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Published in: Clinical Reviews in Allergy & Immunology 1/2010

01-08-2010

Epigenetic Histone Code and Autoimmunity

Authors: Jürgen Dieker, Sylviane Muller

Published in: Clinical Reviews in Allergy & Immunology | Issue 1/2010

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Abstract

The multiple inter-dependent post-translational modifications of histones represent fine regulators of chromatin dynamics. These covalent modifications, including phosphorylation, acetylation, ubiquitination, deimination, and methylation, affect therefore the numerous processes involving chromatin, such as replication, repair, transcription, genome stability, and cell death. Specific enzymes introducing modified residues in histones are precisely regulated, and a single amino acid residue can be subjected to a single or several, independent modifications. Disruption of histone post-translational modifications perturbs the pattern of gene expression, which may result in disease manifestations. It has become evident in recent years that apoptosis-modified histones exert a central role in the induction of autoimmunity, for example in systemic lupus erythematosus and rheumatoid arthritis. Certain histone post-translational modifications are linked to cell death (apoptotic and non-apoptotic cell death) and might be involved in lupus in the activation of normally tolerant lymphocyte subpopulations. In this review, we discuss how these modifications can affect the antigenicity and immunogenicity of histones with potential consequences in the pathogenesis of autoimmune diseases.
Literature
1.
go back to reference Bhaumik SR, Smith E, Shilatifard A (2007) Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14:1008–1016CrossRefPubMed Bhaumik SR, Smith E, Shilatifard A (2007) Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14:1008–1016CrossRefPubMed
2.
go back to reference Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983–994CrossRefPubMed Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983–994CrossRefPubMed
3.
go back to reference Mahler M, Blüthner M, Pollard KM (2003) Advances in B-cell epitope analysis of autoantigens in connective tissue diseases. Clin Immunol 107:65–79CrossRefPubMed Mahler M, Blüthner M, Pollard KM (2003) Advances in B-cell epitope analysis of autoantigens in connective tissue diseases. Clin Immunol 107:65–79CrossRefPubMed
4.
go back to reference Routsias JG, Tzioufas AG, Moutsopoulos HM (2004) The clinical value of intracellular autoantigens B-cell epitopes in systemic rheumatic diseases. Clin Chim Acta 340:1–25CrossRefPubMed Routsias JG, Tzioufas AG, Moutsopoulos HM (2004) The clinical value of intracellular autoantigens B-cell epitopes in systemic rheumatic diseases. Clin Chim Acta 340:1–25CrossRefPubMed
5.
go back to reference LeFeber WP, Norris DA, Ryan SR et al (1984) Ultraviolet light induces binding of antibodies to selected nuclear antigens on cultured human keratinocytes. J Clin Invest 74:1545–1551CrossRefPubMed LeFeber WP, Norris DA, Ryan SR et al (1984) Ultraviolet light induces binding of antibodies to selected nuclear antigens on cultured human keratinocytes. J Clin Invest 74:1545–1551CrossRefPubMed
6.
go back to reference Casciola-Rosen LA, Anhalt G, Rosen A (1994) Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 179:1317–1330CrossRefPubMed Casciola-Rosen LA, Anhalt G, Rosen A (1994) Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 179:1317–1330CrossRefPubMed
7.
go back to reference Casiano CA, Tan EM (1996) Recent developments in the understanding of antinuclear autoantibodies. Int Arch Allergy Immunol 111:308–313CrossRefPubMed Casiano CA, Tan EM (1996) Recent developments in the understanding of antinuclear autoantibodies. Int Arch Allergy Immunol 111:308–313CrossRefPubMed
8.
go back to reference Utz PJ, Gensler TJ, Anderson P (2000) Death, autoantigen modifications, and tolerance. Arthritis Res 2:101–114CrossRefPubMed Utz PJ, Gensler TJ, Anderson P (2000) Death, autoantigen modifications, and tolerance. Arthritis Res 2:101–114CrossRefPubMed
9.
go back to reference Rodenburg RJT, Raats HMJ, Pruijn GJM, van Venrooij WJ (2000) Cell death: a trigger of autoimmunity? BioEssay 22:627–636CrossRef Rodenburg RJT, Raats HMJ, Pruijn GJM, van Venrooij WJ (2000) Cell death: a trigger of autoimmunity? BioEssay 22:627–636CrossRef
10.
go back to reference Rovere P, Sabbadini MG, Fazzini F et al (2000) Remnants of suicidal cells fostering systemic autoaggression. Apoptosis in the origin and maintenance of autoimmunity. Arthritis Rheum 43:1663–1672CrossRefPubMed Rovere P, Sabbadini MG, Fazzini F et al (2000) Remnants of suicidal cells fostering systemic autoaggression. Apoptosis in the origin and maintenance of autoimmunity. Arthritis Rheum 43:1663–1672CrossRefPubMed
11.
go back to reference Gaipl US, Kuhn A, Sheriff A et al (2006) Clearance of apoptotic cells in human SLE. Curr Dir Autoimmun 9:173–187PubMed Gaipl US, Kuhn A, Sheriff A et al (2006) Clearance of apoptotic cells in human SLE. Curr Dir Autoimmun 9:173–187PubMed
12.
go back to reference Munoz LE, van Bavel C, Franz S, Berden J, Herrmann M, van der Vlag J (2008) Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus 17:371–375CrossRefPubMed Munoz LE, van Bavel C, Franz S, Berden J, Herrmann M, van der Vlag J (2008) Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus 17:371–375CrossRefPubMed
13.
go back to reference Dumortier H, Muller S (2007) Histone autoantibodies. In: Shoenfeld Y, Meroni PL, Gershwin E (eds) Textbook of autoantibodies, chapter 22, 2nd edn. Elsevier, Amsterdam, pp 169–176 Dumortier H, Muller S (2007) Histone autoantibodies. In: Shoenfeld Y, Meroni PL, Gershwin E (eds) Textbook of autoantibodies, chapter 22, 2nd edn. Elsevier, Amsterdam, pp 169–176
14.
go back to reference Cheung WL, Ajiro K, Samejima K et al (2003) Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113:507–517CrossRefPubMed Cheung WL, Ajiro K, Samejima K et al (2003) Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113:507–517CrossRefPubMed
15.
go back to reference Monestier M, Fasy TM, Losman MJ, Novick KE, Muller S (1993) Structure and binding properties of monoclonal antibodies to core histones from autoimmune mice. Mol Immunol 30:1069–1075CrossRefPubMed Monestier M, Fasy TM, Losman MJ, Novick KE, Muller S (1993) Structure and binding properties of monoclonal antibodies to core histones from autoimmune mice. Mol Immunol 30:1069–1075CrossRefPubMed
16.
go back to reference Monestier M, Decker P, Briand JP, Gabriel JL, Muller S (2000) Molecular and structural properties of three autoimmune IgG monoclonal antibodies to histone H2B. J Biol Chem 275:13558–13563CrossRefPubMed Monestier M, Decker P, Briand JP, Gabriel JL, Muller S (2000) Molecular and structural properties of three autoimmune IgG monoclonal antibodies to histone H2B. J Biol Chem 275:13558–13563CrossRefPubMed
17.
go back to reference Fournel S, Muller S (2003) Synthetic peptides in the diagnosis of systemic autoimmune diseases. Curr Prot Peptide Sci 4:261–276CrossRef Fournel S, Muller S (2003) Synthetic peptides in the diagnosis of systemic autoimmune diseases. Curr Prot Peptide Sci 4:261–276CrossRef
18.
go back to reference Lu L, Kaliyaperumal A, Boumpas DT, Datta SK (1999) Major peptide autoepitopes for nucleosome-specific T cells of human lupus. J Clin Invest 104:345–355CrossRefPubMed Lu L, Kaliyaperumal A, Boumpas DT, Datta SK (1999) Major peptide autoepitopes for nucleosome-specific T cells of human lupus. J Clin Invest 104:345–355CrossRefPubMed
19.
go back to reference Kaliyaperumal A, Mohan C, Wu W, Datta SK (1996) Nucleosomal peptide epitopes for nephritis-inducing T helper cells of murine lupus. J Exp Med 183:2459–2469CrossRefPubMed Kaliyaperumal A, Mohan C, Wu W, Datta SK (1996) Nucleosomal peptide epitopes for nephritis-inducing T helper cells of murine lupus. J Exp Med 183:2459–2469CrossRefPubMed
20.
go back to reference Sköldberg F, Rönnblom L, Thornemo M et al (2002) Identification of AHNAK as a novel autoantigen in systemic lupus erythematosus. Biochem Biophys Res Commun 291:951–958CrossRefPubMed Sköldberg F, Rönnblom L, Thornemo M et al (2002) Identification of AHNAK as a novel autoantigen in systemic lupus erythematosus. Biochem Biophys Res Commun 291:951–958CrossRefPubMed
21.
go back to reference Stemmer C, Briand JP, Muller S (1994) Mapping of linear epitopes of human histone H1 recognized by rabbit anti-H1/H5 antisera and antibodies from autoimmune patients. Mol Immunol 31:1037–1046CrossRefPubMed Stemmer C, Briand JP, Muller S (1994) Mapping of linear epitopes of human histone H1 recognized by rabbit anti-H1/H5 antisera and antibodies from autoimmune patients. Mol Immunol 31:1037–1046CrossRefPubMed
22.
go back to reference Dieker JW, Fransen JH, Van Bavel CC et al (2007) Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum 56:1921–1933CrossRefPubMed Dieker JW, Fransen JH, Van Bavel CC et al (2007) Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum 56:1921–1933CrossRefPubMed
23.
go back to reference Batova I, Kowal C, May R, Scharff MD, Diamond B (2008) Human recombinant Fab fragments with sub-nanomolar affinities for acetylated histones. J Immunol Methods 329:1–10CrossRefPubMed Batova I, Kowal C, May R, Scharff MD, Diamond B (2008) Human recombinant Fab fragments with sub-nanomolar affinities for acetylated histones. J Immunol Methods 329:1–10CrossRefPubMed
24.
go back to reference Hu N, Qiu X, Luo Y et al (2008) Abnormal histone modifications patterns in lupus CD4+ T cells. J Rheumatol 35:804–810PubMed Hu N, Qiu X, Luo Y et al (2008) Abnormal histone modifications patterns in lupus CD4+ T cells. J Rheumatol 35:804–810PubMed
25.
go back to reference Garcia BA, Busby SA, Shabanowitz J, Hunt DF, Mishra N (2005) Resetting the epigenetic histone code in the MRL-lpr/lpr mouse model of lupus by histone acetylase inhibition. J Proteome Res 4:2032–2042CrossRefPubMed Garcia BA, Busby SA, Shabanowitz J, Hunt DF, Mishra N (2005) Resetting the epigenetic histone code in the MRL-lpr/lpr mouse model of lupus by histone acetylase inhibition. J Proteome Res 4:2032–2042CrossRefPubMed
26.
go back to reference Mishra N, Reilly CM, Brown DR, Ruiz P, Gilkeson GS (2003) Histone deacetylase inhibitors modulate renal disease in the MRL-lpr/lpr mouse. J Clin Invest 111:539–552PubMed Mishra N, Reilly CM, Brown DR, Ruiz P, Gilkeson GS (2003) Histone deacetylase inhibitors modulate renal disease in the MRL-lpr/lpr mouse. J Clin Invest 111:539–552PubMed
27.
go back to reference Reilly CM, Mishra N, Miller JM et al (2004) Modulation of renal disease in MRL/lpr mice by suberoylanilide hydroxamic acid. J Immunol 173:4171–4178PubMed Reilly CM, Mishra N, Miller JM et al (2004) Modulation of renal disease in MRL/lpr mice by suberoylanilide hydroxamic acid. J Immunol 173:4171–4178PubMed
28.
go back to reference Marushige Y, Marushige K (1995) Disappearance of ubiquitinated histone H2A during chromatin condensation in TGF beta 1-induced apoptosis. Anticancer Res 15:267–272PubMed Marushige Y, Marushige K (1995) Disappearance of ubiquitinated histone H2A during chromatin condensation in TGF beta 1-induced apoptosis. Anticancer Res 15:267–272PubMed
29.
go back to reference Mimnaugh EG, Kayastha G, McGovern NB et al (2001) Caspase-dependent deubiquitination of monoubiquitinated nucleosomal histone H2A induced by diverse apoptogenic stimuli. Cell Death Differ 8:1182–1196CrossRefPubMed Mimnaugh EG, Kayastha G, McGovern NB et al (2001) Caspase-dependent deubiquitination of monoubiquitinated nucleosomal histone H2A induced by diverse apoptogenic stimuli. Cell Death Differ 8:1182–1196CrossRefPubMed
30.
go back to reference Plaué S, Muller S, Van Regenmortel MHV (1989) A branched, synthetic octapeptide of ubiquinated histone H2A as target of autoantibodies. J Exp Med 169:1607–1617CrossRefPubMed Plaué S, Muller S, Van Regenmortel MHV (1989) A branched, synthetic octapeptide of ubiquinated histone H2A as target of autoantibodies. J Exp Med 169:1607–1617CrossRefPubMed
31.
go back to reference Muller S, Briand JP, Van Regenmortel MHV (1988) Presence of antibodies to ubiquitin during the autoimmune response associated with systemic lupus erythematosus. Proc Natl Acad Sci USA 85:8176–8180CrossRefPubMed Muller S, Briand JP, Van Regenmortel MHV (1988) Presence of antibodies to ubiquitin during the autoimmune response associated with systemic lupus erythematosus. Proc Natl Acad Sci USA 85:8176–8180CrossRefPubMed
32.
go back to reference Ravirajan CT, Kalsi J, Winska-Wiloch H et al (1992) Antigen binding diversity of human hybridoma autoantibodies derived from splenocytes of patients with SLE. Lupus 1:157–165CrossRefPubMed Ravirajan CT, Kalsi J, Winska-Wiloch H et al (1992) Antigen binding diversity of human hybridoma autoantibodies derived from splenocytes of patients with SLE. Lupus 1:157–165CrossRefPubMed
33.
go back to reference Stöckl F, Muller S, Batsford S et al (1994) A role for histones and ubiquitin in lupus nephritis? Clin Nephrol 41:10–17PubMed Stöckl F, Muller S, Batsford S et al (1994) A role for histones and ubiquitin in lupus nephritis? Clin Nephrol 41:10–17PubMed
34.
go back to reference Elouaai F, Lule J, Benoist H et al (1994) Autoimmunity to histones, ubiquitin, and ubiquitinated histone H2A in NZB x NZW an MRL-lpr/lpr mice. Anti-histone antibodies are concentrated in glomerular eluates of lupus mice. Nephrol Dialysis Transpl 9:362–366 Elouaai F, Lule J, Benoist H et al (1994) Autoimmunity to histones, ubiquitin, and ubiquitinated histone H2A in NZB x NZW an MRL-lpr/lpr mice. Anti-histone antibodies are concentrated in glomerular eluates of lupus mice. Nephrol Dialysis Transpl 9:362–366
35.
go back to reference Mézière C, Stöckl F, Batsford S, Vogt A, Muller S (1994) Antibodies to DNA, chromatin core particles and histones in mice with graft-versus-host disease and their involvement in glomerular injury. Clin Exp Immunol 98:287–294PubMedCrossRef Mézière C, Stöckl F, Batsford S, Vogt A, Muller S (1994) Antibodies to DNA, chromatin core particles and histones in mice with graft-versus-host disease and their involvement in glomerular injury. Clin Exp Immunol 98:287–294PubMedCrossRef
36.
go back to reference Reumaux D, Mézière C, Colombel JF, Duthilleul P, Muller S (1995) Distinct production of antibodies to nuclear components in ulcerative colitis and Crohn’s disease. Clin Immunol Immunopathol 77:349–357CrossRefPubMed Reumaux D, Mézière C, Colombel JF, Duthilleul P, Muller S (1995) Distinct production of antibodies to nuclear components in ulcerative colitis and Crohn’s disease. Clin Immunol Immunopathol 77:349–357CrossRefPubMed
37.
go back to reference Kanai Y, Kawaminami Y, Miwa M et al (1977) naturally-occurring antibodies to poly(ADP-ribose) in patients with systemic lupus erythematosus. Nature 265:175–177CrossRefPubMed Kanai Y, Kawaminami Y, Miwa M et al (1977) naturally-occurring antibodies to poly(ADP-ribose) in patients with systemic lupus erythematosus. Nature 265:175–177CrossRefPubMed
38.
go back to reference Muller S, Briand JP, Barakat S et al (1994) Autoantibodies reacting with poly(ADP-ribose) and with a zinc-finger functional domain of poly(ADP-ribose)polymerase involved in the recognition of damaged DNA. Clin Immunol Immunopathol 73:187–196CrossRefPubMed Muller S, Briand JP, Barakat S et al (1994) Autoantibodies reacting with poly(ADP-ribose) and with a zinc-finger functional domain of poly(ADP-ribose)polymerase involved in the recognition of damaged DNA. Clin Immunol Immunopathol 73:187–196CrossRefPubMed
39.
go back to reference Decker P, Briand JP, De Murcia G, Pero RW, Isenberg DA, Muller S (1998) Zinc is an essential co-factor for recognition of the DNA-binding domain of poly(ADP-ribose) polymerase by antibodies in autoimmune rheumatic and bowel diseases. Arthritis Rheum 41:918–926CrossRefPubMed Decker P, Briand JP, De Murcia G, Pero RW, Isenberg DA, Muller S (1998) Zinc is an essential co-factor for recognition of the DNA-binding domain of poly(ADP-ribose) polymerase by antibodies in autoimmune rheumatic and bowel diseases. Arthritis Rheum 41:918–926CrossRefPubMed
40.
go back to reference Thibeault L, Hengartner M, Lagueux J, Poirier G, Muller S (1992) Rearrangement of the nucleosome structure in chromatin by poly (ADP-ribose). Biochim Biophys Acta 1121:317–324PubMed Thibeault L, Hengartner M, Lagueux J, Poirier G, Muller S (1992) Rearrangement of the nucleosome structure in chromatin by poly (ADP-ribose). Biochim Biophys Acta 1121:317–324PubMed
41.
go back to reference Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ (2003) PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 25:1106–1118CrossRefPubMed Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ (2003) PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. Bioessays 25:1106–1118CrossRefPubMed
42.
go back to reference Schellekens GA, de Jong BA, van den Hoogen FH, van de Putte LB, van Venrooij WJ (1998) Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J Clin Invest 101:273–281CrossRefPubMed Schellekens GA, de Jong BA, van den Hoogen FH, van de Putte LB, van Venrooij WJ (1998) Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J Clin Invest 101:273–281CrossRefPubMed
43.
go back to reference Girbal-Neuhauser E, Durieux JJ, Arnaud M et al (1999) The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J Immunol 162:585–594PubMed Girbal-Neuhauser E, Durieux JJ, Arnaud M et al (1999) The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J Immunol 162:585–594PubMed
44.
go back to reference Masson-Bessière C, Sebbag M, Girbal-Neuhauser E et al (2001) The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol 166:4177–4184PubMed Masson-Bessière C, Sebbag M, Girbal-Neuhauser E et al (2001) The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol 166:4177–4184PubMed
45.
go back to reference Cuthbert GL, Daujat S, Snowden AW et al (2004) Histone deimination antagonizes arginine methylation. Cell 118:545–553CrossRefPubMed Cuthbert GL, Daujat S, Snowden AW et al (2004) Histone deimination antagonizes arginine methylation. Cell 118:545–553CrossRefPubMed
46.
go back to reference Wang Y, Wysocka J, Sayegh J et al (2004) Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306:279–283CrossRefPubMed Wang Y, Wysocka J, Sayegh J et al (2004) Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306:279–283CrossRefPubMed
47.
go back to reference Wang Y, Li M, Stadler S et al (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184:205–213CrossRefPubMed Wang Y, Li M, Stadler S et al (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184:205–213CrossRefPubMed
48.
go back to reference Neeli I, Khan SN, Radic M (2008) Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 180:1895–1902PubMed Neeli I, Khan SN, Radic M (2008) Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 180:1895–1902PubMed
49.
go back to reference Brahms H, Raymackers J, Union A, de Keyser F, Meheus L, Lührmann R (2000) The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies. J Biol Chem 275:17122–17129CrossRefPubMed Brahms H, Raymackers J, Union A, de Keyser F, Meheus L, Lührmann R (2000) The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies. J Biol Chem 275:17122–17129CrossRefPubMed
50.
go back to reference Mahler M, Stinton LM, Fritzler MJ (2005) Improved serological differentiation between systemic lupus erythematosus and mixed connective tissue disease by use of an SmD3 peptide-based immunoassay. Clin Diagn Lab Immunol 12:107–113PubMed Mahler M, Stinton LM, Fritzler MJ (2005) Improved serological differentiation between systemic lupus erythematosus and mixed connective tissue disease by use of an SmD3 peptide-based immunoassay. Clin Diagn Lab Immunol 12:107–113PubMed
51.
go back to reference Mahler M, Fritzler MJ, Blüthner M (2005) Identification of a SmD3 epitope with a single symmetrical dimethylation of an arginine residue as a specific target of a subpopulation of anti-Sm antibodies. Arthritis Res Ther 7:R19–R29CrossRefPubMed Mahler M, Fritzler MJ, Blüthner M (2005) Identification of a SmD3 epitope with a single symmetrical dimethylation of an arginine residue as a specific target of a subpopulation of anti-Sm antibodies. Arthritis Res Ther 7:R19–R29CrossRefPubMed
52.
go back to reference Piacentini M, Colizzi V (1999) Tissue transglutaminase: apoptosis versus autoimmunity. Immunol Today 20:130–134CrossRefPubMed Piacentini M, Colizzi V (1999) Tissue transglutaminase: apoptosis versus autoimmunity. Immunol Today 20:130–134CrossRefPubMed
53.
go back to reference Khan MA, Dixit K, Jabeen S, Moinuddin AK (2009) Impact of peroxynitrite modification on structure and immunogenicity of H2A histone. Scand J Immunol 69:99–109CrossRefPubMed Khan MA, Dixit K, Jabeen S, Moinuddin AK (2009) Impact of peroxynitrite modification on structure and immunogenicity of H2A histone. Scand J Immunol 69:99–109CrossRefPubMed
54.
go back to reference Young GW, Hoofring SA, Mamula MJ et al (2005) Structural integrity of histone H2B in vivo requires the activity of protein L-isoaspartate O-methyltransferase, a putative protein repair enzyme. J Biol Chem 280:26094–26098CrossRefPubMed Young GW, Hoofring SA, Mamula MJ et al (2005) Structural integrity of histone H2B in vivo requires the activity of protein L-isoaspartate O-methyltransferase, a putative protein repair enzyme. J Biol Chem 280:26094–26098CrossRefPubMed
55.
go back to reference Muller S, Isabey A, Couppez M, Plaué S, Sommermeyer G, Van Regenmortel MHV (1987) Specificity of antibodies raised against triacetylated histone H4. Mol Immunol 24:779–789CrossRefPubMed Muller S, Isabey A, Couppez M, Plaué S, Sommermeyer G, Van Regenmortel MHV (1987) Specificity of antibodies raised against triacetylated histone H4. Mol Immunol 24:779–789CrossRefPubMed
56.
go back to reference Kuo WN, Kreahling JM, Shanbhag VP, Shanbhag PP, Mewar M (2000) Protein nitration. Mol Cell Biochem 214:121–129CrossRefPubMed Kuo WN, Kreahling JM, Shanbhag VP, Shanbhag PP, Mewar M (2000) Protein nitration. Mol Cell Biochem 214:121–129CrossRefPubMed
57.
go back to reference Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279–289CrossRefPubMed Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279–289CrossRefPubMed
58.
go back to reference Urbonaviciute V, Fürnrohr BG, Meister S et al (2008) Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 205:3007–3018CrossRefPubMed Urbonaviciute V, Fürnrohr BG, Meister S et al (2008) Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 205:3007–3018CrossRefPubMed
59.
go back to reference Dieker JW, van der Vlag J, Berden JH (2002) Triggers for anti-chromatin autoantibody production in SLE. Lupus 11:856–864CrossRefPubMed Dieker JW, van der Vlag J, Berden JH (2002) Triggers for anti-chromatin autoantibody production in SLE. Lupus 11:856–864CrossRefPubMed
60.
go back to reference Arnheim N, Calabrese P (2009) Understanding what determines the frequency and pattern of human germline mutations. Nat Rev Genet 10:478–488CrossRefPubMed Arnheim N, Calabrese P (2009) Understanding what determines the frequency and pattern of human germline mutations. Nat Rev Genet 10:478–488CrossRefPubMed
61.
go back to reference Barros SP, Offenbacher S (2009) Epigenetics: connecting environment and genotype to phenotype and disease. J Dent Res 88:400–408CrossRefPubMed Barros SP, Offenbacher S (2009) Epigenetics: connecting environment and genotype to phenotype and disease. J Dent Res 88:400–408CrossRefPubMed
62.
go back to reference Figueiredo LM, Cross GA, Janzen CJ (2009) Epigenetic regulation in African trypanosomes: a new kid on the block. Nat Rev Microbiol 7:504–513CrossRefPubMed Figueiredo LM, Cross GA, Janzen CJ (2009) Epigenetic regulation in African trypanosomes: a new kid on the block. Nat Rev Microbiol 7:504–513CrossRefPubMed
63.
go back to reference Hewagama A, Richardson B (2009) The genetics and epigenetics of autoimmune diseases. J Autoimmun 33:3–11CrossRefPubMed Hewagama A, Richardson B (2009) The genetics and epigenetics of autoimmune diseases. J Autoimmun 33:3–11CrossRefPubMed
64.
65.
go back to reference Invernizzi P, Pasini S, Selmi C, Gershwin ME, Podda M (2009) Female predominance and X chromosome defects in autoimmune diseases. J Autoimmun 33:12–16CrossRefPubMed Invernizzi P, Pasini S, Selmi C, Gershwin ME, Podda M (2009) Female predominance and X chromosome defects in autoimmune diseases. J Autoimmun 33:12–16CrossRefPubMed
66.
go back to reference Larizza D, Calcaterra V, Martinetti M (2009) Autoimmune stigmata in Turner syndrome: when lacks an X chromosome. J Autoimmun 33:25–30CrossRefPubMed Larizza D, Calcaterra V, Martinetti M (2009) Autoimmune stigmata in Turner syndrome: when lacks an X chromosome. J Autoimmun 33:25–30CrossRefPubMed
67.
go back to reference Persani L, Rossetti R, Cacciatore C, Bonomi M (2009) Primary Ovarian Insufficiency: X chromosome defects and autoimmunity. J Autoimmun 33:35–41CrossRefPubMed Persani L, Rossetti R, Cacciatore C, Bonomi M (2009) Primary Ovarian Insufficiency: X chromosome defects and autoimmunity. J Autoimmun 33:35–41CrossRefPubMed
68.
go back to reference Sawalha AH, Harley JB, Scofield RH (2009) Autoimmunity and Klinefelter's syndrome: when men have two X chromosomes. J Autoimmun 33:31–34CrossRefPubMed Sawalha AH, Harley JB, Scofield RH (2009) Autoimmunity and Klinefelter's syndrome: when men have two X chromosomes. J Autoimmun 33:31–34CrossRefPubMed
69.
go back to reference Wells AD (2009) New insights into the molecular basis of T cell anergy: anergy factors, avoidance sensors, and epigenetic imprinting. J Immunol 182:7331–7341CrossRefPubMed Wells AD (2009) New insights into the molecular basis of T cell anergy: anergy factors, avoidance sensors, and epigenetic imprinting. J Immunol 182:7331–7341CrossRefPubMed
70.
go back to reference Zernicka-Goetz M, Morris SA, Bruce AW (2009) Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat Rev Genet 10:467–477CrossRefPubMed Zernicka-Goetz M, Morris SA, Bruce AW (2009) Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat Rev Genet 10:467–477CrossRefPubMed
Metadata
Title
Epigenetic Histone Code and Autoimmunity
Authors
Jürgen Dieker
Sylviane Muller
Publication date
01-08-2010
Publisher
Humana Press Inc
Published in
Clinical Reviews in Allergy & Immunology / Issue 1/2010
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-009-8173-7

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