Epigenetics in human autoimmunity

Autoimmunity

Volumn 41, Issue 4, 2008, Pages 278-286

  Strickland, Faith ^a   Richardson, Bruce ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Atopic dermatitis; DNA methylation; Epigenetics; Lupus; Psoriasis; Vitiligo

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; AZACITIDINE; CONCANAMYCIN A; DNA ANTIBODY; DNA METHYLTRANSFERASE; FILAGGRIN; GAMMA INTERFERON; HYDRALAZINE; INTERLEUKIN 4 ANTIBODY; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; METHOTREXATE; MITOGEN ACTIVATED PROTEIN KINASE; PROCAINAMIDE; PROTEIN TYROSINE PHOSPHATASE SHP 1; STRESS ACTIVATED PROTEIN KINASE;

ANTIBODY PRODUCTION; ATOPIC DERMATITIS; AUTOIMMUNE DISEASE; AUTOIMMUNE SKIN DISEASE; AUTOIMMUNITY; AUTOREGULATION; CD4+ T LYMPHOCYTE; DISEASE PREDISPOSITION; DNA DEMETHYLATION; DNA METHYLATION; DRUG INDUCED DISEASE; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; EPIGENETICS; FRAGILE X SYNDROME; GENE LOCUS; GENE MUTATION; GENETIC REGULATION; GENETIC SUSCEPTIBILITY; GENOME IMPRINTING; HEREDITY; HISTONE MODIFICATION; HUMAN; METHYLATION; NONHUMAN; PATHOGENICITY; PATHOPHYSIOLOGY; PROTEIN MODIFICATION; PSORIASIS; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; T LYMPHOCYTE ACTIVATION; VITILIGO;

ARTHRITIS, RHEUMATOID; DNA METHYLATION; EPIGENESIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; PSORIASIS; SCLERODERMA, DIFFUSE; T-LYMPHOCYTES;

EID: 42649095663     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.1080/08916930802024616     Document Type: Review

References (84)

1. Harley, JB, Kelly, JA and Kaufman, KM (2006) Unraveling the genetics of systemic lupus erythematosus. Springer Semin Immunopathol, 28, pp. 119-130.
2. Cooper, GS, Parks, CG, Treadwell, EL, Clair, EW St., Gilkeson, GS and Dooley, MA (2004) Occupational risk factors for the development of systemic lupus erythematosus. J Rheumatol, 31, pp. 1928-1933.
3. Jarvinen, P. and Aho, K. (1994) Twin studies in rheumatic diseases. Semin Arthritis Rheum, 24, pp. 19-28.
4. Rao, T. and Richardson, B. (1999) Environmentally induced autoimmune diseases: Potential mechanisms. Environ Health Perspect, 107, pp. 737-742.
5. Richardson, B. (1986) Effect of an inhibitor of DNA methylation on T cells. II. 5-Azacytidine induces self-reactivity in antigen-specific T4+ cells. Hum Immunol, 17, pp. 456-470.
6. Richardson, BC, Liebling, MR and Hudson, JL (1990) CD4+ cells treated with DNA methylation inhibitors induce autologous B cell differentiation. Clin Immunol Immunopathol, 55, pp. 368-381.
7. Richardson, BC, Strahler, JR, Pivirotto, TS, Quddus, J., Bayliss, GE, Gross, LA, O'Rourke, KS, Powers, D., Hanash, SM and Johnson, MA (1992) Phenotypic and functional similarities between 5-azacytidine-treated T cells and a T cell subset in patients with active systemic lupus erythematosus. Arthritis Rheum, 35, pp. 647-662.
8. Lu, Q., Ray, D., Gutsch, D. and Richardson, B. (2002) Effect of DNA methylation and chromatin structure on ITGAL expression. Blood, 99, pp. 4503-4508.
9. Richardson, B., Powers, D., Hooper, F., Yung, RL and O'Rourke, K. (1994) Lymphocyte function-associated antigen 1 overexpression and T cell autoreactivity. Arthritis Rheum, 37, pp. 1363-1372.
10. Yung, R., Powers, D., Johnson, K., Amento, E., Carr, D., Laing, T., Yang, J., Chang, S., Hemati, N. and Richardson, B. (1996) Mechanisms of drug-induced lupus. II. T cells overexpressing lymphocyte function-associated antigen 1 become autoreactive and cause a lupuslike disease in syngeneic mice. J Clin Invest, 97, pp. 2866-2871.
11. Wulfing, C., Sumen, C., Sjaastad, MD, Wu, LC, Dustin, ML and Davis, MM (2002) Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat Immunol, 3, pp. 42-47.
12. Rolink, AG, Pals, ST and Gleichmann, E. (1983) Allosuppressor and allohelper T cells in acute and chronic graft-vs.-host disease. II. F1 recipients carrying mutations at H-2K and/or I-A. J Exp Med, 157, pp. 755-771.
13. Quddus, J., Johnson, KJ, Gavalchin, J., Amento, EP, Chrisp, CE, Yung, RL and Richardson, BC (1993) 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, 92, pp. 38-53.
14. Kaplan, MJ, Lewis, EE, Shelden, EA, Somers, E., Pavlic, R., McCune, WJ and Richardson, BC (2002) The apoptotic ligands TRAIL, TWEAK, and Fas ligand mediate monocyte death induced by autologous lupus T cells. J Immunol, 169, pp. 6020-6029.
15. Lu, Q., Wu, A., Ray, D., Deng, C., Attwood, J., Hanash, S., Pipkin, M., Lichtenheld, M. and Richardson, B. (2003) DNA methylation and chromatin structure regulate T cell perforin gene expression. J Immunol, 170, pp. 5124-5132.
16. Kaplan, MJ, Lu, Q., Wu, A., Attwood, J. and Richardson, B. (2004) Demethylation of promoter regulatory elements contributes to perforin overexpression in CD4+ lupus T cells. J Immunol, 172, pp. 3652-3661.
17. Denny, MF, Chandaroy, P., Killen, PD, Caricchio, R., Lewis, EE, Richardson, BC, Lee, KD, Gavalchin, J. and Kaplan, MJ (2006) Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J Immunol, 176, pp. 2095-2104.
18. Oelke, K., Lu, Q., Richardson, D., Wu, A., Deng, C., Hanash, S. and Richardson, B. (2004) Overexpression of CD70 and overstimulation of IgG synthesis by lupus T cells and T cells treated with DNA methylation inhibitors. Arthritis Rheum, 50, pp. 1850-1860.
19. Lu, Q., Wu, A., Tesmer, L., Ray, D., Yousif, N. and Richardson, B. (2007) Demethylation of CD40LG on the inactive X in T cells from women with lupus. J Immunol, 179, pp. 6352-6358.
20. Lu, Q., Wu, A., Tesmer, L., Ray, D., Yousif, N. and Richardson, B. (2007) Demethylation of CD40LG on the inactive X in T cells from women with lupus. J Immunol, 179, pp. 6352-6358.
21. Reiner, SL (2005) Epigenetic control in the immune response. Hum Mol Genet, 14, pp. R41-R46.
22. Lu, Q., Wu, A. and Richardson, BC (2005) Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J Immunol, 174, pp. 6212-6219.
23. Yung, RL and Richardson, BC (1994) Drug-induced lupus. Rheum Dis Clin North Am, 20, pp. 61-86.
24. Batchelor, JR, Welsh, KI, Tinoco, RM, Dollery, CT, Hughes, GR, Bernstein, R., Ryan, P., Naish, PF, Aber, GM, Bing, RF and Russell, GI (1980) Hydralazine-induced systemic lupus erythematosus: Influence of HLA-DR and sex on susceptibility. Lancet, 1, pp. 1107-1109.
25. Lee, BH, Yegnasubramanian, S., Lin, X. and Nelson, WG (2005) Procainamide is a specific inhibitor of DNA methyltransferase 1. J Biol Chem, 280, pp. 40749-40756.
26. Scheinbart, LS, Johnson, MA, Gross, LA, Edelstein, SR and Richardson, BC (1991) Procainamide inhibits DNA methyltransferase in a human T cell line. J Rheumatol, 18, pp. 530-534.
27. Deng, C., Lu, Q., Zhang, Z., Rao, T., Attwood, J., Yung, R. and Richardson, B. (2003) Hydralazine may induce autoimmunity by inhibiting extracellular signal-regulated kinase pathway signaling. Arthritis Rheum, 48, pp. 746-756.
28. Mazari, L., Ouarzane, M. and Zouali, M. (2007) Subversion of B lymphocyte tolerance by hydralazine, a potential mechanism for drug-induced lupus. Proc Natl Acad Sci USA, 104, pp. 6317-6322.
29. Deng, C., Kaplan, MJ, Yang, J., Ray, D., Zhang, Z., McCune, WJ, Hanash, SM and Richardson, BC (2001) Decreased Ras-mitogen-activated protein kinase signaling may cause DNA hypomethylation in T lymphocytes from lupus patients. Arthritis Rheum, 44, pp. 397-407.
30. Gorelik, G., Fang, J-Y, Wu, A., Sawalha, A. and Richardson, B. (2007) Impaired T cell PKC delta activation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. J Immunol, 179, pp. 5553-5563.
31. Gorelik, G., Fang, JY, Wu, A., Sawalha, AH and Richardson, B. (2007) Impaired T cell protein kinase Cdelta activation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. J Immunol, 179, pp. 5553-5563.
32. Miyamoto, A., Nakayama, K., Imaki, H., Hirose, S., Jiang, Y., Abe, M., Tsukiyama, T., Nagahama, H., Ohno, S., Hatakeyama, S. and Nakayama, KI (2002) Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature, 416, pp. 865-869.
33. Richardson, B., Scheinbart, L., Strahler, J., Gross, L., Hanash, S. and Johnson, M. (1990) Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum, 33, pp. 1665-1673.
34. Kammer, GM, Perl, A., Richardson, BC and Tsokos, GC (2002) Abnormal T cell signal transduction in systemic lupus erythematosus. Arthritis Rheum, 46, pp. 1139-1154.
35. Oelke, K. and Richardson, B. (2004) Decreased T cell ERK pathway signaling may contribute to the development of lupus through effects on DNA methylation and gene expression. Int Rev Immunol, 23, pp. 315-331.
36. Crow, MK and Kirou, KA (2001) Regulation of CD40 ligand expression in systemic lupus erythematosus. Curr Opin Rheumatol, 13, pp. 361-369.
37. Richardson, BC, Yung, RL, Johnson, KJ, Rowse, PE and Lalwani, ND (1996) Monocyte apoptosis in patients with active lupus. Arthritis Rheum, 39, pp. 1432-1434.
38. Lu, Q., Kaplan, M., Ray, D., Ray, D., Zacharek, S., Gutsch, D. and Richardson, B. (2002) Demethylation of ITGAL (CD11a) regulatory sequences in systemic lupus erythematosus. Arthritis Rheum, 46, pp. 1282-1291.
39. Mishra, N., Brown, DR, Olorenshaw, IM and Kammer, GM (2001) Trichostatin A reverses skewed expression of CD154, interleukin-10, and interferon-gamma gene and protein expression in lupus T cells. Proc Natl Acad Sci USA, 98, pp. 2628-2633.
40. Marks, PA and Dokmanovic, M. (2005) Histone deacetylase inhibitors: Discovery and development as anticancer agents. Expert Opin Investig Drugs, 14, pp. 1497-1511.
41. Kim, YI, Logan, JW, Mason, JB and Roubenoff, R. (1996) DNA hypomethylation in inflammatory arthritis: Reversal with methotrexate. J Lab Clin Med, 128, pp. 165-172.
42. Wang, Y., Fan, PS and Kahaleh, B. (2006) Association between enhanced type I collagen expression and epigenetic repression of the FLI1 gene in scleroderma fibroblasts. Arthritis Rheum, 54, pp. 2271-2279.
43. Ozbalkan, Z., Bagislar, S., Kiraz, S., Akyerli, CB, Ozer, HT, Yavuz, S., Birlik, AM, Calguneri, M. and Ozcelik, T. (2005) Skewed X chromosome inactivation in blood cells of women with scleroderma. Arthritis Rheum, 52, pp. 1564-1570.
44. Ozcelik, T., Uz, E., Akyerli, CB, Bagislar, S., Mustafa, CA, Gursoy, A., Akarsu, N., Toruner, G., Kamel, N. and Gullu, S. (2006) Evidence from autoimmune thyroiditis of skewed X-chromosome inactivation in female predisposition to autoimmunity. Eur J Hum Genet, 14, pp. 791-797.
45. Millington, GW (2006) Genomic imprinting and dermatological disease. Clin Exp Dermatol, 31, pp. 681-688.
46. Bos, J. (1997) Skin immune system, pp. 3-16. CRC Press, Boca Raton, FL
47. Luger, T. (1997) Skin immune system, pp. 271-310. CRC Press, Boca Raton, FL
48. Kang, K., Poster, A., Nedorost, S., Stevens, S. and Cooper, K. (2003) Dermatology, pp. 199-214. Mosby, New York
49. Yawalkar, N., Hunger, RE, Buri, C., Schmid, S., Egli, F., Brand, CU, Mueller, C., Pichler, WJ and Braathen, LR (2001) A comparative study of the expression of cytotoxic proteins in allergic contact dermatitis and psoriasis: Spongiotic skin lesions in allergic contact dermatitis are highly infiltrated by T cells expressing perforin and granzyme B. Am J Pathol, 158, pp. 803-808.
50. Taylor, RS, Baadsgaard, O., Hammerberg, C. and Cooper, KD (1991) Hyperstimulatory CD1a+CD1b+CD36+ Langerhans cells are responsible for increased autologous T lymphocyte reactivity to lesional epidermal cells of patients with atopic dermatitis. J Immunol, 147, pp. 3794-3802.
51. Kondo, H., Ichikawa, Y. and Imokawa, G. (1998) Percutaneous sensitization with allergens through barrier-disrupted skin elicits a Th2-dominant cytokine response. Eur J Immunol, 28, pp. 769-779.
52. Palmer, CN, Irvine, AD, Terron-Kwiatkowski, A., Zhao, Y., Liao, H., Lee, SP, Goudie, DR, Sandilands, A., Campbell, LE, Smith, FJ, O'Regan, GM, Watson, RM, Cecil, JE, Bale, SJ, Compton, JG, DiGiovanna, JJ, Fleckman, P., Lewis-Jones, S., Arseculeratne, G., Sergeant, A., Munro, CS, Houate, B El, McElreavey, K., Halkjaer, LB, Bisgaard, H., Mukhopadhyay, M. and McLean, WH (2006) Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet, 38, pp. 441-446.
53. Larsen, FS, Holm, NV and Henningsen, K. (1986) Atopic dermatitis. A genetic-epidemiologic study in a population-based twin sample. J Am Acad Dermatol, 15, pp. 487-494.
54. Nakamura, T., Sekigawa, I., Ogasawara, H., Mitsuishi, K., Hira, K., Ikeda, S. and Ogawa, H. (2006) Expression of DNMT-1 in patients with atopic dermatitis. Arch Dermatol Res, 298, pp. 253-256.
55. Kuwabara, N., Kondo, N., Fukutomi, O., Fujii, H. and Orii, T. (1995) Methylation patterns of I epsilon region in B cells stimulated with interleukin 4 and Epstein-Barr virus in patients with a high level of serum IgE. Eur J Immunogenet, 22, pp. 265-275.
56. Lorenzo, PRs, Kuwabara, N., Kondo, N. and Orii, T. (1995) IgE production by B-cells stimulated with interleukin-4 and Epstein-Barr virus in patients with elevated serum IgE levels. J Investig Allergol Clin Immunol, 5, pp. 78-81.
57. Wrone-Smith, T. and Nickoloff, BJ (1996) Dermal injection of immunocytes induces psoriasis. J Clin Invest, 98, pp. 1878-1887.
58. Nickoloff, BJ and Nestle, FO (2004) Recent insights into the immunopathogenesis of psoriasis provide new therapeutic opportunities. J Clin Invest, 113, pp. 1664-1675.
59. Brandrup, F., Holm, N., Grunnet, N., Henningsen, K. and Hansen, HE (1982) Psoriasis in monozygotic twins: Variations in expression in individuals with identical genetic constitution. Acta Derm Venereol, 62, pp. 229-236.
60. Duffy, DL, Spelman, LS and Martin, NG (1993) Psoriasis in Australian twins. J Am Acad Dermatol, 29, pp. 428-434.
61. Zhang, Q., Wang, HY, Marzec, M., Raghunath, PN, Nagasawa, T. and Wasik, MA (2005) STAT3- and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc Natl Acad Sci USA, 102, pp. 6948-6953.
62. Bruecher-Encke, B., Griffin, JD, Neel, BG and Lorenz, U. (2001) Role of the tyrosine phosphatase SHP-1 in K562 cell differentiation. Leukemia, 15, pp. 1424-1432.
63. Ruchusatsawat, K., Wongpiyabovorn, J., Shuangshoti, S., Hirankarn, N. and Mutirangura, A. (2006) SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. J Mol Med, 84, pp. 175-182.
64. Sano, S., Chan, KS, Carbajal, S., Clifford, J., Peavey, M., Kiguchi, K., Itami, S., Nickoloff, BJ and DiGiovanni, J. (2005) Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat Med, 11, pp. 43-49.
65. Zhang, K., Zhang, R., Li, X., Yin, G., Niu, X. and Hou, R. (2007) The mRNA expression and promoter methylation status of the p16 gene in colony-forming cells with high proliferative potential in patients with psoriasis. Clin Exp Dermatol, 32, pp. 702-708.
66. Snowden, JA and Heaton, DC (1997) Development of psoriasis after syngeneic bone marrow transplant from psoriatic donor: Further evidence for adoptive autoimmunity. Br J Dermatol, 137, pp. 130-132.
67. Woods, AC and Mant, MJ (2006) Amelioration of severe psoriasis with psoriatic arthritis for 20 years after allogeneic haematopoietic stem cell transplantation. Ann Rheum Dis, 65, p. 697.
68. Kastelan, M., Massari, L Prpic, Gruber, F., Zamolo, G., Zauhar, G., Coklo, M. and Rukavina, D. (2004) Perforin expression is upregulated in the epidermis of psoriatic lesions. Br J Dermatol, 151, pp. 831-836.
69. Giblin, PA and Lemieux, RM (2006) LFA-1 as a key regulator of immune function: Approaches toward the development of LFA-1-based therapeutics. Curr Pharm Des, 12, pp. 2771-2795.
70. Gladman, DD (1994) Natural history of psoriatic arthritis. Baillieres Clin Rheumatol, 8, pp. 379-394.
71. Rahman, P., Gladman, DD, Schentag, CT and Petronis, A. (1999) Excessive paternal transmission in psoriatic arthritis. Arthritis Rheum, 42, pp. 1228-1231.
72. Karason, A., Gudjonsson, JE, Upmanyu, R., Antonsdottir, AA, Hauksson, VB, Runasdottir, EH, Jonsson, HH, Gudbjartsson, DF, Frigge, ML, Kong, A., Stefansson, K., Valdimarsson, H. and Gulcher, JR (2003) A susceptibility gene for psoriatic arthritis maps to chromosome 16q: Evidence for imprinting. Am J Hum Genet, 72, pp. 125-131.
73. Howitz, J., Brodthagen, H., Schwartz, M. and Thomsen, K. (1977) Prevalence of vitiligo. Arch Dermatol, 113, pp. 47-52.
74. Das, SK, Majumder, PP, Chakraborty, R., Majumdar, TK and Haldar, B. (1985) Studies on vitiligo. Genet Epidemiol, 2, pp. 71-78.
75. Nordlund, J., Ortonne, J. and LePoole, I. (2006) The pigmentary system: Physiology and pathophysiology, pp. 551-598. Blackwell, Oxford
76. Alkhateeb, A., Fain, PR, Thody, A., Bennett, DC and Spritz, RA (2003) Epidemiology of vitiligo and associated autoimmune diseases in Caucasian probands and their families. Pigment Cell Res, 16, pp. 208-214.
77. Laberge, G., Mailloux, CM, Gowan, K., Holland, P., Bennett, DC, Fain, PR and Spritz, RA (2005) Early disease onset and increased risk of other autoimmune diseases in familial generalized vitiligo. Pigment Cell Res, 18, pp. 300-305.
78. Spritz, RA (2007) The genetics of generalized vitiligo and associated autoimmune diseases. Pigment Cell Res, 20, pp. 271-278.
79. Jin, Y., Mailloux, CM, Gowan, K., Riccardi, SL, LaBerge, G., Bennett, DC, Fain, PR and Spritz, RA (2007) NALP1 in vitiligo-associated multiple autoimmune disease. N Engl J Med, 356, pp. 1216-1225.
80. Spritz, RA, Gowan, K., Bennett, DC and Fain, PR (2004) Novel vitiligo susceptibility loci on chromosomes 7 (AIS2) and 8 (AIS3), confirmation of SLEV1 on chromosome 17, and their roles in an autoimmune diathesis. Am J Hum Genet, 74, pp. 188-191.
81. Taieb, A. (2007) NALP1 and the inflammasomes: Challenging our perception of vitiligo and vitiligo-related autoimmune disorders. Pigment Cell Res, 20, pp. 260-262.
82. Antony, PA, Piccirillo, CA, Akpinarli, A., Finkelstein, SE, Speiss, PJ, Surman, DR, Palmer, DC, Chan, CC, Klebanoff, CA, Overwijk, WW, Rosenberg, SA and Restifo, NP (2005) CD8+T cell immunity against a tumor/ self-antigen is augmented by CD4+T helper cells and hindered by naturally occurring T regulatory cells. J Immunol, 174, pp. 2591-2601.
83. Sreekumar, GP, Erf, GF and Smyth Jr, JR (1996) 5-azacytidine treatment induces autoimmune vitiligo in parental control strains of the Smyth line chicken model for autoimmune vitiligo. Clin Immunol Immunopathol, 81, pp. 136-144.
84. Schauenstein, K., Csordas, A., Kromer, G., Dietrich, H. and Wick, G. (1991) In vivo treatment with 5-azacytidine causes degeneration of central lymphatic organs and induces autoimmune disease in the chicken. Int J Exp Pathol, 72, pp. 311-318.