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Baculovirus genes affecting host function

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Abstract

Baculoviruses are insect-specific viruses. These large DNA viruses encode many genes in addition to those required to replicate and build new virions. These auxiliary genes provide selective advantages to the virus for invading and infecting host insects. Eight of these genes, which help the virus overcome insect defenses against invasion, are discussed. These include genes whose products help the virus traverse physical or physiological barriers and those that overcome host immune defenses.

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References

  • Afonso C. L.; Tulman E. R.; Lu Z.; Balinsky C. A.; Moser B. A.; Becnel J. J.; Rock D. L.; Kutish G. F. Genome sequence of a baculovirus pathogenic for Culex nigripalpus. J. Virol. 75: 11157–11165; 2001. doi:10.1128/JVI.75.22.11157-11165.2001.

    PubMed  CAS  Google Scholar 

  • Barber G. N. Host defense, viruses and apoptosis. Cell Death Differ. 8: 113–126; 2001. doi:10.1038/sj.cdd.4400823.

    PubMed  CAS  Google Scholar 

  • Bergan V.; Jagus R.; Lauksund S.; Kileng O.; Robertsen B. The Atlantic salmon Z-DNA binding protein kinase phosphorylates translation initiation factor 2 alpha and constitutes a unique orthologue to the mammalian dsRNA-activated protein kinase R. FEBS Journal 275: 184–197; 2008.

    PubMed  CAS  Google Scholar 

  • Bertin J.; Mendrysa S. M.; LaCount D. J.; Gaur S.; Krebs J. F.; Armstrong R. C.; Tomaselli K. J.; Friesen P. D. Apoptotic suppression by baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like protease. J. Virol. 70: 6251–6259; 1996.

    PubMed  CAS  Google Scholar 

  • Birnbaum M. J.; Clem R. J.; Miller L. K. An Apoptosis-Inhibiting Gene from a Nuclear Polyhedrosis-virus encoding a polypeptide with Cys/His sequence motif. J. Virol. 68: 2521–2528; 1994.

    PubMed  CAS  Google Scholar 

  • Bischoff D. S.; Slavicek J. M. Molecular analysis of an enhancin gene in the Lymantria dispar nuclear polyhedrosis virus. J. Virol. 71: 8133–8140; 1997.

    PubMed  CAS  Google Scholar 

  • Blair J. E.; Hedges S. B. Molecular phylogeny and divergence times of deuterostome animals. Mol. Biol. Evol. 22: 2275–2284; 2005. doi:10.1093/molbev/msi225.

    PubMed  CAS  Google Scholar 

  • Bump N. J.; Hackett M.; Hugunin M.; Seshagiri S.; Brady K.; Chen P.; Ferenz C.; Franklin S.; Ghayur T.; Li P.; Licari P.; Mankovich J.; Shi L. F.; Greenberg A. H.; Miller L. K.; Wong W. W. Inhibition of ICE family proteases by baculovirus antiapoptotic protein P35. Science 269: 1885–1888; 1995. doi:10.1126/science.7569933.

    PubMed  CAS  Google Scholar 

  • Campbell, C. L.; Keene, K. M.; Brackney, D. E.; Olson, K. E.; Blair, C. D.; Wilusz, J.; Foy, B. D. Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol. 8: 47; 2008.

    Google Scholar 

  • Chen C. J.; Quentin M. E.; Brennan L. A.; Kukel C.; Thiem S. M. Lymantria dispar nucleopolyhedrovirus hrf-1 expands the larval host range of Autographa californica nucleopolyhedrovirus. J. Virol. 72: 2526–2531; 1998.

    PubMed  CAS  Google Scholar 

  • Chen J.-Y.; Bottjer D. J.; Oliveri P.; Dornbos S. Q.; Gao F.; Ruffins S.; Chi H.; Li C.-W.; Davidson E. H. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305: 218–222; 2004. doi:10.1126/science.1099213.

    PubMed  CAS  Google Scholar 

  • Chen Y.-R.; Wu C.-Y.; Lee S.-T.; Wu Y.-J.; Lo C.-F.; Tsai M.-F.; Wang C.-H. Genomic and host range studies of Maruca vitrata nucleopolyhedrovirus. J. Gen. Virol. 89: 2315–2330; 2008. doi:10.1099/vir.0.2008/001412-0.

    PubMed  CAS  Google Scholar 

  • Cheng G. F.; Feng Z. D.; Bin H. Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2 alpha dephosphorylation by the gamma(1)34.5 protein. J. Virol. 79: 1379–1388; 2005. doi:10.1128/JVI.79.3.1379-1388.2005.

    PubMed  CAS  Google Scholar 

  • Clem R. J. Baculoviruses and apoptosis: the good, the bad, and the ugly. Cell Death Differ. 8: 137–143; 2001. doi:10.1038/sj.cdd.4400821.

    PubMed  CAS  Google Scholar 

  • Clem, R. J. The role of apoptosis in defense against baculovirus infection in insects. In: Griffin, D. (ed) Role of apoptosis in infection. Springer, Berlin, pp 113–129; 2005.

  • Clem R. J. Baculoviruses and apoptosis: a diversity of genes and responses. Curr. Drug Targets 8: 1069–1074; 2007. doi:10.2174/138945007782151405.

    PubMed  CAS  Google Scholar 

  • Clem R. J.; Fechheimer M.; Miller L. K. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254: 1388–1390; 1991. doi:10.1126/science.1962198.

    PubMed  CAS  Google Scholar 

  • Crook N. E.; Clem R. J.; Miller L. K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67: 2168–2174; 1993.

    PubMed  CAS  Google Scholar 

  • Detvisitsakun C.; Berretta M. F.; Lehiy C.; Passarelli A. L. Stimulation of cell motility by a viral fibroblast growth factor homolog: proposal for a role in viral pathogenesis. Virology 336: 308–317; 2005. doi:10.1016/j.virol.2005.03.013.

    PubMed  CAS  Google Scholar 

  • Detvisitsakun C.; Hutfless E. L.; Berretta M. F.; Passarelli A. L. Analysis of a baculovirus lacking a functional viral fibroblast growth factor homolog. Virology 346: 258–265; 2006. doi:10.1016/j.virol.2006.01.016.

    PubMed  CAS  Google Scholar 

  • Dever T. E.; Sripriya R.; McLachlin J. R.; Lu J. F.; Fabian J. R.; Kimball S. R.; Miller L. K. Disruption of cellular translational control by a viral truncated eukaryotic translation initiation factor 2 alpha kinase homolog. Proc. Natl. Acad. Sci. U. S. A. 95: 4164–4169; 1998. doi:10.1073/pnas.95.8.4164.

    PubMed  CAS  Google Scholar 

  • Dickson J. A.; Friesen P. D. Identification of upstream promoter elements mediating early transcription from the 35,000-molecular-weight protein gene of Autographa californica nuclear polyhedrosis virus. J. Virol. 65: 4006–4016; 1991.

    PubMed  CAS  Google Scholar 

  • Dimarcq J. L.; Imler J. L.; Lanot R.; Ezekowitz R. A. B.; Hoffmann J. A.; Janeway C. A.; Lagueux M. Treatment of l(2)mbn Drosophila tumorous blood cells with the steroid hormone ecdysone amplifies the inducibility of antimicrobial peptide gene expression. Insect Biochem. Mol. Biol. 27: 877–886; 1997. doi:10.1016/S0965-1748(97)00072-6.

    PubMed  CAS  Google Scholar 

  • Dostert C.; Jouanguy E.; Irving P.; Troxler L.; Galiana-Arnoux D.; Hetru C.; Hoffmann J. A.; Imler J. L. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 6: 946–953; 2005. doi:10.1038/ni1237.

    PubMed  CAS  Google Scholar 

  • Douzery E. J. P.; Snell E. A.; Bapteste E.; Delsuc F. D. R.; Philippe H. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc. Natl. Acad. Sci. U. S. A. 101: 15386–15391; 2004. doi:10.1073/pnas.0403984101.

    PubMed  CAS  Google Scholar 

  • Du Q. S.; Lehavi D.; Faktor O.; Qi Y. P.; Chejanovsky N. Isolation of an apoptosis suppressor gene of the Spodoptera littoralis nucleopolyhedrovirus. J. Virol. 73: 1278–1285; 1999.

    PubMed  CAS  Google Scholar 

  • Du X. L.; Thiem S. M. Responses of insect cells to baculovirus infection: protein synthesis shutdown and apoptosis. J. Virol. 71: 7866–7872; 1997.

    PubMed  CAS  Google Scholar 

  • Duckett C. S.; Nava V. E.; Gedrich R. W.; Clem R. J.; VanDongen J. L.; Gilfillan M. C.; Shiels H.; Hardwick J. M.; Thompson C. B. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. Embo J. 15: 2685–2694; 1996.

    PubMed  CAS  Google Scholar 

  • Engelhard E. K.; Kammorgan L. N. W.; Washburn J. O.; Volkman L. E. The insect tracheal system—a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc. Natl. Acad. Sci. U. S. A. 91: 3224–3227; 1994. doi:10.1073/pnas.91.8.3224.

    PubMed  CAS  Google Scholar 

  • Escasa S. R.; Lauzon H. A. M.; Mathur A. C.; Krell P. J.; Arif B. M. Sequence analysis of the Choristoneura occidentalis granulovirus genome. J. Gen. Virol. 87: 1917–1933; 2006. doi:10.1099/vir.0.81792-0.

    PubMed  CAS  Google Scholar 

  • Federici B. A. Baculovirus pathogenesis. In: Miller L. K. (ed) The baculoviruses. Plenum, New York, pp 33–59; 1997.

    Google Scholar 

  • Federici B. A.; Stern V. M. Replication and occlusion of a granulosis virus in larval and adult midgut epithelium of the Western grapeleaf skeletonizer, Harrisina brillians. J. Invertebr. Pathol. 56: 401–414; 1990. doi:10.1016/0022-2011(90)90128-S.

    Google Scholar 

  • Fisher A. J.; dela Cruz W.; Zoog S. J.; Schneider C. L.; Friesen P. D. Crystal structure of baculovirus P35: role of a novel reactive site loop in apoptotic caspase inhibition. EMBO J. 18: 2031–2039; 1999. doi:10.1093/emboj/18.8.2031.

    PubMed  CAS  Google Scholar 

  • Flatt T.; Heyland A.; Rus F.; Porpiglia E.; Sherlock C.; Yamamoto R.; Garbuzov A.; Palli S. R.; Tatar M.; Silverman N. Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J. Exp. Biol. 211: 2712–2724; 2008. doi:10.1242/jeb.014878.

    PubMed  CAS  Google Scholar 

  • Flipsen J. T. M.; Martens J. W. M.; Vanoers M. M.; Vlak J. M.; Vanlent J. W. M. Passage of Autographa californica nuclear polyhedrosis virus through the midgut epithelium of Spodoptera exigua larvae. Virology 208: 328–335; 1995. doi:10.1006/viro.1995.1156.

    PubMed  CAS  Google Scholar 

  • Friesen P. D. Insect viruses. In: Knipe D. M.; Howley P. M. (eds) Fields virology. 5th ed. Lippincott Williams & Wilkins, Philadelphia, pp 707–736; 2007.

    Google Scholar 

  • Friesen P. D.; Miller L. K. Divergent transcription of early 35-kilodalton and 94-kilodalton protein genes encoded by the Hindiii K genome fragment of the Bbaculovirus Autographa californica nuclear polyhedrosis virus. J. Virol. 61: 2264–2272; 1987.

    PubMed  CAS  Google Scholar 

  • Galiana-Arnoux D.; Dostert C.; Schneemann A.; Hoffmann J. A.; Imler J. L. Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat. Immunol. 7: 590–597; 2006. doi:10.1038/ni1335.

    PubMed  CAS  Google Scholar 

  • Galloway C. S.; Wang P.; Winstanley D.; Jones I. M. Comparison of the bacterial Enhancin-like proteins from Yersinia and Bacillus spp. with a baculovirus Enhancin. J. Invertebr. Pathol. 90: 134–137; 2005. doi:10.1016/j.jip.2005.06.008.

    PubMed  CAS  Google Scholar 

  • Garcia M. A.; Meurs E. F.; Esteban M. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89: 799–811; 2007. doi:10.1016/j.biochi.2007.03.001.

    PubMed  CAS  Google Scholar 

  • Garcia-Maruniak A.; Maruniak J. E.; Zanotto P. M. A.; Doumbouya A. E.; Liu J. C.; Merritt T. A.; Lanoie J. S. Sequence analysis of the genome of the Neodiprion sertifer nucleopolyhedrovirus. J. Virol. 78: 7036–7051; 2004. doi:10.1128/JVI.78.13.7036-7051.2004.

    PubMed  CAS  Google Scholar 

  • Gillespie J. P.; Kanost M. R.; Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611–643; 1997. doi:10.1146/annurev.ento.42.1.611.

    PubMed  CAS  Google Scholar 

  • Goodwin R. H.; Tompkins G. J.; McCawley P. Gypsy moth cell lines divergent in viral susceptibility. 1. Culture and identification. In Vitro 14: 485–494; 1978.

    PubMed  CAS  Google Scholar 

  • Granados R. R. Early events in infection of Heliothis zea midgut cells by a baculovirus. Virology 90: 170–174; 1978. doi:10.1016/0042-6822(78)90347-1.

    PubMed  CAS  Google Scholar 

  • Granados R. R. Infectivity and mode of action of baculoviruses. Biotechnol. Bioeng. 22: 1377–1405; 1980. doi:10.1002/bit.260220707.

    Google Scholar 

  • Green M. C.; Monser K. P.; Clem R. J. Ubiquitin protein ligase activity of the anti-apoptotic baculovirus protein Op-IAP3. Virus Res. 105: 89–96; 2004. doi:10.1016/j.virusres.2004.04.017.

    PubMed  CAS  Google Scholar 

  • Gröner A. Specificity and safety of baculoviruses. In: Granados R. R.; Federici B. A. (eds) The biology of baculoviruses, vol. 1: biological properties and molecular biology. CRC, Boca Raton, pp 177–202; 1986.

    Google Scholar 

  • Guy M. P.; Friesen P. D. Reactive-site cleavage residues confer target specificity to baculovirus P49, a dimeric member of the P35 family of caspase inhibitors. J. Virol. 82: 7504–7514; 2008. doi:10.1128/JVI.00231-08.

    PubMed  CAS  Google Scholar 

  • Guzo D.; Rathburn H.; Guthrie K.; Dougherty E. Viral and host cellular transcription in Autographa californica nuclear polyhedrosis virus-infected gypsy moth cell lines. J. Virol. 66: 2966–2972; 1992.

    PubMed  CAS  Google Scholar 

  • Harrison R. L.; Puttler B.; Popham H. J. R. Genomic sequence analysis of a fast-killing isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus. J. Gen. Virol. 89: 775–790; 2008. doi:10.1099/vir.0.83566-0.

    PubMed  CAS  Google Scholar 

  • Hashimoto Y.; Corsaro B. G.; Granados R. R. Location and nucleotide-sequence of the gene encoding the viral enhancing factor of the Trichoplusia ni granulosis virus. J. Gen. Virol. 72: 2645–2651; 1991. doi:10.1099/0022-1317-72-11-2645.

    PubMed  CAS  Google Scholar 

  • Hayakawa T.; Ko R.; Okano K.; Seong S. I.; Goto C.; Maeda S. Sequence analysis of the Xestia c-nigrum granulovirus genome. Virology 262: 277–297; 1999. doi:10.1006/viro.1999.9894.

    PubMed  CAS  Google Scholar 

  • Hedges L. M.; Johnson K. N. Induction of host defence responses by Drosophila C virus. J. Gen. Virol. 89: 1497–1501; 2008. doi:10.1099/vir.0.83684-0.

    PubMed  CAS  Google Scholar 

  • Herniou E. A.; Olszewski J. A.; Cory J. S.; O’Reilly D. R. The genome sequence and evolution of baculoviruses. Annu. Rev. Entomol. 48: 211–234; 2003. doi:10.1146/annurev.ento.48.091801.112756.

    PubMed  CAS  Google Scholar 

  • Herniou E. A.; Olszewski J. A.; O’Reilly D. R.; Cory J. S. Ancient coevolution of baculoviruses and their insect hosts. J. Virol. 78: 3244–3251; 2004. doi:10.1128/JVI.78.7.3244-3251.2004.

    PubMed  CAS  Google Scholar 

  • Herniou E. A.; Jehle J. A. Baculovirus phylogeny and evolution. Curr. Drug Targets 8: 1043–1050; 2007. doi:10.2174/138945007782151306.

    PubMed  CAS  Google Scholar 

  • Hirai M.; Terenius O.; Li W.; Faye I. Baculovirus and dsRNA induce Hemolin, but no antibacterial activity, in Antheraea pernyi. Insect Mol. Biol. 13: 399–405; 2004. doi:10.1111/j.0962-1075.2004.00497.x.

    PubMed  CAS  Google Scholar 

  • Hu C. Y.; Zhang Y. B.; Huang G. P.; Zhang Q. Y.; Gui H. F. Molecular cloning and characterisation of a fish PKR-like gene from cultured CAB cells induced by UV-inactivated virus. Fish Shellfish Immunol. 17: 353–366; 2004. doi:10.1016/j.fsi.2004.04.009.

    PubMed  CAS  Google Scholar 

  • Ikeda M.; Reimbold E. A.; Thiem S. M. Functional analysis of the baculovirus host range gene, hrf-1. Virology 332: 602–613; 2005. doi:10.1016/j.virol.2004.12.001.

    PubMed  CAS  Google Scholar 

  • Ikeda M.; Shikata M.; Shirata N.; Chaeychomsri S.; Kobayashi M. Gene organization and complete sequence of the Hyphantria cunea nucleopolyhedrovirus genome. J. Gen. Virol. 87: 2549–2562; 2006. doi:10.1099/vir.0.81930-0.

    PubMed  CAS  Google Scholar 

  • Ikeda M.; Yanagimoto K.; Kobayashi M. Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321: 359–371; 2004. doi:10.1016/j.virol.2004.01.002.

    PubMed  CAS  Google Scholar 

  • Ishikawa H.; Ikeda M.; Alves C. A. F.; Thiem S. M.; Kobayashi M. Host range factor 1 from Lymantria dispar nucleopolyhedrovirus (NPV) is an essential viral factor required for productive infection of NPVs in IPLB-Ld652Y cells derived from L-dispar. J. Virol. 78: 12703–12708; 2004. doi:10.1128/JVI.78.22.12703-12708.2004.

    PubMed  CAS  Google Scholar 

  • Ishikawa H.; Ikeda M.; Yanagimoto K.; Alves C. A. F.; Katou Y.; Lavina-Caoili B. A.; Kobayashi M. Induction of apoptosis in an insect cell line, IPLB-Ld652Y, infected with nucleopolyhedroviruses. J. Gen. Virol. 84: 705–714; 2003. doi:10.1099/vir.0.18815-0.

    PubMed  CAS  Google Scholar 

  • Isler J. A.; Skalet A. H.; Alwine J. C. Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 79: 6890–6899; 2005. doi:10.1128/JVI.79.11.6890-6899.2005.

    PubMed  CAS  Google Scholar 

  • 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. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch. Virol. 151: 1257–1266; 2006. doi:10.1007/s00705-006-0763-6.

    PubMed  CAS  Google Scholar 

  • Kanost M. R.; Jiang H. B.; Yu X. Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 198: 97–105; 2004. doi:10.1111/j.0105-2896.2004.0121.x.

    PubMed  CAS  Google Scholar 

  • Katsuma S.; Daimon T.; Mita K.; Shimada T. Lepidopteran ortholog of Drosophila breathless is a receptor for the baculovirus fibroblast growth factor. J. Virol. 80: 5474–5481; 2006a. doi:10.1128/JVI.00248-06.

    PubMed  CAS  Google Scholar 

  • Katsuma S.; Horie S.; Daimon T.; Iwanaga M.; Shimada T. In vivo and in vitro analyses of a Bombyx mori nucleopolyhedrovirus mutant lacking functional vfgf. Virology 355: 62–70; 2006b. doi:10.1016/j.virol.2006.07.008.

    PubMed  CAS  Google Scholar 

  • Katsuma S.; Shimada T.; Kobayashi M. Characterization of the baculovirus Bombyx mori nucleopolyhedrovirus gene homologous to the mammalian FGF gene family. Virus Genes 29: 211–217; 2004. doi:10.1023/B:VIRU.0000036381.11779.dd.

    PubMed  CAS  Google Scholar 

  • Keene K. M.; Foy B. D.; Sanchez-Vargas I.; Beaty B. J.; Blair C. D.; Olson K. E. RNA interference acts as a natural antiviral response to O’nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 101: 17240–17245; 2004. doi:10.1073/pnas.0406983101.

    PubMed  CAS  Google Scholar 

  • Ko J. H.; Asano A.; Kon Y.; Watanabe T.; Agui T. Characterization of the chicken PKR: Polymorphism of the gene and antiviral activity against vesicular stomatitis virus. Jpn J Vet Res 51: 123–133; 2004.

    PubMed  Google Scholar 

  • Kumar M.; Shanker S.; Rawat V. P. S.; Das R. H. Characterization of the antiapoptotic (p35) gene homologue of Spodoptera litura nucleopolyhedrosis virus (SlNPV). Mol. Biol. Rep. 28: 167–173; 2001. doi:10.1023/A:1015240518798.

    PubMed  CAS  Google Scholar 

  • LaCount D. J.; Friesen P. D. Role of early and late replication events in induction of apoptosis by baculoviruses. J. Virol. 71: 1530–1537; 1997.

    PubMed  CAS  Google Scholar 

  • Langland J. O.; Cameron J. M.; Heck M. C.; Jancovich J. K.; Jacobs B. L. Inhibition of PKR by RNA and DNA viruses. Virus Res. 119: 100–110; 2006. doi:10.1016/j.virusres.2005.10.014.

    PubMed  CAS  Google Scholar 

  • Lannan E.; Vandergaast R.; Friesen P. D. Baculovirus caspase inhibitors P49 and P35 block virus-induced apoptosis downstream of effector caspase DrICE activation in Drosophila melanogaster cells. J. Virol. 81: 9319–9330; 2007. doi:10.1128/JVI.00247-07.

    PubMed  CAS  Google Scholar 

  • Lauzon H. A. M.; Garcia-Maruniak A.; Zanotto P.; Clemente J. C.; Herniou E. A.; Lucarotti C. J.; Arif B. M.; Maruniak J. E. Genomic comparison of Neodiprion sertifer and Neodiprion lecontei nucleopolyhedroviruses and identification of potential hymenopteran baculovirus-specific open reading frames. J. Gen. Virol. 87: 1477–1489; 2006. doi:10.1099/vir.0.81727-0.

    PubMed  CAS  Google Scholar 

  • Lauzon H. A. M.; Lucarotti C. J.; Krell P. J.; Feng Q. L.; Retnakaran A.; Arif B. M. Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J. Virol. 78: 7023–7035; 2004. doi:10.1128/JVI.78.13.7023-7035.2004.

    PubMed  CAS  Google Scholar 

  • Lemaitre B.; Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697–743; 2007. doi:10.1146/annurev.immunol.25.022106.141615.

    PubMed  CAS  Google Scholar 

  • Lepore L. S.; Roelvink P. R.; Granados R. R. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J. Invertebr. Pathol. 68: 131–140; 1996. doi:10.1006/jipa.1996.0070.

    PubMed  CAS  Google Scholar 

  • Li Y. H.; Miller L. K. Expression and functional analysis of a baculovirus gene encoding a truncated protein kinase homolog. Virology 206: 314–323; 1995. doi:10.1016/S0042-6822(95)80047-6.

    PubMed  CAS  Google Scholar 

  • Lilley C. E.; Schwartz R. A.; Weitzman M. D. Using or abusing: viruses and the cellular DNA damage response. Trends Microbiol. 15: 119–126; 2007. doi:10.1016/j.tim.2007.01.003.

    PubMed  CAS  Google Scholar 

  • Lindbo J. A.; Dougherty W. G. Plant pathology and RNAi: a brief history. Annu. Rev. Phytopathol. 43: 191–204; 2005. doi:10.1146/annurev.phyto.43.040204.140228.

    PubMed  CAS  Google Scholar 

  • Liu Q. Z.; Qi Y. P.; Chejanovsky N. Identification and classification of the Spodoptera littoralis nucleopolyhedrovirus inhibitor of apoptosis gene. Virus Genes 26: 143–149; 2003. doi:10.1023/A:1023483313003.

    PubMed  Google Scholar 

  • Luque T.; Finch R.; Crook N.; O’Reilly D. R.; Winstanley D. The complete sequence of the Cydia pomonella granulovirus genome. J. Gen. Virol. 82: 2531–2547; 2001.

    PubMed  CAS  Google Scholar 

  • Maguire T.; Harrison P.; Hyink O.; Kalmakoff J.; Ward V. K. The inhibitors of apoptosis of Epiphyas postvittana nucleopolyhedrovirus. J. Gen. Virol. 81: 2803–2811; 2000.

    PubMed  CAS  Google Scholar 

  • Marques J. T.; Carthew R. W. A call to arms: coevolution of animal viruses and host innate immune responses. Trends Genet. 23: 359–364; 2007. doi:10.1016/j.tig.2007.04.004.

    PubMed  CAS  Google Scholar 

  • McClintock J. T.; Dougherty E. M. Superinfection of baculovirus-infected gypsy moth cells with the nuclear polyhedrosis viruses of Autographa californica and Lymantria dispar. Virus Res. 7: 351–364; 1987. doi:10.1016/0168-1702(87)90048-7.

    CAS  Google Scholar 

  • McClintock J. T.; Dougherty E. M.; Weiner R. M. Semipermissive replication of a nuclear polyhedrosis virus of Autographa californica in a gypsy moth cell line. J. Virol. 57: 197–204; 1986.

    PubMed  CAS  Google Scholar 

  • Means J. C.; Penabaz T.; Clem R. J. Identification and functional characterization of AMVp33, a novel homolog of the baculovirus caspase inhibitor p35 found in Amsacta moorei entomopoxvirus. Virology 358: 436–447; 2007. doi:10.1016/j.virol.2006.08.043.

    PubMed  CAS  Google Scholar 

  • Miller L. K. The baculoviruses. Plenum, New York1997.

    Google Scholar 

  • Mohr I. Neutralizing innate host defenses to control viral translation in HSV-1 infected cells. Int. Rev. Immunol. 23: 199–220; 2004. doi:10.1080/08830180490265600.

    PubMed  CAS  Google Scholar 

  • Moissiard G.; Voinnet O. Viral suppression of RNA silencing in plants. Mol. Plant Pathol. 5: 71–82; 2004. doi:10.1111/j.1364-3703.2004.00207.x.

    CAS  Google Scholar 

  • Morris T. D.; Todd J. W.; Fisher B.; Miller L. K. Identification of Lef-7—a baculovirus gene affecting late gene-expression. Virology 200: 360–369; 1994. doi:10.1006/viro.1994.1200.

    PubMed  CAS  Google Scholar 

  • Moser B. A.; Becnel J. J.; White S. E.; Afonso C.; Kutish G.; Shanker S.; Almira E. Morphological and molecular evidence that Culex nigripalpus baculovirus is an unusual member of the family Baculoviridae. J. Gen. Virol. 82: 283–297; 2001.

    PubMed  CAS  Google Scholar 

  • Nissen M. S.; Friesen P. D. Molecular analysis of the transcriptional regulatory region of an early baculovirus gene. J. Virol. 63: 493–503; 1989.

    PubMed  CAS  Google Scholar 

  • O’Reilly D. R. Baculovirus-encoded ecdysteroid Udp-glucosyltransferases. Insect Biochem. Mol. Biol. 25: 541–550; 1995. doi:10.1016/0965-1748(94)00105-Q.

    CAS  Google Scholar 

  • O’Reilly D. R.; Miller L. K. A baculovirus blocks insect molting by producing ecdysteroid Udp-glucosyl transferase. Science 245: 1110–1112; 1989. doi:10.1126/science.2505387.

    PubMed  CAS  Google Scholar 

  • O’Reilly D. R.; Miller L. K. Improvement of a baculovirus pesticide by deletion of the EGT gene. Bio-Technology 9: 1086–1089; 1991.

    CAS  Google Scholar 

  • Pang Y.; Yu J. X.; Wang L. H.; Hu X. H.; Bao W. D.; Li G.; Chen C.; Han H.; Hu S. N.; Yang H. M. Sequence analysis of the Spodoptera litura multicapsid nucleopolyhedrovirus genome. Virology 287: 391–404; 2001. doi:10.1006/viro.2001.1056.

    PubMed  CAS  Google Scholar 

  • Pavio N.; Romano P. R.; Graczyk T. M.; Feinstone S. M.; Taylor D. R. Protein synthesis and endoplasmic reticulum stress can be modulated by the hepatitis C virus envelope protein E2 through the eukaryotic initiation factor 2 alpha kinase PERK. J. Virol. 77: 3578–3585; 2003. doi:10.1128/JVI.77.6.3578-3585.2003.

    PubMed  CAS  Google Scholar 

  • Pearson M. N.; Rohrmann G. F. Transfer, incorporation, and substitution of envelope fusion proteins among members of the Baculoviridae, Orthomyxoviridae, and Metaviridae (insect retrovirus) families. J. Virol. 76: 5301–5304; 2002. doi:10.1128/JVI.76.11.5301-5304.2002.

    PubMed  CAS  Google Scholar 

  • Peterson K. J.; Lyons J. B.; Nowak K. S.; Takacs C. M.; Wargo M. J.; McPeek M. A. Estimating metazoan divergence times with a molecular clock. Proc. Natl. Acad. Sci. U. S. A. 101: 6536–6541; 2004. doi:10.1073/pnas.0401670101.

    PubMed  CAS  Google Scholar 

  • Prasad M. D.; Han S. J.; Nagaraju J.; Lee W. J.; Brey P. T. Cloning and characterization of an eukaryotic initiation factor-2 alpha kinase from the silkworm, Bombyx mori. Biochim. Biophys. Acta Gene Struct. Expr. 1628: 56–63; 2003.

    Google Scholar 

  • Qi Y.; Liu Q.; Peng Y.; Li L.; Pei Z.; Liu Y. Identification of apoptosis-inhibiting gene in Leucania separata nuclear polyhedrosis virus. Arch. Virol. 146: 2149–2163; 2001. doi:10.1007/s007050170026.

    PubMed  CAS  Google Scholar 

  • Randall R. E.; Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89: 1–47; 2008. doi:10.1099/vir.0.83391-0.

    PubMed  CAS  Google Scholar 

  • Rothenburg S.; Deigendesch N.; Dey M.; Dever T. E.; Tazi L. Double-stranded RNA-activated protein kinase PKR of fishes and amphibians: varying the number of double-stranded RNA binding domains and lineage-specific duplications. BMC Biology 6: 12; 2008.

    PubMed  Google Scholar 

  • Rothenburg S.; Deigendesch N.; Dittmar K.; Koch-Nolte F.; Haag F.; Lowenhaupt K.; Rich A. A PKR-like eukaryotic initiation factor 2 alpha kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains. Proc. Natl. Acad. Sci. U. S. A. 102: 1602–1607; 2005. doi:10.1073/pnas.0408714102.

    PubMed  CAS  Google Scholar 

  • Roulston A.; Marcellus R. C.; Branton P. E. Viruses and apoptosis. Annu. Rev. Microbiol. 53: 577–628; 1999. doi:10.1146/annurev.micro.53.1.577.

    PubMed  CAS  Google Scholar 

  • Salvesen G. S.; Duckett C. S. IAP proteins: Blocking the road to death’s door. Nat. Rev. Mol. Cell Biol. 3: 401–410; 2002. doi:10.1038/nrm830.

    PubMed  CAS  Google Scholar 

  • Stanley D.; Shapiro M. Eicosanoid biosynthesis inhibitors increase the susceptibility of Lymantria dispar to nucleopolyhedrovirus LdMNPV. J. Invertebr. Pathol. 95: 119–124; 2007. doi:10.1016/j.jip.2007.02.002.

    PubMed  CAS  Google Scholar 

  • Sun S. C.; Lindstrom I.; Boman H. G.; Faye I.; Schmidt O. Hemolin—an insect-immune protein belonging to the immunoglobulin superfamily. Science 250: 1729–1732; 1990. doi:10.1126/science.2270488.

    PubMed  CAS  Google Scholar 

  • Tanada Y.; Hukuhara T. Enhanced infection of a nuclear-polyhedrosis virus in larvae of armyworm, Pseudaletia unipuncta, by a factor in capsule of a granulosis virus. J. Invertebr. Pathol. 17: 116–126; 1971.

    CAS  Google Scholar 

  • Terenius O. Hemolin—a lepidopteran anti-viral defense factor? Dev. Comp. Immunol. 32: 311–316; 2008. doi:10.1016/j.dci.2007.09.006.

    PubMed  CAS  Google Scholar 

  • Terenius O.; Bettencourt R.; Lee S. Y.; Li W. L.; Soderhall K.; Faye I. RNA interference of Hemolin causes depletion of phenoloxidase activity in Hyalophora cecropia. Dev. Comp. Immunol. 31: 571–575; 2007. doi:10.1016/j.dci.2006.09.006.

    PubMed  CAS  Google Scholar 

  • Terra W. R. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol. 47: 47–61; 2001. doi:10.1002/arch.1036.

    PubMed  CAS  Google Scholar 

  • Thiem S. M.; Chejanovsky N. The role of baculovirus apoptotic suppressors in AcMNPV-mediated translation arrest in Ld652Y cells. Virology 319: 292–305; 2004. doi:10.1016/j.virol.2003.11.003.

    PubMed  CAS  Google Scholar 

  • Thiem S. M.; Du X. L.; Quentin M. E.; Berner M. M. Identification of a baculovirus gene that promotes Autographa californica nuclear polyhedrosis virus replication in a nonpermissive insect cell line. J. Virol. 70: 2221–2229; 1996.

    PubMed  CAS  Google Scholar 

  • Trudeau D.; Washburn J. O.; Volkman L. E. Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J. Virol. 75: 996–1003; 2001. doi:10.1128/JVI.75.2.996-1003.2001.

    PubMed  CAS  Google Scholar 

  • van Rij R. P.; Saleh M. C.; Berry B.; Foo C.; Houk A.; Antoniewski C.; Andino R. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 20: 2985–2995; 2006. doi:10.1101/gad.1482006.

    PubMed  Google Scholar 

  • Vaux D. L.; Silke J. IAPs, RINGs and ubiquitylation. Nat. Rev. Mol. Cell Biol. 6: 287–297; 2005. doi:10.1038/nrm1621.

    PubMed  CAS  Google Scholar 

  • Vucic D.; Kaiser W. J.; Miller L. K. A mutational analysis of the baculovirus inhibitor of apoptosis Op-IAP. J. Biol. Chem. 273: 33915–33921; 1998. doi:10.1074/jbc.273.51.33915.

    PubMed  CAS  Google Scholar 

  • Wang L.; Salem T. Z.; Lynn D. E.; Cheng X.-W. Slow cell infection, inefficient primary infection and inability to replicate in the fat body determine the host range of Thysanoplusia orichalcea nucleopolyhedrovirus. J. Gen. Virol. 89: 1402–1410; 2008. doi:10.1099/vir.0.2008/000695-0.

    PubMed  CAS  Google Scholar 

  • Wang P.; Granados R. R. An intestinal mucin is the target substrate for a baculovirus enhancin. Proc. Natl. Acad. Sci. U. S. A. 94: 6977–6982; 1997. doi:10.1073/pnas.94.13.6977.

    PubMed  CAS  Google Scholar 

  • Wang X. H.; Aliyari R.; Li W. X.; Li H. W.; Kim K.; Carthew R.; Atkinson P.; Ding S. W. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312: 452–454; 2006. doi:10.1126/science.1125694.

    PubMed  CAS  Google Scholar 

  • Washburn J. O.; Haas-Stapleton E. J.; Tan F. F.; Beckage N. E.; Volkman L. E. Co-infection of Manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by Autographa californica M Nucleopolyhedrovirus. J. Insect Physiol. 46: 179–190; 2000. doi:10.1016/S0022-1910(99)00115-8.

    PubMed  CAS  Google Scholar 

  • Washburn J. O.; Kirkpatrick B. A.; Volkman L. E. Insect protection against viruses. Nature 383: 767–767; 1996. doi:10.1038/383767a0.

    CAS  Google Scholar 

  • Waterhouse R. M.; Kriventseva E. V.; Meister S.; Xi Z. Y.; Alvarez K. S.; Bartholomay L. C.; Barillas-Mury C.; Bian G. W.; Blandin S.; Christensen B. M.; Dong Y. M.; Jiang H. B.; Kanost M. R.; Koutsos A. C.; Levashina E. A.; Li J. Y.; Ligoxygakis P.; MacCallum R. M.; Mayhew G. F.; Mendes A.; Michel K.; Osta M. A.; Paskewitz S.; Shin S. W.; Vlachou D.; Wang L. H.; Wei W. Q.; Zheng L. B.; Zou Z.; Severson D. W.; Raikhel A. S.; Kafatos F. C.; Dimopoulos G.; Zdobnov E. M.; Christophides G. K. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316: 1738–1743; 2007. doi:10.1126/science.1139862.

    PubMed  CAS  Google Scholar 

  • Wright C. W.; Means J. C.; Penabaz T.; Clem R. J. The baculovirus anti-apoptotic protein Op-IAP does not inhibit Drosophila caspases or apoptosis in Drosophila S2 cells and instead sensitizes S2 cells to virus-induced apoptosis. Virology 335: 61–71; 2005. doi:10.1016/j.virol.2005.02.007.

    PubMed  CAS  Google Scholar 

  • Xi Z.; Ramirez J. L.; Dimopoulos G. The Aedes aegypti Toll pathway controls dengue virus infection. PLoS Pathog. 4: e1000098; 2008. doi:10.1371/journal.ppat.1000098.

    PubMed  Google Scholar 

  • Xiao H.; Qi Y. Genome sequence of Leucania seperata nucleopolyhedrovirus. Virus Genes 35: 845–856; 2007. doi:10.1007/s11262-007-0106-z.

    PubMed  CAS  Google Scholar 

  • Zambon R. A.; Nandakumar M.; Vakharia V. N.; Wu L. P. The Toll pathway is important for an antiviral response in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 102: 7257–7262; 2005. doi:10.1073/pnas.0409181102.

    PubMed  CAS  Google Scholar 

  • Zambon R. A.; Vakharia V. N.; Wu L. P. RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell Microbiol. 8: 880–889; 2006. doi:10.1111/j.1462-5822.2006.00688.x.

    PubMed  CAS  Google Scholar 

  • Zoog S. J.; Schiller J. J.; Wetter J. A.; Chejanovsky N.; Friesen P. D. Baculovirus apoptotic suppressor P49 is a substrate inhibitor of initiator caspases resistant to P35 in vivo. EMBO J. 21: 5130–5140; 2002. doi:10.1038/sj.emboj.7594736.

    PubMed  CAS  Google Scholar 

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  1. Department of Entomology, Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48825, USA

    Suzanne M. Thiem

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Thiem, S.M. Baculovirus genes affecting host function. In Vitro Cell.Dev.Biol.-Animal 45, 111–126 (2009). https://doi.org/10.1007/s11626-008-9170-5

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