Citrullination of Histone H3 Interferes with HP1-Mediated Transcriptional Repression

PLoS Genetics

Volumn 8, Issue 9, 2012, Pages

  Sharma, Priyanka ^a   Azebi, Saliha ^a   England, Patrick ^b   Christensen, Tove ^c   Møller Larsen, Anné ^c   Petersen, Thor ^d   Batsché, Eric ^a   Muchardt, Christian ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c AARHUS UNIVERSITY   (Denmark)

^d AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDINE; CITRULLINE; HETEROCHROMATIN PROTEIN 1; HISTONE H3; INTERLEUKIN 8; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ANTIBODY SPECIFICITY; ARTICLE; BINDING SITE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOGENOUS RETROVIRUS; ENZYME REACTIVATION; FEMALE; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MULTIPLE SCLEROSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MODIFICATION; SURFACE PLASMON RESONANCE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ADULT; CHROMOSOMAL PROTEINS, NON-HISTONE; CITRULLINE; ENDOGENOUS RETROVIRUSES; FEMALE; GENE EXPRESSION REGULATION; HEK293 CELLS; HISTONES; HUMANS; HYDROLASES; IMMUNITY, INNATE; INTERLEUKIN-8; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MALE; MCF-7 CELLS; MIDDLE AGED; MULTIPLE SCLEROSIS; ORNITHINE; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

HUMAN ENDOGENOUS RETROVIRUSES;

EID: 84866933793     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002934     Document Type: Article

References (78)

1. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG, (2000) Multiple sclerosis. N Engl J Med 343: 938-952.
2. O'Brien K, Gran B, Rostami A, (2010) T-cell based immunotherapy in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunotherapy 2: 99-115.
3. Chitnis T, (2007) The role of CD4 T cells in the pathogenesis of multiple sclerosis. International review of neurobiology 79: 43-72.
4. Imitola J, Chitnis T, Khoury SJ, (2005) Cytokines in multiple sclerosis: from bench to bedside. Pharmacol Ther 106: 163-177.
5. Brudek T, Christensen T, Aagaard L, Petersen T, Hansen HJ, et al. (2009) B cells and monocytes from patients with active multiple sclerosis exhibit increased surface expression of both HERV-H Env and HERV-W Env, accompanied by increased seroreactivity. Retrovirology 6: 104.
6. Christensen T, (2010) HERVs in neuropathogenesis. J Neuroimmune Pharmacol 5: 326-335.
7. Perron H, Lang A, (2010) The human endogenous retrovirus link between genes and environment in multiple sclerosis and in multifactorial diseases associating neuroinflammation. Clin Rev Allergy Immunol 39: 51-61.
8. Deaton AM, Bird A, (2011) CpG islands and the regulation of transcription. Genes & development 25: 1010-1022.
9. Walsh CP, Chaillet JR, Bestor TH, (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nature Genetics 20: 116-117.
10. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
11. Hutnick LK, Huang X, Loo T-C, Ma Z, Fan G, (2010) Repression of retrotransposal elements in mouse embryonic stem cells is primarily mediated by a DNA methylation-independent mechanism. Journal of Biological Chemistry 285: 21082-21091.
12. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, et al. (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
13. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, et al. (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell stem cell 8: 676-687.
14. Martens JHA, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, et al. (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 24: 800-812.
15. Mulligan P, Westbrook TF, Ottinger M, Pavlova N, Chang B, et al. (2008) CDYL bridges REST and histone methyltransferases for gene repression and suppression of cellular transformation. Molecular Cell 32: 718-726.
16. Fischle W, Franz H, Jacobs SA, Allis CD, Khorasanizadeh S, (2008) Specificity of the chromodomain Y chromosome family of chromodomains for lysine-methylated ARK(S/T) motifs. The Journal of biological chemistry 283: 19626-19635.
17. Bernstein E, Duncan EM, Masui O, Gil J, Heard E, et al. (2006) Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Molecular and cellular biology 26: 2560-2569.
18. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, et al. (2001) Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. The EMBO Journal 20: 5232-5241.
19. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
20. Lachner M, O'Carroll D, Rea S, Mechtler K, et al. (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
21. Kim J, Daniel J, Espejo A, Lake A, Krishna M, et al. (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO reports 7: 397-403.
22. Iwase S, Lan F, Bayliss P, de la Torre-Ubieta L, Huarte M, et al. (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128: 1077-1088.
23. Rottach A, Frauer C, Pichler G, Bonapace IM, Spada F, et al. (2010) The multi-domain protein Np95 connects DNA methylation and histone modification. Nucleic acids research 38: 1796-1804.
24. Wolf D, Hug K, Goff SP, (2008) TRIM28 mediates primer binding site-targeted silencing of Lys1,2 tRNA-utilizing retroviruses in embryonic cells. Proceedings of the National Academy of Sciences of the United States of America 105: 12521-12526.
25. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, et al. (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
26. Maksakova IA, Goyal P, Bullwinkel J, Brown JP, Bilenky M, et al. (2011) H3K9me3-binding proteins are dispensable for SETDB1/H3K9me3-dependent retroviral silencing. Epigenetics & chromatin 4: 12.
27. Eissenberg JC, Elgin SC, (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10: 204-210.
28. Kwon SH, Workman JL, (2008) The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. Mol Cells 26: 217-227.
29. El Gazzar M, Yoza BK, Hu JY, Cousart SL, McCall CE, (2007) Epigenetic silencing of tumor necrosis factor alpha during endotoxin tolerance. J Biol Chem 282: 26857-26864.
30. Yoza BK, McCall CE, (2011) Facultative heterochromatin formation at the IL-1 beta promoter in LPS tolerance and sepsis. Cytokine 53: 145-152.
31. Chen X, El Gazzar M, Yoza BK, McCall CE, (2009) The NF-kappaB factor RelB and histone H3 lysine methyltransferase G9a directly interact to generate epigenetic silencing in endotoxin tolerance. J Biol Chem 284: 27857-27865.
32. Ndlovu MN, Van Lint C, Van Wesemael K, Callebert P, Chalbos D, et al. (2009) Hyperactivated NF-{kappa}B and AP-1 transcription factors promote highly accessible chromatin and constitutive transcription across the interleukin-6 gene promoter in metastatic breast cancer cells. Mol Cell Biol 29: 5488-5504.
33. Saint-André V, Batsché E, Rachez C, Muchardt C, (2011) Histone H3 lysine 9 trimethylation and HP1γ favor inclusion of alternative exons. Nat Struct Mol Biol.
34. Lavigne M, Eskeland R, Azebi S, Saint-André V, Jang SM, et al. (2009) Interaction of HP1 and Brg1/Brm with the Globular Domain of Histone H3 Is Required for HP1-Mediated Repression. PLoS Genet 5: e1000769 doi:10.1371/journal.pgen.1000769.
35. Mateescu B, Bourachot B, Rachez C, Ogryzko V, Muchardt C, (2008) Regulation of an inducible promoter by an HP1beta-HP1gamma switch. EMBO Rep 9: 267-272.
36. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, et al. (2007) Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. Embo J 26: 412-423.
37. Chéné I, Basyuk E, Lin YL, Triboulet R, Knezevich A, et al. (2007) Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. Embo J 26: 424-435.
38. Pedersen MT, Helin K, (2010) Histone demethylases in development and disease. Trends in Cell Biology 20: 662-671.
39. Mateescu B, England P, Halgand F, Yaniv M, Muchardt C, (2004) Tethering of HP1 proteins to chromatin is relieved by phosphoacetylation of histone H3. EMBO Rep.
40. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, et al. (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-1122.
41. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, et al. (2010) Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers. Cell 142: 967-980.
42. Di Lorenzo A, Bedford MT, (2011) Histone arginine methylation. FEBS LETTERS 585: 2024-2031.
43. Bedford MT, Clarke SG, (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13.
44. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, et al. (2004) Histone deimination antagonizes arginine methylation. Cell 118: 545-553.
45. Wang Y, Wysocka J, Sayegh J, Lee YH, Perlin JR, et al. (2004) Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306: 279-283.
46. Nakashima K, Hagiwara T, Yamada M, (2002) Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J Biol Chem 277: 49562-49568.
47. Raijmakers R, Zendman AJ, Egberts WV, Vossenaar ER, Raats J, et al. (2007) Methylation of arginine residues interferes with citrullination by peptidylarginine deiminases in vitro. J Mol Biol 367: 1118-1129.
48. Migliori V, Phalke S, Bezzi M, Guccione E, (2010) Arginine/lysine-methyl/methyl switches: biochemical role of histone arginine methylation in transcriptional regulation. Epigenomics 2: 119-137.
49. Hagiwara T, Hidaka Y, Yamada M, (2005) Deimination of histone H2A and H4 at arginine 3 in HL-60 granulocytes. Biochemistry 44: 5827-5834.
50. Li P, Yao H, Zhang Z, Li M, Luo Y, et al. (2008) Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol Cell Biol 28: 4745-4758.
51. Yao H, Li P, Venters BJ, Zheng S, Thompson PR, et al. (2008) Histone Arg modifications and p53 regulate the expression of OKL38, a mediator of apoptosis. J Biol Chem 283: 20060-20068.
52. Denis H, Deplus R, Putmans P, Yamada M, Metivier R, et al. (2009) Functional connection between deimination and deacetylation of histones. Mol Cell Biol 29: 4982-4993.
53. Zhang X, Gamble MJ, Stadler S, Cherrington BD, Causey CP, et al. (2011) Genome-Wide Analysis Reveals PADI4 Cooperates with Elk-1 to Activate c-Fos Expression in Breast Cancer Cells. PLoS Genet 7: e1002112 doi:10.1371/journal.pgen.1002112.
54. Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, et al. (2003) Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet 34: 395-402.
55. Ikari K, Kuwahara M, Nakamura T, Momohara S, Hara M, et al. (2005) Association between PADI4 and rheumatoid arthritis: a replication study. Arthritis Rheum 52: 3054-3057.
56. Kang CP, Lee HS, Ju H, Cho H, Kang C, et al. (2006) A functional haplotype of the PADI4 gene associated with increased rheumatoid arthritis susceptibility in Koreans. Arthritis Rheum 54: 90-96.
57. Anzilotti C, Pratesi F, Tommasi C, Migliorini P, (2009) Peptidylarginine deiminase 4 and citrullination in health and disease. Autoimmun Rev.
58. Mastronardi FG, Wood DD, Mei J, Raijmakers R, Tseveleki V, et al. (2006) Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: a role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. J Neurosci 26: 11387-11396.
59. Wang-Johanning F, Rycaj K, Plummer JB, Li M, Yin B, et al. (2012) Immunotherapeutic potential of anti-human endogenous retrovirus-k envelope protein antibodies in targeting breast tumors. Journal of the National Cancer Institute 104: 189-210.
60. Skundric DS, Cai J, Cruikshank WW, Gveric D, (2006) Production of IL-16 correlates with CD4+ Th1 inflammation and phosphorylation of axonal cytoskeleton in multiple sclerosis lesions. J Neuroinflammation 3: 13.
61. Vaknin-Dembinsky A, Balashov K, Weiner HL, (2006) IL-23 is increased in dendritic cells in multiple sclerosis and down-regulation of IL-23 by antisense oligos increases dendritic cell IL-10 production. J Immunol 176: 7768-7774.
62. Hung HC, Lin CY, Liao YF, Hsu PC, Tsay GJ, et al. (2007) The functional haplotype of peptidylarginine deiminase IV (S55G, A82V and A112G) associated with susceptibility to rheumatoid arthritis dominates apoptosis of acute T leukemia Jurkat cells. Apoptosis 12: 475-487.
63. Arita K, Shimizu T, Hashimoto H, Hidaka Y, Yamada M, et al. (2006) Structural basis for histone N-terminal recognition by human peptidylarginine deiminase 4. Proc Natl Acad Sci U S A 103: 5291-5296.
64. Muchardt C, Guilleme M, Seeler JS, Trouche D, Dejean A, et al. (2002) Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep 3: 975-981.
65. Dong S, Zhang Z, Takahara H, (2007) Estrogen-enhanced peptidylarginine deiminase type IV gene (PADI4) expression in MCF-7 cells is mediated by estrogen receptor-alpha-promoted transfactors activator protein-1, nuclear factor-Y, and Sp1. Mol Endocrinol 21: 1617-1629.
66. Luo Y, Arita K, Bhatia M, Knuckley B, Lee YH, et al. (2006) Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry 45: 11727-11736.
67. de Parseval N, Casella J, Gressin L, Heidmann T, (2001) Characterization of the three HERV-H proviruses with an open envelope reading frame encompassing the immunosuppressive domain and evolutionary history in primates. Virology 279: 558-569.
68. Mallet F, Bouton O, Prudhomme S, Cheynet V, Oriol G, et al. (2004) The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. Proc Natl Acad Sci USA 101: 1731-1736.
69. Straub RH, (2007) The complex role of estrogens in inflammation. Endocrine reviews 28: 521-574.
70. Orton SM, Herrera BM, Yee IM, Valdar W, Ramagopalan SV, et al. (2006) Sex ratio of multiple sclerosis in Canada: a longitudinal study. The Lancet Neurology 5: 932-936.
71. Conti L, De Palma R, Rolla S, Boselli D, Rodolico G, et al. (2012) Th17 Cells in Multiple Sclerosis Express Higher Levels of JAK2, Which Increases Their Surface Expression of IFN-γR2. Journal of immunology (Baltimore, Md: 1950) 188: 1011-1018.
72. Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, et al. (2009) JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461: 819-822.
73. Kim JK, Mastronardi FG, Wood DD, Lubman DM, Zand R, et al. (2003) Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Molecular & cellular proteomics: MCP 2: 453-462.
74. Batsché 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.
75. Poser CM, Paty DW, Scheinberg L, McDonald WI, Davis FA, et al. (1983) New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 13: 227-231.
76. Wilcoxon F, (1945) Individual comparisons by ranking methods. Biometrics Bulletin 1: 80-83.
77. Stolarov J, Chang K, Reiner A, Rodgers L, Hannon GJ, et al. (2001) Design of a retroviral-mediated ecdysone-inducible system and its application to the expression profiling of the PTEN tumor suppressor. Proc Natl Acad Sci U S A 98: 13043-13048.
78. Shechter D, Dormann HL, Allis CD, Hake SB, (2007) Extraction, purification and analysis of histones. Nat Protoc 2: 1445-1457.