Epigenetics and SLE: RFX1 downregulation causes CD11a and CD70 overexpression by altering epigenetic modifications in lupus CD4+ T cells

Journal of Autoimmunity

Volumn 35, Issue 1, 2010, Pages 58-69

  Zhao, Ming ^a   Sun, Yimin ^b   Gao, Fei ^a   Wu, Xiaoyan ^a   Tang, Jinling ^a   Yin, Heng ^a   Luo, Yongqi ^a   Richardson, Bruce ^c   Lu, Qianjin ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b NATIONAL ENGINEERING RESEARCH CENTER FOR BEIJING BIOCHIP TECHNOLOGY   (China)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

DNA (cytosine 5 ) methyltransferase 1; DNA methylation; Histone deacetylase 1; RFX1; Systemic lupus erythematosus; T cells

Indexed keywords

CD70 ANTIGEN; DNA; HISTONE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; REGULATORY FACTOR X 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA BINDING PROTEIN; HDAC1 PROTEIN, HUMAN; HISTONE DEACETYLASE 1; REGULATORY FACTOR X TRANSCRIPTION FACTORS; SMALL INTERFERING RNA;

ACETYLATION; ADULT; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MOLECULAR CLONING; PATHOLOGY; PROMOTER REGION;

ACETYLATION; ADULT; ANIMALS; ANTIGENS, CD11A; ANTIGENS, CD70; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CLONING, MOLECULAR; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE 1; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; PROMOTER REGIONS, GENETIC; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 77953288009     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.02.002     Document Type: Article

References (62)

1. Hewagama A., Richardson B. The genetics and epigenetics of autoimmune diseases. J Autoimmun 2009, 33:3-11.
2. Moser K.L., Kelly J.A., Lessard C.J., Harley J.B. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun 2009, 10:373-379.
3. Jarvinen P., Aho K. Twin studies in rheumatic diseases. Semin Arthritis Rheum 1994, 24:19-28.
4. Deapen D., Escalante A., Weinrib L., Horwitz D., Bachman B., Roy-Burman P., et al. A revised estimate of twin concordance in systemic lupus erythematosus. Arthritis Rheum 1992, 35:311-318.
5. + cells treated with DNA methylation inhibitors induce autologous B cell differentiation. Clin Immunol Immunopathol 1990, 55:368-381.
6. Yung R., Chang S., Hemati N., Johnson K., Richardson B. Mechanisms of drug-induced lupus. IV. Comparison of procainamide and hydralazine with analogs in vitro and in vivo. Arthritis Rheum 1997, 40:1436-1443.
7. Lu Q., Kaplan M., Ray D., Ray D., Zacharek S., Gutsch D., et al. Demethylation of ITGAL (CD11a) regulatory sequences in systemic lupus erythematosus. Arthritis Rheum 2002, 46:1282-1291.
8. 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.
9. Gahmberg C.G. Leukocyte adhesion: CD11/CD18 integrins and intercellular adhesion molecules. Curr Opin Cell Biol 1997, 9:643-650.
10. Shimaoka M., Springer T.A. Therapeutic antagonists and conformational regulation of integrin function. Nat Rev Drug Discov 2003, 2:703-716.
11. Kevil C.G., Hicks M.J., He X., Zhang J., Ballantyne C.M., Raman C., et al. Loss of LFA-1, but not Mac-1, protects MRL/MpJ-Fas(lpr) mice from autoimmune disease. Am J Pathol 2004, 165:609-616.
12. Kobata T., Jacquot S., Kozlowski S., Agematsu K., Schlossman S.F., Morimoto C. CD27-CD70 interactions regulate B-cell activation by T cells. Proc Natl Acad Sci U S A 1995, 92:11249-11253.
13. Oelke K., Lu Q., Richardson D., Wu A., Deng C., Hanash S., et al. 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.
14. Cameron E.E., Bachman K.E., Myohanen S., Herman J.G., Baylin S.B. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999, 21:103-107.
15. Tenbrock K., Juang Y.T., Leukert N., Roth J., Tsokos G.C. The transcriptional repressor cAMP response element modulator alpha interacts with histone deacetylase 1 to repress promoter activity. J Immunol 2006, 177:6159-6164.
16. Esteve P.O., Chin H.G., Pradhan S. Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. Proc Natl Acad Sci U S A 2005, 102:1000-1005.
17. Eberharter A., Becker P.B. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 2002, 3:224-229.
18. Robertson K.D., Jones P.A. DNA methylation: past, present and future directions. Carcinogenesis 2000, 21:461-467.
19. Qiao J.Y., Shao W., Wei H.J., Sun Y.M., Zhao Y.C., Xing W.L., et al. Novel high-throughput profiling of human transcription factors and its use for systematic pathway mapping. J Proteome Res 2008, 7:2769-2779.
20. 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.
21. Bombardier C., Gladman D.D., Urowitz M.B., Caron D., Chang C.H. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 1992, 35:630-640.
22. Shao W., Wei H.J., Qiao J.Y., Zhao Y.C., Sun Y.M., Zhou Y.X., et al. Parallel profiling of active transcription factors using an oligonucleotide array-based transcription factor assay (OATFA). J Proteome Res 2005, 4:1451-1456.
23. Ren C., Zhao M., Yang X., Li D., Jiang X., Wang L., et al. Establishment and applications of Epstein-Barr virus-based episomal vectors in human embryonic stem cells. Stem Cells 2006, 24:1338-1347.
24. Tenbrock K., Kyttaris V.C., Ahlmann M., Ehrchen J.M., Tolnay M., Melkonyan H., et al. The cyclic AMP response element modulator regulates transcription of the TCR zeta-chain. J Immunol 2005, 175:5975-5980.
25. Sengupta P., Xu Y., Wang L., Widom R., Smith B.D. Collagen alpha1(I) gene (COL1A1) is repressed by RFX family. J Biol Chem 2005, 280:21004-21014.
26. Xu Y., Sengupta P.K., Seto E., Smith B.D. Regulatory factor for X-box family proteins differentially interact with histone deacetylases to repress collagen alpha2(I) gene (COL1A2) expression. J Biol Chem 2006, 281:9260-9270.
27. Wang K.R., Nemoto T., Yokota Y. RFX1 mediates the serum-induced immediate early response of Id2 gene expression. J Biol Chem 2007, 282:26167-26177.
28. Macaluso M., Cinti C., Russo G., Russo A., Giordano A. pRb2/p130-E2F4/5-HDAC1-SUV39H1-p300 and pRb2/p130-E2F4/5-HDAC1-SUV39H1-DNMT1 multimolecular complexes mediate the transcription of estrogen receptor-alpha in breast cancer. Oncogene 2003, 22:3511-3517.
29. Lu Q., Wu A., Ray D., Deng C., Attwood J., Hanash S., et al. DNA methylation and chromatin structure regulate T cell perforin gene expression. J Immunol 2003, 170:5124-5132.
30. 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.
31. Reith W., Herrero-Sanchez C., Kobr M., Silacci P., Berte C., Barras E., et al. MHC class II regulatory factor RFX has a novel DNA-binding domain and a functionally independent dimerization domain. Genes Dev 1990, 4:1528-1540.
32. Emery P., Durand B., Mach B., Reith W. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res 1996, 24:803-807.
33. Gajiwala K.S., Chen H., Cornille F., Roques B.P., Reith W., Mach B., et al. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 2000, 403:916-921.
34. Durand B., Vandaele C., Spencer D., Pantalacci S., Couble P. Cloning and characterization of dRFX, the Drosophila member of the RFX family of transcription factors. Gene 2000, 246:285-293.
35. Huang M., Zhou Z., Elledge S.J. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 1998, 94:595-605.
36. Swoboda P., Adler H.T., Thomas J.H. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 2000, 5:411-421.
37. Wu S.Y., McLeod M. The sak1+ gene of Schizosaccharomyces pombe encodes an RFX family DNA-binding protein that positively regulates cyclic AMP-dependent protein kinase-mediated exit from the mitotic cell cycle. Mol Cell Biol 1995, 15:1479-1488.
38. Nakayama A., Murakami H., Maeyama N., Yamashiro N., Sakakibara A., Mori N., et al. Role for RFX transcription factors in non-neuronal cell-specific inactivation of the microtubule-associated protein MAP1A promoter. J Biol Chem 2003, 278:233-240.
39. Senti G., Swoboda P. Distinct isoforms of the RFX transcription factor DAF-19 regulate ciliogenesis and maintenance of synaptic activity. Mol Biol Cell 2008, 19:5517-5528.
40. Katan Y., Agami R., Shaul Y. The transcriptional activation and repression domains of RFX1, a context-dependent regulator, can mutually neutralize their activities. Nucleic Acids Res 1997, 25:3621-3628.
41. Katan-Khaykovich Y., Shaul Y. RFX1, a single DNA-binding protein with a split dimerization domain, generates alternative complexes. J Biol Chem 1998, 273:24504-24512.
42. Iwama A., Pan J., Zhang P., Reith W., Mach B., Tenen D.G., et al. Dimeric RFX proteins contribute to the activity and lineage specificity of the interleukin-5 receptor alpha promoter through activation and repression domains. Mol Cell Biol 1999, 19:3940-3950.
43. Ma K., Zheng S., Zuo Z. The transcription factor regulatory factor X1 increases the expression of neuronal glutamate transporter type 3. J Biol Chem 2006, 281:21250-21255.
44. Zajac-Kaye M., Ben-Baruch N., Kastanos E., Kaye F.J., Allegra C. Induction of Myc-intron-binding polypeptides MIBP1 and RFX1 during retinoic acid-mediated differentiation of haemopoietic cells. Biochem J 2000, 345(Pt 3):535-541.
45. Liu M., Lee B.H., Mathews M.B. Involvement of RFX1 protein in the regulation of the human proliferating cell nuclear antigen promoter. J Biol Chem 1999, 274:15433-15439.
46. Seydel F., Garrigan E., Stutevoss B., Belkin N., Makadia B., Carter J., et al. GM-CSF induces STAT5 binding at epigenetic regulatory sites within the Csf2 promoter of non-obese diabetic (NOD) mouse myeloid cells. J Autoimmun 2008, 31:377-384.
47. Razin A., Cedar H. DNA methylation and gene expression. Microbiol Rev 1991, 55:451-458.
48. Lee P.P., Fitzpatrick D.R., Beard C., Jessup H.K., Lehar S., Makar K.W., et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001, 15:763-774.
49. Deng C., Kaplan M.J., Yang J., Ray D., Zhang Z., McCune W.J., et al. Decreased Ras-mitogen-activated protein kinase signaling may cause DNA hypomethylation in T lymphocytes from lupus patients. Arthritis Rheum 2001, 44:397-407.
50. + lupus T cells. J Immunol 2004, 172:3652-3661.
51. Sano H., Compton L.J., Shiomi N., Steinberg A.D., Jackson R.A., Sasaki T. Low expression of human histocompatibility leukocyte antigen-DR is associated with hypermethylation of human histocompatibility leukocyte antigen-DR alpha gene regions in B cells from patients with systemic lupus erythematosus. J Clin Invest 1985, 76:1314-1322.
52. Ohashi Y., Ueda M., Kawase T., Kawakami Y., Toda M. Identification of an epigenetically silenced gene, RFX1, in human glioma cells using restriction landmark genomic scanning. Oncogene 2004, 23:7772-7779.
53. Katan-Khaykovich Y., Shaul Y. Nuclear import and DNA-binding activity of RFX1. Evidence for an autoinhibitory mechanism. Eur J Biochem 2001, 268:3108-3116.
54. Chen L., Smith L., Johnson M.R., Wang K., Diasio R.B., Smith J.B. Activation of protein kinase C induces nuclear translocation of RFX1 and down-regulates c-myc via an intron 1 X box in undifferentiated leukemia HL-60 cells. J Biol Chem 2000, 275:32227-32233.
55. Gorelik G., Fang J.Y., Wu A., Sawalha A.H., Richardson B. Impaired T cell protein kinase C delta activation decreases ERK pathway signaling in idiopathic and hydralazine-induced lupus. J Immunol 2007, 179:5553-5563.
56. Miyamoto A., Nakayama K., Imaki H., Hirose S., Jiang Y., Abe M., et al. Increased proliferation of B cells and auto-immunity in mice lacking protein kinase C delta. Nature 2002, 416:865-869.
57. Invernizzi P., Pasini S., Selmi C., Gershwin M.E., Podda M. Female predominance and X chromosome defects in autoimmune diseases. J Autoimmun 2009, 33:12-16.
58. Invernizzi P. Future directions in genetic for autoimmune diseases. J Autoimmun 2009, 33:1-2.
59. Sawalha A.H., Webb R., Han S., Kelly J.A., Kaufman K.M., Kimberly R.P., et al. Common variants within MECP2 confer risk of systemic lupus erythematosus. PLoS One 2008, 3:e1727.
60. Larizza D., Calcaterra V., Martinetti M. Autoimmune stigmata in Turner syndrome: when lacks an X chromosome. J Autoimmun 2009, 33:25-30.
61. Sawalha A.H., Harley J.B., Scofield R.H. Autoimmunity and Klinefelter's syndrome: when men have two X chromosomes. J Autoimmun 2009, 33:31-34.
62. Persani L., Rossetti R., Cacciatore C., Bonomi M. Primary ovarian insufficiency: X chromosome defects and autoimmunity. J Autoimmun 2009, 33:35-41.