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Cotesia plutellae bracovirus suppresses expression of an antimicrobial peptide, cecropin, in the diamondback Moth, Plutella xylostella, challenged by bacteria

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Abstract

An endoparasitoid wasp, Cotesia plutellae, induces significant immunosuppression of host insect, Plutella xylostella. This study was focused on suppression in humoral immune response of P. xylostella parasitized by C. plutellae. An EST database of P. xylostella provided a putative cecropin gene (PxCec) which is 627 bp long and encodes 66 amino acids. A signal peptide (22 amino acids) is predicted and two putative O-glycosylation sites in threonine are located at positions 58 and 64. Without bacterial infection, PxCec was expressed in pupa and adult stages but not in the egg and larval stages. Upon bacterial challenge, however, the larvae expressed PxCec as early as 3 h post infection (PI) and maintained high expression levels at 12–24 h PI. By 48 h PI, its expression noticeably diminished. All tested tissues of bacteria-infected P. xylostella showed PxCec expression. However, other microbes, such as virus and fungus, did not induce the PxCec expression. Parasitization by C. plutellae suppressed the expression of PxCec in response to bacterial challenge. Among the parasitic factors of C. plutellae, its symbiotic virus (C. plutellae bracovirus: CpBV) alone was able to inhibit the expression of PxCec of P. xylostella challenged by bacteria. These results indicate that PxCec expression is regulated by both immune and developmental processes in P. xylostella. The parasitization by C. plutellae inhibited the expression of PxCec by the wasp’s symbiotic virus.

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References

  • Bae, S. and Y. Kim. 2004. Host physiological changes due to parasitism of a braconid wasp, Cotesia plutellae, on diamondback moth, Plutella xylostella. Comp. Biochem. Physiol. A. 138, 39–44.

    Article  CAS  Google Scholar 

  • Bae, S. and Y. Kim. 2009. IkB genes encoded in Cotesia plutellae bracovirus suppress an antiviral response and enhance baculovirus pathogenicity against the diamondback moth, Plutella xylostella. J. Invertebr. Pathol. 102, 79–87.

    Article  CAS  PubMed  Google Scholar 

  • Baeuerle, P.A. 1998. Ikappa B-NF-kappa B structures: at the interface of inflammation control. Cell 95, 729–731.

    Article  CAS  PubMed  Google Scholar 

  • Barat-Houari, M., F. Hilliou, F.X. Jousset, L. Sofer, E. Deleury, J. Rocher, M. Ravallec, L. Galibert, P. Delobel, R. Feyereisen, P. Fournier, and A.N. Volkoff. 2006. Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels. BMC Genomics 7, 160.

    Article  CAS  PubMed  Google Scholar 

  • Beckage, N.E. 2008. Insect immunology. Academic Press, New York, N.Y., USA.

    Google Scholar 

  • Bettencourt, R., O. Terenius, and I. Faye. 2002. Hemolin gene silencing by dsRNA injected into Cecropia pupae is lethal to next generation embryos. Insect Mol. Biol. 11, 267–271.

    Article  CAS  PubMed  Google Scholar 

  • Boman, H.G., I.A. Boman, D. Andreu, Z. Li, R.B. Merrifield, G. Schlenstedt, and R. Zimmermann. 1989. Chemical synthesis and enzymatic processing of precursor forms of cecropins A and B. J. Biol. Chem. 264, 5852–5860.

    CAS  PubMed  Google Scholar 

  • Brennan, C.A. and K.V. Anderson. 2004. Drosophila: the genetics of innate immune recognition and response. Annu. Rev. Immunol. 22, 457–483.

    Article  CAS  PubMed  Google Scholar 

  • Bulet, P. and R. Stocklin. 2005. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12, 3–11.

    Article  CAS  PubMed  Google Scholar 

  • Christensen, B., J. Fink, R.B. Merrifield, and R.B. Mauzerall. 1988. Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc. Natl. Acad. Sci. USA 85, 5072–5076.

    Article  CAS  PubMed  Google Scholar 

  • Cui, L., A.L. Soldevila, and B.A. Webb. 1997. Expression and hemocyte-targeting of a Campoletis sonorensis polydnavirus cysteinerich gene in Heliothis virescens larvae. Arch. Insect Biochem. Physiol. 36, 251–271.

    Article  CAS  PubMed  Google Scholar 

  • Eum, J.H., R.S. Young, S.M. Yoe, S.W. Kang, and S.S. Han. 2007. Analysis of the immune-inducible genes of Plutella xylostella using expressed sequence tags and cDNA microarray. Dev. Comp. Immunol. 31, 1107–1120.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J. 1989. PHYLIP: Phylogeny Inference Package version 3.5c. Cladistics 5, 164–166.

    Google Scholar 

  • Gudmundsson, G.H., D.A. Lidholm, B. Åsling, R. Gan, and H.G. Boman. 1991. The cecropin locus, cloning and expression of a gene cluster encoding three antibacterial peptides in Hyalophora cecropia. J. Biol. Chem. 266, 11510–11517.

    CAS  PubMed  Google Scholar 

  • Hara, S., K. Taniai, Y. Kato, and M. Yamakawa. 1994. Isolation and amidation of the non-amidated form of cecropin D from larvae of Bombyx mori. Comp. Biochem. Physiol. 108, 303–308.

    Google Scholar 

  • Hong, S.M., T. Kusakabe, J.M. Lee, T. Tatsuke, Y. Kawaguchi, M.W. Kang, S.W. Kang, K.A. Kim, and S.K. Nho. 2008. Structure and expression analysis of the Cecropin-E gene from the silkworm, Bombyx mori. Biosci. Biotechnol. Biochem. 72, 1992–1998.

    Article  CAS  PubMed  Google Scholar 

  • Hong, R.W., M. Shchepetov, J.N. Weiser, and P.H. Axelsen. 2003. Transcriptional profile of the Escherichia coli response to the antimicrobial insect peptide cecropin A. Antimicrob. Agents Chemother. 47, 1–6.

    Article  CAS  PubMed  Google Scholar 

  • Hultmark, D., T. Steiner, T. Rasmuson, and H.G. Boman. 1980. Insect immunity: purification and properties of three inducible bacterial proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 106, 7–16.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, A.M.A. and Y. Kim. 2006. Parasitism by Cotesia plutellae alters the hemocyte population and immunological function of the diamond back moth, Plutella xylostella. J. Insect Physiol. 52, 943–950.

    Article  CAS  PubMed  Google Scholar 

  • Kim, Y., N.A. Basio, A.M. Ibrahim, and S. Bae. 2006. Gene structure of Cotesia plutellae bracovirus (CpBV)-IkB and its expression pattern in diamondback moth, Plutella xylostella, parasitized by Cotesia plutellae. Kor. J. Appl. Entomol. 45, 1–10.

    Google Scholar 

  • Kim, Y., J.Y. Choi, and Y.H. Je. 2007. Cotesia plutellae bracovirus genome and its function in altering insect physiology. J. Asia Pac. Entomol. 10, 181–191.

    Article  CAS  Google Scholar 

  • Krell, P.J., M.D. Summers, and S.B. Vinson. 1982. Virus with a multipartite superhelical DNA genome from the ichneumonid parasitoid Campoletis sonorensis. Virol. 43, 859–870.

    CAS  Google Scholar 

  • Kroemer, J.A. and B.A. Webb. 2004. Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu. Rev. Entomol. 49, 431–456.

    Article  CAS  PubMed  Google Scholar 

  • Kylsten, P., C. Samakovlis, and D. Hultmark. 1990. The cecropin locus in Drosophila: a compact gene cluster involved in the response to infection. EMBO J. 9, 217–224.

    CAS  PubMed  Google Scholar 

  • Madanagopal, N. and Y. Kim. 2007. A putative protein translation inhibitory factor encoded in Cotesia plutellae bracovirus suppresses host hemocyte-spreading behavior. J. Insect Physiol. 53, 1283–1292.

    Article  CAS  Google Scholar 

  • Nalini, M., J.Y. Choi, Y.H. Je, I. Hwang, and Y. Kim. 2008. Immunoevasive property of a polydnaviral product, CpBV-lectin, protects the parasitoid egg from hemocytic encapsulation of Plutella xylostella (Lepidoptera: Yponomeutidae). J. Insect Physiol. 54, 1125–1131.

    Article  CAS  PubMed  Google Scholar 

  • Petersen, U.M., L. Kadalayil, K.P. Rehorn, D.K. Hoshizaki, R. Reuter, and Y. Engström. 1999. Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif. EMBO J. 18, 4013–4022.

    Article  CAS  PubMed  Google Scholar 

  • Plunkett, R.M., S.I. Murray, and C.A. Lowenberger. 2009. Generation and characterization of the antibacterial activity of a novel hybrid antimicrobial peptide comprising functional domains from different insect cecropins. Can. J. Microbiol. 55, 520–528.

    Article  CAS  PubMed  Google Scholar 

  • Roos, E., G. Bjorklund, and Y. Engstrom. 1998. In vivo regulation of tissue-specific and LPS-inducible expression of the Drosophila Cecropin genes. Insect Mol. Biol. 7, 51–62.

    Article  CAS  PubMed  Google Scholar 

  • Russell, V. and P.E. Dunn. 1996. Antibacterial proteins in the midgut of Manduca sexta during metamorphosis. J. Insect Physiol. 42, 65–71.

    Article  Google Scholar 

  • Shai, Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipids bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55–70.

    Article  CAS  PubMed  Google Scholar 

  • Silvestro, L. and P.H. Axelsen. 2000. Membrane-induced folding of cecropin A. Biophys. J. 79, 14665–1477.

    Article  Google Scholar 

  • Silvestro, L., J.N. Weiser, and P.H. Axelsen. 2000. Antibacterial and antimembrane activities of cecropin A in Escherichia coli. Antimicrob. Agents Chemother. 44, 602–607.

    Article  CAS  PubMed  Google Scholar 

  • Steiner, H., D. Andreu, and R.B. Merrifield. 1988. Binding and action of cecropin and cecropin analogues: antimicrobial proteins from insects. Biochim. Biophys. Acta 939, 260–266.

    Article  CAS  PubMed  Google Scholar 

  • Stoltz, D.B., P.J. Krell, and S.B. Vinson. 1984. Polydnaviridae — a proposed family of insect viruses with segmented, double-stranded, circular DNA genomes. Intervirology 21, 1–4.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka, H., A. Sagisaka, Y. Nakajima, K. Fujita, S. Imanishi, and M. Yamakawa. 2009. Correlation of differential expression of silkworm antimicrobial peptide genes with different amounts of Rel family proteins and their gene transcriptional activity. Biosci. Biotechnol. Biochem. 73, 599–606.

    Article  CAS  PubMed  Google Scholar 

  • Tanura K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.

    Article  CAS  Google Scholar 

  • Theilmann, D.A. and M.D. Summers. 1986. Molecular analysis of Campoletis sonorensis virus DNA in the lepidopteran host Heliothis virescens. J. Gen. Virol. 67, 1961–1969.

    Article  CAS  PubMed  Google Scholar 

  • Thoetkiattikul, H., M.H. Beck, and M.R. Strand. 2005. Inhibitor kappaB-like proteins from a polydnavirus inhibit NF-kappaB activation and suppress the insect immune response. Proc. Natl. Acad. Sci. USA 102, 11426–11431.

    Article  CAS  PubMed  Google Scholar 

  • Tingvall, T.Ö., E. Roos, and Y. Engström. 2001. The imd gene is required for local Cecropin expression in Drosophila barrier epithelia. EMBO Rep. 21, 239–243.

    Article  Google Scholar 

  • van Hofsten, P., I. Faye, K. Kockum, J.Y. Lee, K.G. Xanthopoulos, I.A. Boman, H.G. Boman, Å. Engström, D. Andreu, and R.B. Merrifield. 1985. Molecular cloning, cDNA sequencing, and chemical synthesis of cecropin B from Hyalophora cecropia. Proc. Natl. Acad. Sci. USA 82, 2240–2243.

    Article  PubMed  Google Scholar 

  • Vizioli, J. and M. Salzet. 2002. Antimicrobial peptides from animals: focus on invertebrates, Trends Pharmacol. Sci. 23, 494–496.

    CAS  Google Scholar 

  • Wael, G. and Y. Kim. 2009. N-terminal tail of a viral histone H4 encoded in Cotesia plutellae bracovirus is essential to suppress gene expression of host histone H4. Insect Mol. Biol. 18, 111–118.

    Article  Google Scholar 

  • Webb, B.A., N.E. Beckage, Y. Hayakawa, P.J. Krell, B. Lanzrein, D.B. Stoltz, M.R. Strand, and M.D. Summers. 2000. Polydnaviridae, pp. 253–260. In M.H.V. van Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, and R.B. Wickner (eds.), Virus Taxonomy, Academic Press, New York, N.Y., USA.

    Google Scholar 

  • Webb, B.A. and M.R. Strand. 2005. The biology and genomes of polydnavirus, pp. 323–360. In L.I. Gilbert, K. Iatrou, and S.S. Gill (eds.), Comprehensive Molecular Insect Science, Elsevier, New York, N.Y., USA.

    Google Scholar 

  • Yamano, Y., M. Matsumoto, K. Inoue, T. Kawabata, and I. Morishima. 1994. Cloning of cDNAs for cecropin A and B, and expression of the genes in the silkworm, Bombyx mori. Biosci. Biotech. Biochem. 58, 1476–1478.

    Article  CAS  Google Scholar 

  • Yang, J., S. Furukawa, A. Sagisaka, J. Ishibashi, K. Taniani, T. Shono, and M. Yamakawa. 1999. cDNA cloning and gene expression of cecropin D, an antibacterial protein in the silkworm, Bombyx mori. Comp. Biochem. Physiol. B. 122, 409–414.

    Article  CAS  PubMed  Google Scholar 

  • Zambon, R.A., M. Nandakumar, V.N. Vakharia, and L.P. Wu. 2005. The Toll pathway is important for an antiviral response in Drosophila. Proc. Natl. Acad. Sci. USA 102, 7257–7262.

    Article  CAS  PubMed  Google Scholar 

  • Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415, 389–395.

    Article  CAS  PubMed  Google Scholar 

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Barandoc, K.P., Kim, J. & Kim, Y. Cotesia plutellae bracovirus suppresses expression of an antimicrobial peptide, cecropin, in the diamondback Moth, Plutella xylostella, challenged by bacteria. J Microbiol. 48, 117–123 (2010). https://doi.org/10.1007/s12275-009-9261-3

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