Dissecting complex epigenetic alterations in human lupus

Arthritis Research and Therapy

Volumn 15, Issue 1, 2012, Pages

  Patel, Dipak R ^a   Richardson, Bruce C ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HYDRALAZINE; MICRORNA; PROCAINAMIDE;

AGE DISTRIBUTION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CHROMATIN STRUCTURE; DISEASE SEVERITY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC PREDISPOSITION; HISTONE MODIFICATION; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; NONHUMAN; OXIDATIVE STRESS; RECURRENT DISEASE; REVIEW; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; TWINS; VALIDATION PROCESS; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; T LYMPHOCYTE;

AUTOIMMUNITY; EPIGENESIS, GENETIC; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; T-LYMPHOCYTES;

EID: 84873316594     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4125     Document Type: Review

References (55)

1. Richardson B. Primer: epigenetics of autoimmunity. Nat Clin Pract Rheumatol 2007, 3:521-527.
2. Li Y, Liu Y, Strickland FM, Richardson B. Age-dependent decreases in DNA methyltransferase levels and low transmethylation micronutrient levels synergize to promote overexpression of genes implicated in autoimmunity and acute coronary syndromes. Exp Gerontol 2010, 45:312-322. 10.1016/j.exger.2009.12.008, 2838973, 20035856.
3. Gorelik GJ, Yarlagadda S, Richardson BC. Protein kinase Cdelta oxidation contributes to ERK inactivation in lupus T cells. Arthritis Rheum 2012, 64:2964-2974. 10.1002/art.34503, 22549474.
4. Richardson B. Impact of aging on DNA methylation. Ageing Res Rev 2003, 2:245-261. 10.1016/S1568-1637(03)00010-2, 12726774.
5. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005, 102:10604-10609. 10.1073/pnas.0500398102, 1174919, 16009939.
6. Kim HP, Leonard WJ. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J Exp Med 2007, 204:1543-1551. 2118651, 17591856.
7. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol 2009, 9:91-105. 10.1038/nri2487, 19151746.
8. Rozendaal L, Pals ST, Gleichmann E, Melief CJ. Persistence of allospecific helper T cells is required for maintaining autoantibody formation in lupuslike graft-versus-host disease. Clin Exp Immunol 1990, 82:527-532. 1535512, 2148286.
9. Quddus J, Johnson KJ, Gavalchin J, Amento EP, Chrisp CE, Yung RL, Richardson BC. 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. 10.1172/JCI116576, 293525, 7686923.
10. Cornacchia E, Golbus J, Maybaum J, Strahler J, Hanash S, Richardson B. Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity. J Immunol 1988, 140:2197-2200.
11. Walport MJ. Lupus, DNase and defective disposal of cellular debris. Nat Genet 2000, 25:135-136. 10.1038/75963, 10835621.
12. Lu Q, Wu A, Tesmer L, Ray D, Yousif N, Richardson B. Demethylation of CD40LG on the inactive × in T cells from women with lupus. J Immunol 2007, 179:6352-6358.
13. Young HA. Regulation of interferon-gamma gene expression. J Interferon Cytokine Res 1996, 16:563-568. 10.1089/jir.1996.16.563, 8877725.
14. Yung R, Williams R, Johnson K, Phillips C, Stoolman L, Chang S, Richardson B. Mechanisms of drug-induced lupus. III. Sex-specific differences in T cell homing may explain increased disease severity in female mice. Arthritis Rheum 1997, 40:1334-1343.
15. 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. 10.1002/art.1780331109, 2242063.
16. Golbus J, Palella TD, Richardson BC. Quantitative changes in T cell DNA methylation occur during differentiation and ageing. Eur J Immunol 1990, 20:1869-1872. 10.1002/eji.1830200836, 2209694.
17. Tan EM, Smolen JS, McDougal JS, Butcher BT, Conn D, Dawkins R, Fritzler MJ, Gordon T, Hardin JA, Kalden JR, Lahita RG, Maini RN, Rothfield NF, Smeenk R, Takasaki Y, van Venrooij WJ, Wiik A, Wilson M, Koziol JA. A critical evaluation of enzyme immunoassays for detection of antinuclear autoantibodies of defined specificities. I. Precision, sensitivity, and specificity. Arthritis Rheum 1999, 42:455-464. 10.1002/1529-0131(199904)42:3<455::AID-ANR10>3.0.CO;2-3, 10088768.
18. Sawalha AH, Jeffries M, Webb R, Lu Q, Gorelik G, Ray D, Osban J, Knowlton N, Johnson K, Richardson B. Defective T-cell ERK signaling induces interferonregulated gene expression and overexpression of methylation-sensitive genes similar to lupus patients. Genes Immun 2008, 9:368-378. 10.1038/gene.2008.29, 2825163, 18523434.
19. Strickland FM, Hewagama A, Lu Q, Wu A, Hinderer R, Webb R, Johnson K, Sawalha AH, Delaney C, Yung R, Richardson BC. Environmental exposure, estrogen and two × chromosomes are required for disease development in an epigenetic model of lupus. J Autoimmun 2012, 38:J135-143. 10.1016/j.jaut.2011.11.001, 22142890.
20. Gorelik G, Richardson B. Key role of ERK pathway signaling in lupus. Autoimmunity 2010, 43:17-22. 10.3109/08916930903374832, 2819407, 19961364.
21. Zandman-Goddard G, Solomon M, Rosman Z, Peeva E, Shoenfeld Y. Environment and lupus-related diseases. Lupus 2012, 21:241-250. 10.1177/0961203311426568, 22065092.
22. Chiurchiu V, Maccarrone M. Chronic inflammatory disorders and their redox control: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2011, 15:2605-2641. 10.1089/ars.2010.3547, 21391902.
23. Oates JC, Gilkeson GS. The biology of nitric oxide and other reactive intermediates in systemic lupus erythematosus. Clin Immunol 2006, 121:243-250. 10.1016/j.clim.2006.06.001, 2765327, 16861040.
24. Basu D, Liu Y, Wu A, Yarlagadda S, Gorelik GJ, Kaplan MJ, Hewagama A, Hinderer RC, Strickland FM, Richardson BC. Stimulatory and inhibitory killer Ig-like receptor molecules are expressed and functional on lupus T cells. J Immunol 2009, 183:3481-3487. 10.4049/jimmunol.0900034, 2730421, 19675166.
25. Liu Y, Kuick R, Hanash S, Richardson B. DNA methylation inhibition increases T cell KIR expression through effects on both promoter methylation and transcription factors. Clin Immunol 2009, 130:213-224. 10.1016/j.clim.2008.08.009, 2655730, 18945643.
26. Sunahori K, Juang YT, Kyttaris VC, Tsokos GC. 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. 10.4049/jimmunol.1000340, 3148941, 21346232.
27. Jeffries MA, Dozmorov M, Tang Y, Merrill JT, Wren JD, Sawalha AH. Genomewide DNA methylation patterns in CD4+ T cells from patients with systemic lupus erythematosus. Epigenetics 2011, 6:593-601. 10.4161/epi.6.5.15374, 3121972, 21436623.
28. Kornberg RD, Lorch Y. Chromatin-modifying and -remodeling complexes. Curr Opin Genet Dev 1999, 9:148-151. 10.1016/S0959-437X(99)80022-7, 10322131.
29. Lee DY, Hayes JJ, Pruss D, Wolffe AP. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 1993, 72:73-84. 10.1016/0092-8674(93)90051-Q, 8422685.
30. Ura K, Kurumizaka H, Dimitrov S, Almouzni G, Wolffe AP. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression. EMBO J 1997, 16:2096-2107. 10.1093/emboj/16.8.2096, 1169812, 9155035.
31. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837. 10.1016/j.cell.2007.05.009, 17512414.
32. Lachner M, O'Sullivan RJ, Jenuwein T. An epigenetic road map for histone lysine methylation. J Cell Sci 2003, 116(Pt 11):2117-2124.
33. Murr R. Interplay between different epigenetic modifications and mechanisms. Adv Genet 2010, 70:101-141.
34. Hu N, Qiu X, Luo Y, Yuan J, Zhang G, Zhou Y, Su Y, Lu Q. Abnormal histone modification patterns in lupus CD4+ T cells. J Rheumatol 2008, 35:804-810.
35. Zhao M, Wu X, Zhang Q, Luo S, Liang G, Su Y, Tan Y, Lu Q. RFX1 regulates CD70 and CD11a expression in lupus T cells by recruiting the histone methyltransferase SUV39H1. Arthritis Res Ther 2010, 12:R227. 10.1186/ar3214, 3046540, 21192791.
36. 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. 10.1016/j.jaut.2010.02.002, 20223637.
37. Zhou Y, Qiu X, Luo Y, Yuan J, Zhong Q, Zhao M, Lu Q. Histone modifications and methyl-CpG-binding domain protein levels at the TNFSF7 (CD70) promoter in SLE CD4+ T cells. Lupus 2011, 20:1365-1371. 10.1177/0961203311413412, 21865261.
38. Zhang Q, Long H, Liao J, Zhao M, Liang G, Wu X, Zhang P, Ding S, Luo S, Lu Q. Inhibited expression of hematopoietic progenitor kinase 1 associated with loss of jumonji domain containing 3 promoter binding contributes to autoimmunity in systemic lupus erythematosus. J Autoimmun 2011, 37:180-189. 10.1016/j.jaut.2011.09.006, 22014533.
39. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002, 19167326.
40. 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. 10.1002/art.34505, 22549634.
41. Yu D, Tan AH, Hu X, Athanasopoulos V, Simpson N, Silva DG, Hutloff A, Giles KM, Leedman PJ, Lam KP, Goodnow CC, Vinuesa CG. Roquin represses autoimmunity by limiting inducible T-cell co-stimulator messenger RNA. Nature 2007, 450:299-303. 10.1038/nature06253, 18172933.
42. 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. 10.4049/jimmunol.0904060, 20483747.
43. 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. 10.1002/art.30196, 21538319.
44. Stagakis E, Bertsias G, Verginis P, Nakou M, Hatziapostolou M, Kritikos H, Iliopoulos D, Boumpas DT. Identification of novel microRNA signatures linked to human lupus disease activity and pathogenesis: miR-21 regulates aberrant T cell responses through regulation of PDCD4 expression. Ann Rheum Dis 2011, 70:1496-1506. 10.1136/ard.2010.139857, 21602271.
45. Fan W, Liang D, Tang Y, Qu B, Cui H, Luo X, Huang X, Chen S, Higgs BW, Jallal B, Yao Y, Harley JB, Shen N. Identification of microRNA-31 as a novel regulator contributing to impaired IL-2 production in T cells from patients with systemic lupus erythematosus. Arthritis Rheum 2012, 64:3715-3725. 10.1002/art.34596, 22736314.
46. Zhao X, Tang Y, Qu B, Cui H, Wang S, Wang L, Luo X, Huang X, Li J, Chen S, Shen N. MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthritis Rheum 2010, 62:3425-3435. 10.1002/art.27632, 20589685.
47. Tang Y, Luo X, Cui H, Ni X, Yuan M, Guo Y, Huang X, Zhou H, de Vries N, Tak PP, Chen S, Shen N. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signalling proteins. Arthritis Rheum 2009, 60:1065-1075. 10.1002/art.24436, 19333922.
48. Garchow BG, Bartulos Encinas O, Leung YT, Tsao PY, Eisenberg RA, 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. 10.1002/emmm.201100171, 3258486,3258486, 21882343.
49. Lessard CJ, Adrianto I, Ice JA, Wiley GB, Kelly JA, Glenn SB, Adler AJ, Li H, Rasmussen A, Williams AH, Ziegler J, Comeau ME, Marion M, Wakeland BE, Liang C, Ramos PS, Grundahl KM, Gallant CJ, Alarcon-Riquelme ME, Alarcon GS, Anaya JM, Bae SC, Boackle SA, Brown EE, Chang DM, Cho SK, Criswell LA, Edberg JC, Freedman BI, Gilkeson GS, et al. Identification of IRF8, TMEM39A, and IKZF3-ZPBP2 as susceptibility loci for systemic lupus erythematosus in a large-scale multiracial replication study. Am J Hum Genet 2012, 90:648-660. 10.1016/j.ajhg.2012.02.023, 3322228, 22464253.
50. Webb R, Kelly JA, Somers EC, Hughes T, Kaufman KM, Sanchez E, Nath SK, Bruner G, Alarcon-Riquelme ME, Gilkeson GS, Kamen DL, Richardson BC, Harley JB, Sawalha AH. Early disease onset is predicted by a higher genetic risk for lupus and is associated with a more severe phenotype in lupus patients. Ann Rheum Dis 2011, 70:151-156. 10.1136/ard.2010.141697, 3034281, 20881011.
51. Taylor KE, Chung SA, Graham RR, Ortmann WA, Lee AT, Langefeld CD, Jacob CO, Kamboh MI, Alarcon-Riquelme ME, Tsao BP, Moser KL, Gaffney PM, Harley JB, Petri M, Manzi S, Gregersen PK, Behrens TW, Criswell LA. Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet 2011, 7:e1001311. 10.1371/journal.pgen.1001311, 3040652, 21379322.
52. Crow MK, Kirou KA. Regulation of CD40 ligand expression in systemic lupus erythematosus. Curr Opin Rheumatol 2001, 13:361-369. 10.1097/00002281-200109000-00004, 11604589.
53. Higuchi T, Aiba Y, Nomura T, Matsuda J, Mochida K, Suzuki M, Kikutani H, Honjo T, Nishioka K, Tsubata T. Cutting edge: ectopic expression of CD40 ligand on B cells induces lupus-like autoimmune disease. J Immunol 2002, 168:9-12.
54. Scofield RH, Bruner GR, Namjou B, Kimberly RP, Ramsey-Goldman R, Petri M, Reveille JD, Alarcon GS, Vila LM, Reid J, Harris B, Li S, Kelly JA, Harley JB. Klinefelter's syndrome (47,XXY) in male systemic lupus erythematosus patients: support for the notion of a gene-dose effect from the × chromosome. Arthritis Rheum 2008, 58:2511-2517. 10.1002/art.23701, 2824898, 18668569.
55. Sawalha AH, Wang L, Nadig A, Somers EC, McCune WJ, Hughes T, Merrill JT, Scofield RH, Strickland FM, Richardson B. Sex-specific differences in the relationship between genetic susceptibility, T cell DNA demethylation and lupus flare severity. J Autoimmun 2012, 38:J216-222. 10.1016/j.jaut.2011.11.008, 22305513.