Akirin specifies NF-κB selectivity of Drosophila innate immune response via chromatin remodeling

EMBO Journal

Volumn 33, Issue 20, 2014, Pages 2349-2362

  Bonnay, François ^a   Nguyen, Xuan Hung ^a   Cohen Berros, Eva ^a   Troxler, Laurent ^a   Batsche, Eric ^b   Camonis, Jacques ^c   Takeuchi, Osamu ^d   Reichhart, Jean Marc ^a   Matt, Nicolas ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT PASTEUR   (France)

^c INSTITUT CURIE   (France)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Chromatin remodeling; Drosophila; Innate immune response; NF B

Indexed keywords

AKIRIN PROTEIN; BRM PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR PROTEIN; PROTEIN SWI; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELISH; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG; AKIRIN1 PROTEIN, DROSOPHILA; BAP60 PROTEIN, DROSOPHILA; BRM PROTEIN, DROSOPHILA; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; OSA PROTEIN, DROSOPHILA; RELISH PROTEIN, DROSOPHILA; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; EPIGENETICS; GENE ACTIVATION; GENE TARGETING; GENETIC MARKER; GENETIC TRANSCRIPTION; IMMUNE DEFICIENCY; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; PROTEIN ANALYSIS; PROTEOMICS; ANIMAL; FEMALE; GENETICS; MALE; METABOLISM; MUTATION; PROMOTER REGION; TRANSCRIPTION INITIATION; TWO HYBRID SYSTEM;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; IMMUNITY, INNATE; MALE; MUTATION; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEOMICS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84911479016     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488456     Document Type: Article

References (56)

1. Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW, (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21: 5245-5254
2. Batsche E, Yaniv M, Muchardt C, (2006) The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 13: 22-29
3. Bonnay F, Cohen-Berros E, Hoffmann M, Kim SY, Boulianne GL, Hoffmann JA, Matt N, Reichhart JM, (2013) big bang gene modulates gut immune tolerance in Drosophila. Proc Natl Acad Sci USA 110: 2957-2962
4. Bou Aoun R, Hetru C, Troxler L, Doucet D, Ferrandon D, Matt N, (2011) Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J Innate Immun 3: 52-64
5. Corden JL, (1990) Tails of RNA polymerase II. Trends Biochem Sci 15: 383-387
6. Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM, (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35: D486-D491
7. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B, (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 21: 2568-2579
8. Deaton AM, Bird A, (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010-1022
9. Ferrandon D, Imler JL, Hetru C, Hoffmann JA, (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7: 862-874
10. Fromont-Racine M, Rain JC, Legrain P, (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 16: 277-282
11. Fukuyama H, Verdier Y, Guan Y, Makino-Okamura C, Shilova V, Liu X, Maksoud E, Matsubayashi J, Haddad I, Spirohn K, Ono K, Hetru C, Rossier J, Ideker T, Boutros M, Vinh J, Hoffmann JA, (2013) Landscape of protein-protein interactions in Drosophila immune deficiency signaling during bacterial challenge. Proc Natl Acad Sci USA 110: 10717-10722
12. Ghosh S, Hayden MS, (2012) Celebrating 25 years of NF-kappaB research. Immunol Rev 246: 5-13
13. Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E, Vijayadamodar G, Pochart P, Machineni H, Welsh M, Kong Y, Zerhusen B, Malcolm R, Varrone Z, Collis A, Minto M, et al, (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727-1736
14. Goto A, Fukuyama H, Imler JL, Hoffmann JA, (2014) The chromatin regulator DMAP1 modulates activity of the NF-kappaB transcription factor Relish in the Drosophila innate immune response. J Biol Chem 289: 20470-20476.
15. Goto A, Kumagai T, Kumagai C, Hirose J, Narita H, Mori H, Kadowaki T, Beck K, Kitagawa Y, (2001) A Drosophila haemocyte-specific protein, hemolectin, similar to human von Willebrand factor. Biochem J 359: 99-108
16. Goto A, Matsushita K, Gesellchen V, El Chamy L, Kuttenkeuler D, Takeuchi O, Hoffmann JA, Akira S, Boutros M, Reichhart JM, (2008) Akirins are highly conserved nuclear proteins required for NF-kappaB-dependent gene expression in Drosophila and mice. Nat Immunol 9: 97-104
17. Guillemette B, Drogaris P, Lin HH, Armstrong H, Hiragami-Hamada K, Imhof A, Bonneil E, Thibault P, Verreault A, Festenstein RJ, (2011) H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet 7: e1001354
18. Guruharsha KG, Obar RA, Mintseris J, Aishwarya K, Krishnan RT, Vijayraghavan K, Artavanis-Tsakonas S, (2012) Drosophila protein interaction map (DPiM): a paradigm for metazoan protein complex interactions. Fly 6: 246-253
19. Hargreaves DC, Horng T, Medzhitov R, (2009) Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138: 129-145
20. Hayden MS, Ghosh S, (2012) NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234
21. Hedengren M, Asling B, Dushay MS, Ando I, Ekengren S, Wihlborg M, Hultmark D, (1999) Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol Cell 4: 827-837
22. Hetru C, Hoffmann JA, (2009) NF-kappaB in the immune response of Drosophila. Cold Spring Harb Perspect Biol 1: a000232
23. Hoffmann JA, Reichhart JM, (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3: 121-126
24. Hrdlicka L, Gibson M, Kiger A, Micchelli C, Schober M, Schock F, Perrimon N, (2002) Analysis of twenty-four Gal4 lines in Drosophila melanogaster. Genesis 34: 51-57
25. Imler JL, Bulet P, (2005) Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy 86: 1-21
26. Irving P, Troxler L, Heuer TS, Belvin M, Kopczynski C, Reichhart JM, Hoffmann JA, Hetru C, (2001) A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci USA 98: 15119-15124
27. Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, McCord RA, Ongaigui KC, Boxer LD, Chang HY, Chua KF, (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136: 62-74
28. Kuttenkeuler D, Pelte N, Ragab A, Gesellchen V, Schneider L, Blass C, Axelsson E, Huber W, Boutros M, (2010) A large-scale RNAi screen identifies Deaf1 as a regulator of innate immune responses in Drosophila. J Innate Immun 2: 181-194
29. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA, (2001) Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 7: 1291-1297
30. Lemaitre B, Reichhart JM, Hoffmann JA, (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. Macqueen DJ, Johnston IA, (2009) Evolution of the multifaceted eukaryotic akirin gene family. BMC Evol Biol 9: 34
32. Maeda S, Omata M, (2008) Inflammation and cancer: role of nuclear factor-kappaB activation. Cancer Sci 99: 836-842
33. Mohrmann L, Langenberg K, Krijgsveld J, Kal AJ, Heck AJ, Verrijzer CP, (2004) Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol Cell Biol 24: 3077-3088
34. Moller A, Avila FW, Erickson JW, Jackle H, (2005) Drosophila BAP60 is an essential component of the Brahma complex, required for gene activation and repression. J Mol Biol 352: 329-337
35. Moshkin YM, Mohrmann L, van Ijcken WF, Verrijzer CP, (2007) Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol Cell Biol 27: 651-661
36. Mukherji A, Kobiita A, Ye T, Chambon P, (2013) Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153: 812-827
37. Nanty L, Carbajosa G, Heap GA, Ratnieks F, van Heel DA, Down TA, Rakyan VK, (2011) Comparative methylomics reveals gene-body H3K36me3 in Drosophila predicts DNA methylation and CpG landscapes in other invertebrates. Genome Res 21: 1841-1850
38. Nowak SJ, Aihara H, Gonzalez K, Nibu Y, Baylies MK, (2012) Akirin links twist-regulated transcription with the Brahma chromatin remodeling complex during embryogenesis. PLoS Genet 8: e1002547
39. Oeckinghaus A, Hayden MS, Ghosh S, (2011) Crosstalk in NF-kappaB signaling pathways. Nat Immunol 12: 695-708
40. Pal S, Wu J, Wu LP, (2008) Microarray analyses reveal distinct roles for Rel proteins in the Drosophila immune response. Dev Comp Immunol 32: 50-60
41. Papoulas O, Beek SJ, Moseley SL, McCallum CM, Sarte M, Shearn A, Tamkun JW, (1998) The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development 125: 3955-3966
42. Paredes JC, Welchman DP, Poidevin M, Lemaitre B, (2011) Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35: 770-779
43. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, Black JC, Hoffmann A, Carey M, Smale ST, (2009) A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138: 114-128
44. Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R, Imbalzano AN, Smale ST, (2006) Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev 20: 282-296
45. Reichhart JM, Gubb D, Leclerc V, (2011) The Drosophila serpins: multiple functions in immunity and morphogenesis. Methods Enzymol 499: 205-225
46. Rutschmann S, Jung AC, Zhou R, Silverman N, Hoffmann JA, Ferrandon D, (2000) Role of Drosophila IKK gamma in a toll-independent antibacterial immune response. Nat Immunol 1: 342-347
47. Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ, (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319: 777-782
48. Smale ST, (2010) Selective transcription in response to an inflammatory stimulus. Cell 140: 833-844
49. Stoven S, Ando I, Kadalayil L, Engstrom Y, Hultmark D, (2000) Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep 1: 347-352
50. Stoven S, Silverman N, Junell A, Hedengren-Olcott M, Erturk D, Engstrom Y, Maniatis T, Hultmark D, (2003) Caspase-mediated processing of the Drosophila NF-kappaB factor Relish. Proc Natl Acad Sci USA 100: 5991-5996
51. Tartey S, Matsushita K, Vandenbon A, Ori D, Imamura T, Mino T, Standley DM, Hoffmann JA, Reichhart JM, Akira S, Takeuchi O, (2014) Akirin2 is critical for inducing inflammatory genes by bridging IκB-ζ and the SWI/SNF complex. EMBO J 33: 2332-2348
52. Tauszig S, Jouanguy E, Hoffmann JA, Imler JL, (2000) Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc Natl Acad Sci USA 97: 10520-10525
53. Tauszig-Delamasure S, Bilak H, Capovilla M, Hoffmann JA, Imler JL, (2002) Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat Immunol 3: 91-97
54. Vidal S, Khush RS, Leulier F, Tzou P, Nakamura M, 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
55. Vojtek AB, Hollenberg SM, Cooper JA, (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74: 205-214
56. Wang W, (2003) The SWI/SNF family of ATP-dependent chromatin remodelers: similar mechanisms for diverse functions. Curr Top Microbiol Immunol 274: 143-169