Akirin2 is critical for inducing inflammatory genes by bridging IκB-ζ and the SWI/SNF complex

EMBO Journal

Volumn 33, Issue 20, 2014, Pages 2332-2348

  Tartey, Sarang ^a,b,c,d   Matsushita, Kazufumi ^e   Vandenbon, Alexis ^f   Ori, Daisuke ^a,b   Imamura, Tomoko ^a,b   Mino, Takashi ^a,b   Standley, Daron M ^f   Hoffmann, Jules A ^g   Reichhart, Jean Marc ^g   Akira, Shizuo ^c,d   Takeuchi, Osamu ^a,b,c  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e HYOGO COLLEGE OF MEDICINE   (Japan)

^f Laboratory of Systems Immunology WPI Immunology Frontier Research Center (IFReC)   (Japan)

^g INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

chromatin remodeling; cytokine; gene regulation; innate immunity; macrophages

Indexed keywords

AKIRIN 2; BRG1 ASSOCIATED FACTOR 60 PROTEIN; BRG1 PROTEIN; I KAPPA B; I KAPPA B ZETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NUCLEAR PROTEIN; PROTEIN SWI; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR SNF; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AKIRIN2 PROTEIN, MOUSE; CYTOKINE; MULTIPROTEIN COMPLEX; NFKBIZ PROTEIN, MOUSE; NONHISTONE PROTEIN; PROTEIN BINDING; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BONE MARROW CELL; CELL ACTIVATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; EMBRYO; FEMALE; GENE EXPRESSION; GENE INDUCTION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE GENE; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; INNATE IMMUNITY; LISTERIA; LISTERIOSIS; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOSOME; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; ANIMAL; CELL NUCLEUS; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LISTERIA MONOCYTOGENES; MALE; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; LISTERIA MONOCYTOGENES; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; SEQUENCE DELETION; TRANSCRIPTIONAL ACTIVATION;

EID: 84911473747     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488447     Document Type: Article

References (48)

1. Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D, (2000) Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103: 667-678
2. Beutler B, (2009) Microbe sensing, positive feedback loops, and the pathogenesis of inflammatory diseases. Immunol Rev 227: 248-263
3. Bhatt DM, Pandya-Jones A, Tong AJ, Barozzi I, Lissner MM, Natoli G, Black DL, Smale ST, (2012) Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 150: 279-290
4. Cairns BR, (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461: 193-198
5. Chen J, Ivashkiv LB, (2010) IFN-gamma abrogates endotoxin tolerance by facilitating Toll-like receptor-induced chromatin remodeling. Proc Natl Acad Sci USA 107: 19438-19443
6. Chi T, Yan Z, Xue Y, Wang W, (2004) Purification and functional analysis of the mammalian SWI/SNF-family of chromatin-remodeling complexes. Methods Enzymol 377: 299-316
7. Clapier CR, Cairns BR, (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304
8. Coles AH, Gannon H, Cerny A, Kurt-Jones E, Jones SN, (2010) Inhibitor of growth-4 promotes IkappaB promoter activation to suppress NF-kappaB signaling and innate immunity. Proc Natl Acad Sci USA 107: 11423-11428
9. Debril MB, Gelman L, Fayard E, Annicotte JS, Rocchi S, Auwerx J, (2004) Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60c subunit. J Biol Chem 279: 16677-16686
10. Dyson HJ, Wright PE, (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208
11. Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, Chernov A, Coutinho P, Saccone V, Consalvi S, Williams R, Wang K, Wu Z, Baranovskaya S, Miller A, Dilworth FJ, Puri PL, (2012) Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J 31: 301-316
12. 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
13. 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
14. Honda K, Taniguchi T, (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658
15. Hsiao PW, Fryer CJ, Trotter KW, Wang W, Archer TK, (2003) BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23: 6210-6220
16. Kayama H, Ramirez-Carrozzi VR, Yamamoto M, Mizutani T, Kuwata H, Iba H, Matsumoto M, Honda K, Smale ST, Takeda K, (2008) Class-specific regulation of pro-inflammatory genes by MyD88 pathways and IkappaBzeta. J Biol Chem 283: 12468-12477
17. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG, (2004) Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432: 107-112
18. Lores P, Visvikis O, Luna R, Lemichez E, Gacon G, (2010) The SWI/SNF protein BAF60b is ubiquitinated through a signalling process involving Rac GTPase and the RING finger protein Unkempt. FEBS J 277: 1453-1464
19. Macqueen DJ, Johnston IA, (2009) Evolution of the multifaceted eukaryotic akirin gene family. BMC Evol Biol 9: 34
20. Marshall A, Salerno MS, Thomas M, Davies T, Berry C, Dyer K, Bracegirdle J, Watson T, Dziadek M, Kambadur R, Bower R, Sharma M, (2008) Mighty is a novel promyogenic factor in skeletal myogenesis. Exp Cell Res 314: 1013-1029
21. Matsushita K, Takeuchi O, Standley DM, Kumagai Y, Kawagoe T, Miyake T, Satoh T, Kato H, Tsujimura T, Nakamura H, Akira S, (2009) Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature 458: 1185-1190
22. Medzhitov R, (2008) Origin and physiological roles of inflammation. Nature 454: 428-435
23. Medzhitov R, Horng T, (2009) Transcriptional control of the inflammatory response. Nat Rev Immunol 9: 692-703
24. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, Raney BJ, Pohl A, Malladi VS, Li CH, Lee BT, Learned K, Kirkup V, Hsu F, Heitner S, Harte RA, et al, (2013) The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 41: D64-D69
25. Miyake T, Satoh T, Kato H, Matsushita K, Kumagai Y, Vandenbon A, Tani T, Muta T, Akira S, Takeuchi O, (2010) IkappaBzeta is essential for natural killer cell activation in response to IL-12 and IL-18. Proc Natl Acad Sci USA 107: 17680-17685
26. 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
27. Motoyama M, Yamazaki S, Eto-Kimura A, Takeshige K, Muta T, (2005) Positive and negative regulation of nuclear factor-kappaB-mediated transcription by IkappaB-zeta, an inducible nuclear protein. J Biol Chem 280: 7444-7451
28. Negishi H, Yanai H, Nakajima A, Koshiba R, Atarashi K, Matsuda A, Matsuki K, Miki S, Doi T, Aderem A, Nishio J, Smale ST, Honda K, Taniguchi T, (2012) Cross-interference of RLR and TLR signaling pathways modulates antibacterial T cell responses. Nat Immunol 13: 659-666
29. 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
30. Oeckinghaus A, Hayden MS, Ghosh S, (2011) Crosstalk in NF-kappaB signaling pathways. Nat Immunol 12: 695-708
31. Okamoto K, Iwai Y, Oh-Hora M, Yamamoto M, Morio T, Aoki K, Ohya K, Jetten AM, Akira S, Muta T, Takayanagi H, (2010) IkappaBzeta regulates T(H)17 development by cooperating with ROR nuclear receptors. Nature 464: 1381-1385
32. Okuma A, Hoshino K, Ohba T, Fukushi S, Aiba S, Akira S, Ono M, Kaisho T, Muta T, (2013) Enhanced Apoptosis by Disruption of the STAT3-IkappaB-zeta Signaling Pathway in Epithelial Cells Induces Sjogren's Syndrome-like Autoimmune Disease. Immunity 38: 450-460
33. Puri PL, Mercola M, (2012) BAF60 A, B, and Cs of muscle determination and renewal. Genes Dev 26: 2673-2683
34. 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
35. Salerno MS, Dyer K, Bracegirdle J, Platt L, Thomas M, Siriett V, Kambadur R, Sharma M, (2009) Akirin1 (Mighty), a novel promyogenic factor regulates muscle regeneration and cell chemotaxis. Exp Cell Res 315: 2012-2021
36. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, Miyake T, Matsushita K, Okazaki T, Saitoh T, Honma K, Matsuyama T, Yui K, Tsujimura T, Standley DM, Nakanishi K, Nakai K, Akira S, (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11: 936-944
37. Sha WC, Liou HC, Tuomanen EI, Baltimore D, (1995) Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 80: 321-330
38. Sun L, Wu J, Du F, Chen X, Chen ZJ, (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339: 786-791
39. Takeuchi JK, Bruneau BG, (2009) Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 459: 708-711
40. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820
41. Wang Y, Wong RH, Tang T, Hudak CS, Yang D, Duncan RE, Sul HS, (2013) Phosphorylation and recruitment of BAF60c in chromatin remodeling for lipogenesis in response to insulin. Mol Cell 49: 283-297
42. Weinmann AS, Mitchell DM, Sanjabi S, Bradley MN, Hoffmann A, Liou HC, Smale ST, (2001) Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat Immunol 2: 51-57
43. Weinmann AS, Plevy SE, Smale ST, (1999) Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity 11: 665-675
44. Yamamoto M, Yamazaki S, Uematsu S, Sato S, Hemmi H, Hoshino K, Kaisho T, Kuwata H, Takeuchi O, Takeshige K, Saitoh T, Yamaoka S, Yamamoto N, Yamamoto S, Muta T, Takeda K, Akira S, (2004) Regulation of Toll/IL-1-receptor-mediated gene expression by the inducible nuclear protein IkappaBzeta. Nature 430: 218-222
45. Yamazaki S, Muta T, Takeshige K, (2001) A novel IkappaB protein, IkappaB-zeta, induced by proinflammatory stimuli, negatively regulates nuclear factor-kappaB in the nuclei. J Biol Chem 276: 27657-27662
46. Yan Z, Cui K, Murray DM, Ling C, Xue Y, Gerstein A, Parsons R, Zhao K, Wang W, (2005) PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev 19: 1662-1667
47. Yudkovsky N, Logie C, Hahn S, Peterson CL, (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev 13: 2369-2374
48. Zhou L, Nazarian AA, Smale ST, (2004) Interleukin-10 inhibits interleukin-12 p40 gene transcription by targeting a late event in the activation pathway. Mol Cell Biol 24: 2385-2396