View Article]
     [Google Scholar]
  22. Mcintosh AH, Ignoffo CM. Characterization of five cell lines established from species of Heliothis. Appl entomol Zool 1983; 18:262–269 [View Article]
     [Google Scholar]
  23. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 1938; 27:493–497 [View Article]
     [Google Scholar]
  24. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
     [Google Scholar]
  25. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015; 12:357–360 [View Article] [PubMed]
     [Google Scholar]
  26. Cheng C-H, Liu S-M, Chow T-Y, Hsiao Y-Y, Wang D-P 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]
  27. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article]
     [Google Scholar]
  28. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 2015; 33:290–295 [View Article] [PubMed]
     [Google Scholar]
  29. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 2016; 11:1650–1667 [View Article] [PubMed]
     [Google Scholar]
  30. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 2015; 43:e47 [View Article]
     [Google Scholar]
  31. Law CW, Chen Y, Shi W, Smyth GK. Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 2014; 15:R29 [View Article] [PubMed]
     [Google Scholar]
  32. Szklarczyk D, Kirsch R, Koutrouli M, Nastou K, Mehryary F et al. The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res 2023; 51:D638–D646 [View Article] [PubMed]
     [Google Scholar]
  33. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
     [Google Scholar]
  34. Kolde R, Kolde MR. Package ‘pheatmap'. R package 2015; 1:790
     [Google Scholar]
  35. Charrad M, Ghazzali N, Boiteau V, Niknafs A. NbClust: an R package for determining the relevant number of clusters in a data set. J Stat Softw 2014; 61:1–36 [View Article]
     [Google Scholar]
  36. Bailey TL, Johnson J, Grant CE, Noble WS. The MEME suite. Nucleic Acids Res 2015; 43:W39–49 [View Article]
     [Google Scholar]
  37. McLeay RC, Bailey TL. Motif enrichment analysis: a unified framework and an evaluation on chip data. BMC Bioinf 2010; 11:165 [View Article]
     [Google Scholar]
  38. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. Quantifying similarity between motifs. Genome Biol 2007; 8:1–9 [View Article]
     [Google Scholar]
  39. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011; 27:1017–1018 [View Article] [PubMed]
     [Google Scholar]
  40. Lu Z, Berry K, Hu Z, Zhan Y, Ahn TH et al. TSSr: an R package for comprehensive analyses of TSS sequencing data. NAR Genom Bioinform 2021; 3:lqab108 [View Article]
     [Google Scholar]
  41. Chevignon G, Thézé J, Cambier S, Poulain J, Da Silva C et al. Functional annotation of Cotesia congregata bracovirus: identification of viral genes expressed in parasitized host immune tissues. J Virol 2014; 88:8795–8812 [View Article] [PubMed]
     [Google Scholar]
  42. Shrestha A, Bao K, Chen W, Wang P, Fei Z et al. Transcriptional responses of the Trichoplusia ni midgut to oral infection by the Baculovirus Autographa californica multiple nucleopolyhedrovirus. J Virol 2019; 93:10 [View Article] [PubMed]
     [Google Scholar]
  43. Rivas HG, Schmaling SK, Gaglia MM. Shutoff of host gene expression in influenza A virus and herpesviruses: similar mechanisms and common themes. Viruses 2016; 8:102 [View Article]
     [Google Scholar]
  44. Wu YL, Wu CP, Liu CY, Lee ST, Lee HP et al. Heliothis zea nudivirus 1 gene hhi1 induces apoptosis which is blocked by the hz-iap2 gene and a noncoding gene, pag1. J Virol 2011; 85:6856–6866 [View Article]
     [Google Scholar]
  45. Burke GR, Walden KKO, Whitfield JB, Robertson HM, Strand MR. Widespread genome reorganization of an obligate virus mutualist. PLoS Genet 2014; 10:e1004660 [View Article]
     [Google Scholar]
  46. Hefferon KL. Baculovirus late expression factors. Microb Physiol 2004; 7:89–101 [View Article]
     [Google Scholar]
  47. Yang Y-T, Lee D-Y, Wang Y, Hu J-M, Li W-H 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]
  48. Kariithi HM, Meki IK, Boucias DG, Abd-Alla AM. Hytrosaviruses: current status and perspective. Curr Opin Insect Sci 2017; 22:71–78 [View Article] [PubMed]
     [Google Scholar]
  49. Tomalski MD, Wu JG, Miller LK. The location, sequence, transcription, and regulation of a baculovirus DNA polymerase gene. Virol 1988; 167:591–600 [View Article] [PubMed]
     [Google Scholar]
  50. Chen R, Wang H, Mansky LM. Roles of uracil-DNA glycosylase and dUTPase in virus replication. J Gen Virol 2002; 83:2339–2345 [View Article] [PubMed]
     [Google Scholar]
  51. Chu E, Allegra CJ. The role of thymidylate synthase as an RNA binding protein. Bioessays 1996; 18:191–198 [View Article] [PubMed]
     [Google Scholar]
  52. Chen HH, Tso DJ, Yeh WB, Cheng HJ, Wu TF. The thymidylate synthase gene of Hz‐1 virus: A gene captured from its lepidopteran host. Insect Molecular Biology 2001; 10:495–503 [View Article]
     [Google Scholar]
  53. Eriksson S, Munch-Petersen B, Johansson K, Ecklund H. Structure and function of cellular deoxyribonucleoside kinases. Cell Mol Life Sci 2002; 59:1327–1346 [View Article]
     [Google Scholar]
  54. Wintersberger E. Regulation and biological function of thymidine kinase. Biochem Soc Trans 1997; 25:303–308 [View Article]
     [Google Scholar]
  55. Reichard P. Interactions between deoxyribonucleotide and DNA synthesis. Annu Rev Biochem 1988; 57:349–374 [View Article] [PubMed]
     [Google Scholar]
  56. Reichard P. Ribonucleotide reductase and deoxyribonucleotide pools. Basic Life Sci 1985; 31:33–45 [View Article] [PubMed]
     [Google Scholar]
  57. Wu DD, Zhang YP. Eukaryotic origin of a metabolic pathway in virus by horizontal gene transfer. Genomics 2011; 98:367–369 [View Article] [PubMed]
     [Google Scholar]
  58. Slack J, Arif BM. The baculoviruses occlusion‐derived virus: virion structure and function. Adv Virus Res 2006; 69:99–165 [View Article]
     [Google Scholar]
  59. Seo D, Gammon DB. Manipulation of host microtubule networks by viral microtubule-associated proteins. Viruses 2022; 14:979 [View Article] [PubMed]
     [Google Scholar]
  60. Wang X, Liu X, Makalliwa GA, Li J, Wang H et al. Per os infectivity factors: a complicated and evolutionarily conserved entry machinery of baculovirus. Sci China Life Sci 2017; 60:806–815 [View Article] [PubMed]
     [Google Scholar]
  61. Boogaard B, van Oers MM, van Lent JWM. An advanced view on baculovirus per os infectivity factors. Insects 2018; 9:84 [View Article] [PubMed]
     [Google Scholar]
  62. Kariithi HM, van Oers MM, Vlak JM, Vreysen MJB, Parker AG et al. Virology, epidemiology and pathology of Glossina hytrosavirus, and its control prospects in laboratory colonies of the tsetse fly, Glossina pallidipes (diptera; glossinidae). Insects 2013; 4:287–319 [View Article] [PubMed]
     [Google Scholar]
  63. Wu W, Lin T, Pan L, Yu M, Li Z et al. Autographa californica multiple nucleopolyhedrovirus nucleocapsid assembly is interrupted upon deletion of the 38K gene. J Virol 2006; 80:11475–11485 [View Article] [PubMed]
     [Google Scholar]
  64. 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]
  65. Jiantao L, Zhu L, Zhang S, Deng Z, Huang Z et al. The Autographa californica multiple nucleopolyhedrovirus ac110 gene encodes a new per os infectivity factor. Virus Research 2016; 221:30–37 [View Article]
     [Google Scholar]
  66. Zhang H, Kuang W, Fu C, Li J, Wang M et al. AC81 Is a putative disulfide isomerase involved in baculoviral disulfide bond formation. J Virol 2022; 96:e0116722 [View Article] [PubMed]
     [Google Scholar]
  67. Russell RLQ, Rohrmann GF. Characterization of P91, a protein associated with virions of an Orgyia pseudotsugata baculovirus. Virol 1997; 233:210–223 [View Article]
     [Google Scholar]
  68. Wang M, Tuladhar E, Shen S, Wang H, van Oers MM et al. Specificity of baculovirus P6.9 basic DNA-binding proteins and critical role of the C terminus in virion formation. J Virol 2010; 84:8821–8828 [View Article] [PubMed]
     [Google Scholar]
  69. Kim W. Characterization of Genome and Structural Proteins of the Sexually Transmitted Insect Virus,Hz-2V University of Massachusetts Amherst; 2009
     [Google Scholar]
  70. 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]
  71. Dong F, Wang J, Deng R, Wang X. Autographa californica multiple nucleopolyhedrovirus gene ac81 is required for nucleocapsid envelopment. Virus Res 2016; 221:47–57 [View Article]
     [Google Scholar]
  72. Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A et al. New developments in the InterPro database. Nucleic Acids Res 2007; 35:D224–D228 [View Article]
     [Google Scholar]
  73. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–W37 [View Article]
     [Google Scholar]
  74. Byers NM, Vandergaast RL, Friesen PD. Baculovirus inhibitor-of-apoptosis Op-IAP3 blocks apoptosis by interaction with and stabilization of a host insect cellular IAP. J Virol 2016; 90:533–544 [View Article]
     [Google Scholar]
  75. Boogaard B, van Lent JWM, Theilmann DA, Erlandson MA, van Oers MM. Baculoviruses require an intact ODV entry-complex to resist proteolytic degradation of per os infectivity factors by co-occluded proteases from the larval host. J Gen Virol 2017; 98:3101–3110 [View Article] [PubMed]
     [Google Scholar]
  76. 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]
  77. Guarino LA, Xu B, Jin J, Dong W. A virus-encoded RNA polymerase purified from baculovirus-infected cells. J Virol 1998; 72:7985–7991 [View Article] [PubMed]
     [Google Scholar]
  78. Berretta MF, Ferrelli ML, Salvador R, Sciocco A, Romanowski V. Baculovirus gene expression. In Current Issues in Molecular Virology-Viral Genetics and Biotechnological Applications: IntechOpen 2013
     [Google Scholar]
  79. Kelly BJ, King LA, Possee RD. Introduction to baculovirus molecular biology. Methods Mol Biol 2016; 1350:25–50 [View Article] [PubMed]
     [Google Scholar]
  80. Chaitanya K. Structure and Organization of Virus Genomes. Genome and Genomics: From Archaea to Eukaryotes Singapur: Springer; 2019 pp 1–30
     [Google Scholar]
  81. Kumar JP. The sine oculis homeobox (SIX) family of transcription factors as regulators of development and disease. Cell Mol Life Sci 2009; 66:565–583 [View Article] [PubMed]
     [Google Scholar]
  82. Jusiak B, Wang F, Karandikar UC, Kwak S-J, Wang H et al. Genome-wide DNA binding pattern of the homeodomain transcription factor sine oculis (So) in the developing eye of Drosophila melanogaster. Genom Data 2014; 2:153–155 [View Article] [PubMed]
     [Google Scholar]
  83. Oliver G, Mailhos A, Wehr R, Copeland NG, Jenkins NA et al. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Devt 1995; 121:4045–4055 [View Article]
     [Google Scholar]
  84. Jones JDG, Dangl JL. The plant immune system. Nature 2006; 444:323–329 [View Article]
     [Google Scholar]
  85. Fei Q, Zhang Y, Xia R, Meyers BC. Small RNAs add zing to the zig-zag-zig model of plant defenses. MPMI 2016; 29:165–169 [View Article]
     [Google Scholar]
  86. Pritchard L, Birch PRJ. The zigzag model of plant-microbe interactions: is it time to move on?. Mol Plant Pathol 2014; 15:865–870 [View Article] [PubMed]
     [Google Scholar]
  87. Jin S, Cheng T, Jiang L, Lin P, Yang Q et al. Identification of a new sprouty protein responsible for the inhibition of the Bombyx mori nucleopolyhedrovirus reproduction. PLoS ONE 2014; 9:e99200 [View Article]
     [Google Scholar]
  88. Sánchez EG, Quintas A, Nogal M, Castelló A, Revilla Y. African swine fever virus controls the host transcription and cellular machinery of protein synthesis. Virus Res 2013; 173:58–75 [View Article] [PubMed]
     [Google Scholar]
  89. McGrath J, Roy P, Perrin BJ. Stereocilia morphogenesis and maintenance through regulation of actin stability. Semin Cell Dev Biol 2017; 65:88–95 [View Article] [PubMed]
     [Google Scholar]
  90. Volkman LE. Baculovirus infectivity and the actin cytoskeleton. Curr Drug Targets 2007; 8:1075–1083 [View Article] [PubMed]
     [Google Scholar]
  91. Horníková L, Bruštíková K, Huérfano S, Forstová J. Nuclear cytoskeleton in virus infection. Int J Mol Sci 2022; 23:578 [View Article] [PubMed]
     [Google Scholar]
  92. Khorramnejad A, Perdomo HD, Palatini U, Bonizzoni M, Gasmi L. Cross talk between viruses and insect cells cytoskeleton. Viruses 2021; 13:1658 [View Article] [PubMed]
     [Google Scholar]
  93. Xing L, Yuan C, Wang M, Lin Z, Shen B et al. Dynamics of the interaction between cotton bollworm Helicoverpa armigera and nucleopolyhedrovirus as revealed by integrated transcriptomic and proteomic analyses. Mol Cell Proteomics 2017; 16:1009–1028 [View Article] [PubMed]
     [Google Scholar]
  94. Feng M, Fei S, Xia J, Zhang M, Wu H et al. Global metabolic profiling of baculovirus infection in silkworm hemolymph shows the importance of amino-acid metabolism. Viruses 2021; 13:841 [View Article] [PubMed]
     [Google Scholar]
  95. Mayer KA, Stöckl J, Zlabinger GJ, Gualdoni GA. Hijacking the supplies: metabolism as a novel facet of virus-host interaction. Front Immunol 2019; 10:1533 [View Article] [PubMed]
     [Google Scholar]
  96. Thaker SK, Ch’ng J, Christofk HR. Viral hijacking of cellular metabolism. BMC Biol 2019; 17:59 [View Article] [PubMed]
     [Google Scholar]
  97. Sanchez EL, Lagunoff M. Viral activation of cellular metabolism. Virol 2015; 479–480:609–618 [View Article] [PubMed]
     [Google Scholar]
  98. Dubrez L, Causse S, Borges Bonan N, Dumétier B, Garrido C. Heat-shock proteins: chaperoning DNA repair. Oncogene 2020; 39:516–529 [View Article] [PubMed]
     [Google Scholar]
  99. Haslbeck M, Vierling E. A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 2015; 427:1537–1548 [View Article] [PubMed]
     [Google Scholar]
  100. Zhao L, Jones W. Expression of heat shock protein genes in insect stress responses. Invertebr Surviv J 2012; 9:93–101
     [Google Scholar]
  101. Merkling SH, Overheul GJ, van Mierlo JT, Arends D, Gilissen C et al. The heat shock response restricts virus infection in Drosophila. Sci Rep 2015; 5:12758 [View Article] [PubMed]
     [Google Scholar]
  102. Janewanthanakul S, Supungul P, Tang S, Tassanakajon A. Heat shock protein 70 from Litopenaeus vannamei (LvHSP70) is involved in the innate immune response against white spot syndrome virus (WSSV) infection. Dev Comp Immunol 2020; 102:103476 [View Article] [PubMed]
     [Google Scholar]
  103. Lyupina YV, Zatsepina OG, Timokhova AV, Orlova OV, Kostyuchenko MV et al. New insights into the induction of the heat shock proteins in baculovirus infected insect cells. Virol 2011; 421:34–41 [View Article] [PubMed]
     [Google Scholar]
  104. Cao M, Wei C, Zhao L, Wang J, Jia Q et al. DnaJA1/Hsp40 is co-opted by influenza A virus to enhance its viral RNA polymerase activity. J Virol 2014; 88:14078–14089 [View Article]
     [Google Scholar]
  105. Khachatoorian R, French SW. Chaperones in hepatitis C virus infection. World J Hepatol 2016; 8:9–35 [View Article] [PubMed]
     [Google Scholar]
  106. Oka OBV, Pringle MA, Schopp IM, Braakman I, Bulleid NJ. ERdj5 is the ER reductase that catalyzes the removal of non-native disulfides and correct folding of the LDL receptor. Mol Cell 2013; 50:793–804 [View Article] [PubMed]
     [Google Scholar]
  107. Sohn S-Y, Kim J-H, Baek K-W, Ryu W-S, Ahn B-Y. Turnover of hepatitis B virus X protein is facilitated by Hdj1, a human Hsp40/DnaJ protein. Biochem Biophys Res Commun 2006; 347:764–768 [View Article] [PubMed]
     [Google Scholar]
  108. Lyupina YV, Dmitrieva SB, Timokhova AV, Beljelarskaya SN, Zatsepina OG et al. An important role of the heat shock response in infected cells for replication of baculoviruses. Virol 2010; 406:336–341 [View Article] [PubMed]
     [Google Scholar]
  109. Xiao A, Wong J, Luo H. Viral interaction with molecular chaperones: role in regulating viral infection. Arch Virol 2010; 155:1021–1031 [View Article] [PubMed]
     [Google Scholar]
  110. Kurzik-Dumke U, Lohmann E. Sequence of the new Drosophila melanogaster small heat-shock-related gene, lethal(2) essential for life [l(2)efl], at locus 59F4,5. Gene 1995; 154:171–175 [View Article] [PubMed]
     [Google Scholar]
  111. Raut S, Mallik B, Parichha A, Amrutha V, Sahi C et al. RNAi-mediated reverse genetic screen identified Drosophila chaperones regulating eye and neuromuscular junction morphology. G3: Genes, Genomes, Genetics 2017; 7:2023–2038 [View Article]
     [Google Scholar]
  112. Brutscher LM, Daughenbaugh KF, Flenniken ML. Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense. Sci Rep 2017; 7:6448 [View Article] [PubMed]
     [Google Scholar]
  113. Lopez W, Page AM, Carlson DJ, Ericson BL, Cserhati MF et al. Analysis of immune-related genes during Nora virus infection of Drosophila melanogaster using next generation sequencing. AIMS Microbiol 2018; 4:123–139 [View Article] [PubMed]
     [Google Scholar]
  114. Runtuwene LR, Kawashima S, Pijoh VD, Tuda JSB, Hayashida K et al. The lethal(2)-essential-for-life [L(2)EFL] gene family modulates dengue virus infection in Aedes aegypti. IJMS 2020; 21:7520 [View Article]
     [Google Scholar]
  115. Mayer MP. Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev Physiol Biochem Pharmacol 2005; 153:1–46 [View Article] [PubMed]
     [Google Scholar]
  116. Yingsunthonwattana W, Junprung W, Supungul P, Tassanakajon A. Heat shock protein 90 of Pacific white shrimp (Litopenaeus vannamei) is possibly involved in promoting white spot syndrome virus infection. Fish Shellfish Immunol 2022; 128:405–418 [View Article]
     [Google Scholar]
  117. Nikapitiya C, Dorrington T, Gómez-Chiarri M. The role of histones in the immune responses of aquatic invertebrates. Invertebr Surviv J 2013; 10:94–101
     [Google Scholar]
  118. Wolffe AP, Hayes JJ. Chromatin disruption and modification. Nucleic Acid Res 1999; 27:711–720 [View Article]
     [Google Scholar]
  119. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin?. J Cell Biol 2012; 198:773–783 [View Article]
     [Google Scholar]
  120. Parseghian MH, Luhrs KA. Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 2006; 84:589–604 [View Article] [PubMed]
     [Google Scholar]
  121. Encinas-García T, Loreto-Quiroz DL, Mendoza-Cano F, Peña-Rodriguez A, Fimbres-Olivarria D et al. White spot syndrome virus down-regulates expression of histones H2A and H4 of Penaeus vannamei to promote viral replication. Dis Aquat Organ 2019; 137:73–79 [View Article] [PubMed]
     [Google Scholar]
  122. Nayyar N, Kaur I, Malhotra P, Bhatnagar RK. Quantitative proteomics of Sf21 cells during baculovirus infection reveals progressive host proteome changes and its regulation by viral miRNA. Sci Rep 2017; 7:10902 [View Article] [PubMed]
     [Google Scholar]
  123. Ooi BG, Miller LK. Regulation of host RNA levels during baculovirus infection. Virol 1988; 166:515–523 [View Article] [PubMed]
     [Google Scholar]
  124. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 2009; 27:84–90 [View Article] [PubMed]
     [Google Scholar]
  125. Kasai S, Scott JG. A house fly gene homologous to the zinc finger proto-oncogene Gfi-1. Biochem Biophys Res Commun 2001; 283:644–647 [View Article] [PubMed]
     [Google Scholar]
  126. Tanada Y, Hess RT. Granulosis Viruses. Atlas of Invertebrate Viruses. In Baculoviridae CRC Press; 2017 pp 227–257 [View Article]
     [Google Scholar]
  127. Winstanley D, Crook NE. Replication of Cydia pomonella granulosis virus in cell cultures. J Gen Virol 1993; 74 (Pt 8):1599–1609 [View Article] [PubMed]
     [Google Scholar]
  128. Henikoff S, Ahmad K. Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 2005; 21:133–153 [View Article]
     [Google Scholar]
  129. Lee GE, Byun J, Lee CJ, Cho YY. Molecular mechanisms for the regulation of nuclear membrane integrity. IJMS 2023; 24:15497 [View Article]
     [Google Scholar]
  130. Simões M, Rino J, Pinheiro I, Martins C, Ferreira F. Alterations of nuclear architecture and epigenetic signatures during African swine fever virus infection. Viruses 2015; 7:4978–4996 [View Article]
     [Google Scholar]
  131. Porwal M, Cohen S, Snoussi K, Popa-Wagner R, Anderson F et al. Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog 2013; 9:e1003671 [View Article]
     [Google Scholar]
  132. Silva L, Cliffe A, Chang L, Knipe DM. Role for A-type lamins in herpesviral DNA targeting and heterochromatin modulation. PLoS Pathog 2008; 4:e1000071 [View Article]
     [Google Scholar]
  133. Cibulka J, Fraiberk M, Forstova J. Nuclear actin and lamins in viral infections. Viruses 2012; 4:325–347 [View Article]
     [Google Scholar]
  134. Snoussi K, Kann M. Interaction of parvoviruses with the nuclear envelope. Adv Biol Regul 2014; 54:39–49 [View Article] [PubMed]
     [Google Scholar]
  135. Bézier A, Herbinière J, Lanzrein B, Drezen J-M. Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. J Invertebr Pathol 2009; 101:194–203 [View Article] [PubMed]
     [Google Scholar]
  136. Wyler T, Lanzrein B. Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. II. Ultrastructural analysis of calyx cell development, virion formation and release. J Gen Virol 2003; 84:1151–1163 [View Article]
     [Google Scholar]
  137. Christen U. Molecular mimicry. In Autoantibodies Elsevier; 2014 pp 35–42
     [Google Scholar]
  138. Gad W, Kim Y. A viral histone H4 encoded by Cotesia plutellae bracovirus inhibits haemocyte-spreading behaviour of the diamondback moth, Plutella xylostella. J Gen Virol 2008; 89:931–938 [View Article]
     [Google Scholar]
  139. Kim J, Kim Y. Transient expression of a viral histone H4, CpBV-H4, suppresses immune-associated genes of Plutella xylostella and Spodoptera exigua. J Asia Pac Entomol 2010; 13:313–318 [View Article]
     [Google Scholar]
  140. Avgousti DC, Della Fera AN, Otter CJ, Herrmann C, Pancholi NJ et al. Adenovirus core protein VII downregulates the DNA damage response on the host genome. J Virol 2017; 91:10 [View Article] [PubMed]
     [Google Scholar]
  141. Kulej K, Avgousti DC, Sidoli S, Herrmann C, Della Fera AN et al. Time-resolved global and chromatin proteomics during herpes simplex virus type 1 (HSV-1) infection. Mol Cell Proteomics 2017; 16:S92–S107 [View Article] [PubMed]
     [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.002066
Loading
Transcriptional dynamics during Heliothis zea nudivirus 1 infection in an ovarian cell line from Helicoverpa zea
J. Gen. Virol. 106, 002066 (2025); https://doi.org/10.1099/jgv.0.002066
/content/journal/jgv/10.1099/jgv.0.002066
/content/journal/jgv/10.1099/jgv.0.002066
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed

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