DNA methylation perspectives in the pathogenesis of autoimmune diseases

Clinical Immunology

Volumn 164, Issue , 2016, Pages 21-27

  Sun, Bao ^a,b   Hu, Lei ^a,b   Luo, Zhi Ying ^a,b   Chen, Xiao Ping ^a,b   Zhou, Hong Hao ^a,b   Zhang, Wei ^a,b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

DNA methylation; Immune related genes; Multiple sclerosis; Rheumatoid arthritis; Systemic lupus erythematosus; Type 1 diabetes

Indexed keywords

ANIMAL; AUTOIMMUNE DISEASE; DNA METHYLATION; GENETICS; HUMAN;

ANIMALS; AUTOIMMUNE DISEASES; DNA METHYLATION; HUMANS;

EID: 84955589089     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.01.011     Document Type: Review

References (82)

1. Shoenfeld Y., Selmi C., Zimlichman E., Gershwin M.E. The autoimmunologist: geoepidemiology, a new center of gravity, and prime time for autoimmunity. J. Autoimmun. 2008, 31:325-330.
2. Lu Q. The critical importance of epigenetics in autoimmunity. J. Autoimmun. 2013, 41:1-5.
3. Ellis J.A., Kemp A.S., Ponsonby A.L. Gene-environment interaction in autoimmune disease. Expert Rev. Mol. Med. 2014, 16:e4.
4. Richardson B., Ray D., Yung R. Murine models of lupus induced by hypomethylated T cells. Methods Mol. Med. 2004, 102:285-294.
5. Bernstein B.E., Meissner A., Lander E.S. The mammalian epigenome. Cell 2007, 128:669-681.
6. Lee P.P., Fitzpatrick D.R., Beard C., Jessup H.K., Lehar S., Makar K.W., Perez-Melgosa M., Sweetser M.T., Schlissel M.S., Nguyen S., Cherry S.R., Tsai J.H., Tucker S.M., Weaver W.M., Kelso A., Jaenisch R., Wilson C.B. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001, 15:763-774.
7. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16:6-21.
8. Antequera F., Bird A. Number of CpG islands and genes in human and mouse. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11995-11999.
9. Ellis J.A., Munro J.E., Chavez R.A., Gordon L., Joo J.E., Akikusa J.D., Allen R.C., Ponsonby A.L., Craig J.M., Saffery R. Genome-scale case-control analysis of CD4+ T-cell DNA methylation in juvenile idiopathic arthritis reveals potential targets involved in disease. Clinical Epigenetics 2012, 4:20.
10. Rodriguez E., Baurecht H., Wahn A.F., Kretschmer A., Hotze M., Zeilinger S., Klopp N., Illig T., Schramm K., Prokisch H., Kuhnel B., Gieger C., Harder J., Cifuentes L., Novak N., Weidinger S. An integrated epigenetic and transcriptomic analysis reveals distinct tissue-specific patterns of DNA methylation associated with atopic dermatitis. J. Investig. Dermatol. 2014, 134:1873-1883.
11. Vedove C.D., Del Giglio M., Schena D., Girolomoni G. Drug-induced lupus erythematosus. Arch. Dermatol. Res. 2008, 301:99-105.
12. Uetrecht J. Current trends in drug-induced autoimmunity. Autoimmun. Rev. 2005, 4:309-314.
13. Deng C., Lu Q., Zhang Z., Rao T., Attwood J., Yung R., Richardson B. Hydralazine may induce autoimmunity by inhibiting extracellular signal-regulated kinase pathway signaling. Arthritis Rheum. 2003, 48:746-756.
14. Quddus J., Johnson K.J., Gavalchin J., Amento E.P., Chrisp C.E., Yung R.L., Richardson B.C. Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is sufficient to cause a lupus-like disease in syngeneic mice. J. Clin. Invest. 1993, 92:38-53.
15. Lee B.H., Yegnasubramanian S., Lin X., Nelson W.G. Procainamide is a specific inhibitor of DNA methyltransferase 1. J. Biol. Chem. 2005, 280:40749-40756.
16. Gorelik G.J., Yarlagadda S., Patel D.R., Richardson B.C. Protein kinase Cdelta oxidation contributes to ERK inactivation in lupus T cells. Arthritis Rheum. 2012, 64:2964-2974.
17. Deng C., Kaplan M.J., Yang J., Ray D., Zhang Z., McCune W.J., Hanash S.M., Richardson B.C. Decreased Ras-mitogen-activated protein kinase signaling may cause DNA hypomethylation in T lymphocytes from lupus patients. Arthritis Rheum. 2001, 44:397-407.
18. Gorelik G., Richardson B. Aberrant T cell ERK pathway signaling and chromatin structure in lupus. Autoimmun. Rev. 2009, 8:196-198.
19. Gorelik G., Fang J.Y., Wu A., Sawalha A.H., Richardson B. Impaired T Cell protein kinase C Activation decreases ERK Pathway signaling in idiopathic and hydralazine-induced lupus. J. Immunol. 2007, 179:5553-5563.
20. Oelke K., Lu Q., Richardson D., Wu A., Deng C., Hanash S., Richardson B. Overexpression of CD70 and overstimulation of IgG synthesis by lupus T cells and T cells treated with DNA methylation inhibitors. Arthritis Rheum. 2004, 50:1850-1860.
21. Sunahori K., Nagpal K., Hedrich C.M., Mizui M., Fitzgerald L.M., Tsokos G.C. 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, 288:21936-21944.
22. Strickland F.M., Li Y., Johnson K., Sun Z., Richardson B.C. CD4(+) T cells epigenetically modified by oxidative stress cause lupus-like autoimmunity in mice. J. Autoimmun. 2015, 62:75-80.
23. Li Y., Gorelik G., Strickland F.M., Richardson B.C. Oxidative stress, T cell DNA methylation, and lupus. Arthritis Rheum. 2014, 66:1574-1582.
24. Zhang Y., Zhao M., Sawalha A.H., Richardson B., Lu Q. Impaired DNA methylation and its mechanisms in CD4(+)T cells of systemic lupus erythematosus. J. Autoimmun. 2013, 41:92-99.
25. Richardson B., Scheinbart L., Strahler J., Gross L., Hanash S., Johnson M. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum. 1990, 33:1665-1673.
26. Lu Q., Kaplan M., Ray D., Ray D., Zacharek S., Gutsch D., Richardson B. Demethylation of ITGAL (CD11a) regulatory sequences in systemic lupus erythematosus. Arthritis Rheum. 2002, 46:1282-1291.
27. Kaplan M.J., Lu Q., Wu A., Attwood J., Richardson B. Demethylation of promoter regulatory elements contributes to perforin overexpression in CD4+ lupus T cells. J. Immunol. 2004, 172:3652-3661.
28. Lu Q., Wu A., Richardson B.C. Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J. Immunol. 2005, 174:6212-6219.
29. Lu Q., Wu A., Tesmer L., Ray D., Yousif N., Richardson B. Demethylation of CD40LG on the inactive X in T cells from women with lupus. J. Immunol. 2007, 179:6352-6358.
30. Zhao M., Sun Y., Gao F., Wu X., Tang J., Yin H., Luo Y., Richardson B., Lu Q. Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4+ T cells. J. Autoimmun. 2010, 35:58-69.
31. Li Y., Zhao M., Yin H., Gao F., Wu X., Luo Y., Zhao S., Zhang X., Su Y., Hu N., Long H., Richardson B., Lu Q. Overexpression of the growth arrest and DNA damage-induced 45alpha gene contributes to autoimmunity by promoting DNA demethylation in lupus T cells. Arthritis Rheum. 2010, 62:1438-1447.
32. Li Y., Huang C., Zhao M., Liang G., Xiao R., Yung S., Chan T.M., Lu Q. 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.
33. Sunahori K., Juang Y.T., Kyttaris V.C., Tsokos G.C. Promoter hypomethylation results in increased expression of protein phosphatase 2A in T cells from patients with systemic lupus erythematosus. J. Immunol. 2011, 186:4508-4517.
34. Lal G., Zhang N., van der Touw W., Ding Y., Ju W., Bottinger E.P., Reid S.P., Levy D.E., Bromberg J.S. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J. Immunol. 2009, 182:259-273.
35. Liu Y., Chen Y., Richardson B. Decreased DNA methyltransferase levels contribute to abnormal gene expression in "senescent" CD4(+)CD28(-) T cells. Clinical Immunology (Orlando, Fla.) 2009, 132:257-265.
36. Zhao M., Tang J., Gao F., Wu X., Liang Y., Yin H., Lu Q. Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus. J. Biomed. Biotechnol. 2010, 2010:931018.
37. Wu Z., Mei X., Zhao D., Sun Y., Song J., Pan W., Shi W. DNA methylation modulates HERV-E expression in CD4+ T cells from systemic lupus erythematosus patients. J. Dermatol. Sci. 2015, 77:110-116.
38. Coit P., Jeffries M., Altorok N., Dozmorov M.G., Koelsch K.A., Wren J.D., Merrill J.T., McCune W.J., Sawalha A.H. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naive CD4+ T cells from lupus patients. J. Autoimmun. 2013, 43:78-84.
39. Renauer P., Coit P., Jeffries M.A., Merrill J.T., McCune W.J., Maksimowicz-McKinnon K., Sawalha A.H. DNA methylation patterns in naive CD4+ T cells identify epigenetic susceptibility loci for malar rash and discoid rash in systemic lupus erythematosus. Lupus Science & Medicine 2015, 2:e000101.
40. Coit P., Renauer P., Jeffries M.A., Merrill J.T., McCune W.J., Maksimowicz-McKinnon K., Sawalha A.H. Renal involvement in lupus is characterized by unique DNA methylation changes in naive CD4+ T cells. J. Autoimmun. 2015, 61:29-35.
41. Chung S.A., Nititham J., Elboudwarej E., Quach H.L., Taylor K.E., Barcellos L.F., Criswell L.A. Genome-wide assessment of differential DNA methylation associated with autoantibody production in systemic lupus erythematosus. PLoS One 2015, 10:e0129813.
42. Garaud S., Le Dantec C., Jousse-Joulin S., Hanrotel-Saliou C., Saraux A., Mageed R.A., Youinou P., Renaudineau Y. IL-6 modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation. J. Immunol. 2009, 182:5623-5632.
43. Fali T., Le Dantec C., Thabet Y., Jousse S., Hanrotel C., Youinou P., Brooks W.H., Perl A., Renaudineau Y. DNA methylation modulates HRES1/p28 expression in B cells from patients with lupus. Autoimmunity 2014, 47:265-271.
44. Garchow B.G., Bartulos Encinas O., Leung Y.T., Tsao P.Y., Eisenberg R.A., Caricchio R., Obad S., Petri A., Kauppinen S., Kiriakidou M. Silencing of microRNA-21 in vivo ameliorates autoimmune splenomegaly in lupus mice. EMBO Mol. Med. 2011, 3:605-615.
45. Pan W., Zhu S., Yuan M., Cui H., Wang L., Luo X., Li J., Zhou H., Tang Y., Shen N. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly and indirectly targeting DNA methyltransferase 1. J. Immunol. 2010, 184:6773-6781.
46. Zhao S., Wang Y., Liang Y., Zhao M., Long H., Ding S., Yin H., Lu Q. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum. 2011, 63:1376-1386.
47. Ding S., Liang Y., Zhao M., Liang G., Long H., Zhao S., Wang Y., Yin H., Zhang P., Zhang Q., Lu Q. Decreased microRNA-142-3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthritis Rheum. 2012, 64:2953-2963.
48. Nile C.J., Read R.C., Akil M., Duff G.W., Wilson A.G. Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum. 2008, 58:2686-2693.
49. Fu L.H., Ma C.L., Cong B., Li S.J., Chen H.Y., Zhang J.G. Hypomethylation of proximal CpG motif of interleukin-10 promoter regulates its expression in human rheumatoid arthritis. Acta Pharmacol. Sin. 2011, 32:1373-1380.
50. de la Rica L., Urquiza J.M., Gomez-Cabrero D., Islam A.B., Lopez-Bigas N., Tegner J., Toes R.E., Ballestar E. Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression. J. Autoimmun. 2013, 41:6-16.
51. Takami N., Osawa K., Miura Y., Komai K., Taniguchi M., Shiraishi M., Sato K., Iguchi T., Shiozawa K., Hashiramoto A., Shiozawa S. Hypermethylated promoter region of DR3, the death receptor 3 gene, in rheumatoid arthritis synovial cells. Arthritis Rheum. 2006, 54:779-787.
52. Karouzakis E., Rengel Y., Jungel A., Kolling C., Gay R.E., Michel B.A., Tak P.P., Gay S., Neidhart M., Ospelt C. DNA methylation regulates the expression of CXCL12 in rheumatoid arthritis synovial fibroblasts. Genes and Immunity 2011, 12:643-652.
53. Karouzakis E., Trenkmann M., Gay R.E., Michel B.A., Gay S., Neidhart M. Epigenome analysis reveals TBX5 as a novel transcription factor involved in the activation of rheumatoid arthritis synovial fibroblasts. J. Immunol. 2014, 193:4945-4951.
54. Glossop J.R., Emes R.D., Nixon N.B., Haworth K.E., Packham J.C., Dawes P.T., Fryer A.A., Mattey D.L., Farrell W.E. Genome-wide DNA methylation profiling in rheumatoid arthritis identifies disease-associated methylation changes that are distinct to individual T- and B-lymphocyte populations. Epigenetics 2014, 9:1228-1237.
55. Fukuhara T., Tomiyama T., Yasuda K., Ueda Y., Ozaki Y., Son Y., Nomura S., Uchida K., Okazaki K., Kinashi T. Hypermethylation of MST1 in IgG4-related autoimmune pancreatitis and rheumatoid arthritis. Biochem. Biophys. Res. Commun. 2015, 463:968-974.
56. Kennedy A., Schmidt E.M., Cribbs A.P., Penn H., Amjadi P., Syed K., Read J.E., Green P., Gregory B., Brennan F.M. A novel upstream enhancer of FOXP3, sensitive to methylation-induced silencing, exhibits dysregulated methylation in rheumatoid arthritis Treg cells. Eur. J. Immunol. 2014, 44:2968-2978.
57. Cribbs A.P., Kennedy A., Penn H., Amjadi P., Green P., Read J.E., Brennan F., Gregory B., Williams R.O. Methotrexate restores regulatory T Cell function through demethylation of the FoxP3 upstream enhancer in patients with rheumatoid arthritis. Arthritis Rheum. 2015, 67:1182-1192.
58. Kojima A., Kobayashi T., Ito S., Murasawa A., Nakazono K., Yoshie H. Tumor necrosis factor-alpha gene promoter methylation in Japanese adults with chronic periodontitis and rheumatoid arthritis. J. Periodontal Res. 2015, [Epub ahead of print].
59. Stanczyk J., Ospelt C., Karouzakis E., Filer A., Raza K., Kolling C., Gay R., Buckley C.D., Tak P.P., Gay S., Kyburz D. Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation. Arthritis Rheum. 2011, 63:373-381.
60. Miao C.G., Yang Y.Y., He X., Huang C., Huang Y., Qin D., Du C.L., Li J. MicroRNA-152 modulates the canonical Wnt pathway activation by targeting DNA methyltransferase 1 in arthritic rat model. Biochimie 2014, 106:149-156.
61. Kucukali C.I., Kurtuncu M., Coban A., Cebi M., Tuzun E. Epigenetics of multiple sclerosis: an updated review. Neruomol. Med. 2015, 17:83-96.
62. Kumagai C., Kalman B., Middleton F.A., Vyshkina T., Massa P.T. Increased promoter methylation of the immune regulatory gene SHP-1 in leukocytes of multiple sclerosis subjects. J. Neuroimmunol. 2012, 246:51-57.
63. Christophi G.P., Panos M., Hudson C.A., Tsikkou C., Mihai C., Mejico L.J., Jubelt B., Massa P.T. Interferon-beta treatment in multiple sclerosis attenuates inflammatory gene expression through inducible activity of the phosphatase SHP-1. Clinical Immunology (Orlando, Fla.) 2009, 133:27-44.
64. Mastronardi F.G., Noor A., Wood D.D., Paton T., Moscarello M.A. Peptidyl argininedeiminase 2 CpG island in multiple sclerosis white matter is hypomethylated. J. Neurosci. Res. 2007, 85:2006-2016.
65. Perron H., Lang A. The human endogenous retrovirus link between genes and environment in multiple sclerosis and in multifactorial diseases associating neuroinflammation. Clin. Rev. Allergy Immunol. 2010, 39:51-61.
66. Calabrese R., Valentini E., Ciccarone F., Guastafierro T., Bacalini M.G., Ricigliano V.A., Zampieri M., Annibali V., Mechelli R., Franceschi C., Salvetti M., Caiafa P. TET2 gene expression and 5-hydroxymethylcytosine level in multiple sclerosis peripheral blood cells. Biochim. Biophys. Acta 2014, 1842:1130-1136.
67. Graves M., Benton M., Lea R., Boyle M., Tajouri L., Macartney-Coxson D., Scott R., Lechner-Scott J. Methylation differences at the HLA-DRB1 locus in CD4+ T-cells are associated with multiple sclerosis. Multiple Sclerosis Journal 2013, 20:1033-1041.
68. Bos S.D., Page C.M., Andreassen B.K., Elboudwarej E., Gustavsen M.W., Briggs F., Quach H., Leikfoss I.S., Bjolgerud A., Berge T., Harbo H.F., Barcellos L.F. Genome-wide DNA methylation profiles indicate CD8+ T cell hypermethylation in multiple sclerosis. PLoS One 2015, 10:e0117403.
69. Cox M.B., Cairns M.J., Gandhi K.S., Carroll A.P., Moscovis S., Stewart G.J., Broadley S., Scott R.J., Booth D.R., Lechner-Scott J. MicroRNAs miR-17 and miR-20a inhibit T cell activation genes and are under-expressed in MS whole blood. PLoS One 2010, 5:e12132.
70. Stankov K., Benc D., Draskovic D. Genetic and epigenetic factors in etiology of diabetes mellitus type 1. Pediatrics 2013, 132:1112-1122.
71. Disanto G., Vcelakova J., Pakpoor J., Elangovan R.I., Sumnik Z., Ulmannova T., Ebers G.C., Ramagopalan S.V., Stechova K. DNA methylation in monozygotic quadruplets affected by type 1 diabetes. Diabetologia 2013, 56:2093-2095.
72. Stefan M., Zhang W., Concepcion E., Yi Z., Tomer Y. DNA methylation profiles in type 1 diabetes twins point to strong epigenetic effects on etiology. J. Autoimmun. 2014, 50:33-37.
73. Rakyan V.K., Beyan H., Down T.A., Hawa M.I., Maslau S., Aden D., Daunay A., Busato F., Mein C.A., Manfras B., Dias K.R., Bell C.G., Tost J., Boehm B.O., Beck S., Leslie R.D. Identification of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet. 2011, 7:e1002300.
74. Bell C.G., Teschendorff A.E., Rakyan V.K., Maxwell A.P., Beck S., Savage D.A. Genome-wide DNA methylation analysis for diabetic nephropathy in type 1 diabetes mellitus. BMC Med. Genet. 2010, 3:33.
75. Agardh E., Lundstig A., Perfilyev A., Volkov P., Freiburghaus T., Lindholm E., Ronn T., Agardh C.D., Ling C. Genome-wide analysis of DNA methylation in subjects with type 1 diabetes identifies epigenetic modifications associated with proliferative diabetic retinopathy. BMC Medicine 2015, 13:182.
76. Fradin D., Le Fur S., Mille C., Naoui N., Groves C., Zelenika D., McCarthy M.I., Lathrop M., Bougneres P. Association of the CpG methylation pattern of the proximal insulin gene promoter with type 1 diabetes. PLoS One 2012, 7:e36278.
77. Belot M.P., Fradin D., Mai N., Le Fur S., Zelenika D., Kerr-Conte J., Pattou F., Lucas B., Bougneres P. CpG methylation changes within the IL2RA promoter in type 1 diabetes of childhood onset. PLoS One 2013, 8:e68093.
78. Gu T., Falhammar H., Gu H.F., Brismar K. Epigenetic analyses of the insulin-like growth factor binding protein 1 gene in type 1 diabetes and diabetic nephropathy. Clinical Epigenetics 2014, 6:10.
79. Chen H., Lan H.Y., Roukos D.H., Cho W.C. Application of microRNAs in diabetes mellitus. J. Endocrinol. 2014, 222:R1-R10.
80. Glossop J.R., Nixon N.B., Emes R.D., Haworth K.E., Packham J.C., Dawes P.T., Fryer A.A., Mattey D.L., Farrell W.E. Epigenome-wide profiling identifies significant differences in DNA methylation between matched-pairs of T- and B-lymphocytes from healthy individuals. Epigenetics 2013, 8:1188-1197.
81. Maltby V.E., Graves M.C., Lea R.A., Benton M.C., Sanders K.A., Tajouri L., Scott R.J., Lechner-Scott J. Genome-wide DNA methylation profiling of CD8+ T cells shows a distinct epigenetic signature to CD4+ T cells in multiple sclerosis patients. Clinical Epigenetics 2015, 7:118.
82. Carpenter S., Aiello D., Atianand M.K., Ricci E.P., Gandhi P., Hall L.L., Byron M., Monks B., Henry-Bezy M., Lawrence J.B., O'Neill L.A., Moore M.J., Caffrey D.R., Fitzgerald K.A. A long noncoding RNA mediates both activation and repression of immune response genes. Science 2013, 341:789-792.