Skip to main content
PMC home page
Virologica Sinica logoLink to Virologica Sinica
. 2016 Apr 28;31(3):240–248. doi: 10.1007/s12250-016-3710-z

Characterization of the viral fibroblast growth factor homolog of Helicoverpa armigera single nucleopolyhedrovirus

Feifei Yin 1,2, Ruikun Du 1, Wenhua Kuang 1, Guang Yang 1, Hualin Wang 1, Fei Deng 1, Zhihong Hu 1, Manli Wang 1,✉
PMCID: PMC8193389  PMID: 27142667

Abstract

Fibroblast growth factor (FGF) is found throughout multicellular organisms; however, fgf homologs (vfgf) have only been identified among viruses in lepidopteran baculoviruses. The function of vFGFs from Group I alphabaculoviruses, including Autographa californica multiple nucleopolyhedrovirus (AcMNPV) and Bombyx mori nucleopolyhedrovirus (BmNPV), involves accelerated killing of infected larvae by both viruses. The vFGF of Group II alphabaculovirus is structurally different from that of Group I alphabaculovirus, with a larger C-terminal region and additional N-linked glycosylation sites. In this study, we characterized the Group II alphabaculovirus vFGF of Helicoverpa armigera single nucleopolyhedrovirus (HearNPV). The transcription and expression of vfgf was detected at 3 h and 16 h post-infection in HearNPV-infected cells. To further study vFGF function, we constructed vfgf-knockout and -repaired HearNPV bacmids and investigated their affect in both cultured cells and insects. Deletion of vfgf had no effect on budded-virus production or viral DNA replication in cultured HzAM1 cells. However, bioassays showed that HearNPV vfgf deletion significantly increased the median lethal dose and delayed the median lethal time by ∼12 h in the host insect when the virus was delivered orally. These results suggested that vFGF is an important virulent factor for HearNPV infection and propagation in vivo.

graphic file with name 12250_2016_3710_Fig1_HTML.jpg

Electronic Supplementary Material

Supplementary material is available for this article at 10.1007/s12250-016-3710-z and is accessible for authorized users.

Keywords: deletion, function, Helicoverpa armigera single nucleopolyhedrovirus (HearNPV), infectivity, vfgf

Electronic supplementary material

12250_2016_3710_MOESM1_ESM.pdf (108.4KB, pdf)

Supplementary material, approximately 108 KB.

Footnotes

These authors contributed equally to this work.

ORCID: 0000-0001-8701-3530

References

  1. Dai W, Deng F, Wang H, Yuan L, Hu Z. The Transcription Profiles of Nine HaSNPV Genes. Virol Sin. 2006;21:47–51. [Google Scholar]
  2. Detvisitsakun C, Berretta MF, Lehiy C, Passarelli AL. Stimulation of cell motility by a viral fibroblast growth factor homolog: proposal for a role in viral pathogenesis. Virology. 2005;336:308–317. doi: 10.1016/j.virol.2005.03.013. [DOI] [PubMed] [Google Scholar]
  3. Detvisitsakun C, Cain EL, Passarelli AL. The Autographa californica M nucleopolyhedrovirus fibroblast growth factor accelerates host mortality. Virology. 2007;365:70–78. doi: 10.1016/j.virol.2007.03.027. [DOI] [PubMed] [Google Scholar]
  4. Detvisitsakun C, Hutfless EL, Berretta MF, Passarelli AL. Analysis of a baculovirus lacking a functional viral fibroblast growth factor homolog. Virology. 2006;346:258–265. doi: 10.1016/j.virol.2006.01.016. [DOI] [PubMed] [Google Scholar]
  5. Engelhard EK, Kam-Morgan LNW, Washburn J, Volkman LE. The insect tracheal system: A conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc Natl Acad Sci USA. 1994;91:3224–3227. doi: 10.1073/pnas.91.8.3224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Federici BA. Baculovirus pathogenesis. In: Miller LK, editor. In: The baculoviruses. New York, N.Y: Plenum Press; 1997. pp. 33–60. [Google Scholar]
  7. Funk CJ, Braunagel SC, Rohrmann GF. Baculovirus structure. In: Miller LK, editor. In: The baculoviruses. New York: Plenum Press; 1997. pp. 7–32. [Google Scholar]
  8. Hayakawa T, Rohrmann GF, Hashimoto Y. Patterns of genome organization and content in lepidopteran baculoviruses. Virology. 2000;278:1–12. doi: 10.1006/viro.2000.0668. [DOI] [PubMed] [Google Scholar]
  9. Herniou EA, Luque T, Chen X, Vlak JM, Winstanley D, Cory JS, O'Reilly DR. Use of whole genome sequence data to infer baculovirus phylogeny. J Virol. 2001;75:8117–8126. doi: 10.1128/JVI.75.17.8117-8126.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Herniou EA, Olszewski JA, Cory JS, O'Reilly DR. The genome sequence and evolution of baculoviruses. Annu Rev Entomol. 2003;48:211–234. doi: 10.1146/annurev.ento.48.091801.112756. [DOI] [PubMed] [Google Scholar]
  11. Hou S, Chen X, Wang H, Tao M, Hu Z. Efficient method to generate homologous recombinant baculovirus genomes in E. coli. BioTechniques. 2002;32:783–789. doi: 10.2144/02324st04. [DOI] [PubMed] [Google Scholar]
  12. Huang H, Wang M, Deng F, Hou D, Arif BM, Wang H, Hua Z. The ha72 Core Gene of Baculovirus Is Essential for Budded Virus Production and Occlusion-Derived Virus Embedding, and Amino Acid K22 Plays an Important Role in Its Function. J Virol. 2014;88:705–709. doi: 10.1128/JVI.02281-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hyink O, Dellow RA, Olsen MJ, Caradoc-Davies KMB, Drake K, Herniou EA, Cory JS, O’Reilly DR, Ward VK. Whole genome analysis of the Epiphyas postvittana nucleopolyhedrovirus. J Gen Virol. 2002;83:957–971. doi: 10.1099/0022-1317-83-4-957. [DOI] [PubMed] [Google Scholar]
  14. Itoh N, Ornitz DM. Evolution of the Fgf and Fgfr gene families. Trends Genet. 2004;20:563–569. doi: 10.1016/j.tig.2004.08.007. [DOI] [PubMed] [Google Scholar]
  15. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol. 2006;151:1257–1266. doi: 10.1007/s00705-006-0763-6. [DOI] [PubMed] [Google Scholar]
  16. Katsuma S, Daimon T, Horie S, Kobayashi M, Shimada T. N-linked glycans of Bombyx mori nucleopolyhedrovirus fibroblast growth factor are crucial for its secretion. Biochem Biophys Res Commun. 2006;350:1069–1075. doi: 10.1016/j.bbrc.2006.10.001. [DOI] [PubMed] [Google Scholar]
  17. 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. 2006;355:62–70. doi: 10.1016/j.virol.2006.07.008. [DOI] [PubMed] [Google Scholar]
  18. Katsuma S, Shimada T, Kobayashi M. Characterization of the baculovirus Bombyx mori nucleopolyhedrovirus gene homologous to mammalian FGF gene family. Virus Genes. 2004;29:211–217. doi: 10.1023/B:VIRU.0000036381.11779.dd. [DOI] [PubMed] [Google Scholar]
  19. Kuzio J, Pearson MN, Harwood SH, Funk CJ, Evans JT, Slavicek JM, Rohrmann GF. Sequence and Analysis of the Genome of a Baculovirus Pathogenic for Lymantria dispar. Virology. 1999;253:17–34. doi: 10.1006/viro.1998.9469. [DOI] [PubMed] [Google Scholar]
  20. Lange M, Jehle JA. The genome of the Cryptophlebia leucotreta granulovirus. Virology. 2003;317:220–236. doi: 10.1016/S0042-6822(03)00515-4. [DOI] [PubMed] [Google Scholar]
  21. Li Q, Donly C, Li L, Willis LG, Theilmann DA, Erlandson M. Sequence and Organization of the Mamestra configurata Nucleopolyhedrovirus Genome. Virology. 2002;294:106–121. doi: 10.1006/viro.2001.1313. [DOI] [PubMed] [Google Scholar]
  22. Luo S, Zhang Y, Xu X, Westenberg M, Vlak JM, Wang H, Hu Z, Deng F. Helicoverpa armigera nucleopolyhedrovirus occlusion- derived virus-associated protein, HA100, affects oral in- fectivity in vivo but not virus replication in vitro. J Gen Virol. 2011;92:1324–1331. doi: 10.1099/vir.0.029116-0. [DOI] [PubMed] [Google Scholar]
  23. Ma X, Shang J, Yang Z, Bao Y, Xiao Q, Zhang C. Genome sequence and organization of a nucleopolyhedrovirus that infects the tea looper caterpillar, Ectropis obliqua. Virology. 2007;30:235–246. doi: 10.1016/j.virol.2006.10.024. [DOI] [PubMed] [Google Scholar]
  24. Means JC, Passarelli AL. Viral fibroblast growth factor, matrix metalloproteases, and caspases are associated with enhancing systemic infection by baculoviruses. Proc Natl Acad Sci U S A. 2010;107:9825–9830. doi: 10.1073/pnas.0913582107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oers M, Abma-Henkens MHC, Herniou EA, Groot J, Peters S, Vlak aJM. Genome sequence of Chrysodeixis chalcites nucleopolyhedrovirus, a baculovirus with two DNA photolyase genes. J Gen Virol. 2005;86:2069–2080. doi: 10.1099/vir.0.80964-0. [DOI] [PubMed] [Google Scholar]
  26. Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol. 2001;2:3001–3012. doi: 10.1186/gb-2001-2-3-reviews3005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Popovici C, Roubin R, Coulier F, Birnbaum D. An evolutionary history of the FGF superfamily. Bioessays. 2005;27:849–857. doi: 10.1002/bies.20261. [DOI] [PubMed] [Google Scholar]
  28. Robertson JL, Savin NE, Preisler HK, Russell RM. Bioassays with Arthropods CRC Press, Boca Raton. 2007. [Google Scholar]
  29. Sato M, Kornberg TB. FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev Cell. 2002;3:195–207. doi: 10.1016/S1534-5807(02)00202-2. [DOI] [PubMed] [Google Scholar]
  30. Song J, Wang R, Deng F, Wang H, Hu Z. Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol. 2008;89:2331–2338. doi: 10.1099/vir.0.2008/002352-0. [DOI] [PubMed] [Google Scholar]
  31. Sun X, Wu D, Sun X, Jin L, Ma Y, Bonning BC, Peng H, Hu Z. Impact of Helicoverpa armigera nucleopolyhedroviruses expressing a cathepsin L-like protease on target and nontarget insect species on cotton. Biol Control. 2009;49:77–83. doi: 10.1016/j.biocontrol.2008.12.011. [DOI] [Google Scholar]
  32. Wang H, Deng F, Pijlman GP, Chen X, Sun X, Vlak JM, Hu Z. Cloning of biologically active genomes from a Helicoverpa armigera single-nucleocapsid nucleopolyhedrovirus isolate by using a bacterial artificial chromosome. Virus Res. 2003;97:57–63. doi: 10.1016/j.virusres.2003.07.001. [DOI] [PubMed] [Google Scholar]
  33. Wang M, Tan Y, Yin F, Deng F, Vlak JM, Hu Z, Wang H. The F protein of Helicoverpa armigera single nucleopolyhedrovirus can be substituted functionally with its homologue from Spodoptera exigua multiple nucleopolyhedrovirus. J Gen Virol. 2008;89:791–798. doi: 10.1099/vir.0.83466-0. [DOI] [PubMed] [Google Scholar]
  34. Yin F, Wang M, Tan Y, Deng F, Vlak JM, Hu Z, Wang H. A functional F analogue of Autographa californica nucleopolyhedrovirus GP64 from the Agrotis segetum granulovirus. J Virol. 2008;82:8922–8926. doi: 10.1128/JVI.00493-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yin F, Zhu Z, Liu X, Hou D, Wang J, Zhang L, Wang M, Kou Z, Wang H, Deng F, Hu Z. The Complete Genome of a New Betabaculovirus from Clostera anastomosis. PLoS One. 2015;10:e0132792. doi: 10.1371/journal.pone.0132792. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

12250_2016_3710_MOESM1_ESM.pdf (108.4KB, pdf)

Supplementary material, approximately 108 KB.

Articles from Virologica Sinica are provided here courtesy of Wuhan Institute of Virology, Chinese Academy of Sciences

RESOURCES