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Modulation of immune responses to parasitoids by polydnaviruses

Published online by Cambridge University Press:  16 March 2011

N. E. Beckage
N. E. Beckage
Affiliation:
Department of Entomology, University of California-Riverside, Riverside, CA 92521, USA
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Summary

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Parasitoids are parasites that invariably kill their host. Polydnaviruses are injected by parasitoid wasps into the body cavity of their insect host and cause immunosuppression, allowing the parasitoid to develop in the absence of encapsulation. One of the targets of the polydnaviruses are the haemocytes of the host, which undergo significant changes in response to entry of the virus. In some systems, haemocyte apoptosis is induced, or haemocyte clumping may be seen; in others, the cells round up and fail to adhere to a substrate. Effects on haemocytes may be transitory or permanent (cell death). Various polydnavirus gene products have been identified that interfere with normal haemocyte function. Phenoloxidase activity also is inhibited during parasitism, and the effect is inducible by polydnavirus. In some systems, venom components may act synergistically with polydnavirus in mediating the virally-induced effects on the host immune system. Polydnaviruses are powerful influences on the host immune system, which serve to permit successful development of the parasitoid without triggering the host immune response.

Keywords

Invertebrate immune responsehaemocytepolydnavirusparasitoid.

References

Adamo, S. A., Linn, C. E. & Beckage, N. E. (1997). Correlation between changes in host behaviour and octopamine levels in the tobacco hornworm Manduca sexta parasitized by the gregarious braconid parasitoid wasp Cotesia congregata. Journal of Experimental Biology 200, 117–127.CrossRefGoogle ScholarPubMed
Albrecht, U., Pfister-Wilhelm, R., Gruber, A., Stettler, P., Heiniger, P., Kurt, E., Schumperli, D. & Lanzrein, B. (1994). Polydnavirus of the parasitic wasp Chelonus inantitus (Braconidae): characterization, genome organization and time point of replication. Journal of General Virology 75, 3353–3363.CrossRefGoogle ScholarPubMed
Asgari, S., Hellers, M. & Schmidt, O. (1996). Host haemocyte inactivation by an insect parasitoid: transient expression of a polydnavirus gene. Journal of General Virology 77, 2653–2662.CrossRefGoogle ScholarPubMed
Asgari, S. & Schmidt, O. (1994). Passive protection eggs from the parasitoid, Cotesia rubecula, in the host, Pieris rapae. Journal of Insect Physiology 40, 789–795.CrossRefGoogle Scholar
Beckage, N. E. (1997). The parasitic wasp's secret weapon. Scientific American 77, 32–37.Google Scholar
Beckage, N. E. (1998). Parasitoids and polydnaviruses.Bioscience 48, 305–311.CrossRefGoogle Scholar
Beckage, N. E., Metcalf, J. S., Nesbit, D. J., Schliefer, K. W., Zetlan, S. R. & Buron, I. De (1989). Host hemolymph monophenoloxidase activity in parasitized Manduca sexta larvae and evidence for inhibition by wasp polydnavirus. Insect Biochemistry 20, 285–294.CrossRefGoogle Scholar
Beckage, N. E., Templeton, T. J., Nielsen, B. D., Cook, D. I. & Stoltz, D. B. (1987). Parasitism-induced hemolymph polypeptides in Manduca sexta (L.) larvae parasitized by the braconid wasp Cotesia congregata (Say). Insect Biochemistry 17, 439–455.CrossRefGoogle Scholar
Blissard, G. W., Fleming, J. G. W., Vinson, S. B. & Summers, M. D. (1986). Campoletis sonorensis virus: expression in Heliothis virescens and identification expressed sequences. Journal of Insect Physiology 32, 351–359.CrossRefGoogle Scholar
Blissard, G. W., Theilmann, D. A. & Summers, M. D. (1989). Segment W of Campolitis sonorensis virus: expression, gene products, and organization. Virology 169, 78–89.CrossRefGoogle ScholarPubMed
Buron, I. & Beckage, N. E. (1992). Characterization of a polydnavirus (PDV) and virus-like filamentous particle (VLP) in the braconid wasp Cotesia congregata (Hymenoptera: Braconidae). Journal of Invertebrate Pathology 59, 315–327.CrossRefGoogle Scholar
Cook, D. I., Stoltz, D. B. & Vinson, S. B. (1984). Induction of a new haemolymph glycoprotein in larvae of permissive hosts parasitized by Campoletis sonorensis. Insect Biochemistry 14, 45–50.CrossRefGoogle Scholar
Cui, L. & Webb, B. A. (1996). Isolation and characterization of a member of the cysteine-rich gene family from Campoletis sonorensis polydnavirus. Journal of General Virology 77, 797–809.CrossRefGoogle ScholarPubMed
Davies, D. H., Strand, M. R. & Vinson, S. B. (1987). Changes in differential haemocyte count and in vitro behaviour of plasmatocytes from host Heliothis virescens caused by Campoletis sonorensis polydnavirus. Journal of Insect Physiology 33, 143–153.CrossRefGoogle Scholar
Davies, D. H. & Vinson, S. B. (1986). Passive evasion by eggs of the braconid parasitoid Cardiochiles nigriceps from encapsulation in vitro by haemocytes of host Heliothis virescens. Journal of Insect Physiology 32, 1003–1010.CrossRefGoogle Scholar
Dib-Hajj, S. D., Webb, B. A. & Summers, M. D. (1993). Structure and evolutionary implications of a ‘cysteine rich’ Campoletis sonorensis polydnavirus gene family. Proceedings of the National Academy of Sciences, USA 90, 3765–3769.CrossRefGoogle ScholarPubMed
Dushay, M. S. & Beckage, N. E. (1993). Dose-dependent separation of Cotesia congregata-associated polydnavirus effects on Manduca sexta larval development and immunity. Journal of Insect Physiology 39, 1029–1040.CrossRefGoogle Scholar
Edson, K. M., Vinson, S. B., Stoltz, D. B. & Summers, M. D. (1980). Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host. Science 211, 582–583.CrossRefGoogle Scholar
Feddersen, I., Sander, K. & Schmidt, O. (1986). Virus-like particles with host protein-like antigenic determinants protect an insect parasitoid from encapsulation. Experientia 42, 1278–1281.CrossRefGoogle Scholar
Federici, B. A. (1991). Viewing polydnaviruses as gene vectors of endoparasitic Hymenoptera. Redia 74, 387–392.Google Scholar
Fleming, J. G. W. (1992). Polydnaviruses: mutualists and pathogens. Annual Review of Entomology 37, 401–425.CrossRefGoogle ScholarPubMed
Fleming, J. G. W., Blissard, G. W., Summers, M. D. & Vinson, S. B. (1983). Expression of Campoletis sonorensis virus in the parasitized host, Heliothis virescens. Journal of Virology 48, 74–78.CrossRefGoogle ScholarPubMed
Fleming, J. G. W. & Summers, M. D. (1986). Campoletis sonorensis endoparasitic wasps contain forms of C. sonorensis virus DNA suggestive of integrated and extrachromosomal polydnavirus DNAs. Journal of Virology 57, 552–562.CrossRefGoogle ScholarPubMed
Fleming, J. G. W. & Summers, M. D. (1991). Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proceedings of the National Academy of Sciences, USA 88, 9770–9774.CrossRefGoogle ScholarPubMed
Gruber, A., Stettler, P., Heineger, P., Schumpli, D. & Lanzrein, B. (1996). Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp genome and excised only in later pupal and adult stages of the female. Journal of General Virology 77, 2873–2879.CrossRefGoogle ScholarPubMed
Guzo, D. & Stoltz, D. B. (1987). Observations on cellular immunity and parasitism in the tussock moth. Journal of Insect Physiology 33, 19–31.CrossRefGoogle Scholar
Harwood, S. H. & Beckage, N. E. (1994). Purification and characterization of an early-expressed polydnavirusinduced protein from the hemolymph of Manduca sexta parasitized by Cotesia congregata. Insect Biochemistry and Molecular Biology 24, 685–698.CrossRefGoogle Scholar
Harwood, S. H., Grosovsky, A. J., Cowles, E. A., Davis, J. W. & Beckage, N. E. (1994). An abundantly expressed hemolymph glycoprotein isolated from new parasitized Manduca sexta larvae is a polydnavirus gene product. Virology 205, 381–392.CrossRefGoogle Scholar
Hayakawa, Y. (1995). Growth-blocking peptide: an insect biogenic peptide that prevents the onset of metamorphosis. Journal of Insect Physiology 41, 1–6.CrossRefGoogle Scholar
Hayakaya, Y., Yazaki, I., Yamanaka, A. & Tanaka, T. (1994). Expression of polydnavirus genes from the parasitoid wasp Cotesia kariyai in two noctuid hosts. Insect Molecular Biology 3, 97–103.CrossRefGoogle Scholar
Hellers, M., Beck, M., Theopold, U., Kamei, M. & Schmidt, O. (1996). Multiple alleles encoding a viruslike particle protein in the ichneumonid endoparasitoid Venturia canescens. Insect Molecular Biology 5, 239–249.CrossRefGoogle ScholarPubMed
Lavine, M. D. & Beckage, N. E. (1995). Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitology Today 11, 368–378.CrossRefGoogle ScholarPubMed
Lavine, M. D. & Beckage, N. E. (1996). Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata. Journal of Insect Physiology 42, 39–49.CrossRefGoogle Scholar
Li, X. & Webb, B. A. (1994). Apparent functional role for a cysteine-rich polydnavirus protein in suppression of the insect cellular immune response. Journal of Virology 68, 7482–7482.CrossRefGoogle ScholarPubMed
Luckhart, S. & Webb, B. A. (1996). Interaction of a wasp ovarian protection and polydnavirus in host immune suppression. Developmental and Comparative Immunology 20, 1–21.CrossRefGoogle ScholarPubMed
Noguchi, H., Hayakawa, Y. & Downer, R. G. H. (1995). Elevation of dopamine levels in parasitized insect larvae. Insect Biochemistry and Molecular Biology 25, 197–200.CrossRefGoogle Scholar
Quicke, D. L. J. (1997). Parasitic Insects. New York: Chapman & Hall.Google Scholar
Rizki, R. M. & Rizki, T. M. (1984). Selective destruction of a blood cell type by a parasitoid wasp. Proceedings of the National Academy of Sciences, USA 81, 6154–6156.CrossRefGoogle ScholarPubMed
Rizki, R. M. & Rizki, T. M. (1990). Parasitoid virus-like particles destroy Drosophila cellular immunity. Proceedings of the National Academy of Sciences, USA 87, 8388–8392.CrossRefGoogle ScholarPubMed
Ross, D. R. & Dunn, P. E. (1989). Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta larvae to bacterial infection. Developmental and Comparative Immunology 13, 205–216.CrossRefGoogle ScholarPubMed
Rotheram, S. (1973). The surface of the egg of a parasitic insect. I. The surface of the egg and the first instar larva of Nemeritis. Proceedings of the Royal Society Series B 183, 179–194.Google Scholar
Savary, S., Beckage, N., Tan, F., Periquet, G. & Drezen, J. M. (1997). Excision of the polydnavirus chromosomal EP1 sequence of the parasitoid Cotesia congregata (Braconidae, Microgasterinae) at potential recombinase binding sites. Journal of General Virology 78, 3125–3134.CrossRefGoogle Scholar
Schmidt, O. & Theopold, U. (1991). Immune defense and suppression in insects. BioEssays 13, 343–346.CrossRefGoogle Scholar
Shelby, K. S. & Webb, B. A. (1994). Polydnavirus infection inhibits synthesis of an insect plasma protein, arylphorin. Journal of General Virology 75, 2285–2292.CrossRefGoogle ScholarPubMed
Shelby, K. S. & Webb, B. A. (1997). Polydnavirus infection inhibits translation of specific growth-associated host proteins. Insect Biochemistry and Molecular Biology 27, 263–270.CrossRefGoogle ScholarPubMed
Soldevila, A. I., Heuston, S. & Webb, B. A. (1997). Purification and analysis of a polydnavirus gene product expressed using a poly-histidine baculovirus vector. Insect Biochemistry and Molecular Biology 27, 201–211.CrossRefGoogle ScholarPubMed
Soldevila, A. I. & WEBB, B. A. (1996). Expression of polydnavirus genes under polydnavirus promoter regulation in insect larvae infected with baculovirus recombinants. Journal of General Virology 77, 1379–1388.CrossRefGoogle ScholarPubMed
Sroka, P. & Vinson, S. B. (1978). Phenoloxidase activity in the haemolymph of parasitized and unparasitized Heliothis virescens. Insect Biochemistry 8, 399–402.CrossRefGoogle Scholar
Stoltz, D. B. (1990). Evidence for chromosomal transmission of polydnavirus DNA. Journal of General Virology 71, 1051–1056.CrossRefGoogle ScholarPubMed
Stoltz, D. B. (1993). The polydnavirus life cycle. In Parasites and Pathogens of Insects. (ed. Beckage, N. E., Thompson, S. N. & Federici, B. A.), vol. 1, pp. 167–189. New York, Academic Press.CrossRefGoogle Scholar
Stoltz, D. B. & Cook, D. I. (1983). Inhibition of host phenoloxidase activity by parasitoid Hymenoptera. Experientia 39, 1022–1024.CrossRefGoogle Scholar
Stoltz, D. B. & GUZO, D. (1986). Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. Journal of Insect Physiology 32, 377–388.CrossRefGoogle Scholar
Stoltz, D. B., Guzo, D., Belland, E. R., Lucarotti, C. J. & Mackinnon, E. A. (1988). Venom promotes uncoating in vitro and persistence in vivo of DNA from a braconid polydnavirus. Journal of General Virology 69, 903–907.CrossRefGoogle Scholar
Stoltz, D. B., Krell, P., Summers, M. D. & Vinson, S. B. (1984). Polydnaviridae – a proposed family of insect viruses with segmented, double-stranded, circular DNA genomes. Intervirology 21, 1–4.CrossRefGoogle ScholarPubMed
Strand, M. R. (1994). Microplitis demolitor polydnavirus infects and expresses in specific morphotypes of Pseudoplusia includens haemocytes. Journal of General Virology 75, 3007–3020.CrossRefGoogle ScholarPubMed
Strand, M. R. & Dover, B. A. (1991). Developmental disruption of Pseudoplusia includens and Heliothis virescens by the calyx fluid and venom of Microplitis demolitor. Archives of Insect Biochemistry and Physiology 18, 131–145.CrossRefGoogle ScholarPubMed
Strand, M. R., McKENZIE, D. I., Grassl, V., Dover, B. A. & Aiken, J. M. (1992). Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens. Journal of General Virology 73, 1627–1635.CrossRefGoogle ScholarPubMed
Strand, M. R. & Noda, T. (1991). Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor. Journal of Insect Physiology 37, 839–850.CrossRefGoogle Scholar
Strand, M. R. & Pech, L. L. (1995a). Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 31–56.CrossRefGoogle ScholarPubMed
Strand, M. R. & Pech, L. L. (1995b). Microplitis demolitor polydnavirus induced apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. Journal of General Virology 76, 283–291.CrossRefGoogle ScholarPubMed
Strand, M. R., Witherell, R. A. & Trudeau, D. (1997). Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. Journal of Virology 71, 2146–2156.CrossRefGoogle ScholarPubMed
Theilmann, D. A. & Summers, M. D. (1988). Identification and comparison of Campoletis sonorensis virus transcripts expressed from four genomic segments in the insect hosts Campoletis sonorensis and Heliothis virescens. Virology 167, 329–341.Google ScholarPubMed
Theopold, U., Krause, E. & Schmidt, O. (1994). Cloning of a VLP-protein coding gene from a parasitoid wasp Venturia canescens. Archives of Insect Biochemistry and Physiology 26, 137–145.CrossRefGoogle ScholarPubMed
Vinson, S. B. (1990). How parasitoids deal with the immune system of their host: an overview. Archives of Insect Biochemistry and Physiology 13, 3–27.CrossRefGoogle Scholar
Wago, H. & Tanaka, T. (1989). Synergistic effects of calyx fluid and venom of Apanteles kariyai Watanabe (Hymenoptera: Braconidae) on the granular cells of Pseudaletia separata Walker (Lepidoptera: Noctuidae). Zoological Science 6, 691–696.Google Scholar
Washburn, J. O., Kirkpatrick, B. A. & Volkman, L. E. (1996). Insect protection against viruses. Nature 383, 767.CrossRefGoogle Scholar
Webb, B. A. & Luckhart, S. (1994). Evidence for an early immunosuppressive role for related Campoletis sonorensis venom and ovarian proteins in Heliothis Virescens. Archives of Insect Biochemistry and Physiology 26, 147–163.CrossRefGoogle ScholarPubMed
Webb, B. A. & Luckhart, S. (1996). Factors mediating short- and long-term immune suppression in a parasitized insect. Journal of Insect Physiology 42, 33–40.CrossRefGoogle Scholar
Webb, B. A. & Summers, M. D. (1990). Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proceedings of the National Academy of Sciences, USA 87, 4961–4965.CrossRefGoogle ScholarPubMed
Webb, B. A. & Summers, M. D. (1992). Stimulation of polydnavirus replication by 20-hydroxyecdyone. Experientia 48, 1018–1022.CrossRefGoogle Scholar
Whitfield, J. B. (1993). Mutualistic viruses and the evolution of host ranges in endoparasitoid Hymenoptera. In Parasitoid Community Ecology (ed. Hawkins, B. A. & Sheehan, W.), pp. 163–176, Oxford, Oxford University Press.Google Scholar
Willott, E., Trenczek, T., Thrower, L. W. & Kanost, M. R. (1994). Immunochemical identification of insect hemocyte populations: monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. European Journal of Cell Biology 65, 417–423.Google ScholarPubMed
Xu, D. & Stoltz, D. B. (1991). Evidence for a chromosomal location of polydnavirus DNA in the ichneumonid parasitoid Hyposoter exiguae. Journal of Virology 65, 6693–6704.CrossRefGoogle Scholar
Yamanaka, A., Hayakawa, Y., Noda, H., Nakashima, N. & Watanabe, H. (1996). Characteristization of polydnavirus-encoded mRNA in parasitized army worm larvae. Insect Biochemistry and Molecular Biology 26, 529–536.CrossRefGoogle Scholar