A multilayered defense against infection: combinatorial control of insect immune genes

Trends in Genetics

Volumn 23, Issue 7, 2007, Pages 342-349

  Uvell, Hanna ^a   Engström, Ylva ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; HOX PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR REL;

EPITHELIUM; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IMMUNITY; INFECTION; INSECT; MICROORGANISM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; DIMERIZATION; FEMALE; GENES, INSECT; IMMUNE SYSTEM; INFECTION; INSECT PROTEINS; INSECTS; MALE; MODELS, BIOLOGICAL; NF-KAPPA B; PROMOTER REGIONS (GENETICS); SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

HEXAPODA;

EID: 34250711204     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2007.05.003     Document Type: Review

References (82)

1. Theopold U., et al. Coagulation in arthropods: defence, wound closure and healing. Trends Immunol. 25 (2004) 289-294
2. Meister M. Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 16 (2004) 10-15
3. Lemaitre B., and Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25 (2007) 697-743
4. Sadd B.M., and Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol. 16 (2006) 1206-1210
5. Pham L.N., et al. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog. 3 (2007) e26
6. Watson F.L., et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309 (2005) 1874-1878
7. Dong Y., et al. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol. 4 (2006) e229
8. Siva-Jothy M.T., et al. Insect immunity: an evolutionary ecology perspective. Adv. Insect Physiol. 32 (2005) 1-48
9. Uttenweiler-Joseph S., et al. Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 11342-11347
10. Steiner H. Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol. Rev. 198 (2004) 83-96
11. Royet J., and Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat. Rev. Microbiol. 5 (2007) 264-277
12. Kim Y.S., 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
13. Gottar M., et al. Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127 (2006) 1425-1437
14. Lemaitre B., et al. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9465-9469
15. Hedengren M., et al. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol. Cell 4 (1999) 827-837
16. 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 (2001) 1900-1912
17. Kallio J., et al. Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells. Microbes Infect. 7 (2005) 811-819
18. Delaney J.R., et al. Cooperative control of Drosophila immune responses by the JNK and NF-κB signaling pathways. EMBO J. 25 (2006) 3068-3077
19. Boutros M., et al. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3 (2002) 711-722
20. De Gregorio E., et al. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 12590-12595
21. De Gregorio E., et al. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 21 (2002) 2568-2579
22. Irving P., et al. A genome-wide analysis of immune responses in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 15119-15124
23. Johansson K.C., et al. Microarray analysis of immune challenged Drosophila hemocytes. Exp. Cell Res. 305 (2005) 145-155
24. Park J.M., et al. Targeting of TAK1 by the NF-κB protein Relish regulates the JNK-mediated immune response in Drosophila. Genes Dev. 18 (2004) 584-594
25. Agaisse H., and Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol. Rev. 198 (2004) 72-82
26. Tzou P., et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13 (2000) 737-748
27. Selsted M.E., and Ouellette A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6 (2005) 551-557
28. Zasloff M. Defending the epithelium. Nat. Med. 12 (2006) 607-608
29. Ferrandon D., et al. A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. EMBO J. 17 (1998) 1217-1227
30. Önfelt Tingvall T., et al. The imd gene is required for local Cecropin expression in Drosophila barrier epithelia. EMBO Rep. 2 (2001) 239-243
31. Tingvall T.O., et al. The GATA factor Serpent is required for the onset of the humoral immune response in Drosophila embryos. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3884-3888
32. Ryu J.H., et al. The homeobox gene Caudal regulates constitutive local expression of antimicrobial peptide genes in Drosophila epithelia. Mol. Cell. Biol. 24 (2004) 172-185
33. Senger K., et al. GATA factors participate in tissue-specific immune responses in Drosophila larvae. Proc. Natl. Acad. Sci. U S A 103 (2006) 15957-15962
34. Zaidman-Remy A., et al. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24 (2006) 463-473
35. McGettigan J., et al. Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem. Mol. Biol. 35 (2005) 741-754
36. Liehl P., et al. Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog. 2 (2006) e56
37. Ryu J.H., et al. An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunity. EMBO J. 25 (2006) 3693-3701
38. Samakovlis C., et al. The andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. EMBO J. 10 (1991) 163-169
39. McGraw L.A., et al. Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14 (2004) 1509-1514
40. Peng J., et al. Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Curr. Biol. 15 (2005) 1690-1694
41. Moussian B., and Uv A.E. An ancient control of epithelial barrier formation and wound healing. Bioessays 27 (2005) 987-990
42. Kim T., et al. Downregulation of lipopolysaccharide response in Drosophila by negative crosstalk between the AP1 and NF-κB signaling modules. Nat Immunol 6 (2005) 211-218
43. Brandt S.M., et al. Secreted bacterial effectors and host-produced eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol. 2 (2004) e418
44. Bischoff V., et al. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog. 2 (2006) e14
45. Engström Y., et al. κB-like motifs regulate the induction of immune genes in Drosophila. J. Mol. Biol. 232 (1993) 327-333
46. Kappler C., et al. Insect immunity. Two 17 bp repeats nesting a κB-related sequence confer inducibility to the diptericin gene and bind a polypeptide in bacteria-challenged Drosophila. EMBO J. 12 (1993) 1561-1568
47. Ip Y.T., et al. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 75 (1993) 753-763
48. Reichhart J.M., et al. Expression and nuclear translocation of the rel/NF-κB-related morphogen dorsal during the immune response of Drosophila. C. R. Acad. Sci. III 316 (1993) 1218-1224
49. Petersen U.M., et al. The dorsal-related immunity factor, Dif, is a sequence-specific trans- activator of Drosophila Cecropin gene expression. EMBO J. 14 (1995) 3146-3158
50. Stöven S., et al. Activation of the Drosophila NF-κB factor Relish by rapid endoproteolytic cleavage. EMBO Rep. 1 (2000) 347-352
51. Han Z.S., and Ip Y.T. Interaction and specificity of Rel-related proteins in regulating Drosophila immunity gene expression. J. Biol. Chem. 274 (1999) 21355-21361
52. Meng X., et al. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappa B factor. Genes Dev. 13 (1999) 792-797
53. Rutschmann S., et al. The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila. Immunity 12 (2000) 569-580
54. Lemaitre B., et al. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86 (1996) 973-983
55. Lehming N., et al. Interactions of a Rel protein with its inhibitor. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10242-10246
56. Tatei K., and Levine M. Specificity of Rel-inhibitor interactions in Drosophila embryos. Mol. Cell. Biol. 15 (1995) 3627-3634
57. Gross I., et al. Drosophila immunity: a comparative analysis of the Rel proteins dorsal and Dif in the induction of the genes encoding diptericin and cecropin. Nucleic Acids Res. 24 (1996) 1238-1245
58. Stein D., et al. The Dorsal-related immunity factor (Dif) can define the dorsal-ventral axis of polarity in the Drosophila embryo. Development 125 (1998) 2159-2169
59. Wu L.P., and Anderson K.V. Regulated nuclear import of Rel proteins in the Drosophila immune response. Nature 392 (1998) 93-97
60. Hedengren-Olcott M., et al. Differential activation of the NF-κB-like factors Relish and Dif in Drosophila melanogaster by fungi and Gram-positive bacteria. J. Biol. Chem. 279 (2004) 21121-21127
61. Senger K., et al. Immunity regulatory DNAs share common organizational features in Drosophila. Mol. Cell 13 (2004) 19-32
62. Engström Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev. Comp. Immunol. 4-5 (1999) 345-358
63. Uvell H., and Engström Y. Functional characterization of a novel promoter element required for an innate immune response in Drosophila. Mol. Cell. Biol. 23 (2003) 8272-8281
64. Park J.M., et al. Signal-induced transcriptional activation by Dif requires the dTRAP80 Mediator module. Mol. Cell. Biol. 23 (2003) 1358-1367
65. Kim Y.J., and Lis J.T. Interactions between subunits of Drosophila Mediator and activator proteins. Trends Biochem. Sci. 30 (2005) 245-249
66. Yagi Y., and Ip Y.T. Helicase89B is a Mot1p/BTAF1 homologue that mediates an antimicrobial response in Drosophila. EMBO Rep. 6 (2005) 1088-1094
67. Kadalayil L., et al. Adjacent GATA and κB-like motifs regulate the expression of a Drosophila immune gene. Nucleic Acids Res. 25 (1997) 1233-1239
68. Petersen U.-M., et al. Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif. EMBO J. 18 (1999) 4013-4022
69. Letting D.L., et al. Formation of a tissue-specific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol. Cell. Biol. 23 (2003) 1334-1340
70. Shapira M., et al. A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 14086-14091
71. Junell A., et al. Isolation of regulators of Drosophila immune defense genes by a double interaction screen in yeast. Insect Biochem. Mol. Biol. 37 (2007) 202-212
72. Ochoa-Espinosa A., and Small S. Developmental mechanisms and cis-regulatory codes. Curr. Opin. Genet. Dev. 16 (2006) 165-170
73. Hultmark D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15 (2003) 12-19
74. Bulet P., et al. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 198 (2004) 169-184
75. Tzou P., et al. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2152-2157
76. Hayden M.S., and Ghosh S. Signaling to NF-κB. Genes Dev. 18 (2004) 2195-2224
77. Bresnick E.H., et al. Developmental control via GATA factor interplay at chromatin domains. J. Cell. Physiol. 205 (2005) 1-9
78. Gehring W.J., et al. Homeodomain proteins. Annu. Rev. Biochem. 63 (1994) 487-526
79. Morgan R. Hox genes: a continuation of embryonic patterning?. Trends Genet. 22 (2006) 67-69
80. Ryan A.K., and Rosenfeld M.G. POU domain family values: flexibility, partnerships, and developmental codes. Genes Dev. 11 (1997) 1207-1225
81. Samakovlis C., et al. The immune response in Drosophila: pattern of cecropin expression and biological activity. EMBO J. 9 (1990) 2969-2976
82. Reichhart J.M., et al. Insect immunity: developmental and inducible activity of the Drosophila diptericin promoter. EMBO J. 11 (1992) 1469-1477