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Review Article

Epigenetic regulation of cytokine expression in systemic lupus erythematosus with special focus on T cells

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Pages 234-241 | Received 25 Jan 2013, Accepted 28 Apr 2013, Published online: 24 Apr 2014

References

  • Tsokos, G. C. 2011. Systemic lupus erythematosus. N Engl J Med. 365: 2110–2121
  • Truedsson, L., A. A. Bengtsson, and G. Sturfelt. 2007. Complement deficiencies and systemic lupus erythematosus. Autoimmunity. 40: 560–566
  • Hedrich, C. M., and G. C. Tsokos. 2011. Epigenetic mechanisms in systemic lupus erythematosus and other autoimmune diseases. Trends Mol Med. 17: 714–724
  • Hedrich, C. M., and J. H. Bream. 2010. Cell type-specific regulation of IL-10 expression in inflammation and disease. Immunol Res. 47: 185–206
  • Brenner, C., and F. Fuks. 2006. DNA methyltransferases: facts, clues, mysteries. Curr Top Microbiol Immunol. 301: 45–66
  • Brenner, C., and F. Fuks. 2007. A methylation rendezvous: reader meets writers. Dev Cell. 12: 843–844
  • Deplus, R., C. Brenner, W. A. Burgers, P. Putmans, T. Kouzarides, de, L. Y., and Fuks, F. 2002. Dnmt3L is a transcriptional repressor that recruits histone deacetylase. Nucl Acids Res. 30: 3831–3838
  • Esteve, P. O., H. G. Chin, A. Smallwood, G. R. Feehery, O. Gangisetty, A. R. Karpf, M. F. Carey, and S. Pradhan. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 20: 3089–3103
  • Smallwood, A., P. O. Esteve, S. Pradhan, and M. Carey. 2007. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21: 1169–1178
  • Brooks, W. H., D. C. Le, J. O. Pers, P. Youinou, and Y. Renaudineau. 2010. Epigenetics and autoimmunity. J Autoimmun. 34: J207–J219
  • Grolleau-Julius, A., D. Ray, and R. L. Yung. 2010. The role of epigenetics in aging and autoimmunity. Clin Rev Allergy Immunol. 39: 42–50
  • Renaudineau, Y. 2010. The revolution of epigenetics in the field of autoimmunity. Clin Rev Allergy Immunol. 39: 1–2
  • Renaudineau, Y., and P. Youinou. 2011. Epigenetics and autoimmunity, with special emphasis on methylation. Keio J Med. 60: 10–16
  • Wilson, C. B., K. W. Makar, M. Shnyreva, and D. R. Fitzpatrick. 2005. DNA methylation and the expanding epigenetics of T cell lineage commitment. Semin Immunol. 17: 105–119
  • Richardson, B. C. 2008. Epigenetics and autoimmunity. Overview Autoimmunity. 41: 243–244
  • Strickland, F. M., and B. C. Richardson. 2008. Epigenetics in human autoimmunity. Epigenetics in autoimmunity – DNA methylation in systemic lupus erythematosus and beyond. Autoimmunity. 41: 278–286
  • Schoenborn, J. R., and C. B. Wilson. 2007. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol. 96: 41–101
  • Hofmann, S. R., A. Rosen-Wolff, G. C. Tsokos, and C. M. Hedrich. 2012. Biological properties and regulation of IL-10 related cytokines and their contribution to autoimmune disease and tissue injury. Clin Immunol. 143: 116–127
  • Hedrich, C. M., A. Ramakrishnan, D. Dabitao, F. Wang, D. Ranatunga, and J. H. Bream. 2010. Dynamic DNA methylation patterns across the mouse and human IL10 genes during CD4+ T cell activation; influence of IL-27. Mol Immunol. 48: 73–81
  • Hofmann, S. R., J. Moller, T. Rauen, D. Paul, M. Gahr, Z. Rosen-Wolff, S. Brenner, and C. M. Hedrich. 2012. Dynamic CpG–DNA methylation of Il10 and Il19 in CD4+ T lymphocytes and macrophages: effects on tissue-specific gene expression. Klin Padiatr. 224: 53–60
  • Liu, Y., Y. Chen, and B. Richardson. 2009. Decreased DNA methyltransferase levels contribute to abnormal gene expression in “senescent” CD4+CD28−. T cells Clin Immunol. 132: 257–265
  • Lal, G., N. Zhang, T. W. van der, Y. Ding, W. Ju, E. P. Bottinger, S. P. Reid, et al. 2009. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol. 182: 259–273
  • Zhao, M., J. Tang, F. Gao, X. Wu, Y. Liang, H. Yin, and Q. Lu. 2010. Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus. J Biomed Biotechnol. 2010: 931018
  • Rauen, T., C. M. Hedrich, Y. T. Juang, K. Tenbrock, and G. C. Tsokos. 2011. cAMP-responsive element modulator CREM.alpha protein induces interleukin 17A expression and mediates epigenetic alterations at the interleukin-17A gene locus in patients with systemic lupus erythematosus. J Biol Chem. 286: 43437–43446
  • Ohl, K., and K. Tenbrock. 2011. Inflammatory cytokines in systemic lupus erythematosus. J Biomed Biotechnol. 2011: 432595
  • Apostolidis, S. A., L. A. Lieberman, K. Kis-Toth, J. C. Crispin, and G. C. Tsokos. 2011. The dysregulation of cytokine networks in systemic lupus erythematosus. J Interferon Cytokine Res. 31: 769–779
  • Apostolidis, S. A., J. C. Crispin, and G. C. Tsokos. 2011. IL-17-producing T cells in lupus nephritis. Lupus. 20: 120–124
  • Iwakura, Y., H. Ishigame, S. Saijo, and S. Nakae. 2011. Functional specialization of interleukin-17 family members. Immunity. 34: 149–162
  • Hedrich, C. M., T. Rauen, K. Kis-Toth, V. C. Kyttaris, and G. C. Tsokos. 2012. cAMP-responsive element modulator alpha CREMalpha. suppresses IL-17F protein expression in T lymphocytes from patients with systemic lupus erythematosus SLE J Biol Chem. 287: 4715–4725
  • Hedrich, C. M., T. Rauen, and G. C. Tsokos. 2011. cAMP-responsive element modulator CREM.alpha protein signaling mediates epigenetic remodeling of the human interleukin-2 gene: implications in systemic lupus erythematosus. J Biol Chem. 286: 43429–43436
  • Crispin, J. C., and G. C. Tsokos. 2009. Transcriptional regulation of IL-2 in health and autoimmunity. Autoimmun Rev. 8: 190–195
  • Hedrich, C. M., J. C. Crispin, T. Rauen, C. Ioannidis, S. A. Apostolidis, M. S. Lo, V. C. Kyttaris, and G. C. Tsokos. 2012 cAMP response element modulator? controls IL2 and IL17A expression during CD4 lineage commitment and subset distribution in lupus. Proc Natl Acad Sci U S A. 109: 16606--16611
  • Lu, Q., A. Wu, and B. C. Richardson. 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: 6212–6219
  • Zhou, Y., X. Qiu, Y. Luo, J. Yuan, Y. Li, Q. Zhong, M. Zhao, and Q. Lu. 2011. Histone modifications and methyl-CpG-binding domain protein levels at the TNFSF7 CD70 promoter in SLE CD4+ T cells. Lupus. 20: 1365–1371
  • Singer, N. G., B. C. Richardson, D. Powers, F. Hooper, F. Lialios, J. Endres, C. M. Bott, and D. A. Fox. 1996. Role of the CD6 glycoprotein in antigen-specific and autoreactive responses of cloned human T lymphocytes. Immunology. 88: 537–543
  • Lu, Q., M. Kaplan, D. Ray, D. Ray, S. Zacharek, D. Gutsch, and B. Richardson. 2002. Demethylation of ITGAL CD11a. regulatory sequences in systemic lupus erythematosus Arthritis Rheum. 46: 1282–1291
  • Zhao, M., Y. Sun, F. Gao, X. Wu, J. Tang, H. Yin, H. Y. Luo, et al. 2010. Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4+ T cells. J Autoimmun. 35: 58–69
  • Lu, Q., A. Wu, L. Tesmer, D. Ray, N. Yousif, and B. Richardson. 2007. Demethylation of CD40LG on the inactive X in T cells from women with lupus. J Immunol. 179: 6352–6358
  • Garaud, S., D. C. Le, S. Jousse-Joulin, C. Hanrotel-Saliou, A. Saraux, R. A. Mageed, P. Youinou, and Y. Renaudineau. 2009. IL-6 modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation. J Immunol. 182: 5623–5632
  • Garaud, S., P. Youinou, and Y. Renaudineau. 2011. DNA methylation and B-cell autoreactivity. Adv Exp Med Biol. 711: 50–60
  • Nile, C. J., R. C. Read, M. Akil, G. W. Duff, and A. G. Wilson. 2008. Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum. 58: 2686–2693
  • Neidhart, M., J. Rethage, S. Kuchen, P. Kunzler, R. M. Crowl, M. E. Billingham, R. E. Gay, and S. Gay. 2000. Retrotransposable L1 elements expressed in rheumatoid arthritis synovial tissue: association with genomic DNA hypomethylation and influence on gene expression. Arthritis Rheum. 43: 2634–2647
  • Sullivan, K. E., A. Suriano, K. Dietzmann, J. Lin, D. Goldman, and M. A. Petri. 2007. The TNFalpha locus is altered in monocytes from patients with systemic lupus erythematosus. Clin Immunol. 123: 74–81
  • Hofmann, S. R., T. Schwarz, J. C. Moller, H. Morbach, A. Schnabel, A. Rosen-Wolff, H. J. Girschick, and C. M. Hedrich. 2011. Chronic non-bacterial osteomyelitis is associated with impaired Sp1 signaling, reduced IL10 promoter phosphorylation, and reduced myeloid IL-10 expression. Clin Immunol. 141: 317–327
  • Hofmann, S. R., H. Morbach, T. Schwarz, A. Rosen-Wolff, H. J. Girschick, and C. M. Hedrich. 2012. Attenuated TLR4/MAPK signaling in monocytes from patients with CRMO results in impaired IL-10 expression. Clin Immunol. 145: 69–76
  • Bollati, V., J. Schwartz, R. Wright, A. Litonjua, L. Tarantini, H. Suh, D. Sparrow, P. Vokonas, and A. Baccarelli. 2009. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 130: 234–239
  • Liu, Y., R. Kuick, S. Hanash, and B. Richardson. 2009. DNA methylation inhibition increases T cell KIR expression through effects on both promoter methylation and transcription factors. Clin Immunol. 130: 213–224
  • Invernizzi, P., S. Pasini, C. Selmi, M. Miozzo, and M. Podda. 2008. Skewing of X chromosome inactivation in autoimmunity. Autoimmunity. 41: 272–277
  • Pennell, L. M., C. L. Galligan, and E. N. Fish. 2012. Sex affects immunity. J Autoimmun. 38: J282–J291
  • Tiniakou, E., K. H. Costenbader, and M. A. Kriegel. 2013. Sex-specific environmental influences on the development of autoimmune diseases. Clin Immunol. [Epub ahead of print]. doi: 10.1016/j.clim.2013.02.011
  • Pernis, A. B. 2007. Estrogen and CD4+ T cells. Curr Opin Rheumatol. 19: 414–420
  • Karpuzoglu, E., and M. Zouali. 2011. The multi-faceted influences of estrogen on lymphocytes: toward novel immuno-interventions strategies for autoimmunity management. Clin Rev Allergy Immunol. 40: 16–26
  • Kawana, K., Y. Kawana, and D. J. Schust. 2005. Female steroid hormones use signal transducers and activators of transcription protein-mediated pathways to modulate the expression of T-bet in epithelial cells: a mechanism for local immune regulation in the human reproductive tract. Mol Endocrinol. 19: 2047–2059
  • Kanno, Y., G. Vahedi, K. Hirahara, K. Singleton, and J. J. O'Shea. 2012. Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Annu Rev Immunol. 30: 707–731
  • Moulton, V. R., D. R. Holcomb, M. C. Zajdel, and G. C. Tsokos. 2012. Estrogen upregulates cyclic AMP response element modulator alpha expression and downregulates interleukin-2 production by human T lymphocytes. Mol Med. 18: 370–378
  • England, J. M., and B. J. Bain. 1976. Total and differential leucocyte count. Br J Haematol. 33: 1–7
  • Molloy, E. J., A. J. O'Neill, J. J. Grantham, M. Sheridan-Pereira, J. M. Fitzpatrick, D. W. Webb, and R. W. Watson. 2003. Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood. 102: 2653–2659
  • Hedrich, C. M., and G. C. Tsokos. 2013. Bridging the gap between autoinflammation and autoimmunity. Clin Immunol. [Epub ahead of print]. doi:10.1016/j.clim.2013.03.006
  • Liao, J., G. Liang, S. Xie, H. Zhao, X. Zuo, F. Li, J. Chen, et al. 2012. CD40L demethylation in CD4+ T cells from women with rheumatoid arthritis. Clin Immunol. 145: 13–18
  • Tenbrock, K., Y. T. Juang, V. C. Kyttaris, and G. C. Tsokos. 2007. Altered signal transduction in SLE T cells Rheumatology Oxford. 46: 1525–1530
  • Cooper, G. S., M. A. Dooley, E. L. Treadwell, E. W. St Clair, and G. S. Gilkeson. 2001. Smoking and use of hair treatments in relation to risk of developing systemic lupus erythematosus. J Rheumatol. 28: 2653–2656
  • Cooper, G. S., J. Wither, S. Bernatsky, J. O. Claudio, A. Clarke, J. D. Rioux, and P. R. Fortin. 2010. Occupational and environmental exposures and risk of systemic lupus erythematosus: silica, sunlight, solvents Rheumatology Oxford. 49: 2172–2180
  • Freni-Titulaer, L. W., D. B. Kelley, A. G. Grow, T. W. McKinley, F. C. Arnett, and M. C. Hochberg. 1989. Connective tissue disease in southeastern Georgia: a case-control study of etiologic factors. Am J Epidemiol. 130: 404–409
  • Hardy, C. J., B. P. Palmer, K. R. Muir, and R. J. Powell. 1999. Systemic lupus erythematosus SLE. and hair treatment: a large community based case-control study. Lupus. 8: 541–544
  • Petri, M., and J. Allbritton. 1992. Hair product use in systemic lupus erythematosus. A case-control study. Arthritis Rheum. 35: 625–629
  • Reidenberg, M. M., D. E. Drayer, B. Lorenzo, B. L. Strom, S. L. West, E. S. Snyder, B. Freundlich, and P. D. Stolley. 1993. Acetylation phenotypes and environmental chemical exposure of people with idiopathic systemic lupus erythematosus. Arthritis Rheum. 36: 971–973
  • Sanchez-Guerrero, J., Karlson, E. W., Colditz, G. A., Hunter, D. J., Speizer, F. E., and Liang, M. H. 1996. Hair dye use and the risk of developing systemic lupus erythematosus. Arthritis Rheum. 39: 657–662
  • Wang, J., A. B. Kay, J. Fletcher, M. K. Formica, and T. E. McAlindon. 2008. Is lipstick associated with the development of systemic lupus erythematosus SLE? Clin Rheumatol. 27: 1183–1187
  • Olsson, A. R., T. Skogh, and G. Wingren. 2000. Occupational determinants for rheumatoid arthritis. Scand J Work Environ Health. 26: 243–249
  • Olsson, A. R., T. Skogh, O. Axelson, and G. Wingren. 2004. Occupations and exposures in the work environment as determinants for rheumatoid arthritis. Occup Environ Med. 61: 233–238
  • Deng, C., J. Yang, J. Scott, S. Hanash, and B. C. Richardson. 1998. Role of the ras-MAPK signaling pathway in the DNA methyltransferase response to DNA hypomethylation. Biol Chem. 379: 1113–1120
  • Gorelik, G., and B. Richardson. 2010. Key role of ERK pathway signaling in lupus. Autoimmunity. 43: 17–22
  • Pan, W., S. Zhu, M. Yuan, H. Cui, L. Wang, X. Luo, J. Li, et al. 2010. MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly and indirectly targeting DNA methyltransferase 1. J Immunol. 184: 6773–6781
  • Layer, K., G. Lin, A. Nencioni, W. Hu, A. Schmucker, A. N. Antov, X. Li, et al. 2003. Autoimmunity as the consequence of a spontaneous mutation in Rasgrp1. Immunity. 19: 243–255
  • Zhao, S., Y. Wang, Y. Liang, M. Zhao, H. Long, S. Ding, H. Yin, and Q. Lu. 2011. MicroRNA-126 regulates DNA methylation in CD4+ T cells and contributes to systemic lupus erythematosus by targeting DNA methyltransferase 1. Arthritis Rheum. 63: 1376–1386
  • Qin, H., X. Zhu, J. Liang, J. Wu, Y. Yang, S. Wang, W. Shi, and J. Xu. 2013. MicroRNA-29b contributes to DNA hypomethylation of CD4+ T cells in systemic lupus erythematosus by indirectly targeting DNA methyltransferase 1. J Dermatol Sci. 69: 61–67
  • Rai, K., I. J. Huggins, S. R. James, A. R. Karpf, D. A. Jones, and B. R. Cairns. 2008. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell. 135: 1201–1212
  • Tahiliani, M., K. P. Koh, Y. Shen, W. A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 324: 930–935
  • Zhang, Y., M. Zhao, A. H. Sawalha, B. Richardson, and Q. Lu. 2013. Impaired DNA methylation and its mechanisms in CD4+ T cells of systemic lupus erythematosus. J Autoimmun. 41: 92--99
  • Wu, H., and Y. Zhang. 2011. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev. 25: 2436–2452
  • Williams, K., J. Christensen, and K. Helin. 2012. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 13: 28–35
  • Branco, M. R., G. Ficz, and W. Reik. 2012. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet. 13: 7–13
  • Tenbrock, K., Y. T. Juang, M. Tolnay, and G. C. Tsokos. 2003. The cyclic adenosine 5′-monophosphate response element modulator suppresses IL-2 production in stimulated T cells by a chromatin-dependent mechanism. J Immunol. 170: 2971–2976
  • Hedrich, C. M., T. Rauen, and G. C. Tsokos. 2012. cAMP responsive element modulator (CREM)α induces epigenetic remodeling of IL2 in T lymphocytes from SLE patients. J Immunol. 188 (Meeting Abstract Supplement): 121.2. Available from: http://www.jimmunol.org/cgi/content/meeting_abstract/188/1_MeetingAbstracts/121.2?sid=06afd463-1c29-4e7c-a255-a21a516198a8 [last accessed 6 Jun 2013]
  • Kim, S. J., Y. R. Zou, J. Goldstein, B. Reizis, and B. Diamond. 2011. Tolerogenic function of Blimp-1 in dendritic cells. J Exp Med. 208: 2193–2199
  • Cretney, E., A. Xin, W. Shi, M. Minnich, F. Masson, M. Miasari, G. T. Belz, et al. 2011. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat Immunol. 12: 304–311
  • Kallies, A., E. D. Hawkins, G. T. Belz, D. Metcalf, M. Hommel, L. M. Corcoran, P. D. Hodgkin, and S. L. Nutt. 2006. Transcriptional repressor Blimp-1 is essential for T cell homeostasis and self-tolerance. Nat Immunol. 7: 466–474
  • Kallies, A., A. Xin, G. T. Belz, and S. L. Nutt. 2009. Blimp-1 transcription factor is required for the differentiation of effector CD8+ T cells and memory responses. Immunity. 31: 283–295
  • Nutt, S. L., A. Kallies, and G. T. Belz. 2008. Blimp-1 connects the intrinsic and extrinsic regulation of T cell homeostasis. J Clin Immunol. 28: 97–106
  • Yu, J., C. Angelin–Duclos, J. Greenwood, J. Liao, and K. Calame. 2000. Transcriptional repression by blimp-1 PRDI-BF1. involves recruitment of histone deacetylase. Mol Cell Biol. 20: 2592–2603
  • Gajiwala, K. S., H. Chen, F. Cornille, B. P. Roques, W. Reith, B. Mach, and S. K. Burley. 2000. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature. 403: 916–921
  • Katan, Y., R. Agami, and Y. Shaul. 1997. The transcriptional activation and repression domains of RFX1, a context-dependent regulator, can mutually neutralize their activities. Nucl Acids Res. 25: 3621–3628

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