Activation of Imd pathway in hemocyte confers infection resistance through humoral response in Drosophila

Biochemical and Biophysical Research Communications

Volumn 430, Issue 3, 2013, Pages 1120-1125

  Nelson, Bryce ^a,e   Freisinger, Tina ^a,b   Ishii, Kenichi ^c   Okado, Kiyoshi ^a,d   Shinzawa, Naoaki ^a,c,f   Fukumoto, Shinya ^a   Kanuka, Hirotaka ^a,c,d  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

^d JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF TORONTO   (Canada)

^f EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Antimicrobial peptide; Bacteria; Drosophila; Infection; Innate immunity

Indexed keywords

BACTERIAL PROTEIN; DROSOMYCIN; PROTEIN IMD; UNCLASSIFIED DRUG;

ARTICLE; BLOOD CELL; CELLULAR IMMUNITY; DROSOPHILA MELANOGASTER; FEMALE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMORAL IMMUNITY; INFECTION RESISTANCE; INNATE IMMUNITY; MALE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; UPREGULATION;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEMOCYTES; IMMUNITY, HUMORAL; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

DROSOPHILA MELANOGASTER; NEGIBACTERIA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 84872487492     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.027     Document Type: Article

References (47)

1. Hoffmann J.A. The immune response of Drosophila. Nature 2003, 426:33-38.
2. Brennan C.A., Anderson K.V. Drosophila: the genetics of innate immune recognition and response. Annu. Rev. Immunol. 2004, 22:457-483.
3. Yano T., Mita S., Ohmori H., Oshima Y., Fujimoto Y., Ueda R., Takada H., Goldman W.E., Fukase K., Silverman N., Yoshimori T., Kurata S. Autophagic control of listeria through intracellular innate immune recognition in drosophila. Nat. Immunol. 2008, 9:908-916.
4. Haine E.R., Moret Y., Siva-Jothy M.T., Rolff J. Antimicrobial defense and persistent infection in insects. Science 2008, 322:1257-1259.
5. Brennan C.A., Delaney J.R., Schneider D.S., Anderson K.V. Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body. Curr. Biol. 2007, 17:67-72.
6. Lemaitre B., Meister M., Govind S., Georgel P., Steward R., et al. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J. 1995, 14:536-545.
7. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
8. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., et al. Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 1999, 285:1917-1919.
9. Horng T., Medzhitov R. Drosophila MyD88 is an adapter in the Toll signaling pathway. Proc. Natl. Acad. Sci. USA 2001, 98:12654-12658.
10. Ligoxygakis P., Pelte N., Hoffmann J.A., Reichhart J. Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 2002, 297:114-116.
11. Ip Y.T., Reach M., Engstrom Y., Kadalayil L., Cai H., et al. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 1993, 75:753-763.
12. Nicolas E., Reichhart J.M., Hoffmann J.A., Lemaitre B. In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila. J. Biol. Chem. 1998, 273:10463-10469.
13. 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. 2002, 3:91-97.
14. Lemaitre B., Kromer-Metzger E., Michaut L., Nicolas E., Meister M., et al. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. USA 1995, 92:9465-9469.
15. Hu S., Yang X. dFADD, a novel death domain-containing adapter protein for the Drosophila caspase DREDD. J. Biol. Chem. 2000, 275:30761-30764.
16. Rutschmann S., Jung A.C., Zhou R., Silverman N., Hoffmann J.A., et al. Role of Drosophila IKK gamma in a toll-independent antibacterial immune response. Nat. Immunol. 2000, 1:342-347.
17. Silverman N., Zhou R., Stoven S., Pandey N., Hultmark D., et al. A Drosophila IkappaB kinase complex required for relish cleavage and antibacterial immunity. Genes Dev. 2000, 14:2461-2471.
18. Stoven S., Ando I., Kadalayil L., Engstrom Y., Hultmark D. Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep. 2000, 1:347-352.
19. Georgel P., Naitza S., Kappler C., Ferrandon D., Zachary D., et al. Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev. Cell 2001, 1:503-514.
20. Lu Y., Wu L.P., Anderson K.V. The Antibacterial arm of the Drosophila innate immune response requires an IkappaB Kinase. Genes Dev. 2001, 15:104-110.
21. Vidal S., Khush R.S., Leulier F., Tzou P., Nakamura M., et al. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NFkappaB-dependent innate immune responses. Genes Dev. 2001, 15:1900-1912.
22. Leulier F., Vidal S., Saigo K., Ueda R., Lemaitre B. Inducible expression of double-stranded RNA reveals a role for dFADD in the regulation of the antibacterial response in Drosophila adults. Curr. Biol. 2002, 12:996-1000.
23. Hultmark D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 2003, 15:12-19.
24. Dionne M.S., Schneider D.S. Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis. Model. Mech. 2008, 1:43-49.
25. Hedengren M., Asling B., Dushay M.S., Ando I., Ekengren S., et al. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol. Cell 1999, 4:827-837.
26. Pham L.N., Dionne M.S., Shirasu-Hiza M., Schneider D.S. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 2007, 3:e26.
27. 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. 2002, 21:2568-2579.
28. Rutschmann S., Kilinc A., Ferrandon D. Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J. Immunol. 2002, 168:1542-1546.
29. Tanji T., Hu X., Weber A.N., Ip Y.T. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol. Cell. Biol. 2007, 27:4578-4588.
30. Hedengren-Olcott M., Olcott M.C., Mooney D.T., Ekengren S., Geller B.L., et al. Differential activation of the NF-kappaB-like factors Relish and Dif in Drosophila melanogaster by fungi and Gram-positive bacteria. J. Biol. Chem. 2004, 279:21121-21127.
31. Takehana A., Katsuyama T., Yano T., Oshima Y., Takada H., 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 2002, 99:13705-13710.
32. Leulier F., Parquet C., Pili-Floury S., Ryu J.H., Caroff M., et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat. Immunol. 2003, 4:478-484.
33. Pili-Floury S., Leulier F., Takahashi K., Saigo K., Samain E., et al. 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. 2004, 279:12848-12853.
34. Leone P., Bischoff V., Kellenberger C., Hetru C., Royet J., et al. Crystal structure of Drosophila PGRP-SD suggests binding to DAP-type but not lysine-type peptidoglycan. Mol. Immunol. 2008, 45:2521-2530.
35. Toba G., Ohsako T., Miyata N., Ohtsuka T., Seong K.H., et al. The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 1999, 151:725-737.
36. Hamamoto H., Kurokawa K., Kaito C., Kamura K., Manitra Razanajatovo I., et al. Quantitative evaluation of the therapeutic effects of antibiotics using silkworms infected with human pathogenic microorganisms. Antimicrob. Agents Chemother. 2004, 48:774-779.
37. Elrod-Erickson M., Mishra S., Schneider D. Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 2000, 10:781-784.
38. De Gregorio E., Han S.J., Lee W.J., Baek M.J., Osaki T., et al. An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev. Cell 2002, 3:581-592.
39. Okado K., Shinzawa N., Aonuma H., Nelson B., Fukumoto S., et al. Rapid recruitment of innate immunity regulates variation intracellular pathogen resistance in Drosophila. Biochem. Biophys. Res. Commun. 2009, 379:6-10.
40. Stofanko M., Kwon S.Y., Badenhorst P. A misexpression screen to identify regulators of Drosophila larval hemocyte development. Genetics 2008, 180:253-267.
41. Huh J.R., Foe I., Muro I., Chen C.H., Seol J.H., et al. The Drosophila inhibitor of apoptosis (IAP) DIAP2 is dispensable for cell survival, required for the innate immune response to gram-negative bacterial infection, and can be negatively regulated by the reaper/hid/grim family of IAP-binding apoptosis inducers. J. Biol. Chem. 2007, 282:2056-2068.
42. Ayres J.S., Schneider D.S. A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 2008, 6:2764-2773.
43. Shinzawa N., Nelson B., Aonuma H., Okado K., Fukumoto S., Miura M., Kanuka H. P38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila. Cell Host Microbe 2009, 6:244-252.
44. Tzou P., Ohresser S., Ferrandon D., Capovilla M., Reichhart J.M., et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 2000, 13:737-748.
45. Lau G.W., Goumnerov B.C., Walendziewicz C.L., Hewitson J., Xiao W., et al. The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect. Immun. 2003, 71:4059-4066.
46. Mansfield B.E., Dionne M.S., Schneider D.S., Freitag N.E. Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol. 2003, 5:901-911.
47. Charroux B., Royet J. Elimination of plasmatocytes by targeted apoptosis reveals their orle in multiple aspects of the Drosophila immune response. Proc. Natl. Acad. Sci. USA 2009, 106:9797-9802.