DNA methylation changes on immune cells in Systemic Lupus Erythematosus

References

• Ghodke-Puranik Y, Niewold TB. Immunogenetics of systemic lupus erythematosus: a comprehensive review. J Autoimmun. 2015;64:125–136.
   PubMed Web of Science ®Google Scholar
• Pons-Estel GJ, Alarcón GS, Scofield L, et al. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin Arthritis Rheum. 2010;39(4):257–268.
   PubMed Web of Science ®Google Scholar
• Chen L, Morris DL, Vyse TJ. Genetic advances in systemic lupus erythematosus: an update. Curr Opin Rheumatol. 2017;29(5):423–433.
   PubMed Web of Science ®Google Scholar
• Patel DR, Richardson BC. Dissecting complex epigenetic alterations in human lupus. Arthritis Res Ther. 2012;15(1):201.
   Web of Science ®Google Scholar
• Ospelt C. Epigenetic biomarkers in rheumatology – the future? Swiss Med Wkly. 2016;146:w14312. Available from: http://doi.emh.ch/smw.2016.14312.
   PubMed Web of Science ®Google Scholar
• Jeffries MA, Sawalha AH. Epigenetics in systemic lupus erythematosus: leading the way for specific therapeutic agents. Int J Clin Rheumatol. 2011;6(4):423–438.
   PubMedGoogle Scholar
• Chen SH, Lv QL, Hu L, et al. DNA methylation alterations in the pathogenesis of lupus: DNA methylation alterations in lupus. Clin Exp Immunol. 2017;187(2):185–192.
   PubMed Web of Science ®Google Scholar
• Liu C, Ou T, Wu C, et al. Global DNA methylation, DNMT1, and MBD2 in patients with systemic lupus erythematosus. Lupus. 2011;20(2):131–136.
   PubMed Web of Science ®Google Scholar
• Deng C, Lu Q, Zhang Z, et al. Hydralazine may induce autoimmunity by inhibiting extracellular signal-regulated kinase pathway signaling. Arthritis Rheum. 2003;48(3):746–756.
   PubMed Web of Science ®Google Scholar
• Sun B, Hu L, Luo Z-Y, et al. DNA methylation perspectives in the pathogenesis of autoimmune diseases. Clin Immunol. 2016;164:21–27.
   PubMed Web of Science ®Google Scholar
• Javierre BM, Fernandez AF, Richter J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res. 2010;20(2):170–179.
   PubMed Web of Science ®Google Scholar
• Correia Azevedo P, Murphy G, Isenberg DA. Pathology of systemic lupus erythematosus: the challenges ahead. Methods Mol Biol. 2014;1134:1–16.
   PubMedGoogle Scholar
• Wang Z, Chang C, Lu Q. Epigenetics of CD4+ T cells in autoimmune diseases. Curr Opin Rheumatol. 2017;29(4):361–368.
   PubMed Web of Science ®Google Scholar
• Sawalha AH, Jeffries M, Webb R, et al. Defective T-cell ERK signaling induces interferon-regulated gene expression and overexpression of methylation-sensitive genes similar to lupus patients. Genes Immun. 2008;9(4):368–378.
   PubMed Web of Science ®Google Scholar
• Gorelik G, Sawalha AH, Patel D, et al. T cell PKCδ kinase inactivation induces lupus-like autoimmunity in mice. Clin Immunol. 2015;158(2):193–203.
   PubMed Web of Science ®Google Scholar
• Gorelik G, Fang JY, Wu A, et al. Impaired T cell protein kinase Cδ activation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. J Immunol. 2007;179(8):5553–5563.
   PubMed Web of Science ®Google Scholar
• Sunahori K, Nagpal K, Hedrich CM, et al. The catalytic subunit of protein phosphatase 2A (PP2Ac) promotes DNA hypomethylation by suppressing the phosphorylated mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) kinase (MEK)/phosphorylated ERK/DNMT1 protein pathway in T-cells from controls and systemic lupus erythematosus patients. J Biol Chem. 2013;288(30):21936–21944.
   PubMed Web of Science ®Google Scholar
• Sunahori K, Juang Y-T, Kyttaris VC, et al. Promoter hypomethylation results in increased expression of protein phosphatase 2A in T cells from patients with systemic lupus erythematosus. JI. 2011;186(7):4508–4517.
   Google Scholar
• Patel D, Gorelik G, Richardson B. Protein phosphatase 5 contributes to the overexpression of epigenetically regulated T-lymphocyte genes in patients with lupus. Lupus (Los Angel). 2016;1:120.
   PubMedGoogle Scholar
• Balada E, Felip L, Ordi-Ros J, et al. DUSP23 is over-expressed and linked to the expression of DNMTs in CD4+ T cells from systemic lupus erythematosus patients: DUSP23 and lupus. Clin Exp Immunol. 2017;187(2):242–250.
   PubMed Web of Science ®Google Scholar
• Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011;469(7330):343–349.
   PubMed Web of Science ®Google Scholar
• Tsou P-S, Coit P, Kilian NC, et al. EZH2 modulates the DNA methylome and controls T cell adhesion through junctional adhesion molecule A in lupus patients. Arthritis Rheumatol. 2018;70(1):98–108.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhao M, Yin H, et al. Overexpression of the growth arrest and DNA damage-induced 45α gene contributes to autoimmunity by promoting DNA demethylation in lupus T cells. Arthritis Rheum. 2010;62(5):1438–1447.
   PubMedGoogle Scholar
• Li Y, Huang C, Zhao M, et al. A possible role of HMGB1 in DNA demethylation in CD4+ T cells from patients with systemic lupus erythematosus. Clin Dev Immunol. 2013;2013:1–5.
   Google Scholar
• Sanders MA, Chew E, Flensburg C, et al. MBD4 guards against methylation damage and germ line deficiency predisposes to clonal hematopoiesis and early-onset AML. Blood. 2018;132(14):1526–1534.
   PubMed Web of Science ®Google Scholar
• Liao W, Li M, Wu H, et al. Down-regulation of MBD4 contributes to hypomethylation and overexpression of CD70 in CD4+ T cells in systemic lupus erythematosus. Clin Epigenetics 2017;9:104. Available from: http://clinicalepigeneticsjournal.biomedcentral.com/articles/10.1186/s13148-017-0405-8.
   PubMed Web of Science ®Google Scholar
• Qin H, Zhu X, Liang J, et al. MicroRNA-29b contributes to DNA hypomethylation of CD4+ T cells in systemic lupus erythematosus by indirectly targeting DNA methyltransferase 1. J Dermatol Sci. 2013;69(1):61–67.
   PubMed Web of Science ®Google Scholar
• Zhao S, Wang Y, Liang Y, et al. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum. 2011;63(5):1376–1386.
   PubMedGoogle Scholar
• Ding S, Liang Y, Zhao M, et al. Decreased microRNA-142-3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum. 2012;64(9):2953–2963.
   PubMedGoogle Scholar
• Li D, Chen J, Pei D. The battle between TET proteins and DNA methylation for the right cell. Trends Cell Biol. 2018;28(12):973–975.
   PubMed Web of Science ®Google Scholar
• Zhao M, Li M, Gao X, et al. Downregulation of BDH2 modulates iron homeostasis and promotes DNA demethylation in CD4+ T cells of systemic lupus erythematosus. Clin Immunol. 2018;187:113–121.
   PubMed Web of Science ®Google Scholar
• Zhao M, Sun Y, Gao F, et al. Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4+ T cells. J Autoimmun. 2010;35(1):58–69.
   PubMed Web of Science ®Google Scholar
• Zhao M, Tan Y, Peng Q, et al. IL-6/STAT3 pathway induced deficiency of RFX1 contributes to Th17-dependent autoimmune diseases via epigenetic regulation. Nat Commun. 2018;9:583. Available from: http://www.nature.com/articles/s41467-018-02890-0.
   PubMed Web of Science ®Google Scholar
• Koga T, Ichinose K, Tsokos GC. T cells and IL-17 in lupus nephritis. Clin Immunol. 2017;185:95–99.
   PubMed Web of Science ®Google Scholar
• Jeffries M, Dozmorov M, Tang Y, et al. Genome-wide DNA methylation patterns in CD4+ T cells from patients with systemic lupus erythematosus. Epigenetics. 2011;6(5):593–601.
   PubMed Web of Science ®Google Scholar
• Absher DM, Li X, Waite LL, et al. Genome-wide DNA methylation analysis of systemic lupus erythematosus reveals persistent hypomethylation of interferon genes and compositional changes to CD4+ T-cell populations. O’Shea J, editor. PLoS Genet. 2013;9(8):e1003678.
   PubMed Web of Science ®Google Scholar
• Zhao M, Liu S, Luo S, et al. DNA methylation and mRNA and microRNA expression of SLE CD4+ T cells correlate with disease phenotype. J Autoimmun. 2014;54:127–136.
   PubMed Web of Science ®Google Scholar
• Renauer P, Coit P, Jeffries MA, et al. DNA methylation patterns in naïve CD4+ T cells identify epigenetic susceptibility loci for malar rash and discoid rash in systemic lupus erythematosus. Lupus Sci Med. 2015;2(1):e000101.
   PubMed Web of Science ®Google Scholar
• Lu Q, Wu A, Tesmer L, et al. Demethylation of CD40LG on the inactive X in T cells from women with lupus. J Immunol. 2007;179(9):6352–6358.
   PubMed Web of Science ®Google Scholar
• Coit P, Renauer P, Jeffries MA, et al. Renal involvement in lupus is characterized by unique DNA methylation changes in naïve CD4+ T cells. J Autoimmun. 2015;61:29–35.
   PubMed Web of Science ®Google Scholar
• Hedrich CM, Rauen T, Apostolidis SA, et al. Stat3 promotes IL-10 expression in lupus T cells through trans-activation and chromatin remodeling. Proc Natl Acad Sci USA. 2014;111(37):13457–13462.
   PubMed Web of Science ®Google Scholar
• Zhao M, Tang J, Gao F, et al. Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus. J Biomed Biotechnol. 2010;2010:1–9.
   Google Scholar
• Zhang Q, Ding S, Zhang H, et al. Increased Set1 binding at the promoter induces aberrant epigenetic alterations and up-regulates cyclic adenosine 5’-monophosphate response element modulator alpha in systemic lupus erythematosus. Clin Epigenetics. 2016;8:126. Available from: http://clinicalepigeneticsjournal.biomedcentral.com/articles/10.1186/s13148-016-0294-2.
   PubMed Web of Science ®Google Scholar
• Rauen T, Hedrich CM, Juang Y-T, et al. cAMP-responsive element modulator (CREM)α protein induces interleukin 17A expression and mediates epigenetic alterations at the interleukin-17A gene locus in patients with systemic lupus erythematosus. J Biol Chem. 2011;286(50):43437–43446.
   PubMed Web of Science ®Google Scholar
• Dai R, Lu R, Ahmed SA. The upregulation of genomic imprinted DLK1-Dio3 miRNAs in murine lupus is associated with global DNA hypomethylation. Bobé P, editor. PLoS One. 2016;11(4):e0153509.
   PubMed Web of Science ®Google Scholar
• Wu Z, Li X, Qin H, et al. Ultraviolet B enhances DNA hypomethylation of CD4+ T cells in systemic lupus erythematosus via inhibiting DNMT1 catalytic activity. J Dermatol Sci. 2013;71(3):167–173.
   PubMed Web of Science ®Google Scholar
• Wu Z, Sun Y, Mei X, et al. 17β-oestradiol enhances global DNA hypomethylation in CD4-positive T cells from female patients with lupus, through overexpression of oestrogen receptor-α-mediated downregulation of DNMT1. Clin Exp Dermatol. 2014;39(4):525–532.
   PubMed Web of Science ®Google Scholar
• Li Y, Gorelik G, Strickland FM, et al. Oxidative stress, T Cell DNA methylation, and lupus: oxidative stress and lupus. Arthritis Rheumatol. 2014;66(6):1574–1582.
   PubMed Web of Science ®Google Scholar
• Strickland FM, Li Y, Johnson K, et al. CD4+ T cells epigenetically modified by oxidative stress cause lupus-like autoimmunity in mice. J Autoimmun. 2015;62:75–80.
   PubMed Web of Science ®Google Scholar
• Guo Y, Sawalha AH, Lu Q. Epigenetics in the treatment of systemic lupus erythematosus: potential clinical application. Clin Immunol. 2014;155(1):79–90.
   PubMed Web of Science ®Google Scholar
• Zhang J, Yuan B, Zhang F, et al. Cyclophosphamide perturbs cytosine methylation in jurkat-T cells through LSD1-mediated stabilization of DNMT1 protein. Chem Res Toxicol. 2011;24(11):2040–2043.
   PubMed Web of Science ®Google Scholar
• Peters FS, Peeters AMA, Hofland LJ, et al. Interferon-gamma DNA methylation is affected by mycophenolic acid but not by tacrolimus after T-cell activation. Front Immunol. 2017;8:822.
   PubMed Web of Science ®Google Scholar
• Yang Y, Tang Q, Zhao M, et al. The effect of mycophenolic acid on epigenetic modifications in lupus CD4+ T cells. Clin Immunol. 2015;158(1):67–76.
   PubMed Web of Science ®Google Scholar
• Cribbs AP, Kennedy A, Penn H, et al. Methotrexate restores regulatory T cell function through demethylation of the FoxP3 upstream enhancer in patients with rheumatoid arthritis. Arthritis Rheumatol. 2015;67(5):1182–1192.
   PubMed Web of Science ®Google Scholar
• Renaudineau Y, Garaud S, Le Dantec C, et al. Autoreactive B cells and epigenetics. Clin Rev Allergy Immunol. 2010;39(1):85–94.
   PubMed Web of Science ®Google Scholar
• Scharer CD, Blalock EL, Barwick BG, et al. ATAC-seq on biobanked specimens defines a unique chromatin accessibility structure in naïve SLE B cells. Sci Rep. 2016;6:27030. Available from: http://www.nature.com/articles/srep27030.
   PubMed Web of Science ®Google Scholar
• Scharer CD, Blalock EL, Mi T, et al. Epigenetic programming underpins B cell dysfunction in human SLE. Nat Immunol. 2019;20(8):1071–1082.
   PubMed Web of Science ®Google Scholar
• Rawlings DJ, Metzler G, Wray-Dutra M, et al. Altered B cell signalling in autoimmunity. Nat Rev Immunol. 2017;17(7):421–436.
   PubMed Web of Science ®Google Scholar
• Mihara M, Hashizume M, Yoshida H, et al. IL-6/IL-6 receptor system and its role in physiological and pathological conditions. Clin Sci. 2012;122(4):143–159.
   PubMed Web of Science ®Google Scholar
• Garaud S, Le Dantec C, Jousse-Joulin S, et al. IL-6 modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation. J Immunol. 2009;182(9):5623–5632.
   PubMed Web of Science ®Google Scholar
• Ward JM, Ratliff ML, Dozmorov MG, et al. Human effector B lymphocytes express ARID3a and secrete interferon alpha. J Autoimmun. 2016;75:130–140.
   PubMed Web of Science ®Google Scholar
• Fali T, Le Dantec C, Thabet Y, et al. DNA methylation modulates HRES1/p28 expression in B cells from patients with lupus. Autoimmunity. 2014;47(4):265–271.
   PubMed Web of Science ®Google Scholar
• Zhao M, Zhou Y, Zhu B, et al. IFI44L promoter methylation as a blood biomarker for systemic lupus erythematosus. Ann Rheum Dis. 2016;75(11):1998–2006.
   PubMed Web of Science ®Google Scholar
• Fan H, Zhao G, Ren D, et al. Gender differences of B cell signature related to estrogen-induced IFI44L/BAFF in systemic lupus erythematosus. Immunol Lett. 2017;181:71–78.
   PubMed Web of Science ®Google Scholar
• de Andres MC, Perez-Pampin E, Calaza M, et al. Assessment of global DNA methylation in peripheral blood cell subpopulations of early rheumatoid arthritis before and after methotrexate. Arthritis Res Ther. 2015;17:233. Available from: http://arthritis-research.com/content/17/1/233.
   PubMed Web of Science ®Google Scholar
• Ulff-Møller CJ, Asmar F, Liu Y, et al. Twin DNA methylation profiling reveals flare-dependent interferon signature and B cell promoter hypermethylation in systemic lupus erythematosus. Arthritis Rheumatol. 2018;70(6):878–890.
   PubMed Web of Science ®Google Scholar
• Notley CA, Jordan CK, McGovern JL, et al. DNA methylation governs the dynamic regulation of inflammation by apoptotic cells during efferocytosis. Sci Rep. 2017;7:42204.
   PubMed Web of Science ®Google Scholar
• Sawalha AH. Neutrophils in systemic lupus erythematosus. In: Tsokos GC, editor. Systemic lupus erythematosus. Amsterdam: Academic Press; 2016. p. 127–130. Available from: http://linkinghub.elsevier.com/retrieve/pii/B9780128019177000152.
   Google Scholar
• Coit P, Yalavarthi S, Ognenovski M, et al. Epigenome profiling reveals significant DNA demethylation of interferon signature genes in lupus neutrophils. J Autoimmun. 2015;58:59–66.
   PubMed Web of Science ®Google Scholar
• Sukapan P, Promnarate P, Avihingsanon Y, et al. Types of DNA methylation status of the interspersed repetitive sequences for LINE-1, Alu, HERV-E and HERV-K in the neutrophils from systemic lupus erythematosus patients and healthy controls. J Hum Genet. 2014;59(4):178–188.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Gong K, Denholtz M, et al. Comprehensive characterization of neutrophil genome topology. Genes Dev. 2017;31(2):141–153.
   PubMed Web of Science ®Google Scholar
• Wardowska A, Komorniczak M, Bułło-Piontecka B, et al. Transcriptomic and epigenetic alterations in dendritic cells correspond with chronic kidney disease in lupus nephritis. Front Immunol. 2019;10:2026. Available from: https://www.frontiersin.org/article/10.3389/fimmu.2019.02026/full.
   PubMed Web of Science ®Google Scholar