Twin DNA Methylation Profiling Reveals Flare-Dependent Interferon Signature and B Cell Promoter Hypermethylation in Systemic Lupus Erythematosus

Arthritis and Rheumatology

Volumn 70, Issue 6, 2018, Pages 878-890

  Ulff Møller, Constance J ^a,b   Asmar, Fazila ^c   Liu, Yi ^b   Svendsen, Anders J ^d   Busato, Florence ^b   Grønbæk, Kirsten ^a   Tost, Jörg ^b   Jacobsen, Søren ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CEA Fontenay aux Roses Bâtiment 61   (France)

^c Rigshospitalet   (Denmark)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; ALLOPHYCOCYANIN; ATP13A3 PROTEIN; B3GALT4 PROTEIN; C1ORF65 PROTEIN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; CPSF4L PROTEIN; DISCOIDIN DOMAIN RECEPTOR 1; DOUBLE STRANDED DNA; DTX3L PROTEIN; E1A ASSOCIATED P300 PROTEIN; EIF2AK2 PROTEIN; GTF2A1L PROTEIN; IFI44L PROTEIN; IFITM1 PROTEIN; INTERFERON; LGALS3BP PROTEIN; LOXL1 PROTEIN; NIN PROTEIN; NWD1 PROTEIN; PARP9 PROTEIN; PROTEIN; TACSTD2 PROTEIN; TRANSCRIPTION INTERMEDIARY FACTOR 1 BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 5; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; BLOOD ANALYSIS; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELLS BY BODY ANATOMY; CLINICAL ARTICLE; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DISEASE EXACERBATION; DIZYGOTIC TWINS; DNA METHYLATION; FEMALE; GENOME-WIDE ASSOCIATION STUDY; GRANULOCYTE; HUMAN; INTRACELLULAR SPACE; MALE; MIDDLE AGED; MONOCYTE; MONOZYGOTIC TWINS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; SYSTEMIC LUPUS ERYTHEMATOSUS; YOUNG ADULT; CASE CONTROL STUDY; GENETIC EPIGENESIS; GENETICS; METABOLISM; RECURRENT DISEASE; TWINS;

ADULT; AGED; B-LYMPHOCYTES; CASE-CONTROL STUDIES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INTERFERONS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; SYMPTOM FLARE UP; TWINS, MONOZYGOTIC; YOUNG ADULT;

EID: 85046670210     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.40422     Document Type: Article

References (45)

1. Yang J, Visscher PM, Wray NR. Sporadic cases are the norm for complex disease. Eur J Hum Genet 2010;18:1039–43.
2. Kuo CF, Grainge MJ, Valdes AM, See LC, Luo SF, Yu KH, et al. Familial aggregation of systemic lupus erythematosus and coaggregation of autoimmune diseases in affected families. JAMA Intern Med 2015;175:1518–26.
3. Lawrence JS, Martins CL, Drake GL. A family survey of lupus erythematosus. Part 1. Heritability. J Rheumatol 1987;14:913–21.
4. Morris DL, Sheng Y, Zhang Y, Wang YF, Zhu Z, Tombleson P, et al. Genome-wide association meta-analysis in Chinese and European individuals identifies ten new loci associated with systemic lupus erythematosus. Nat Genet 2016;48:940–6.
5. Ulff-Møller CJ, Svendsen AJ, Viemose LN, Jacobsen S. Concordance of autoimmune disease in a nationwide Danish systemic lupus erythematosus twin cohort. Semin Arthritis Rheum 2018;47:538–44.
6. Ballestar E. Epigenetic alterations in autoimmune rheumatic diseases. Nat Rev Rheumatol 2011;7:263–71.
7. Javierre BM, Fernandez AF, Richter J, Al-Shahrour F, Ignacio Martin-Subero J, Rodriguez-Ubreva J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res 2010;20:170–9.
8. Absher DM, Li X, Waite LL, Gibson A, Roberts K, Edberg J, et al. Genome-wide DNA methylation analysis of systemic lupus erythematosus reveals persistent hypomethylation of interferon genes and compositional changes to CD4+ T-cell populations. PLoS Genet 2013;9:e1003678.
9. Jeffries M, Dozmorov M, Tang Y, Merrill JT, Wren JD, Sawalha AH. Genome-wide DNA methylation patterns in CD4+ T cells from patients with systemic lupus erythematosus. Epigenetics 2011;6:593–601.
10. Coit P, Jeffries M, Altorok N, Dozmorov MG, Koelsch KA, Wren JD, et al. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naïve CD4+ T cells from lupus patients. J Autoimmun 2013;43:78–84.
11. Coit P, Yalavarthi S, Ognenovski M, Zhao W, Hasni S, Wren JD, et al. Epigenome profiling reveals significant DNA demethylation of interferon signature genes in lupus neutrophils. J Autoimmun 2015;58:59–66.
12. Ballestar E. Epigenetics lessons from twins: prospects for autoimmune disease. Clin Rev Allergy Immunol 2010;39:30–41.
13. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén SE, Greco D, et al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One 2012;7:e41361.
14. Liu Z, Davidson A. Taming lupus: a new understanding of pathogenesis is leading to clinical advances. Nat Med 2012;18:871–82.
15. Lynge E, Sandegaard JL, Rebolj M. The Danish National Patient Register. Scand J Public Health 2011;39:30–3.
16. Skytthe A, Ohm Kyvik K, Vilstrup Holm N, Christensen K. The Danish Twin Registry. Scand J Public Health 2011;39:75–8.
17. Pedersen CB, Gotzsche H, Moller JO, Mortensen PB. The Danish Civil Registration System: a cohort of eight million persons. Dan Med Bull 2006;53:441–9.
18. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271–7.
19. Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol 2002;29:288–91.
20. Miceli-Richard C, Wang-Renault SF, Boudaoud S, Busato F, Lallemand C, Bethune K, et al. Overlap between differentially methylated DNA regions in blood B lymphocytes and genetic at-risk loci in primary Sjögren's syndrome. Ann Rheum Dis 2016;75:933–40.
21. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nat Protoc 2007;2:2265–75.
22. ® Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics 2012;4:325–41.
23. The 1000 Genomes Project Consortium, McVean GA, Altshuler DM, Durbin RM, Abecasis GR, Bentley DR, et al. An integrated map of genetic variation from 1,092 human genomes. Nature 2012;491:56–65.
24. Chen Y, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, et al. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics 2013;8:203–9.
25. Medvedeva YA, Lennartsson A, Ehsani R, Kulakovskiy IV, Vorontsov IE, Panahandeh P, et al. EpiFactors: a comprehensive database of human epigenetic factors and complexes. Database (Oxford) 2015;2015:bav067.
26. Teschendorff AE, Gao Y, Jones A, Ruebner M, Beckmann MW, Wachter DL, et al. DNA methylation outliers in normal breast tissue identify field defects that are enriched in cancer. Nat Commun 2016;7:10478.
27. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Cumming H, et al. Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res 2013;41:D1040–6.
28. Bock C, Halbritter F, Carmona FJ, Tierling S, Datlinger P, Assenov Y, et al. Quantitative comparison of DNA methylation assays for biomarker development and clinical applications. Nat Biotechnol 2016;34:726–37.
29. Zhao M, Zhou Y, Zhu B, Wan M, Jiang T, Tan Q, et al. IFI44L promoter methylation as a blood biomarker for systemic lupus erythematosus. Ann Rheum Dis 2016;75:1998–2006.
30. Coit P, Renauer P, Jeffries MA, Merrill JT, McCune WJ, Maksimowicz-McKinnon K, et al. Renal involvement in lupus is characterized by unique DNA methylation changes in naïve CD4+ T cells. J Autoimmun 2015;61:29–35.
31. Imgenberg-Kreuz J, Sandling JK, Almlöf JC, Nordlund J, Signér L, Norheim KB, et al. Genome-wide DNA methylation analysis in multiple tissues in primary Sjögren's syndrome reveals regulatory effects at interferon-induced genes. Ann Rheum Dis 2016;75:2029–36.
32. Higgs BW, Liu Z, White B, Zhu W, White WI, Morehouse C, et al. Patients with systemic lupus erythematosus, myositis, rheumatoid arthritis and scleroderma share activation of a common type I interferon pathway. Ann Rheum Dis 2011;70:2029–36.
33. Kulis M, Merkel A, Heath S, Queirós AC, Schuyler RP, Castellano G, et al. Whole-genome fingerprint of the DNA methylome during human B cell differentiation. Nat Genet 2015;47:746.
34. Salazar-Camarena DC, Ortiz-Lazareno PC, Cruz A, Oregon-Romero E, Machado-Contreras JR, Muñoz-Valle JF, et al. Association of BAFF, APRIL serum levels, BAFF-R, TACI and BCMA expression on peripheral B-cell subsets with clinical manifestations in systemic lupus erythematosus. Lupus 2016;25:582–92.
35. Becker AM, Dao KH, Han BK, Kornu R, Lakhanpal S, Mobley AB, et al. SLE peripheral blood B cell, T cell and myeloid cell transcriptomes display unique profiles and each subset contributes to the interferon signature. PLoS One 2013;8:e67003.
36. Müller G, Höpken UE, Lipp M. The impact of CCR7 and CXCR5 on lymphoid organ development and systemic immunity. Immunol Rev 2003;195:117–35.
37. Hildebrand JM, Yi Z, Buchta CM, Poovassery J, Stunz LL, Bishop GA. Roles of tumor necrosis factor receptor associated factor 3 (TRAF3) and TRAF5 in immune cell functions. Immunol Rev 2011;244:55–74.
38. Yoshimura T, Matsuyama W, Kamohara H. Discoidin domain receptor 1: a new class of receptor regulating leukocyte-collagen interaction. Immunol Res 2005;31:219–30.
39. Glossop JR, Emes RD, Nixon NB, Packham JC, Fryer AA, Mattey DL, et al. Genome-wide profiling in treatment-naive early rheumatoid arthritis reveals DNA methylome changes in T and B lymphocytes. Epigenomics 2016;8:209–24.
40. Mageed R, Isenberg D. Tumour necrosis factor α in systemic lupus erythematosus and anti-DNA autoantibody production. Lupus 2002;11:850–5.
41. Jacob N, Stohl W. Cytokine disturbances in systemic lupus erythematosus. Arthritis Res Ther 2011;13:228.
42. Moulis G, Sommet A, Lapeyre-Mestre M, Montastruc JL. Is the risk of tumour necrosis factor inhibitor-induced lupus or lupus-like syndrome the same with monoclonal antibodies and soluble receptor? A case/non-case study in a nationwide pharmacovigilance database. Rheumatology (Oxford) 2014;53:1864–71.
43. Kalkhoven E. CBP and p300: HATs for different occasions. Biochem Pharmacol 2004;68:1145–55.
44. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 2011;471:189–95.
45. Forster N, Gallinat S, Jablonska J, Weiss S, Elsässer HP, Lutz W. Mice erythematosus-like autoimmune disease in suppresses systemic lupus p300 protein acetyltransferase activity p300 protein acetyltransferase activity suppresses systemic lupus erythematosus-like autoimmune disease in mice 1. J Immunol 2007;178:6941–8.