Increased 5-hydroxymethylcytosine in CD4+ T cells in systemic lupus erythematosus

Journal of Autoimmunity

Volumn 69, Issue , 2016, Pages 64-73

  Zhao, Ming ^a   Wang, Jing ^a   Liao, Wei ^a   Li, Duo ^a   Li, Mengying ^a   Wu, Haijing ^a   Zhang, Yiqun ^a   Gershwin, M Eric ^b   Lu, Qianjin ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CD4+ T cells; CTCF; Epigenetics; Hydroxymethylation; Methylation; SOCS1; Systemic lupus erythematosus

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; GENOMIC DNA; HYDROXYCHLOROQUINE; INTERLEUKIN 15 RECEPTOR ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; METHYLPREDNISOLONE; MITOGEN ACTIVATED PROTEIN KINASE; MYCOPHENOLATE MOFETIL; NEUROTROPHIN; PREDNISONE; SUPPRESSOR OF CYTOKINE SIGNALING 1; TRANSCRIPTION FACTOR CTCF; WNT PROTEIN; 5-HYDROXYMETHYLCYTOSINE; CYTOSINE; IL15RA PROTEIN, HUMAN; INTERLEUKIN 15 RECEPTOR; MESSENGER RNA; NR2F6 PROTEIN, HUMAN; PROTEIN BINDING; STEROID RECEPTOR;

ADULT; ARTICLE; CALCIUM SIGNALING; CD4+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CLINICAL PATHWAY; CONTROLLED STUDY; DNA HYDROXYMETHYLATION; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; IMMUNOREGULATION; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SLEDAI; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION REGULATION; UPREGULATION; WNT SIGNALING PATHWAY; YOUNG ADULT; ANALOGS AND DERIVATIVES; AUTOIMMUNITY; CASE CONTROL STUDY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HIGH THROUGHPUT SEQUENCING; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; METABOLISM; SEVERITY OF ILLNESS INDEX;

ADULT; AUTOIMMUNITY; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CHROMATIN IMMUNOPRECIPITATION; CYTOSINE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, INTERLEUKIN-15; RECEPTORS, STEROID; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; SUPPRESSOR OF CYTOKINE SIGNALING 1 PROTEIN; YOUNG ADULT;

EID: 84960444957     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2016.03.001     Document Type: Article

References (46)

1. Sestak A.L., Furnrohr B.G., Harley J.B., Merrill J.T., Namjou B. The genetics of systemic lupus erythematosus and implications for targeted therapy. Ann. Rheum. Dis. 2011, 70(Suppl. 1):i37-43.
2. Han J.W., Zheng H.F., Cui Y., Sun L.D., Ye D.Q., Hu Z., et al. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat. Genet. 2009, 41:1234-1237.
3. Wang J., Yang S., Chen J.J., Zhou S.M., He S.M., Liang Y.H., et al. Systemic lupus erythematosus: a genetic epidemiology study of 695 patients from China. Arch. Dermatol. Res. 2007, 298:485-491.
4. Seldin M.F. The genetics of human autoimmune disease: a perspective on progress in the field and future directions. J. Autoimmun. 2015, 64:1-12.
5. Ghodke-Puranik Y., Niewold T.B. Immunogenetics of systemic lupus erythematosus: a comprehensive review. J. Autoimmun. 2015, 64:125-136.
6. Babbitt G.A., Coppola E.E., Alawad M.A., Hudson A.O. Can all heritable biology really be reduced to a single dimension?. Gene 2016, 578:162-168.
7. Harden J.L., Krueger J.G., Bowcock A.M. The immunogenetics of Psoriasis: a comprehensive review. J. Autoimmun. 2015, 64:66-73.
8. Hollenbach J.A., Oksenberg J.R. The immunogenetics of multiple sclerosis: a comprehensive review. J. Autoimmun. 2015, 64:13-25.
9. Wu H., Zhao M., Chang C., Lu Q. The real culprit in systemic lupus erythematosus: abnormal epigenetic regulation. Int. J. Mol. Sci. 2015, 16:11013-11033.
10. Zhao M., Wang Z., Yung S., Lu Q. Epigenetic dynamics in immunity and autoimmunity. Int. J. Biochem. Cell Biol. 2015, 67:65-74.
11. Lu Q. The critical importance of epigenetics in autoimmunity. J. Autoimmun. 2013, 41:1-5.
12. Cornec D., Jamin C., Pers J.O. Sjogren's syndrome: where do we stand, and where shall we go?. J. Autoimmun. 2014, 51:109-114.
13. Lawrence M., Daujat S., Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016, 32:42-56.
14. Meroni P.L., Penatti A.E. Epigenetics and systemic lupus erythematosus: unmet needs. Clin. Rev. Allergy Immunol. 2015, 10.1007/s12016-015-8497-4.
15. Zhao M., Liu S., Luo S., Wu H., Tang M., Cheng W., et al. DNA methylation and mRNA and microRNA expression of SLE CD4+ T cells correlate with disease phenotype. J. Autoimmun. 2014, 54:127-136.
16. Nervi C., De Marinis E., Codacci-Pisanelli G. Epigenetic treatment of solid tumours: a review of clinical trials. Clin. Epigenetics 2015, 7:127.
17. Coit P., Yalavarthi S., Ognenovski M., Zhao W., Hasni S., Wren J.D., et al. Epigenome profiling reveals significant DNA demethylation of interferon signature genes in lupus neutrophils. J. Autoimmun. 2015, 58:59-66.
18. Pastor W.A., Aravind L., Rao A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 2013, 14:341-356.
19. Antonopoulou S., Demopoulos C.A., Iatrou C., Moustakas G., Zirogiannis P. Platelet-activating factor acetylhydrolase (PAF-AH) in human kidney. Int. J. Biochem. 1994, 26:1157-1162.
20. Madzo J., Liu H., Rodriguez A., Vasanthakumar A., Sundaravel S., Caces D.B., et al. Hydroxymethylation at gene regulatory regions directs stem/early progenitor cell commitment during erythropoiesis. Cell Rep. 2014, 6:231-244.
21. Ichiyama K., Chen T., Wang X., Yan X., Kim B.S., Tanaka S., et al. The methylcytosine dioxygenase Tet2 promotes DNA demethylation and activation of cytokine gene expression in T cells. Immunity 2015, 42:613-626.
22. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J., Rothfield N.F., et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982, 25:1271-1277.
23. Nestor C.E., Meehan R.R. Hydroxymethylated DNA immunoprecipitation (hmeDIP). Methods Mol. Biol. 2014, 1094:259-267.
24. Zhao M., Liu Q., Liang G., Wang L., Luo S., Tang Q., et al. E4BP4 overexpression: a protective mechanism in CD4+ T cells from SLE patients. J. Autoimmun. 2013, 41:152-160.
25. Ficz G., Branco M.R., Seisenberger S., Santos F., Krueger F., Hore T.A., et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473:398-402.
26. Hahn M.A., Qiu R., Wu X., Li A.X., Zhang H., Wang J., et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell Rep. 2013, 3:291-300.
27. Lee B.K., Iyer V.R. Genome-wide studies of CCCTC-binding factor (CTCF) and cohesin provide insight into chromatin structure and regulation. J. Biol. Chem. 2012, 287:30906-30913.
28. Dubois-Chevalier J., Oger F., Dehondt H., Firmin F.F., Gheeraert C., Staels B., et al. A dynamic CTCF chromatin binding landscape promotes DNA hydroxymethylation and transcriptional induction of adipocyte differentiation. Nucleic Acids Res. 2014, 42:10943-10959.
29. 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.
30. Lei W., Luo Y., Lei W., Luo Y., Yan K., Zhao S., et al. Abnormal DNA methylation in CD4+ T cells from patients with systemic lupus erythematosus, systemic sclerosis, and dermatomyositis. Scand. J. Rheumatol. 2009, 38:369-374.
31. Bhutani N., Burns D.M., Blau H.M. DNA demethylation dynamics. Cell 2011, 146:866-872.
32. Zhao M., Sun Y., Gao F., Wu X., Tang J., Yin H., et al. Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4+ T cells. J. Autoimmun. 2010, 35:58-69.
33. Coit P., Jeffries M., Altorok N., Dozmorov M.G., Koelsch K.A., Wren J.D., et al. 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.
34. Takahashi R., Nishimoto S., Muto G., Sekiya T., Tamiya T., Kimura A., et al. SOCS1 is essential for regulatory T cell functions by preventing loss of Foxp3 expression as well as IFN-γ and IL-17A production. J. Exp. Med. 2011, 208:2055-2067.
35. Takahashi R., Yoshimura A. SOCS1 and regulation of regulatory T cells plasticity. J. Immunol. Res. 2014, 2014:943149.
36. Chan H.C., Ke L.Y., Chang L.L., Liu C.C., Hung Y.H., Lin C.H., et al. Suppressor of cytokine signaling 1 gene expression and polymorphisms in systemic lupus erythematosus. Lupus 2010, 19:696-702.
37. Chen J.Q., Zilahi E., Papp G., Sipka S., Zeher M. Simultaneously increased expression of microRNA-155 and suppressor of cytokine signaling 1 (SOCS1) gene in the peripheral blood mononuclear cells of patients with primary Sjogren's syndrome. Int. J. Rheum. Dis. 2015, 10.1111/1756-185X.12804.
38. Isomaki P., Alanara T., Isohanni P., Lagerstedt A., Korpela M., Moilanen T., et al. The expression of SOCS is altered in rheumatoid arthritis. Rheumatol. Oxf. 2007, 46:1538-1546.
39. Miranda-Carus M.E., Benito-Miguel M., Llamas M.A., Balsa A., Martin-Mola E. Human T cells constitutively express IL-15 that promotes ex vivo T cell homeostatic proliferation through autocrine/juxtacrine loops. J. Immunol. 2005, 175:3656-3662.
40. Baranda L., de la Fuente H., Layseca-Espinosa E., Portales-Perez D., Nino-Moreno P., Valencia-Pacheco G., et al. IL-15 and IL-15R in leucocytes from patients with systemic lupus erythematosus. Rheumatol. Oxf. 2005, 44:1507-1513.
41. Hermann-Kleiter N., Gruber T., Lutz-Nicoladoni C., Thuille N., Fresser F., Labi V., et al. The nuclear orphan receptor NR2F6 suppresses lymphocyte activation and T helper 17-dependent autoimmunity. Immunity 2008, 29:205-216.
42. Hermann-Kleiter N., Meisel M., Fresser F., Thuille N., Muller M., Roth L., et al. Nuclear orphan receptor NR2F6 directly antagonizes NFAT and RORgammat binding to the Il17a promoter. J. Autoimmun. 2012, 39:428-440.
43. Jacquemin C., Schmitt N., Contin-Bordes C., Liu Y., Narayanan P., Seneschal J., et al. OX40 ligand contributes to human lupus pathogenesis by promoting T follicular helper response. Immunity 2015, 42:1159-1170.
44. Matatiele P., Tikly M., Tarr G., Gulumian M. DNA methylation similarities in genes of black South Africans with systemic lupus erythematosus and systemic sclerosis. J. Biomed. Sci. 2015, 22:34.
45. Yang Y., Tang Q., Zhao M., Liang G., Wu H., Li D., et al. The effect of mycophenolic acid on epigenetic modifications in lupus CD4+T cells. Clin. Immunol. 2015, 158:67-76.
46. Bentham J., Morris D.L., Cunninghame Graham D.S., Pinder C.L., Tombleson P., Behrens T.W., et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat. Genet. 2015, 47:1457-1464.