1887

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Volume 88, Issue 1

Characterization of the IB-like gene family in polydnaviruses associated with wasps belonging to different Braconid subfamilies Free

Abstract

Polydnaviruses (PDVs) are obligate symbionts of hymenopteran parasitoids of lepidopteran larvae that induce host immunosuppression and physiological redirection. PDVs include bracoviruses (BVs) and ichnoviruses (IVs), which are associated with braconid and ichneumonid wasps, respectively. In this study, the gene family encoding IB-like proteins in the BVs associated with (CcBV) and (TnBV) was analysed. PDV-encoded IB-like proteins (ANK) are similar to insect and mammalian IB, an inhibitor of the transcription factor nuclear factor B (NF-B), but display shorter ankyrin domains and lack the regulatory domains for signal-mediated degradation and turnover. Phylogenetic analysis of ANK proteins indicates that those of IVs and BVs are closely related, even though these two taxa are believed to lack a common ancestor. Starting from a few hours after parasitization, the transcripts of BV ank genes were detected, at different levels, in several host tissues. The structure of the predicted proteins suggests that they may stably bind NF-B/Rel transcription factors of the tumour necrosis factor (TNF)/Toll immune pathway. Accordingly, after bacterial challenge of host larvae parasitized by , NF-B immunoreactive material failed to enter the nucleus of host haemocytes and fat body cells. Moreover, transfection experiments in human HeLa cells demonstrated that a TnBV ank1 gene product reduced the efficiency of the TNF--induced expression of a reporter gene under NF-B transcriptional control. Altogether, these results suggest strongly that TnBV ANK proteins cause retention of NF-B/Rel factors in the cytoplasm and may thus contribute to suppression of the immune response in parasitized host larvae.

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2007-01-01
2024-04-24
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References

  1. Beckage N. E., Gelman D. B. 2004; Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu Rev Entomol 49:299–330 [CrossRef]
     [Google Scholar]
  2. Beckage N. E., Tan F. F., Schleifer K. W., Lane R. D., Cherubin L. L. 1994; Characterization and biological effects of Cotesia congregata polydnavirus on host larvae of the tobacco hornworm, Manduca sexta . Arch Insect Biochem Physiol 26:165–195 [CrossRef]
     [Google Scholar]
  3. Bergmann A., Stein R., Geisler R., Hagenmaier S., Schmid B., Fernandez N., Schnell B., Nusslein-Volhard C. 1996; A gradient of cytoplasmic Cactus degradation establishes the nuclear localization gradient of the dorsal morphogen in Drosophila . Mech Dev 60:109–123 [CrossRef]
     [Google Scholar]
  4. Choi J. Y., Roh J. Y., Kang J. N., Shim H. J., Woo S. D., Jin B. R., Li M. S., Je Y. H. 2005; Genomic segments cloning and analysis of Cotesia plutellae polydnavirus using plasmid capture system. Biochem Biophys Res Commun 332:487–493 [CrossRef]
     [Google Scholar]
  5. Christophides G. K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P. T., Collins F. H., Danielli A. other authors 2002; Immunity-related genes and gene families in Anopheles gambiae . Science 298:159–165 [CrossRef]
     [Google Scholar]
  6. de Eguileor M., Tettamanti G., Grimaldi A., Perletti G., Congiu T., Rinaldi L., Valvassori R. 2004; Hirudo medicinalis : avascular tissues for clear-cut angiogenesis studies?. Curr Pharm Des 10:1979–1988 [CrossRef]
     [Google Scholar]
  7. De Gregorio E., Spellman P. T., Rubin G. M., Lemaitre B. 2001; Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A 98:12590–12595 [CrossRef]
     [Google Scholar]
  8. Espagne E., Dupuy C., Huguet E., Cattolico L., Provost B., Martins N., Poiriè M., Periquet G., Drezen J.-M. 2004; Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306:286–289 [CrossRef]
     [Google Scholar]
  9. Espagne E., Douris V., Lalmanach G., Provost B., Cattolico L., Lesobre J., Kurata S., Iatrou K., Drezen J.-M., Huguet E. 2005; A virus essential for insect host-parasite interactions encodes cystatins. J Virol 79:9765–9776 [CrossRef]
     [Google Scholar]
  10. Falabella P., Varricchio P., Gigliotti S., Tranfaglia A., Pennacchio F., Malva C. 2003; Toxoneuron nigriceps polydnavirus encodes a putative aspartyl protease highly expressed in parasitized host larvae. Insect Mol Biol 12:9–17 [CrossRef]
     [Google Scholar]
  11. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [CrossRef]
     [Google Scholar]
  12. Ferrarese R., Brivio M., Congiu T., Falabella P., Grimaldi A., Mastore M., Perletti G., Pennacchio F., Sciacca L. other authors 2005; Early suppression of immune response in Heliothis virescens larvae by the endophagous parasitoid Toxoneuron nigriceps . Invertebr Survival J 2:60–68
     [Google Scholar]
  13. Francino M. P. 2005; An adaptive radiation model for the origin of new gene functions. Nat Genet 37:573–577 [CrossRef]
     [Google Scholar]
  14. Fusco F., Bardaro T., Fimiani G., Mercadente V., Miano M. G., Falco G., Israel A., Coutois G., D'Urso M., Ursini M. V. 2004; Molecular analysis of the genetic defect in a large cohort of IP patients and identification of novel NEMO mutations interfering with NF- κ B activation. Hum Mol Genet 13:1763–1773 [CrossRef]
     [Google Scholar]
  15. Ghosh S., Karin M. 2002; Missing pieces in the NF- κ B puzzle. Cell 109:Suppl.S81–S96 [CrossRef]
     [Google Scholar]
  16. Ghosh S., May M. J., Kopp E. B. 1998; NF- κ B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16:225–260 [CrossRef]
     [Google Scholar]
  17. Harwood S. H., Grosovsky A. J., Cowles E. A., Davis J. W., Beckage N. E. 1994; An abundantly expressed hemolymph glycoprotein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. Virology 205:381–392 [CrossRef]
     [Google Scholar]
  18. Hoffmann J. A. 2003; The immune response of Drosophila . Nature 42:33–38
     [Google Scholar]
  19. Hoffmann J. A., Reichhart J. M. 2002; Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3:121–126 [CrossRef]
     [Google Scholar]
  20. Hultmark D. 2003; Drosophila immunity: paths and patterns. Curr Opin Immunol 15:12–19 [CrossRef]
     [Google Scholar]
  21. Huxford T., Huang D. B., Malek S., Ghosh G. 1998; The crystal structure of the I κ B α /NF- κ B complex reveals mechanisms of NF- κ B inactivation. Cell 95:759–770 [CrossRef]
     [Google Scholar]
  22. Kroemer J. A., Webb B. A. 2004; Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu Rev Entomol 49:431–456 [CrossRef]
     [Google Scholar]
  23. Kroemer J. A., Webb B. A. 2005; I κ B-related v ank yrin genes in the Campoletis sonorensis ichnovirus: temporal and tissue-specific patterns of expression in parasitized Heliothis virescens lepidopteran hosts. J Virol 79:7617–7628 [CrossRef]
     [Google Scholar]
  24. Lamberty M., Ades S., Uttenweiler-Joseph S., Brookhart G., Bushey D., Hoffmann J. A., Bulet P. 1999; Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J Biol Chem 274:9320–9326 [CrossRef]
     [Google Scholar]
  25. Lapointe R., Wilson R., Vilaplana L., O'Reilly D. R., Falabella P., Douris V., Bernier-Cardou M., Pennacchio F., Iatrou K. other authors 2005; Expression of a Toxoneuron nigriceps polydnavirus-encoded protein causes apoptosis-like programmed cell death in lepidopteran insect cells. J Gen Virol 86:963–971 [CrossRef]
     [Google Scholar]
  26. Lavine M. D., Strand M. R. 2002; Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309 [CrossRef]
     [Google Scholar]
  27. Ligoxygakis P., Pelte N., Ji C., Leclerc V., Duvic B., Belvin M., Jiang H., Hoffmann J. A., Reichhart J.-M. 2002; A serpin mutant links Toll activation to melanization in the host defence of Drosophila . EMBO J 21:6330–6337 [CrossRef]
     [Google Scholar]
  28. Maddison D., Maddison W. 2000 macclade 4: analysis of phylogeny and character evolution Sunderland, MA: Sinauer Associates;
     [Google Scholar]
  29. Mason N. J., Artis D., Hunter C. A. 2004; New lessons from old pathogens: what parasitic infections have taught us about the role of nuclear factor-kappaB in the regulation of immunity. Immunol Rev 201:48–56 [CrossRef]
     [Google Scholar]
  30. Pennacchio F., Strand M. R. 2006; Evolution of developmental strategies in parasitic hymenoptera. Annu Rev Entomol 51:233–258 [CrossRef]
     [Google Scholar]
  31. Pennacchio F., Falabella P., Vinson S. B. 1998; Regulation of Heliothis virescens prothoracic glands by Cardiochiles nigriceps polydnavirus. Arch Insect Biochem Physiol 38:1–10 [CrossRef]
     [Google Scholar]
  32. Provost B., Varricchio P., Arana E., Espagne E., Falabella P., Huguet E., La Scaleia R., Cattolico L., Poirie M. other authors 2004; Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J Virol 78:13090–13103 [CrossRef]
     [Google Scholar]
  33. Qiu P., Pan P. C., Govind S. 1998; A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125:1909–1920
     [Google Scholar]
  34. Reuther J. Y., Baldwin A. S., Jr. 1999; Apoptosis promotes a caspase-induced amino-terminal truncation of I κ B α that functions as a stable inhibitor of NF- κ B. J Biol Chem 274:20664–20670 [CrossRef]
     [Google Scholar]
  35. Revilla Y., Callejo M., Rodriguez J. M., Culebras E., Nogal M. L., Salas M. L., Vinuela E., Fresno M. 1998; Inhibition of nuclear factor κ B activation by a virus-encoded I κ B-like protein. J Biol Chem 273:5405–5411 [CrossRef]
     [Google Scholar]
  36. Rogers S., Wells R., Rechsteiner M. 1986; Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368 [CrossRef]
     [Google Scholar]
  37. Roth S., Hiromi Y., Godt D., Nusslein-Volhard C. 1991; Cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development 112:371–388
     [Google Scholar]
  38. Russell W. C., Newman C., Williamson D. H. 1975; A simple cytochemical technique for demonstration of DNA in cells infected with mycoplasmas and viruses. Nature 253:461–462 [CrossRef]
     [Google Scholar]
  39. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  40. Schmidt H. A., von Haeseler A. 2003; Maximum-likelihood analysis using tree-puzzle. In Current Protocols in Bioinformatics , Unit 6.6 Edited by Baxevanis A. D., Davison D. B., Page R. D. M., Stormo G., Stein L. New York: Wiley & Sons;
     [Google Scholar]
  41. Shelby K. S., Webb B. A. 1999; Polydnavirus-mediated suppression of insect immunity. J Insect Physiol 45:507–514 [CrossRef]
     [Google Scholar]
  42. Shelby K. S., Cui L., Webb B. A. 1998; Polydnavirus-mediated inhibition of lysozyme gene expression and the antibacterial response. Insect Mol Biol 7:265–272 [CrossRef]
     [Google Scholar]
  43. Silverman N., Maniatis T. 2001; NF- κ B signaling pathways in mammalian and insect innate immunity. Genes Dev 15:2321–2342 [CrossRef]
     [Google Scholar]
  44. Swofford D. L., Olsen G. J., Waddell P. J., Hillis D. M. 1996; Phylogenetic inference. In Molecular Systematics , 2nd edn. pp  407–514 Edited by Hillis D. M., Moritz C., Mable B. K. Sunderland, MA: Sinauer Associates;
     [Google Scholar]
  45. Thoetkiattikul H., Beck M. H., Strand M. R. 2005; Inhibitor κ B-like proteins from a polydnavirus inhibit NF- κ B activation and suppress the insect immune response. Proc Natl Acad Sci U S A 102:11426–11431 [CrossRef]
     [Google Scholar]
  46. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
     [Google Scholar]
  47. Turnbull M. W., Volkoff A. N., Webb B. A., Phelan P. 2005; Functional gap junction genes are encoded by insect viruses. Curr Biol 15:491–492 [CrossRef]
     [Google Scholar]
  48. Webb B. A., Strand M. R. 2005; The biology and genomics of polydnaviruses. In Comprehensive Molecular Insect Science vol. 6 pp  323–360 Edited by Gilbert L. I., Iatrou K., Gill S. S. San Diego, CA: Elsevier;
     [Google Scholar]
  49. Webb B. A., Beckage N. E., Hayakawa Y., Krell P. J., Lanzrein B., Stoltz D. B., Strand M. R., Summers M. D. 2000; Family Polydnaviridae . In Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses pp  253–260 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. San Diego: Academic Press;
     [Google Scholar]
  50. Webb B. A., Strand M. R., Dickey S. E., Beck M. H., Hilgarth R. S., Barney W. E., Kadash K., Kroemer J. A., Lindstrom K. G. other authors 2006; Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347:160–174 [CrossRef]
     [Google Scholar]
  51. Wertheim B., Kraaijeveld A. R., Schuster E., Blanc E., Hopkins M., Pletcher S. D., Strand M. R., Partridge L., Godfray H. C. 2005; Genome-wide gene expression in response to parasitoid attack in Drosophila . Genome Biol 6:R94 [CrossRef]
     [Google Scholar]
  52. Whitfield J. B. 2002; Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 99:7508–7513 [CrossRef]
     [Google Scholar]
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Characterization of the IκB-like gene family in polydnaviruses associated with wasps belonging to different Braconid subfamilies
J. Gen. Virol. 88, 92 (2007); https://doi.org/10.1099/vir.0.82306-0
/content/journal/jgv/10.1099/vir.0.82306-0
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