IL-6 Modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation

Journal of Immunology

Volumn 182, Issue 9, 2009, Pages 5623-5632

  Garaud, Soizic ^a   Le Dantec, Christelle ^a   Jousse Joulin, Sandrine ^b   Hanrotel Saliou, Catherine ^b   Saraux, Alain ^a,b   Mageed, Rizgar A ^a   Youinou, Pierre ^a,b   Renaudineau, Yves ^a,b  

^a Universite de Brest   (France)

^b SERVICE DE RHUMATOLOGIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; BISULFITE; CD19 ANTIGEN; CD5 ANTIGEN; CD70 ANTIGEN; DNA METHYLTRANSFERASE 1; E1A PROTEIN; E1B PROTEIN; ENDONUCLEASE; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; ISOPROTEIN; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2; PROTEIN KINASE SYK; TRANSCRIPTION FACTOR PAX5; AUTOANTIBODY; LYMPHOCYTE ANTIGEN RECEPTOR;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CD5 E1B GENE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; CYTOPLASM; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREGULATION; MALE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; RNA TRANSCRIPTION; SYSTEMIC LUPUS ERYTHEMATOSUS; BIOSYNTHESIS; CELL CULTURE; CLONAL ANERGY; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; PILOT STUDY;

ADULT; AGED; ANTIGENS, CD5; AUTOANTIBODIES; B-LYMPHOCYTE SUBSETS; BASE SEQUENCE; CELLS, CULTURED; CLONAL ANERGY; DNA METHYLATION; DOWN-REGULATION; FEMALE; HUMANS; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PILOT PROJECTS; RECEPTORS, ANTIGEN, B-CELL; TRANSCRIPTION, GENETIC;

EID: 66949176660     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802412     Document Type: Article

References (42)

1. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358: 929-939.
2. Renaudineau, Y., P. O. Pers, B. Bendaoud, C. Jamin, and P. Youinou. 2004. Dysfunctional B cells in SLE. Autoimmun. Rev. 3: 516-523.
3. Leandro, M. J., J. C. Edwards, G. Cambridge, M. R. Ehrenstein, and D. A. Isenberg. 2002. An open study of B lymphocyte depletion in systemic lupus erythematosus. Arthritis Rheum. 46: 2673-2677. (Pubitemid 36118931)
4. Illei, G., C. Yarboro, Y. Shirota, E. Tackey, L. Lapteva, and T. Fleisher. 2006. Tocilizumab (humanized anti IL-6 receptor monoclonal antibody) in patients with systemic lupus erythematosus (SLE): safety, tolerability and preliminary efficacy. Arthritis Rheum. 54 (Suppl): 4043 (Abstract).
5. Finck, B. K., P. S. Linsley, and D. Wofsy. 1994. Treatment of murine lupus with CTLA4Ig. Science 265: 1225-1227.
6. Hom, G., R. R. Graham, B. Modrek, K. E. Taylor, W. Ortmann, S. Garnier, A. T. Lee, S. A. Chung, R. C. Ferreira, P. V. Pant, et al. 2008. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N. Engl. J. Med. 358: 900-909. (Pubitemid 351397089)
7. Ballestar, E., M. Esteller, and B. C. Richardson. 2006. The epigenetic face of systemic lupus erythematosus. J. Immunol. 176: 7143-7147. (Pubitemid 43849013)
8. Zhu, B., Y. Zheng, H. Angliker, S. Schwarz, S. Thiry, M. Siegmann, and J. P. Jost. 2000. 5-Methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. Nucleic Acids Res. 28: 4157-4165.
9. Hendrich, B., and A. Bird. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell Biol. 18: 6538-6547. (Pubitemid 28500543)
10. Schwab, J., and H. Illges. 2001. Regulation of CD21 expression by DNA methylation and histone acetylation. Int. Immunol. 13: 705-710. (Pubitemid 32427873)
11. 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.
12. Piotrowski, P. C., S. Duriagin, and P. P. Jagodzinski. 2005. Expression of HERV clone 4-1 may correlate with blood plasma concentration of anti-U1 RNP and anti-Sm nuclear antibodies. Clin. Rheumatol. 24: 620-624.
13. Deng, C., M. J. Kaplan, J. Yang, D. Ray, Z. Zhang, W. J. McCune, S. M. Hanash, and B. C. Richardson. 2001. Decreased ras-mitogen-activated protein kinase signaling may cause DNA hypomethylation in T lymphocytes from lupus patients. Arthritis Rheum. 44: 397-407.
14. Hippen, K. L., L. E. Tze, and T. W. Behrens. 2000. CD5 maintains tolerance in anergic B cells. J. Exp. Med. 191: 883-890.
15. Jamin, C., G. Magadur, A. Lamour, L. MacKenzie, P. M. Lydyard, P. Katsikis, and P. Youinou. 1992. Cell-free CD5 in patients with rheumatic diseases. Immunol. Lett. 31: 79-84.
16. Lu, X., R. C. Axtell, J. F. Collawn, A. Gilson, L. B. Justement, and C. Raman. 2002. AP2 adaptor complex-dependent internalization of CD5: differential regulation in T and B cells. J. Immunol. 168: 5612-5620. (Pubitemid 34556142)
17. Renaudineau, Y., S. Hillion, A. Saraux, R. A. Mageed, and P. Youinou. 2005. An alternative exon 1 of the CD5 gene regulates CD5 expression in human B lymphocyte. Blood 106: 2781-2789. (Pubitemid 41510754)
18. Renaudineau, Y., S. Vallet, C. Le Dantec, S. Hillion, A. Saraux, and P. Youinou. 2005. Characterization of the human CD5 endogenous retrovirus-E in B lymphocytes. Gene Immun. 6: 663-671. (Pubitemid 41741711)
19. Garaud, S., C. Le Dantec, C. Berthou, P. M. Lydyard, P. Youinou, and Y. Renaudineau. 2008. Selection of the alternative exon 1 from the cd5 gene down-regulates membrane level of the protein in B lymphocytes. J. Immunol. 181: 2010-2018.
20. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of SLE. Arthritis Rheum. 25: 1271-1277.
21. Ushmorov, A., F. Leithäuser, O. Sakk, A. Weinhaüsel, S. W. Popov, P. Möller, and T Wirth. 2006. Epigenetic processes play a major role in B-cell-specific gene silencing in classical Hodgkin lymphoma. Blood 107: 2493-2500. (Pubitemid 43345573)
22. Perl, A., J. D. Rosenblatt, I. S. Chen, J. P. DiVincenzo, R. Bever, B. J. Poiesz, and G. N. Abraham. 1989. Detection and cloning of new HTLV-related endogenous sequences in man. Nucleic Acids Res. 17: 6841-6854. (Pubitemid 19223274)
23. Ruchusatsawat, K., J. Wongpiyabovorn, S. Shuangshoti, N. Hirankarn, and A. Mutirangura. 2006. SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. J. Mol. Med. 84: 175-182. (Pubitemid 43201258)
24. Jones, N. H., M. L. Clabby, D. P. Dialynas, H. J. Huang, L. A. Herzenberg, and J. L. Strominger. 1986. Isolation of complementary DNA clones encoding the human lymphocyte glycoprotein T1/Leu-1. Nature 323: 346-349.
25. Reiss, D., Y. Zhang, and D. L. Mager. 2007. Widely variable endogenous retroviral methylation levels in human placenta. Nucleic Acids Res. 35: 4743-4754. (Pubitemid 47250346)
26. Hillion, S., S. Garaud, V. Devauchelle, A. Bordron, C. Berthou, P. Youinou, and C. Jamin. 2007. IL-6 is responsible for aberrant BCR-mediated regulation of RAG expression in SLE. Immunology 122: 371-380.
27. Robertson, K. D., K. Keyomarsi, F. A. Gonzales, M. Velicescu, and P. A. Jones. 2000. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G(0)/G(1) to S phase transition in normal and tumor cells. Nucleic Acids Res. 28: 2108-2113.
28. Brown, S. E., M. F. Fraga, I. C. Weaver, M. Berdasco, and M. Szyf. 2007. Variations in DNA methylation patterns during the cell cycle of HeLa cells. Epigenetics 2: 54-65. (Pubitemid 46830295)
29. Pullmann, R., Jr., E. Bonilla, P. E. Phillips, F. A. Middleton, and A. Perl. 2008. Haplotypes of the HRES-1 endogenous retrovirus are associated with development and disease manifestations of systemic lupus erythematosus. Arthritis Rheum. 58: 532-540.
30. Zhou, Y., and Q. Lu. 2008. DNA methylation in T cells from idiopathic lupus and drug-induced lupus patients. Autoimmun. Rev. 7: 376-383.
31. Vigorito, E., K. L. Perks, C. Abreu-Goodger, S. Bunting, Z. Xiang, S. Kohlhaas, P. P. Das, E. A. Miska, A. Rodriguez, A. Bradley, et al. 2007. microRNA-155 regulates the generation of Ig class-switched plasma cells. Immunity 27: 847-859. (Pubitemid 350258623)
32. Wang, H., J. Feng, C. F. Qi, Z. Li, H. C. Morse 3rd, and S. H. Clarke. 2007. Transitional B cells lose their ability to receptor edit but retain their potential for positive and negative selection. J. Immunol. 179: 7544-7552.
33. Pang, Y., Y. Norihisa, D. Benjamin, R. R. Kantor, and H. A. Young. 1992. IFN-γ gene expression in human B-cell lines: induction by IL-2, PKC, and possible effect of hypomethylation on gene regulation. Blood 80: 724-732.
34. Huber, L. C., J. Stanczyk, A. Jüngel, and S. Gay. 2007. Epigenetics in inflammatory rheumatic diseases. Arthritis Rheum. 56: 3523-3531.
35. Balada, E., J. Ordi-Ros, S. Serrano-Acedo, L. Martinez-Lostao, M. Rosa-Leyva, and M. Vilardell-Tarrés. 2008. Transcript levels of DNA methyltransferases DNMT1, DNMT3A and DNMT3B in CD4+ T cells from patients with systemic lupus erythematosus. Immunology 124: 339-347. (Pubitemid 351793466)
36. Ogasawara, H., M. Okada, H. Kaneko, T. Hishikawa, I. Sekigawa, and H. Hashimoto. 2003. Possible role of DNA hypomethylation in the induction of SLE: relationship to the transcription of HERV. Clin. Exp. Rheumatol. 21: 733-738. (Pubitemid 38008756)
37. Balada, E., J. Ordi-Ros, S. Serrano-Acedo, L. Martinez-Lostao, and M. Vilardell-Tarrés. 2007. Transcript overexpression of the MBD2 and MBD4 genes in CD4+ T cells from SLE patients. J. Leukocyte Biol. 81: 1609-1616.
38. Sawalha, A. H., M. Jeffries, R. Webb, Q. Lu, G. Gorelik, D. Ray, J. Osban, N. Knowlton, K. Johnson, and B. Richardson. 2008. Defective T-cell ERK signaling induces IFN-regulated gene expression and overexpression of methylation-sensitive genes similar to lupus patients. Genes Immun. 9: 368-378.
39. Qiang, Y. W., M. Kitagawa, M. Higashi, G. Ishii, C. Morimoto, and K. Harigaya. 2000. Activation of MAPK through alpha5/β1 integrin is required for cell cycle progression of B progenitor cell line, Reh, on human marrow stromal cells. Exp. Hematol. 28: 1147-1157.
40. Gysin, S., S. H. Lee, N. M. Dean, and M. McMahon. 2005. Pharmacologic inhibition of RAF->MEK->ERK signaling elicits pancreatic cancer cell cycle arrest through induced expression of p27Kip1. Cancer Res. 65: 4870-4880. (Pubitemid 40740826)
41. Richardson, B., D. Ray, and R. Yung. 2004. Murine models of lupus induced by hypomethylated T cells. Methods Mol. Med. 102: 285-294.
42. Mi, X. B., and F. Q. Zeng. 2008. Hypomethylation of IL-4 and -6 promoters in T cells from SLE patients. Acta Pharmacol. Sin. 29: 105-112.