A serpin mutant links Toll activation to melanization in the host defence of Drosophila

EMBO Journal

Volumn 21, Issue 23, 2002, Pages 6330-6337

  Ligoxygakis, Petros ^a   Pelte, Nadège ^a   Ji, Chuanyi ^a,b   Leclerc, Vincent ^a   Duvic, Bernard ^a   Belvin, Marcia ^a,c   Jiang, Haobo ^a,b   Hoffmann, Jules A ^a   Reichhart, Jean Marc ^a  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c EXELIXIS INC   (United States)

Author keywords

Drosophila; Innate immunity; Melanization; Serine protease cascade; Serpin

Indexed keywords

MUTANT PROTEIN; SERINE PROTEINASE INHIBITOR; SERPIN 27A; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; DROSOPHILA; GENE MUTATION; HEMOLYMPH; IMMUNE RESPONSE; IMMUNOMODULATION; MELANOMA; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; RECEPTOR GENE; TRANSCRIPTION REGULATION;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; HEMOLYMPH; INFECTION; MELANINS; RECEPTORS, CELL SURFACE; SERPINS; TOLL-LIKE RECEPTORS;

ARACHNIDA; HEXAPODA;

EID: 0037011189     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf661     Document Type: Article

References (34)

1. Ashida, M. and Brey, P. (1995) Role of the integument in insect defence: Prophenoloxidase cascade in the cuticular matrix. Proc. Natl. Acad. Sci. USA, 92, 10698-10702.
2. Ashida, M. and Brey, P. (1997) Recent advances in research on the insect prophenoloxidase cascade. In Brey, P.T. and Hultmark, D. (eds). Molecular Mechanisms of Immune Responses in Insects. Chapman and Hall, London, UK, pp. 133-172.
3. Ashida, M. and Sasaki, T. (1994) A target protease activity of serpins in insect hemolymph. Insect Biochem. Mol. Biol., 24, 1037-1041.
4. Brand, A.H. and Perrimon N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
5. Chosa, N., Fukumitsu, T., Fujimoto, K., and Ohnishi, E. (1997). Activation of prophenoloxydase A1 by an activating enzyme in Drosophila melanogaster. Insect Biochem. Mol. Biol., 27, 61-68.
6. De Gregorio, E., Spellman, P.T., Rubin, G.M. and Lemaitre, B. (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA, 98, 12590-12595.
7. De Gregorio, E., Spellman, P.T., Tzou, P., Rubin, G.M. and Lemaitre, B. (2002a) The Toll and Imd pathways are the major regulators of immune response in Drosophila. EMBO J., 21, 2568-2579.
8. De Gregorio, E. et al. (2002b) An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev. Cell. 3, 1-20.
9. Gerttula, S., Jin, Y. and Anderson, K.V. (1988). Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics, 119, 123-133.
10. Govind, S. (1996) Rel signalling pathway and the melanotic tumour phenotype of Drosophila. Biochem. Soc. Trans, 24, 39-44.
11. Hoffmann, J.A. and Reichhart, J.-M. (2002) Drosophila innate immunity: An evolutionary perspective. Nat. Immunol., 3, 121-126.
12. Irving, J.A., Pike, R.N., Lesk, A.M. and Whisstock, J.C. (2000) Phylogeny of the serpin superfamily: Implications of patterns of amino acid conservation for structure and function. Genome Res., 10, 1845-1864.
13. Irving, P., Troxler, L., Heuer, T.S., Belvin, M., Kopczynski, C., Reichhart, J.-M., Hoffmann, J.A. and Hetru, C. (2001) A genome-wide analysis of immune responses in Drosophila. Proc. Natl. Acad. Sci. USA, 98, 15119-15124.
14. Jiang, H. and Kanost, M.R. (1997) Characterisation and functional analysis of 12 naturally occurring reactive site variants of serpin-1 from Manduca sexta. J. Biol. Chem., 272, 1082-1087.
15. Jiang, H. and Kanost, M.R. (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochem. Mol. Biol., 30, 95-105.
16. Jiang, H., Wang, Y. and Kanost, M.R. (1998) Pro-phenoloxydase activating proteinase from an insect, Manduca sexta: A bacteria-inducible protein similar to Drosophila easter. Proc. Natl. Acad. Sci. USA, 95, 12220-12225.
17. Kwon, T.H., Kim, M.S., Choi, H.W., Joo, C.H., Cho, M.Y. and Lee, B.L. (2000) A masquerade-like serine protease homologue is necessary for PO activation in the coleopteran insect Holotrichia diomphalia larvae. Eur. J. Biochem., 267, 6188-6196.
18. Lemaitre, B., Meister, M., Govind, S., Georgel, P. Steward, R., Reichhart, J.M. and Hoffmann, J.A. (1995) Functional analysis and regulation of nuclear import of dorsal during the immune response of Drosophila. EMBO J., 14, 536-545.
19. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.-M. and Hoffmann, J.A. (1996) The dorsoventral regulatory gene cassette spaetzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86, 973-983.
20. Ligoxygakis, P., Pelte, N., Hoffmann, J.A. and Reichhart, J.-M. (2002) Activation of Drosophila Toll during fungal infection by a blood serine protease. Science, 297, 114-116.
21. Manfruelli, P. and Mathey-Prevot, B. (2002) Induction of antimicrobial peptide genes in the absence of any pathogens in mutants exhibiting melanotic masses. 43rd Annual Drosophila Research Conference, Genetics Society of America. Bethesda, MD.
22. Nappi, A.J. and Vass, E. (1993) Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res., 6, 117-126.
23. Nappi, A.J., Vass, E., Frey, F. and Carton, Y. (1995) Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. Eur. J. Cell Biol., 68, 450-456.
24. Park, D.S., Shin, S.W., Hong, S.D. and Park, H.Y. (2000) Immunological detection of serpin in the fall webworm, Hyphandria cunea and its inhibitory activity on the prophenoloxidase system. Mol. Cells, 10, 186-192.
25. Pye, A.E. (1974) Microbial activation of prophenoloxidase from immune insect larvae. Nature, 251, 610-613.
26. Qui, P., Pan, P.C. and Govind, S. (1998) A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development, 125, 1909-1920.
27. Rutschmann, S., Jung, A.C., Hetru, C., Reichhart, J.-M., Hoffmann, J.A. and Ferrandon, D. (2000a) The Rel protein DIF mediates the antifungal but not the antibacterial host defence in Drosophila. Immunity, 12, 569-580.
28. Rutschmann, S., Jung, A.C., Zhou, R., Silverman, N., Hoffmann, J.A. and Ferrandon, D. (2000b) Role of Drosophila IKKγ in a Toll-independent antibacterial immune response. Nat. Immunol., 1, 342-347.
29. Rutschmann, S., Kilinc, A. and Ferrandon, D. (2002) Cutting edge: The Toll pathway is required for resistance to Gram-positive bacterial infections in Drosophila. J. Immunol., 168, 1542-1546.
30. Sen, J. Goltz, J.S., Stevens, L. and Stein, D. (1998) Spatially restricted expression of pipe in the Drosophita egg chamber defines embryonic dorsal-ventral polarity. Cell, 95, 471-481.
31. Silverman, G.A. et al. (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions and a revised nomenclature. J. Biol. Chem., 276, 33293-33296.
32. Spradling, A.C. (1986) P element-mediated transformation. In Roberts, D.B. (ed.), Drosophila: A Practical Approach, IRL Press, Oxford, UK, pp. 175-197.
33. Söderhäll, K. and Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol., 10, 23-28.
34. Zhu, Y. (2001) Identification of Immune-related Genes from the Tobacco Hornworm, Manduca Sexta, and Characterization of Two Immune-Inducible Proteins, Serpin-3 and Leureptin. PhD thesis, Kansas State University, Manhattan, KS.