A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade

Developmental and Comparative Immunology

Volumn 33, Issue 5, 2009, Pages 681-689

  Colinet, Dominique ^a,b,c   Dubuffet, Aurore ^d   Cazes, Dominique ^a,b,c   Moreau, Sébastien ^d   Drezen, Jean Michel ^d   Poirié, Marylène ^a,b,c  

^a Institut National de la Recherche Agronomique   (France)

^b CNRS   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d UNIVERSITÉ DE TOURS   (France)

Author keywords

Drosophila; Immunity; Insect; Parasite; Phenoloxidase cascade; Serine protease; Serpin; Virulence

Indexed keywords

MONOPHENOL MONOOXYGENASE; RECOMBINANT PROTEIN; SERINE PROTEINASE INHIBITOR; VENOM; VIRULENCE FACTOR;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA YAKUBA; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GENETIC CODE; HEMOLYMPH; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; LEPTOPILINA BOULARDI; NONHUMAN; PARASITOID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; WASP;

ARTHROPODA; DROSOPHILA YAKUBA; HEXAPODA; LEPTOPILINA BOULARDI;

EID: 59349121733     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2008.11.013     Document Type: Article

References (57)

1. Schmidt O., Theopold U., and Strand M. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. Bioessays 23 4 (2001) 344-351
2. Carton Y., Poirié M., and Nappi A.J. Insect immune resistance to parasitoids. Insect Science 15 (2008) 67-87
3. Strand M. The insect cellular immune response. Insect Sci 15 (2008) 1-14
4. Williams M.J., Ando I., and Hultmark D. Drosophila melanogaster Rac2 is necessary for a proper cellular immune response. Genes Cells 10 8 (2005) 813-823
5. Cerenius L., and Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol Rev 198 (2004) 116-126
6. Nappi A.J., and Christensen B.M. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol 35 5 (2005) 443-459
7. Cerenius L., Lee B.L., and Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immun 29 6 (2008) 263-271
8. Pennacchio F., and Strand M.R. Evolution of developmental strategies in parasitic hymenoptera. Annu Rev Entomol 51 (2006) 233-258
9. Beckage N., Metcalf J., Nesbit D., Schleifer K., Zetlan S.R., and De Buron I. Host hemolymph monophenoloxidase activity in parasited Manduca sexta larvae and evidence for inhibition by wasp polydnavirus. Insect Biochem 20 3 (1990) 285-294
10. Beck M., Theopold U., and Schmidt O. Evidence for serine protease inhibitor activity in the ovarian calyx fluid of the endoparasitoid Venturia canescens. J Insect Physiol 46 9 (2000) 1275-1283
11. Moreau S.J., Doury G., and Giordanengo P. Intraspecific variation in the effects of parasitism by Asobara tabida on phenoloxidase activity of Drosophila melanogaster larvae. J Invertebr Pathol 76 2 (2000) 151-153
12. Richards E.H., and Edwards J.P. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comp Biochem Physiol B Biochem Mol Biol 127 3 (2000) 289-298
13. Shelby K.S., Adeyeye O.A., Okot-Kotber B.M., and Webb B.A. Parasitism-linked block of host plasma melanization. J Invertebr Pathol 75 3 (2000) 218-225
14. Asgari S., Zhang G., Zareie R., and Schmidt O. A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. Insect Biochem Mol Biol 33 10 (2003) 1017-1024
15. Moreau S.J.M., Eslin P., Giordanengo P., and Doury G. Comparative study of the strategies evolved by two parasitoids of the genus Asobara to avoid the immune response of the host Drosophila melanogaster. Dev Comp Immunol 27 4 (2003) 273-282
16. Beck M., and Strand M. A novel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc Natl Acad Sci USA 104 49 (2007) 19267-19272
17. Zhang G., Lu Z.Q., Jiang H., and Asgari S. Negative regulation of prophenoloxidase (proPO) activation by a clip-domain serine proteinase homolog (SPH) from endoparasitoid venom. Insect Biochem Mol Biol 34 5 (2004) 477-483
18. Carton Y., Boulétreau M., Van Alphen J., and Van Lenteren J. The Drosophila parasitic wasps. In: Ashburner M., Carson H., and Thompson J. (Eds). The genetics and biology of Drosophila (1986), Academic Press, New York/London 347-394
19. Labrosse C., Stasiak K., Lesobre J., Grangeia A., Huguet E., Drezen J.M., and Poirié M. A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera Figitidae)-Drosophila melanogaster interaction. Insect Biochem Mol Biol 35 2 (2005) 93-103
20. Labrosse C., Eslin P., Doury G., Drezen J.M., and Poirié M. Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J Insect Physiol 51 2 (2005) 161-170
21. Colinet D., Schmitz A., Depoix D., Crochard D., and Poirié M. Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens. PLoS Pathog 3 12 (2007) e203
22. Dubuffet A., Dupas S., Frey F., Drezen J.M., Poirie M., and Carton Y. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts. Heredity 98 1 (2007) 21-27
23. Dubuffet A., Doury G., Labrousse C., Drezen J., Carton Y., and Poirie M. Variation of success of Leptopilina boulardi in Drosophila yakuba: the mechanisms explored. Dev Comp Immunol 32 (2008) 597-602
24. Belghazi M., Bathany K., Hountondji C., Grandier-Vazeille X., Manon S., and Schmitter J. Analysis of protein sequences and protein complexes by matrix-assisted laser desorption/ionization mass spectrometry. Proteomics 1 8 (2001) 946-954
25. Edgar R. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 5 (2004) 1792-1797
26. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., and Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 2 (2008) W465-W469
27. Arnold K., Bordoli L., Kopp J., and Schwede T. The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 2 (2006) 195-201
28. Li W., Adams T.E., Kjellberg M., Stenflo J., and Huntington J.A. Structure of native protein C inhibitor provides insight into its multiple functions. J Biol Chem 282 18 (2007) 13759-13768
29. Hooft R., Vriend G., Sander C., and Abola E. Errors in protein structures. Nature 381 6580 (1996) 272
30. Laskowski R., Chistyakov V., and Thornton J. PDBsum more: new summaries and analyses of the known 3D structures of proteins and nucleic acids. Nucleic Acids Res 33 (2005) D266-D268
31. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 12 (1983) 2577-2637
32. Gettins P.G.W. Serpin structure, mechanism, and function. Chem Rev 102 (2002) 4751-4803
33. Jiang H., and Kanost M.R. Characterization and functional analysis of 12 naturally occurring reactive site variants of serpin-1 from Manduca sexta. J Biol Chem 272 2 (1997) 1082-1087
34. Rizki R., and Rizki T. Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophila melanogaster. J Insect Physiol 36 7 (1990) 523-529
35. Leclerc V., Pelte N., El Chamy L., Martinelli C., Ligoxygakis P., Hoffmann J.A., and Reichhart J.M. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep 7 2 (2006) 231-235
36. Strand M.R., and Noda T. Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor. J Insect Physiol 37 11 (1991) 839-850
37. Labrosse C., Carton Y., Dubuffet A., Drezen J.M., and Poirié M. Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. J Insect Physiol 49 5 (2003) 513-522
38. Kohler L.J., Carton Y., Mastore M., and Nappi A.J. Parasite suppression of the oxidations of eumelanin precursors in Drosophila melanogaster. Arch Insect Biochem Physiol 66 2 (2007) 64-75
39. Kanost M.R., Jiang H., and Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198 (2004) 97-105
40. Park D., Shin S., Hong S., and Park H. Immunological detection of serpin in the fall webworm. Hyphantria cunea and its inhibitory activity on the prophenoloxidase system. Mol Cells 10 2 (2000) 186-192
41. De Gregorio E., Han S.J., Lee W.J., Baek M.J., Osaki T., Kawabata S.I., Lee B.L., Iwanaga S., Lemaitre B., and Brey P.T. An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev Cell 3 4 (2002) 581-592
42. Jiang H., Wang Y., Yu X.Q., Zhu Y., and Kanost M. Prophenoloxidase-activating proteinase-3 (pap-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem Mol Biol 33 10 (2003) 1049-1060
43. Zhu Y., Wang Y., Gorman M.J., Jiang H., and Kanost M.R. Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J Biol Chem 278 47 (2003) 46556-46564
44. Tong Y., and Kanost M.R. Manduca sexta serpin-4 and serpin-5 inhibit the prophenol oxidase activation pathway: cDNA cloning, protein expression, and characterization. J Biol Chem 280 15 (2005) 14923-14931
45. Zou Z., and Jiang H. Manduca sexta serpin-6 regulates immune serine proteinases PAP-3 and HP8. cdna cloning, protein expression, inhibition kinetics, and function elucidation. J Biol Chem 280 14 (2005) 14341-14348
46. Michel K., Suwanchaichinda C., Morlais I., Lambrechts L., Cohuet A., Awono-Ambene P.H., Simard F., Fontenille D., Kanost M.R., and Kafatos F.C. Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc Natl Acad Sci USA 103 45 (2006) 16858-16863
47. Scherfer C., Tang H., Kambris Z., Lhocine N., Hashimoto C., and Lemaitre B. Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev Biol 323 2 (2008) 189-196
48. Ligoxygakis P., Pelte N., Ji C., Leclerc V., Duvic B., Belvin M., Jiang H., Hoffmann J.A., and Reichhart J.M. A serpin mutant links toll activation to melanization in the host defence of Drosophila. EMBO J 21 23 (2002) 6330-6337
49. Nappi A.J., Frey F., and Carton Y. Drosophila serpin 27A is a likely target for immune suppression of the blood cell-mediated melanotic encapsulation response. J Insect Physiol 51 2 (2005) 197-205
50. Wertheim B., Kraaijeveld A.R., Schuster E., Blanc E., Hopkins M., Pletcher S.D., Strand M.R., Partridge L., and Godfray H.C.J. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6 11 (2005) R94
51. Schlenke T.A., Morales J., Govind S., and Clark A.G. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog 3 10 (2007) 1486-1501
52. Ling E., and Yu X.Q. Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochem Mol Biol 35 12 (2005) 1356-1366
53. Zang X., and Maizels R.M. Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends Biochem Sci 26 3 (2001) 191-197
54. Knox D.P. Proteinase inhibitors and helminth parasite infection. Parasite Immunol 29 2 (2007) 57-71
55. Russo J., Dupas S., Frey F., Carton Y., and Brehelin M. Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 112 1 (1996) 135-142
56. Wang Y., and Jiang H. Purification and characterization of Manduca sexta serpin-6: a serine proteinase inhibitor that selectively inhibits prophenoloxidase-activating proteinase-3. Insect Biochem Mol Biol 34 4 (2004) 387-395
57. Elliott P., Pei X., Dafforn T., and Lomas D. Topography of a 2.0 A structure of alpha1-antitrypsin reveals targets for rational drug design to prevent conformational disease. Protein Sci 9 7 (2000) 1274-1281