Bacterial recognition and signalling by the Drosophila IMD pathway

Cellular Microbiology

Volumn 7, Issue 4, 2005, Pages 461-469

  Kaneko, Takashi ^a,b   Silverman, Neal ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; DIAMINOPIMELIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N ACETYLMURAMOYLALANINE AMIDASE; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR 1;

BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IMMUNE RESPONSE; INNATE IMMUNITY; INSECT; MAMMAL; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIA; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; IMMUNITY, NATURAL; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

BACTERIA (MICROORGANISMS); HEXAPODA; MAMMALIA;

EID: 15944420868     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00504.x     Document Type: Short Survey

References (68)

1. Bischoff, V., Vignal, C., Boneca, I.G., Michel, T., Hoffmann, J.A., and Royet, J. (2004) Function of the Drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat Immunol 5: 1175-1180.
2. Boutros, M., Agaisse, H., and Perrimon, N. (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 3: 711-722.
3. Cha, G.H., Cho, K.S., Lee, J.H., Kim, M., Kim, E., Park, J., et al. (2003) Discrete functions of TRAF1 and TRAF2 in Drosophila melanogaster mediated by c-Jun N-terminal kinase and NF-kappaB-dependent signaling pathways. Mol Cell Biol 23: 7982-7991.
4. Chang, C.I., Pili-Floury, S.S., Herve, M., Parquet, C., Chelliah, Y., Lemaitre, B., et al. (2004) A Drosophila pattern recognition receptor contains a peptidoglycan docking groove and unusual 1,d-carboxypeptidase activity. PLoS Biol 2: E277.
5. Chen, W., White, M.A., and Cobb, M.H. (2002) Stimulus-specific requirements for MAP3 kinases in activating the JNK pathway. J Biol Chem 277: 49105-49110.
6. Choe, K.M., Werner, T., Stöven, S., Hultmark, D., and Anderson, K.V. (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296: 359-362.
7. Chun, H.J., Zheng, L., Ahmad, M., Wang, J., Speirs, C.K., Siegel, R.M., et al. (2002) Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature 419: 395-399.
8. Cookson, B.T., Cho, H.L., Herwaldt, L.A., and Goldman, W.E. (1989) Biological activities and chemical composition of purified tracheal cytotoxin of Bordetella pertussis. Infect Immun 57: 2223-2229.
9. 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.
10. De Gregorio, E., Spellman, P.T., Tzou, P., Rubin, G.M., and Lemaitre, B. (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 21: 2568-2579.
11. Dushay, M.S., Åsling, B., and Hultmark, D. (1996) Origins of immunity: relish, a compound rel-like gene in the antibacterial defense of Drosophila. Proc Natl Acad Sci USA 93: 10343-10347.
12. Elrod-Erickson, M., Mishra, S., and Schneider, D. (2000) Interactions between the cellular and humoral immune responses in drosophila. Curr Biol 10: 781-784.
13. Galko, M.J., and Krasnow, M.A. (2004) Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol 2: E239.
14. Gelius, E., Persson, C., Karlsson, J., and Steiner, H. (2003) A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem Biophys Res Commun 306: 988-994.
15. Georgel, P., Naitza, S., Kappler, C., Ferrandon, D., Zachary, D., Swimmer, C., et al. (2001) Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev Cell 1: 503-514.
16. Gobert, V., Gottar, M., Matskevich, A.A., Rutschmann, S., Royet, J., Belvin, M., et al. (2003) Dual activation of the Drosophila Toll pathway by two pattern recognition receptors. Science 302: 2126-2130.
17. Goldman, W.E., Klapper, D.G., and Baseman, J.B. (1982) Detection, isolation, and analysis of a released Bordetella pertussis product toxic to cultured tracheal cells. Infect Immun 36: 782-794.
18. Gottar, M., Gobert, V., Michel, T., Belvin, M., Duyk, G., Hoffmann, J.A., et al. (2002) The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416: 640-644.
19. Hetru, C., Troxler, L., and Hoffmann, J.A. (2003) Drosophila melanogaster antimicrobial defense. J Infect Dis 187 (Suppl. 2): S327-S334.
20. Hoffmann, J.A., and Reichhart, J.M. (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3: 121-126.
21. Hu, S., and Yang, X. (2000) dFADD, a novel death domain-containing adapter protein for the Drosophila caspase DREDD. J Biol Chem 275: 30761-30764.
22. Hu, X., Yagi, Y., Tanji, T., Zhou, S., and Ip, Y.T. (2004) Multimerization and interaction of Toll and Spatzle in Drosophila. Proc Natl Acad Sci USA 101: 9369-9374.
23. Irving, P., Troxler, L., Heuer, T.S., Belvin, M., Kopczynski, C., Reichhart, J.M., et al. (2001) A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci USA 98: 15119-15124.
24. Kanayama, A., Seth, R.B., Sun, L., Ea, C.K., Hong, M., Shaito, A., et al. (2004) TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 27: 535-548.
25. Kaneko, T., Goldman, W.E., Mellroth, P., Steiner, H., Fukase, K., Kusumoto, S., et al. (2004) Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20: 637-649.
26. Kang, D., Liu, G., Lundstrom, A., Gelius, E., and Steiner, H. (1998) A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc Natl Acad Sci USA 95: 10078-10082.
27. Kim, M.S., Byun, M., and Oh, B.H. (2003) Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat Immunol 4: 787-793.
28. Lemaitre, B., Kromer-Metzger, E., Michaut, L., Nicolas, E., Meister, M., Georgel, P., et al. (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92: 9465-9469.
29. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.M., and Hoffmann, J.A. (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983.
30. Lemaitre, B., Reichhart, J.M., and Hoffmann, J.A. (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94: 14614-14619.
31. Leulier, F., Rodriguez, A., Khush, R.S., Abrams, J.M., and Lemaitre, B. (2000) The Drosophila caspase Dredd is required to resist Gram-negative bacterial infection. EMBO Rep 1: 353-358.
32. Leulier, F., Vidal, S., Saigo, K., Ueda, R., and Lemaitre, B. (2002) Inducible expression of double-stranded RNA reveals a role for dFADD in the regulation of the antibacterial response in Drosophila adults. Curr Biol 12: 996-1000.
33. Leulier, F., Parquet, C., Pili-Floury, S., Ryu, J.H., Caroff, M., Lee, W.J., et al. (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 4: 478-484.
34. Levashina, E.A., Langley, E., Green, C., Gubb, D., Ashburner, M., Hoffmann, J.A., and Reichhart, J.M. (1999) Constitutive activation of Toll-mediated antifungal defense in serpin-deficient Drosophila. Science 285: 1917-1919.
35. 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.
36. Liu, C., Xu, Z., Gupta, D., and Dziarski, R. (2001) Peptidoglycan recognition proteins: a novel family of four human innate immunity pattern recognition molecules. J Biol Chem 276: 34686-34694.
37. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C.A., Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
38. Mellroth, P., Karlsson, J., and Steiner, H. (2003) A scavenger function for a Drosophila peptidoglycan recognition protein. J Biol Chem 278: 7059-7064.
39. Melly, M.A., McGee, Z.A., and Rosenthal, R.S. (1984) Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis 149: 378-386.
40. Michel, T., Reichhart, J.M., Hoffmann, J.A., and Royet, J. (2001) Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414: 756-759.
41. Ochiai, M., and Ashida, M. (1999) A pattern recognition protein for peptidoglycan. Cloning the cDNA and the gene of the silkworm, Bombyx mori. J Biol Chem 274: 11854-11858.
42. Pili-Floury, S., Leulier, F., Takahashi, K., Saigo, K., Samain, E., Ueda, R., and Lemaitre, B. (2004) In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against Gram-positive bacterial infection in Drosophila adults. J Biol Chem 279: 12848-12853.
43. Ramet, M., Manfruelli, P., Pearson, A., Mathey-Prevot, B., and Ezekowitz, R.A. (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416: 644-648.
44. Rock, F.L., Hardiman, G., Timans, J.C., Kastelein, R.A., and Bazan, J.F. (1998) A family of human receptors structurally related to Drosophila Toll. Proc Natl Acad Sci USA 95: 588-593.
45. Rosenthal, R.S. (1979) Release of soluble peptidoglycan from growing gonococci: hexaminidase and amidase activities. Infect Immun 24: 869-878.
46. Salmena, L., Lemmers, B., Hakem, A., Matysiak-Zablocki, E., Murakami, K., Au, P.Y., et al. (2003) Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev 17: 883-895.
47. Schleifer, K.H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407-477.
48. Silverman, N., and Fitzgerald, K. (2004) DUBbing down innate immunity. Nat Immunol 5: 1010-1012.
49. Silverman, N., and Maniatis, T. (2001) NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev 15: 2321-2342.
50. Silverman, N., Zhou, R., Stöven, S., Pandey, N., Hultmark, D., and Maniatis, T. (2000) A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes Dev 14: 2461-2471.
51. Silverman, N., Zhou, R., Erlich, R.L., Hunter, M., Bernstein, E., Schneider, D., and Maniatis, T. (2003) Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem 278: 48928-48934.
52. Stöven, S., Ando, I., Kadalayil, L., Engström, Y., and Hultmark, D. (2000) Activation of the Drosophila NF-κB factor Relish by rapid endoproteolytic cleavage. EMBO Rep 1: 347-352.
53. Stöven, S., Silverman, N., Junell, A., Hedengren-Olcott, M., Erturk, D., Engstrom, Y., et al. (2003) Caspase-mediated processing of the Drosophila NF-{kappa}B factor Relish. Proc Natl Acad Sci USA 100: 5991-5996.
54. Sun, L., and Chen, Z.J. (2004) The novel functions of ubiquitination in signaling. Curr Opin Cell Biol 16: 119-126.
55. Takeda, K., Kaisho, T., and Akira, S. (2003) Toll-like receptors. Annu Rev Immunol 21: 335-376.
56. Takehana, A., Katsuyama, T., Yano, T., Oshima, Y., Takada, H., Aigaki, T., and Kurata, S. (2002) 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.
57. Takehana, A., Yano, T., Mita, S., Kotani, A., Oshima, Y., and Kurata, S. (2004) Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J 23: 4690-7000.
58. Tauszig, S., Jouanguy, E., Hoffmann, J.A., and Imler, J.L. (2000) Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc Natl Acad Sci USA 97: 10520-10525.
59. Ting, A.T., Pimentel-Muinos, F.X., and Seed, B. (1996) RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1 -initiated apoptosis. EMBO J 15: 6189-6196.
60. Vidal, S., Khush, R.S., Leulier, F., Tzou, P., Nakamura, M., and Lemaitre, B. (2001) Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev 15: 1900-1912.
61. Wang, C., Deng, L., Hong, M., Akkaraju, G.R., Inoue, J., and Chen, Z.J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412: 346-351.
62. Wang, Z.M., Li, X., Cocklin, R.R., Wang, M., Fukase, K., Inamura, S., et al. (2003) Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-L-alanine amidase. J Biol Chem 278: 49044-49052.
63. Weber, A.N., Tauszig-Delamasure, S., Hoffmann, J.A., Lelievre, E., Gascan, H., Ray, K.P., et al. (2003) Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat Immunol 4: 794-800.
64. Werner, T., Liu, G., Kang, D., Ekengren, S., Steiner, H., and Hultmark, D. (2000) A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA 97: 13772-13777.
65. Werner, T., Borge-Renberg, K., Mellroth, P., Steiner, H., and Hultmark, D. (2003) Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J Biol Chem 278: 26319-26322.
66. Wertz, I.E., O'Rourke, K.M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., et al. (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430: 694-699.
67. Yoshida, H., Kinoshita, K., and Ashida, M. (1996) Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem 271: 13854-13860.
68. Zhou, H., Wertz, I., O'Rourke, K., Ultsch, M., Seshagiri, S., Eby, M., et al. (2004) Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 427: 167-171.