DNA methylation of human endogenous retrovirus in systemic lupus erythematosus

Journal of Human Genetics

Volumn 58, Issue 5, 2013, Pages 241-249

  Nakkuntod, Jeerawat ^a   Sukkapan, Pattadon ^a   Avihingsanon, Yingyos ^a   Mutirangura, Apiwat ^a   Hirankarn, Nattiya ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

DNA methylation; HERV; systemic lupus erythematosus

Indexed keywords

AZATHIOPRINE; BISULFITE; CYCLOPHOSPHAMIDE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISOLONE;

ADULT; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; ENDOGENOUS RETROVIRUS; FEMALE; HUMAN; HUMAN CELL; LONG TERMINAL REPEAT; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTOPENIA; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADOLESCENT; ADULT; CELL LINE; CPG ISLANDS; DNA METHYLATION; ENDOGENOUS RETROVIRUSES; FEMALE; GENETIC LOCI; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE SUBSETS; MALE; TERMINAL REPEAT SEQUENCES; YOUNG ADULT;

HUMAN ENDOGENOUS RETROVIRUS; HUMAN ENDOGENOUS RETROVIRUSES;

EID: 84878620373     PISSN: 14345161     EISSN: 1435232X     Source Type: Journal    
DOI: 10.1038/jhg.2013.6     Document Type: Article

References (47)

1. Crispin, J. C., Liossis, S. N., Kis-Toth, K., Lieberman, L. A., Kyttaris, V. C., Juang, Y. T. et al. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol. Med. 16, 47-57 (2010).
2. Hedrich, C. M. & Tsokos, G. C. Epigenetic mechanisms in systemic lupus erythematosus and other autoimmune diseases. Trends Mol. Med. 17, 714-724 (2011).
3. Hughes, T. & Sawalha, A. H. The role of epigenetic variation in the pathogenesis of systemic lupus erythematosus. Arthritis Res. Ther. 13, 245 (2011).
4. Renaudineau, Y. & Youinou, P. Epigenetics and autoimmunity, with special emphasis on methylation. Keio J. Med. 60, 10-16 (2011).
5. Richardson, B., Scheinbart, L., Strahler, J., Gross, L., Hanash, S. & Johnson, M. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum. 33, 1665-1673 (1990).
6. Luo, Y., Li, Y., Su, Y., Yin, H., Hu, N., Wang, S. et al. Abnormal DNA methylation in T cells from patients with subacute cutaneous lupus erythematosus. Br. J. Dermatol. 159, 827-833 (2008).
7. Balada, E., Ordi-Ros, J., Serrano-Acedo, S., Martinez-Lostao, L., Rosa-Leyva, M. & Vilardell-Tarres, M. Transcript levels of DNA methyltransferases DNMT1, DNMT3A and DNMT3B in CD4 T cells from patients with systemic lupus erythematosus. Immunology 124, 339-347 (2008).
8. Balada, E., Ordi-Ros, J., Serrano-Acedo, S., Martinez-Lostao, L. & Vilardell-Tarres, M. Transcript overexpression of the MBD2 and MBD4 genes in CD4 T cells from systemic lupus erythematosus patients. J. Leukoc. Biol. 81, 1609-1616 (2007).
9. Quddus, J., Johnson, K. J., Gavalchin, J., Amento, E. P., Chrisp, C. E., Yung, R. L. et al. 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, 38-53 (1993).
10. Yung, R., Chang, S., Hemati, N., Johnson, K. & Richardson, B. Mechanisms of druginduced lupus. IV. Comparison of procainamide and hydralazine with analogs in vitro and in vivo. Arthritis Rheum. 40, 1436-1443 (1997).
11. Yung, R., Powers, D., Johnson, K., Amento, E., Carr, D., Laing, T. et al. Mechanisms of drug-induced lupus. II. T cells overexpressing lymphocyte function-associated antigen become autoreactive and cause a lupus-like disease in syngeneic mice. J. Clin. Invest. 97, 2866-2871 (1996).
12. Kaplan, M. J., Lu, Q., Wu, A., Attwood, J. & Richardson, B. Demethylation of promoter regulatory elements contributes to perforin overexpression in CD4 lupus T cells. J. Immunol. 172, 3652-3661 (2004).
13. 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. 174, 6212-6219 (2005).
14. 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. 179, 6352-6358 (2007).
15. Sugimura, T. & Ushijima, T. Genetic and epigenetic alterations in carcinogenesis. Mutat. Res. 462, 235-246 (2000).
16. Kaneda, A., Tsukamoto, T., Takamura-Enya, T., Watanabe, N., Kaminishi, M., Sugimura, T. et al. Frequent hypomethylation in multiple promoter CpG islands is associated with global hypomethylation, but not with frequent promoter hypermethylation. Cancer Sci. 95, 58-64 (2004).
17. Bannert, N. & Kurth, R. Retroelements and the human genome: new perspectives on an old relation. Proc. Natl Acad. Sci. USA 101 (Suppl 2), 14572-14579 (2004).
18. Levy, S., Sutton, G., Ng, P. C., Feuk, L., Halpern, A. L., Walenz, B. P. et al. The diploid genome sequence of an individual human. PLoS Biol. 5, e254 (2007).
19. Jordan, I. K., Rogozin, I. B., Glazko, G. V. & Koonin, E. V. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19, 68-72 (2003).
20. Aporntewan, C., Phokaew, C., Piriyapongsa, J., Ngamphiw, C., Ittiwut, C., Tongsima, S. et al. Hypomethylation of intragenic LINE-1 represses transcription in cancer cells through AGO2. PLoS One 6, e17934 (2011).
21. Cordaux, R. & Batzer, M. A. The impact of retrotransposons on human genome evolution. Nat. Rev. 10, 691-703 (2009).
22. Kitkumthorn, N. & Mutirangura, A. Long interspersed nuclear element-1 hypomethylation in cancer: biology and clinical applications. Clin. Epigenetics 2, 315-330 (2011).
23. Saito, K., Kawakami, K., Matsumoto, I., Oda, M., Watanabe, G. & Minamoto, T. Long interspersed nuclear element 1 hypomethylation is a marker of poor prognosis in stage IA non-small cell lung cancer. Clin. Cancer Res. 16, 2418-2426 (2010).
24. Pattamadilok, J., Huapai, N., Rattanatanyong, P., Vasurattana, A., Triratanachat, S., Tresukosol, D. et al. LINE-1 hypomethylation level as a potential prognostic factor for epithelial ovarian cancer. Int. J. Gynecol. Cancer 18, 711-717 (2008).
25. Iramaneerat, K., Rattanatunyong, P., Khemapech, N., Triratanachat, S. & Mutirangura, A. HERV-K hypomethylation in ovarian clear cell carcinoma is associated with a poor prognosis and platinum resistance. Int. J. Gynecol. Cancer 21, 51-57 (2011).
26. Nakkuntod, J., Avihingsanon, Y., Mutirangura, A. & Hirankarn, N. Hypomethylation of LINE-1 but not Alu in lymphocyte subsets of systemic lupus erythematosus patients. Clinica chimica acta; Int. J. Clin. Chem. 412, 1457-1461 (2011).
27. Jintaridth, P. & Mutirangura, A. Distinctive patterns of age-dependent hypomethylation in interspersed repetitive sequences. Physiol. Genomics 41, 194-200 (2011).
28. Okada, M., Ogasawara, H., Kaneko, H., Hishikawa, T., Sekigawa, I., Hashimoto, H. et al. Role of DNA methylation in transcription of human endogenous retrovirus in the pathogenesis of systemic lupus erythematosus. J. Rheumatol. 29, 1678-1682 (2002).
29. Piotrowski, P. C., Duriagin, S. & Jagodzinski, P. P. Expression of human endogenous retrovirus clone 4-1 may correlate with blood plasma concentration of anti-U1 RNP and anti-Sm nuclear antibodies. Clin. Rheumatol. 24, 620-624 (2005).
30. Ejtehadi, H. D., Freimanis, G. L., Ali, H. A., Bowman, S., Alavi, A., Axford, J. et al. The potential role of human endogenous retrovirus K10 in the pathogenesis of rheumatoid arthritis: a preliminary study. Ann. Rheum. Dis. 65, 612-616 (2006).
31. Garaud, S., Le Dantec, C., Jousse-Joulin, S., Hanrotel-Saliou, C., Saraux, A., Mageed, R. A. et al. IL-6 modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation. J. Immunol. 182, 5623-5632 (2009).
32. Gladman, D. D., Ibanez, D. & Urowitz, M. B. Systemic lupus erythematosus disease activity index 2000. J. Rheumatol. 29, 288-291 (2002).
33. Uribe, A. G., Vila, L. M., McGwin, G. Jr, Sanchez, M. L., Reveille, J. D. & Alarcon, G. S. The Systemic lupus activity measure-revised, the Mexican Systemic Lupus Erythematosus Disease Activity Index (SLEDAI), and a modified SLEDAI-2K are adequate instruments to measure disease activity in systemic lupus erythematosus. J. Rheumatol. 31, 1934-1940 (2004).
34. Moskalev, E. A., Zavgorodnij, M. G., Majorova, S. P., Vorobjev, I. A., Jandaghi, P., Bure, I. V. et al. Correction of PCR-bias in quantitative DNA methylation studies by means of cubic polynomial regression. Nucleic Acids Res. 39, e77 (2011).
35. Miller, S. A., Dykes, D. D. & Polesky, H. F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16, 1215 (1988).
36. Jurka, J. Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16, 418-420 (2000).
37. Tusnady, G. E., Simon, I., Varadi, A. & Aranyi, T. BiSearch: primer-design and search tool for PCR on bisulfite-treated genomes. Nucleic Acids Res. 33, e9 (2005).
38. Aranyi, T., Varadi, A., Simon, I. & Tusnady, G. E. The BiSearch web server. BMC Bioinform. 7, 431 (2006).
39. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M. et al. The human genome browser at UCSC. Genome Res. 12, 996-1006 (2002).
40. Benachenhou, F., Jern, P., Oja, M., Sperber, G., Blikstad, V., Somervuo, P. et al. Evolutionary conservation of orthoretroviral long terminal repeats (LTRs) and ab initio detection of single LTRs in genomic data. PLoS One 4, e5179 (2009).
41. Taruscio, D., Floridia, G., Zoraqi, G. K., Mantovani, A. & Falbo, V. Organization and integration sites in the human genome of endogenous retroviral sequences belonging to HERV-E family. Mamm. Genome 13, 216-222 (2002).
42. Reiss, D., Zhang, Y. & Mager, D. L. Widely variable endogenous retroviral methylation levels in human placenta. Nucleic Acids Res. 35, 4743-4754 (2007).
43. Belshaw, R., Dawson, A. L., Woolven-Allen, J., Redding, J., Burt, A. & Tristem, M. Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J. Virol. 79, 12507-12514 (2005).
44. Balada, E., Ordi-Ros, J. & Vilardell-Tarres, M. Molecular mechanisms mediated by human endogenous retroviruses (HERVs) in autoimmunity. Rev. Med. Virol. 19, 273-286 (2009).
45. Crow, M. K. Long interspersed nuclear elements (LINE-1): potential triggers of systemic autoimmune disease. Autoimmunity 43, 7-16 (2010).
46. Perl, A., Fernandez, D., Telarico, T. & Phillips, P. E. Endogenous retroviral pathogenesis in lupus. Curr. Opin. Rheumatol. 22, 483-492 (2010).
47. Wang, G. S., Zhang, M., Li, X. P., Zhang, H., Chen, W., Kan, M. et al. Ultraviolet B exposure of peripheral blood mononuclear cells of patients with systemic lupus erythematosus inhibits DNA methylation. Lupus 18, 1037-1044 (2009).