Sensing infection in Drosophila: Toll and beyond

Seminars in Immunology

Volumn 16, Issue 1, 2004, Pages 43-53

  Ferrandon, Dominique ^a   Imler, Jean Luc ^a   Hoffmann, Jules A ^a  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Gram negative binding protein; Pattern recognition receptor; Peptidoglycan recognition protein; Toll; Glucan recognition protein

Indexed keywords

BETA GLUCAN RECOGNITION PROTEIN; BINDING PROTEIN; CYTOKINE; GRAM NEGATIVE BINDING PROTEIN; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN RECOGNITION PROTEIN; PROTEIN; PROTEIN SPAETZLE; RECEPTOR SUBTYPE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; BACTERIAL INFECTION; DROSOPHILA; FUNGUS; GRAM POSITIVE BACTERIUM; IMMUNE SYSTEM; IMMUNITY; MICROBIAL IMMUNITY; MOLECULAR RECOGNITION; NONHUMAN; PATTERN RECOGNITION; PROTEIN FAMILY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 0742272506     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2003.10.008     Document Type: Article

References (100)

1. Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G.et al. The genome sequence of Drosophila melanogaster. Science. 287:2000;2185-2195.
2. Nappi A.J., Vass E. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell. Res. 6:1993;117-126.
3. Braun A., Hoffmann J.A., Meister M. Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc. Natl. Acad. Sci. U.S.A. 95:1998;14337-14342.
4. Basset A., Khush R.S., Braun A., Gardan L., Boccard F., Hoffmann J.A.et al. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl. Acad. Sci. U.S.A. 97:2000;3376-3381.
5. Agaisse H., Petersen U.M., Boutros M., Mathey-Prevot B., Perrimon N. Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell. 5:2003;441-450.
6. Foley E., O'Farrell P.H. Nitric oxide contributes to induction of innate immune responses to Gram-negative bacteria in Drosophila. Genes Dev. 17:2003;115-125.
7. Lanot R., Zachary D., Holder F., Meister M. Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230:2001;243-257.
8. Meister M., Lagueux M. Drosophila blood cells. Cell. Microbiol. 5:2003;573-580.
9. Bulet P., Hetru C., Dimarcq J.L., Hoffmann D. Antimicrobial peptides in insects; structure and function. Dev. Comp. Immunol. 23:1999;329-344.
10. Hoffmann J.A., Reichhart J.M. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3:2002;121-126.
11. 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. 5:2002;102-110.
12. Silverman N., Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev. 15:2001;2321-2342.
13. Hultmark D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15:2003;12-19.
14. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 86:1996;973-983.
15. Sabatier L., Jouanguy E., Dostert C., Zachary D., Dimarcq J.L., Bulet P.et al. Pherokine-2 and -3: two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. Eur. J. Biochem. 270:2003;3398-3407.
16. Lemaitre B., Reichhart J.M., Hoffmann J.A. Drosophila host defense: differential display of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. U.S.A. 94:1997;14614-14619.
17. Rutschmann S., Jung A.C., Hetru C., Reichhart J.-M., Hoffmann J.A., Ferrandon D. The Rel protein DIF mediates the antifungal, but not the antibacterial, response in Drosophila. Immunity. 12:2000;569-580.
18. Janeway C.A. Jr., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20:2002;197-216.
19. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu. Rev. Immunol. 21:2003;335-376.
20. Tauszig S., Jouanguy E., Hoffmann J.A., Imler J.-L. Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 97:2000;10520-10525.
21. Engstrom Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev. Comp. Immunol. 23:1999;345-358.
22. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 68:1992;201-219.
23. Morisato D., Anderson K. Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu. Rev. Genet. 29:1995;371-399.
24. Nüsslein-Volhard C., Lohs-Schardin M., Sander K., Cremer C. A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature. 283:1980;474-476.
25. Hashimoto C., Hudson K.L., Anderson K.V. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell. 52:1988;269-279.
26. Imler J.-L., Hoffmann J.A. Toll receptors in Drosophila: a family of molecules regulating development and immunity. Curr. Top. Microbiol. Immunol. 270:2002;63-79.
27. Lemaitre B., Meister M., Govind S., Georgel P., Steward R., Reichhart J.-M.et al. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J. 14:1995;536-545.
28. Meng X., Khanuja B.S., Ip Y.T. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev. 13:1999;792-797.
29. Manfruelli P., Reichhart J.M., Steward R., Hoffmann J.A., Lemaitre B. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. EMBO J. 18:1999;3380-3391.
30. Tauszig-Delamasure S., Bilak H., Capovilla M., Hoffmann J.A., Imler J.-L. Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat. Immunol. 3:2002;91-97.
31. Sun H., Bristow B.N., Qu G., Wasserman S.A. A heterotrimeric death domain complex in Toll signaling. Proc. Natl. Acad. Sci. USA. 99:2002;12871-12876.
32. Charatsi I., Luschnig S., Bartoszewski S., Nüsslein-Volhard C., Moussian B. Krapfen/dMyd88 is required for the establishment of dorsoventral pattern in the Drosophila embryo. Mech. Dev. 120:2003;219-226.
33. Kambris Z, Bilak H, D'Alessandro R, Belvin M, Imler J-L, Capovilla M. DmMyD88 controls dorsoventral patterning of the Drosophila embryo. EMBO Rep 2003;4;64-9.
34. Horng T., Medzhitov R. Drosophila MyD88 is an adapter in the Toll signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 98:2001;12654-12658.
35. Mizuguchi K., Parker J.S., Blundell T.L., Gay N.J. Getting knotted: a model for the structure and activation of Spatzle. Trends Biochem. Sci. 23:1998;239-242.
36. Bergner A., Oganessyan V., Muta T., Iwanaga S., Typke D., Huber R. Crystal structure of a coagulogen, the clotting protein from horseshoe crab: a structural homologue of nerve growth factor. EMBO J. 15:1996;6789-6797.
37. DeLotto Y., DeLotto R. Proteolytic processing of the Drosophila Spatzle protein by easter generates a dimeric NGF-like molecule with ventralising activity. Mech. Dev. 72:1998;141-148.
38. Weber A.N., Tauszig-Delamasure S., Hoffmann J.A., Lelievre E., Gascan H., Ray K.P.et al. Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat. Immunol. 4:2003;794-800.
39. DeLotto R., Spierer P. A gene required for the specification of dorsal-ventral pattern in Drosophila appears to encode a serine protease. Nature. 323:1986;688-692.
40. Chasan R., Jin Y., Anderson K.V. Activation of the easter zymogen is regulated by five other genes to define dorsal-ventral polarity in the Drosophila embryo. Development. 115:1992;607-616.
41. Chasan R., Anderson K.V. The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo. Cell. 56:1989;391-400.
42. Morisato D., Anderson K.V. The spatzle gene encodes a component of the extracellular signaling pathway establishing the dorsal-ventral pattern of the Drosophila embryo. Cell. 76:1994;677-688.
43. Schneider D.S., Jin Y., Morisato D., Anderson K.V. A processed form of the Spatzle protein defines dorsal-ventral polarity in the Drosophila embryo. Development. 120:1994;1243-1250.
44. Dissing M., Giordano H., DeLotto R. Autoproteolysis and feedback in a protease cascade directing Drosophila dorsal-ventral cell fate. EMBO J. 20:2001;2387-2393.
45. LeMosy E.K., Tan Y.Q., Hashimoto C. Activation of a protease cascade involved in patterning the Drosophila embryo. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5055-5060.
46. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J.A.et al. Constitutive activation of Toll-mediated antifungal defense in serpin-deficient Drosophila. Science. 285:1999;1917-1919.
47. Ligoxygakis P., Pelte N., Hoffmann J.A., Reichhart J.M. Activation of Drosophila Toll during fungal infection by a blood serine protease. Science. 297:2002;114-116.
48. Green C., Levashina E., McKimmie C., Dafforn T., Reichhart J.M., Gubb D. The necrotic gene in Drosophila corresponds to one of a cluster of three serpin transcripts mapping at 43A1.2. Genetics. 156:2000;1117-1127.
49. Pujol N., Link E.M., Liu L.X., Kurz C.L., Alloing G., Tan M.-W.et al. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr. Biol. 11:2001;809-821.
50. Du X., Poltorak A., Wei Y., Beutler B. Three novel mammalian toll-like receptors: gene structure, expression, and evolution. Eur. Cytokine Netw. 11:2000;362-371.
51. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C.et al. Immunity-related genes and gene families in Anopheles gambiae. Science. 298:2002;159-165.
52. Imler J-L, Zheng M. Biology of Toll receptors: lessons from insects and mammals. J Leukoc Biol 2003, in press.
53. Parker J.S., Mizuguchi K., Gay N.J. A family of proteins related to Spatzle, the toll receptor ligand, are encoded in the Drosophila genome. Proteins. 45:2001;71-80.
54. Poltorak A., He X., Smirnova I., Liu M.Y., Huffel C.V., Du X.et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 282:1998;2085-2088.
55. Bilak H., Tauszig-Delamasure S., Imler J.-L. Toll and Toll-like receptors in Drosophila. Biochem. Soc. Trans. 31:2003;648-651.
56. Luo C., Shen B., Manley J.L., Zheng L. Tehao functions in the Toll pathway in Drosophila melanogaster: possible roles in development and innate immunity. Insect Mol. Biol. 10:2001;457-464.
57. Ooi J.Y., Yagi Y., Hu X., Ip Y.T. The Drosophila Toll-9 activates a constitutive antimicrobial defense. EMBO Rep. 3:2002;82-87.
58. Ligoxygakis P., Bulet P., Reichhart J.M. Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila. EMBO Rep. 3:2002;666-673.
59. Gerttula S., Jin Y.S., Anderson K.V. Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics. 119:1988;123-133.
60. Eldon E., Kooyer S., D'Evelyn D., Duman M., Lawinger P., Botas J. The Drosophila 18 wheeler gene is required for morphogenesis and has striking similarities to Toll. Development. 120:1994;885-899.
61. Kambris Z., Hoffmann J.A., Imler J.-L., Capovilla M. Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expr. Patterns. 2:2002;311-317.
62. Anderson K.V., Jürgens G., Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell. 42:1985;779-789.
63. Anderson K.V., Boka L., Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell. 42:1985;791-798.
64. Chiang C., Beachy P.A. Expression of a novel Toll-like gene spans the parasegment boundary and contributes to hedgehog function in the adult eye of Drosophila. Mech. Dev. 47:1994;225-239.
65. Seppo A., Matani P., Sharrow M., Tiemeyer M. Induction of neuron-specific glycosylation by Tollo/Toll-8, a Drosophila Toll-like receptor expressed in non-neural cells. Development. 130:2003;1439-1448.
66. Yoshida H., Ochiai M., Ashida M. Beta-1,3-glucan receptor and peptidoglycan receptor are present as separate entities within insect prophenoloxidase activating system. Biochem. Biophys. Res. Commun. 141:1986;1177-1184.
67. Ochiai M., Ashida M. Purification of a beta-1,3-glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 263:1988;12056-12062.
68. Yoshida H., Kinoshita K., Ashida M. Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 271:1996;13854-13860.
69. Ochiai M., Ashida M. A pattern recognition protein for peptidoglycan. Cloning the cDNA and the gene of the silkworm, Bombyx mori. J. Biol. Chem. 274:1999;11854-11858.
70. Ochiai M., Ashida M. A pattern-recognition protein for beta-1,3-glucan. The binding domain and the cDNA cloning of beta-1,3-glucan recognition protein from the silkworm, Bombyx mori. J. Biol. Chem. 275:2000;4995-5002.
71. 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. U.S.A. 95:1998;10078-10082.
72. Mellroth P., Karlsson J., Steiner H. A scavenger function for a Drosophila peptidoglycan recognition protein. J. Biol. Chem. 278:2003;7059-7064.
73. Kim M.S., Byun M., Oh B.H. Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat. Immunol. 4:2003;787-793.
74. Gelius E., Persson C., Karlsson J., Steiner H. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem. Biophys. Res. Commun. 306:2003;988-994.
75. Liepinsh E., Genereux C., Dehareng D., Joris B., Otting G. NMR structure of Citrobacter freundii AmpD, comparison with bacteriophage T7 lysozyme and homology with PGRP domains. J. Mol. Biol. 327:2003;833-842.
76. Werner T., Liu G., Kang D., Ekengren S., Steiner H., Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 97:2000;13772-13777.
77. Takehana A., Katsuyama T., Yano T., Oshima Y., Takada H., Aigaki T.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. U.S.A. 99:2002;13705-13710.
78. Michel T., Reichhart J., Hoffmann J.A., Royet J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature. 414:2001;756-759.
79. Gobert V, Gottar M, Matskevich A, Rutschmann S, Royet J, Belvin M, et al. Dual activation of the Drosophila Toll pathway by two pattern recognition receptors. 2003, in press.
80. Gottar M., Gobert V., Michel T., Belvin M., Duyk G., Hoffmann J.A.et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature. 416:2002;640-644.
81. 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. 296:2002;359-362.
82. 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. 416:2002;644-648.
83. Leulier F., Parquet C., Pili-Floury S., Ryu J.H., Caroff M., Lee W.J.et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol. 4:2003;478-484.
84. Werner T, Borge-Renberg K, Mellroth P, Steiner H, Hultmark D. Functional diversity of the Drosophila PGRP-LC gene cluster in the response to LPS and peptidoglycan. J Biol Chem 2003;278:26319-22.
85. Lee W.J., Lee J.D., Kravchenko V.V., Ulevitch R.J., Brey P.T. Purification and molecular cloning of an inducible Gram-negative bacteria-binding protein from the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. U.S.A. 93:1996;7888-7893.
86. Ma C., Kanost M.R. A Beta1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biol. Chem. 275:2000;7505-7514.
87. Zhang R, Cho HY, Kim HS, Ma YG, Osaki T, Kawabata SI, et al. Characterization and properties of a 1,3-β-D-glucan pattern recognition protein of Tenebrio molitor larvae which is specifically degraded by serine protease during prophenoloxidase activation. J Biol Chem 2003;278:42072-9.
88. Kim Y.S., Ryu J.H., Han S.J., Choi K.H., Nam K.B., Jang I.H.et al. Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J. Biol. Chem. 275:2000;32721-32727.
89. Girardin S.E., Boneca I.G., Viala J., Chamaillard M., Labigne A., Thomas G.et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278:2003;8869-8872.
90. Chamaillard M., Hashimoto M., Horie Y., Masumoto J., Qiu S., Saab L.et al. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 4:2003;702-707.
91. Girardin S.E., Boneca I.G., Carneiro L.A., Antignac A., Jehanno M., Viala J.et al. Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science. 300:2003;1584-1587.
92. Girardin SE, Travassos LH, Herve M, Blanot D, Boneca IG, Philpott DJ, et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 2003;278:41702-8.
93. 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. 29:1999;19-24.
94. Beutler B., Rietschel E.T. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3:2003;169-176.
95. Nakamura T., Tokunaga F., Morita T., Iwanaga S. Interaction between lipopolysaccharide and intracellular serine protease zymogen, factor C, from horseshoe crab (Tachypleus tridentatus) hemocytes. J. Biochem. (Tokyo). 103:1988;370-374.
96. Muta T., Iwanaga S. The role of hemolymph coagulation in innate immunity. Curr. Opin. Immunol. 8:1996;41-47.
97. Dziarski R., Platt K.A., Gelius E., Steiner H., Gupta D. Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic Gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S) -deficient mice. Blood. 102:2003;689-697.
98. Tydell C.C., Yount N., Tran D., Yuan J., Selsted M.E. Isolation, characterization, and antimicrobial properties of bovine oligosaccharide- binding protein. A microbicidal granule protein of eosinophils and neutrophils. J. Biol. Chem. 277:2002;19658-19664.
99. Liu C., Gelius E., Liu G., Steiner H., Dziarski R. Mammalian peptidoglycan recognition protein binds peptidoglycan with high affinity, is expressed in neutrophils, and inhibits bacterial growth. J. Biol. Chem. 275:2000;24490-24499.
100. Lee MH, Osaki T, Lee JY, Baek MJ, Zhang R, Park JW, Kawabata SI, Soderhall K, Lee BI. Peptidoglycan recognition proteins involved in 1,3-beta-D-glucan-dependent prophenoloxidase activation system of insect. J Biol Chem 2003. [E-pub ahead of print].