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Vol. 3, No. 1, 2011
Issue release date: December 2010
J Innate Immun 2011;3:65–70
(DOI:10.1159/000320634)

Clotting Factors and Eicosanoids Protect against Nematode Infections

Hyrsl P.a, b · Dobes P.a, b · Wang Z.a · Hauling T.a · Wilhelmsson C.a · Theopold U.a
aDepartment of Molecular Biology and Functional Genomics, Stockholm University, Stockholm, Sweden; bDepartment of Animal Physiology and Immunology, Institute of Experimental Biology, Masaryk University, Brno, Czech Republic
email Corresponding Author

Abstract

We show that hemolymph clotting protects Drosophila melanogaster against infections with an entomopathogenic nematode and its symbiotic bacterium. We also provide biochemical and genetic evidence for an involvement of eicosanoids in the same infection model. Taken together, our results confirm the conserved nature of the immune function of clot formation.


 goto top of outline Key Words

  • Drosophila melanogaster
  • Eicosanoids
  • Entomopathogenic nematodes
  • Heterorhabditis bacteriophora
  • Coagulation
  • Transglutaminase
  • Photorhabdus luminescens

 goto top of outline Abstract

We show that hemolymph clotting protects Drosophila melanogaster against infections with an entomopathogenic nematode and its symbiotic bacterium. We also provide biochemical and genetic evidence for an involvement of eicosanoids in the same infection model. Taken together, our results confirm the conserved nature of the immune function of clot formation.

Copyright © 2010 S. Karger AG, Basel


 goto top of outline References
  1. Theopold U, Dushay MS: Mechanisms of Drosophila immunity – an innate immune system at work. Curr Immunol Rev 2007;3:276–288.
  2. Kawabata S, Koshiba T, Shibata T: The lipopolysaccaride-activated innate immune response network of the horseshoe crab. Invertebr Surv J 2009;6:59–77.
  3. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O: The coagulation of insect hemolymph. Cell Mol Life Sci 2002;59:363–372.
  4. Scherfer C, Karlsson C, Loseva O, et al: Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol 2004;14:625–629.
  5. Karlsson C, Korayem AM, Scherfer C, Loseva O, Dushay MS, Theopold U: Proteomic analysis of the Drosophila larval hemolymph clot. J Biol Chem 2004;279:52033–52041.
  6. Wang Z, Wilhelmsson C, Hyrsl P, et al: Pathogen entrapment by transglutaminase – a conserved early innate immune mechanism. PLoS Pathog 2010;6:e1000763.

    External Resources

  7. Ffrench-Constant R, Waterfield N, Daborn P, et al: Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 2003;26:433–456.
  8. Hallem EA, Rengarajan M, Ciche TA, Sternberg PW: Nematodes, bacteria, and flies: a tripartite model for nematode parasitism. Curr Biol 2007;17:898–904.
  9. Simmons DL, Botting RM, Hla T: Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 2004;56:387–437.
  10. Dietzl G, Chen D, Schnorrer F, et al: A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007;448:151–156.
  11. Korayem AM, Fabbri M, Takahashi K, et al: A Drosophila salivary gland mucin is also expressed in immune tissues: evidence for a function in coagulation and the entrapment of bacteria. Insect Biochem Mol Biol 2004;34:1297–1304.
  12. Scherfer C, Qazi MR, Takahashi K, et al: The Toll immune-regulated Drosophila protein Fondue is involved in hemolymph clotting and puparium formation. Dev Biol 2006;295:156–163.
  13. Lindgren M, Riazi R, Lesch C, Wilhelmsson C, Theopold U, Dushay MS: Fondue and transglutaminase in the Drosophila larval clot. J Insect Physiol 2008;54:586–592.
  14. Bidla G, Lindgren M, Theopold U, Dushay MS: Hemolymph coagulation and phenoloxidase in Drosophila larvae. Dev Comp Immunol 2005;29:669–679.
  15. Theopold U, Schmidt O: Helix pomatia lectin and annexin V, two molecular probes for insect microparticles: possible involvement in hemolymph coagulation. J Insect Physiol 1997;43:667–674.
  16. Stanley D, Miller J, Tunaz H: Eicosanoid actions in insect immunity. J Innate Immun 2009;1:282–290.
  17. Shrestha S, Park Y, Stanley D, Kim Y: Genes encoding phospholipases A2 mediate insect nodulation reactions to bacterial challenge. J Insect Physiol 2010;56:324–332.
  18. Kim Y, Ji D, Cho S, Park Y: Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression. J Invertebr Pathol 2005;89:258–264.
  19. Shrestha S, Kim Y: Biochemical characteristics of immune-associated phospholipase A(2) and its inhibition by an entomopathogenic bacterium, Xenorhabdus nematophila. J Microbiol 2009;47:774–782.
  20. Stramer B, Winfield M, Shaw T, Millard TH, Woolner S, Martin P: Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. EMBO Rep 2008;9:465–471.
  21. Yajima M, Takada M, Takahashi N, et al: A newly established in vitro culture using transgenic Drosophila reveals functional coupling between the phospholipase A2-generated fatty acid cascade and lipopolysaccharide-dependent activation of the immune deficiency (imd) pathway in insect immunity. Biochem J 2003;371:205–210.
  22. Aymeric JL, Givaudan A, Duvic B: Imd pathway is involved in the interaction of Drosophila melanogaster with the entomopathogenic bacteria, Xenorhabdusnematophila and Photorhabdus luminescens. Mol Immunol 2010;47:2342–2348.
  23. Rizki RM, Rizki TM: Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophilamelanogaster. J Insect Physiol 1990;36:523–529.
  24. Braun A, Hoffmann JA, Meister M: Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc Natl Acad Sci USA 1998;95:14337–14342.
  25. Park Y, Kim Y: Xenorhabdus nematophilus inhibits p-bromophenacyl bromide (BPB)-sensitive PLA2 of Spodoptera exigua. Arch Insect Biochem Physiol 2003;54:134–142.
  26. Kubata BK, Duszenko M, Martin KS, Urade Y: Molecular basis for prostaglandin production in hosts and parasites. Trends Parasitol 2007;23:325–331.

 goto top of outline Author Contacts

Dr. Ulrich Theopold
Department of Molecular Biology and Functional Genomics
University of Stockholm
SE–10691 Stockholm (Sweden)
Tel. +46 816 4181, Fax +46 816 6488, E-Mail uli@molbio.su.se


 goto top of outline Article Information

Received: June 23, 2010
Accepted after revision: August 18, 2010
Published online: October 16, 2010
Number of Print Pages : 6
Number of Figures : 3, Number of Tables : 0, Number of References : 26


 goto top of outline Publication Details

Journal of Innate Immunity

Vol. 3, No. 1, Year 2011 (Cover Date: December 2010)

Journal Editor: Herwald H. (Lund), Egesten A. (Lund)
ISSN: 1662-811X (Print), eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

We show that hemolymph clotting protects Drosophila melanogaster against infections with an entomopathogenic nematode and its symbiotic bacterium. We also provide biochemical and genetic evidence for an involvement of eicosanoids in the same infection model. Taken together, our results confirm the conserved nature of the immune function of clot formation.



 goto top of outline Author Contacts

Dr. Ulrich Theopold
Department of Molecular Biology and Functional Genomics
University of Stockholm
SE–10691 Stockholm (Sweden)
Tel. +46 816 4181, Fax +46 816 6488, E-Mail uli@molbio.su.se


 goto top of outline Article Information

Received: June 23, 2010
Accepted after revision: August 18, 2010
Published online: October 16, 2010
Number of Print Pages : 6
Number of Figures : 3, Number of Tables : 0, Number of References : 26


 goto top of outline Publication Details

Journal of Innate Immunity

Vol. 3, No. 1, Year 2011 (Cover Date: December 2010)

Journal Editor: Herwald H. (Lund), Egesten A. (Lund)
ISSN: 1662-811X (Print), eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Theopold U, Dushay MS: Mechanisms of Drosophila immunity – an innate immune system at work. Curr Immunol Rev 2007;3:276–288.
  2. Kawabata S, Koshiba T, Shibata T: The lipopolysaccaride-activated innate immune response network of the horseshoe crab. Invertebr Surv J 2009;6:59–77.
  3. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O: The coagulation of insect hemolymph. Cell Mol Life Sci 2002;59:363–372.
  4. Scherfer C, Karlsson C, Loseva O, et al: Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol 2004;14:625–629.
  5. Karlsson C, Korayem AM, Scherfer C, Loseva O, Dushay MS, Theopold U: Proteomic analysis of the Drosophila larval hemolymph clot. J Biol Chem 2004;279:52033–52041.
  6. Wang Z, Wilhelmsson C, Hyrsl P, et al: Pathogen entrapment by transglutaminase – a conserved early innate immune mechanism. PLoS Pathog 2010;6:e1000763.

    External Resources

  7. Ffrench-Constant R, Waterfield N, Daborn P, et al: Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 2003;26:433–456.
  8. Hallem EA, Rengarajan M, Ciche TA, Sternberg PW: Nematodes, bacteria, and flies: a tripartite model for nematode parasitism. Curr Biol 2007;17:898–904.
  9. Simmons DL, Botting RM, Hla T: Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 2004;56:387–437.
  10. Dietzl G, Chen D, Schnorrer F, et al: A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007;448:151–156.
  11. Korayem AM, Fabbri M, Takahashi K, et al: A Drosophila salivary gland mucin is also expressed in immune tissues: evidence for a function in coagulation and the entrapment of bacteria. Insect Biochem Mol Biol 2004;34:1297–1304.
  12. Scherfer C, Qazi MR, Takahashi K, et al: The Toll immune-regulated Drosophila protein Fondue is involved in hemolymph clotting and puparium formation. Dev Biol 2006;295:156–163.
  13. Lindgren M, Riazi R, Lesch C, Wilhelmsson C, Theopold U, Dushay MS: Fondue and transglutaminase in the Drosophila larval clot. J Insect Physiol 2008;54:586–592.
  14. Bidla G, Lindgren M, Theopold U, Dushay MS: Hemolymph coagulation and phenoloxidase in Drosophila larvae. Dev Comp Immunol 2005;29:669–679.
  15. Theopold U, Schmidt O: Helix pomatia lectin and annexin V, two molecular probes for insect microparticles: possible involvement in hemolymph coagulation. J Insect Physiol 1997;43:667–674.
  16. Stanley D, Miller J, Tunaz H: Eicosanoid actions in insect immunity. J Innate Immun 2009;1:282–290.
  17. Shrestha S, Park Y, Stanley D, Kim Y: Genes encoding phospholipases A2 mediate insect nodulation reactions to bacterial challenge. J Insect Physiol 2010;56:324–332.
  18. Kim Y, Ji D, Cho S, Park Y: Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression. J Invertebr Pathol 2005;89:258–264.
  19. Shrestha S, Kim Y: Biochemical characteristics of immune-associated phospholipase A(2) and its inhibition by an entomopathogenic bacterium, Xenorhabdus nematophila. J Microbiol 2009;47:774–782.
  20. Stramer B, Winfield M, Shaw T, Millard TH, Woolner S, Martin P: Gene induction following wounding of wild-type versus macrophage-deficient Drosophila embryos. EMBO Rep 2008;9:465–471.
  21. Yajima M, Takada M, Takahashi N, et al: A newly established in vitro culture using transgenic Drosophila reveals functional coupling between the phospholipase A2-generated fatty acid cascade and lipopolysaccharide-dependent activation of the immune deficiency (imd) pathway in insect immunity. Biochem J 2003;371:205–210.
  22. Aymeric JL, Givaudan A, Duvic B: Imd pathway is involved in the interaction of Drosophila melanogaster with the entomopathogenic bacteria, Xenorhabdusnematophila and Photorhabdus luminescens. Mol Immunol 2010;47:2342–2348.
  23. Rizki RM, Rizki TM: Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophilamelanogaster. J Insect Physiol 1990;36:523–529.
  24. Braun A, Hoffmann JA, Meister M: Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc Natl Acad Sci USA 1998;95:14337–14342.
  25. Park Y, Kim Y: Xenorhabdus nematophilus inhibits p-bromophenacyl bromide (BPB)-sensitive PLA2 of Spodoptera exigua. Arch Insect Biochem Physiol 2003;54:134–142.
  26. Kubata BK, Duszenko M, Martin KS, Urade Y: Molecular basis for prostaglandin production in hosts and parasites. Trends Parasitol 2007;23:325–331.