The Drosophila immune system detects bacteria through specific peptidoglycan recognition

Nature Immunology

Volumn 4, Issue 5, 2003, Pages 478-484

  Leulier, François ^a   Parquet, Claudine ^b   Pili Floury, Sebastien ^a   Ryu, Ji Hwan ^c   Caroff, Martine ^b   Lee, Won Jae ^c   Mengin Lecreulx, Dominique ^b   Lemaitre, Bruno ^a  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Ewha Womans University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; DIAMINOPIMELIC ACID; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL STRAIN; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IMMUNE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SPECIES DIFFERENCE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BACILLUS THURINGIENSIS; BASE SEQUENCE; DNA; DROSOPHILA; DROSOPHILA PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION; GENES, INSECT; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; INSECT PROTEINS; LAC OPERON; MURAMIDASE; PEPTIDOGLYCAN; PSEUDOMONAS AERUGINOSA; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 0038664357     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni922     Document Type: Article

References (42)

1. Medzhitov, R. & Janeway, C.A. Jr. Innate immunity: the virtues of a nonclonal system of recognition. Cell 91, 295-298 (1997).
2. Tzou, P., De Gregorio, E. & Lemaitre, B. How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr. Opin. Microbiol. 5, 102-110 (2002).
3. Hultmark, D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15, 12-19 (2003).
4. Khush, R.S., Leulier, F. & Lemaitre, B. Drosophila immunity: two paths to NF-κB. Trends Immunol. 22, 260-264 (2001).
5. De Gregorio, E., Spellman, P.T., Tzou, P., Rubin, G.M. & Lemaitre, B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 21, 2568-2579 (2002).
6. Boutros, M., Agaisse, H. & Perrimon, N. Sequential activation of signaling pathways during innate immune response in Drosophila. Dev. Cell 3, 711-722 (2002).
7. Lemaitre, B., Reichhart, J. & Hoffmann, J. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. USA 94, 14614-14619 (1997).
8. Leulier, F., Rodriguez, A., Khush, R.S., Abrams, J.M. & Lemaitre, B. The Drosophiia caspase Dredd is required to resist Gram-negative bacterial infection. EMBO Rep. 1, 353-358 (2000).
9. Rutschmann, S. et al. The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila. Immunity 12, 569-580 (2000).
10. Rutschmann, S. et al. Role of Drosophila IKKγ in a Toll-independent antibacterial immune response. Nat. Immunol. 1, 342-347 (2000).
11. Vidal, S. et al. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-κB-dependent innate immune responses. Genes Dev. 15, 1900-1912 (2001).
12. Hedengren, M. et al. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol. Cell 4, 827-837 (1999).
13. Yoshida, H., Kinoshita, K. & Ashida, M. Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 271, 13854-13860. (1996).
14. Kang, D., Liu, G., Lundstrom, A., Gelius, E. & Steiner, H.A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc. Natl. Acad Sci. USA 95, 10078-10082 (1998).
15. Werner, T. et al. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc. Natl. Acad Sci. USA 97, 13772-13777 (2000).
16. Michel, T., Reichhart, J.M., Hoffmann, J.A. & Royet, J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414, 756-759 (2001).
17. Choe, K.M., Werner, T., Stoven, S., Hultmark, D. & Anderson, K.V. Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296, 359-362 (2002).
18. Gottar, M. et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416, 640-644 (2002).
19. Ramet, M., Manfruelli, P., Pearson, A., Mathey-Prevot, B. & Ezekowitz, R.A. Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416, 644-648 (2002).
20. Takehana, A. et al. Overexpression of a pattern-recognition receptor, peptidoglycan- recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc. Natl. Acad. Sci. USA 99, 13705-13710 (2002).
21. Akira, S.,Takeda, K. & Kaisho, T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680 (2001).
22. Janeway, C.A. Jr. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
23. Samakovlis, C., Asling, B., Boman, H., Gateff, E. & Hultmark, D. In vitro induction of cecropin genes: an immune response in a Drosophila blood cell line. Biochem. Biophys. Res. Commun. 188, 1169-1175 (1992).
24. Imler, J.L., Tauszig, S., Jouanguy, E., Forestier, C. & Hoffmann, J.A. LPS-induced immune response in Drosophila. J. Endotoxin Res. 6, 459-462 (2000).
25. Hirschfeld, M., Ma, Y., Weis, J.H., Vogel, S.N. & Weis, J.J. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J. Immunol. 165, 618-622 (2000).
26. Glauner, B., Holtje, J.V. & Schwarz, U. The composition of the murein of Escherichia coli. J. Biol. Chem. 263, 10088-10095 (1988).
27. Mengin-Lecreulx, D. & van Heijenoort, J. Effect of growth conditions on peptidoglycan content and cytoplasmic steps of its biosynthesis in Escherichia. J. Bacteriol. 163, 208-212 (1985).
28. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. & Hoffmann, J. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983 (1996).
29. Girardin, S.E. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278, 8869-8872 (2003).
30. Inohara, N. et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2: implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512 (2003).
31. Ashida, M., Ishizaki, Y. & Iwahana, H. Activation of pro-phenoloxidase by bacterial cell walls or β-1,3-glucans in plasma of the silkworm, Bombyx mori. Biochem. Biophys. Res. Commun 113, 562-568 (1983).
32. Yoshida, H. & Ashida, M. Microbial activation of two serine enzymes and prophenoloxidase in the plasma fraction of hemolymph of the silkworm, Bombyx mori. Insect Biochem. 16, 539-545 (1986).
33. Schleifer, K.H. & Kandler, O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477 (1972).
34. Park, J.T. Why does Escherichia coli recycle its cell wall peptides? Mol. Microbiol. 17, 421-426 (1995).
35. Pye, A. Microbial activation of prophenoloxidase from immune insect larvae. Nature 251, 610-613 (1974).
36. Iketani, M., Nishimura, H., Akayama, K., Yamano,Y. & Morishima, I. Minimum structure of peptidoglycan required for induction of antibacterial protein synthesis in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 29, 19-24 (1999).
37. Takeuchi, O. et al. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11, 443-451 (1999).
38. Tzou, R, Meister, M. & Lemaitre, B. Methods for studying infection and immunity in Drosophila. Methods Microbiol. 31, 507-529 (2002).
39. Aussel, L., Brisson, J.R., Perry, M.B. & Caroff, M. Structure of the lipid A of Bordetella hinzii ATCC 51730. Rapid Commun. Mass Spectrom. 14, 595-599 (2000).
40. Karibian, D., Deprun, C. & Caroff, M.A comparison of the Lipid A of several Salmonella and Escherichia strains by 252Cf plasma desorption mass spectrometry. J. Bacteriol. 2988-2993 (1993).
41. Shands, J.W. Jr. & Chun, P.W. The dispersion of Gram-negative lipopolysaccharide by deoxycholate. Subunit molecular weight. J. Biol. Chem. 255, 1221-1226 (1980).
42. Datsenko, K.A. & Wanner, B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645 (2000).