Identification of novel markers in rheumatoid arthritis through integrated analysis of DNA methylation and microRNA expression

Journal of Autoimmunity

Volumn 41, Issue , 2013, Pages 6-16

  de la Rica, Lorenzo ^a   Urquiza, José M ^a   Gómez Cabrero, David ^b   Islam, Abul B M M K ^c,d   López Bigas, Nuria ^c,e   Tegnér, Jesper ^b   Toes, René E M ^f   Ballestar, Esteban ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b Stockholm University   (Sweden)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d UNIVERSITY OF DHAKA   (Bangladesh)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DNA methylation; Epigenetic; Integration; MicroRNAs; Rheumatoid arthritis; Rheumatoid arthritis synovial fibroblasts

Indexed keywords

CAPN8 PROTEIN; DIPEPTIDYL PEPTIDASE IV; HOX PROTEIN; INTERLEUKIN 6 RECEPTOR; MICRORNA; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA METHYLATION; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PHENOTYPE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SCREENING; SYNOVIOCYTE;

ARTHRITIS, RHEUMATOID; CPG ISLANDS; DNA METHYLATION; FIBROBLASTS; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOARTHRITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNOVIAL MEMBRANE;

EID: 84875943253     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2012.12.005     Document Type: Article

References (68)

1. Lefevre S., Knedla A., Tennie C., Kampmann A., Wunrau C., Dinser R., et al. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints. Nat Med 2009, 15:1414-1420.
2. Tolboom T.C., van der Helm-Van Mil A.H., Nelissen R.G., Breedveld F.C., Toes R.E., Huizinga T.W. Invasiveness of fibroblast-like synoviocytes is an individual patient characteristic associated with the rate of joint destruction in patients with rheumatoid arthritis. Arthritis Rheum 2005, 52:1999-2002.
3. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev 2011, 25:1010-1022.
4. Ball M.P., Li J.B., Gao Y., Lee J.H., LeProust E.M., Park I.H., et al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 2009, 27:361-368.
5. Rauch T.A., Wu X., Zhong X., Riggs A.D., Pfeifer G.P. A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci U S A 2009, 106:671-678.
6. Tili E., Michaille J.J., Costinean S., Croce C.M. MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheumatol 2008, 4:534-541.
7. Selmi C., Lu Q., Humble M.C. Heritability versus the role of the environment in autoimmunity. J Autoimmun 2012, 39:249-252.
8. Ballestar E. Epigenetics lessons from twins: prospects for autoimmune disease. Clin Rev Allergy Immunol 2010, 39:30-41.
9. Miller F.W., Pollard K.M., Parks C.G., Germolec D.R., Leung P.S., Selmi C., et al. Criteria for environmentally associated autoimmune diseases. J Autoimmun 2012, 39:253-258.
10. Miller F.W., Alfredsson L., Costenbader K.H., Kamen D.L., Nelson L.M., Norris J.M., et al. Epidemiology of environmental exposures and human autoimmune diseases: findings from a National Institute of Environmental Health Sciences Expert Panel Workshop. J Autoimmun 2012, 39:259-271.
11. Selmi C., Leung P.S., Sherr D.H., Diaz M., Nyland J.F., Monestier M., et al. Mechanisms of environmental influence on human autoimmunity: a national institute of environmental health sciences expert panel workshop. J Autoimmun 2012, 39:272-284.
12. Germolec D., Kono D.H., Pfau J.C., Pollard K.M. Animal models used to examine the role of the environment in the development of autoimmune disease: findings from an NIEHS Expert Panel Workshop. J Autoimmun 2012, 39:285-293.
13. Neidhart M., Rethage J., Kuchen S., Kunzler P., Crowl R.M., Billingham M.E., et al. Retrotransposable L1 elements expressed in rheumatoid arthritis synovial tissue: association with genomic DNA hypomethylation and influence on gene expression. Arthritis Rheum 2000, 43:2634-2647.
14. Nile C.J., Read R.C., Akil M., Duff G.W., Wilson A.G. Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum 2008, 58:2686-2693.
15. Karouzakis E., Rengel Y., Jungel A., Kolling C., Gay R.E., Michel B.A., et al. DNA methylation regulates the expression of CXCL12 in rheumatoid arthritis synovial fibroblasts. Genes Immun 2011, 12:643-652.
16. Takami N., Osawa K., Miura Y., Komai K., Taniguchi M., Shiraishi M., et al. Hypermethylated promoter region of DR3, the death receptor 3 gene, in rheumatoid arthritis synovial cells. Arthritis Rheum 2006, 54:779-787.
17. Nakano K., Whitaker J.W., Boyle D.L., Wang W., Firestein G.S. DNA methylome signature in rheumatoid arthritis. Ann Rheum Dis 2012.
18. Niederer F., Trenkmann M., Ospelt C., Karouzakis E., Neidhart M., Stanczyk J., et al. Down-regulation of microRNA-34a* in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance. Arthritis Rheum 2012, 64:1771-1779.
19. Nakamachi Y., Kawano S., Takenokuchi M., Nishimura K., Sakai Y., Chin T., et al. MicroRNA-124a is a key regulator of proliferation and monocyte chemoattractant protein 1 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Arthritis Rheum 2009, 60:1294-1304.
20. Stanczyk J., Ospelt C., Karouzakis E., Filer A., Raza K., Kolling C., et al. Altered expression of microRNA-203 in rheumatoid arthritis synovial fibroblasts and its role in fibroblast activation. Arthritis Rheum 2011, 63:373-381.
21. Bibikova M., Lin Z., Zhou L., Chudin E., Garcia E.W., Wu B., et al. High-throughput DNA methylation profiling using universal bead arrays. Genome Res 2006, 16:383-393.
22. Dessau R.B., Pipper C.B. "R" -project for statistical computing. Ugeskr Laeger 2008, 170:328-330.
23. Du P., Kibbe W.A., Lin S.M. Lumi: a pipeline for processing illumina microarray. Bioinformatics 2008, 24:1547-1548.
24. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80.
25. Falcon S., Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007, 23:257-258.
26. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and bioconductor 2005, 397-420.
27. Maksimovic J., Gordon L., Oshlack A. SWAN: subset-quantile within array normalization for illumina infinium HumanMethylation450 BeadChips. Genome Biol 2012, 13:R44.
28. Touleimat N., Tost J. Complete pipeline for infinium((R)) Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics 2012, 4:325-341.
29. Aryee M.J., Wu Z., Ladd-Acosta C., Herb B., Feinberg A.P., Yegnasubramanian S., et al. Accurate genome-scale percentage DNA methylation estimates from microarray data. Biostatistics 2011, 12:197-210.
30. Herman J.G., Graff J.R., Myohanen S., Nelkin B.D., Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996, 93:9821-9826.
31. Del Rey M.J., Usategui A., Izquierdo E., Canete J.D., Blanco F.J., Criado G., et al. Transcriptome analysis reveals specific changes in osteoarthritis synovial fibroblasts. Ann Rheum Dis 2012, 71:275-280.
32. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
33. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., et al. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500.
34. Kertesz M., Iovino N., Unnerstall U., Gaul U., Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007, 39:1278-1284.
35. Griffiths-Jones S., Grocock R.J., van Dongen S., Bateman A., Enright A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006, 34:D140-D144.
36. Betel D., Wilson M., Gabow A., Marks D.S., Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008, 36:D149-D153.
37. Wang X., El Naqa I.M. Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 2008, 24:325-332.
38. Vergoulis T., Vlachos I.S., Alexiou P., Georgakilas G., Maragkakis M., Reczko M., et al. TarBase 6.0: capturing the exponential growth of miRNA targets with experimental support. Nucleic Acids Res 2011, 40:D222-D229.
39. Xiao F., Zuo Z., Cai G., Kang S., Gao X., Li T. miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res 2009, 37:D105-D110.
40. Yang J.H., Li J.H., Shao P., Zhou H., Chen Y.Q., Qu L.H. starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 2011, 39:D202-D209.
41. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39:D152-D157.
42. Al-Shahrour F., Diaz-Uriarte R., Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 2004, 20:578-580.
43. Sturn A., Quackenbush J., Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002, 18:207-208.
44. Thompson C.A. FDA approves tocilizumab to treat rheumatoid arthritis. Am J Health Syst Pharm 2010, 67:254.
45. Sun H., Gong S., Carmody R.J., Hilliard A., Li L., Sun J., et al. TIPE2, a negative regulator of innate and adaptive immunity that maintains immune homeostasis. Cell 2008, 133:415-426.
46. Swan C., Duroudier N.P., Campbell E., Zaitoun A., Hastings M., Dukes G.E., et al. Identifying and testing candidate genetic polymorphisms in the irritable bowel syndrome (IBS): association with TNFSF15 and TNFalpha. Gut 2012.
47. Yazbeck R., Howarth G.S., Abbott C.A. Dipeptidyl peptidase inhibitors, an emerging drug class for inflammatory disease?. Trends Pharmacol Sci 2009, 30:600-607.
48. Ruth J.H., Shahrara S., Park C.C., Morel J.C., Kumar P., Qin S., et al. Role of macrophage inflammatory protein-3alpha and its ligand CCR6 in rheumatoid arthritis. Lab Invest 2003, 83:579-588.
49. Waldburger J.M., Palmer G., Seemayer C., Lamacchia C., Finckh A., Christofilopoulos P., et al. Autoimmunity and inflammation are independent of class II transactivator type PIV-dependent class II major histocompatibility complex expression in peripheral tissues during collagen-induced arthritis. Arthritis Rheum 2011, 63:3354-3363.
50. Li G., Zhang Y., Qian Y., Zhang H., Guo S., Sunagawa M., et al. Interleukin-17A promotes rheumatoid arthritis synoviocytes migration and invasion under hypoxia by increasing MMP2 and MMP9 expression through NF-kappaB/HIF-1alpha pathway. Mol Immunol 2012, 53:227-236.
51. Solau-Gervais E., Zerimech F., Lemaire R., Fontaine C., Huet G., Flipo R.M. Cysteine and serine proteases of synovial tissue in rheumatoid arthritis and osteoarthritis. Scand J Rheumatol 2007, 36:373-377.
52. Kawano S., Nakamachi Y. miR-124a as a key regulator of proliferation and MCP-1 secretion in synoviocytes from patients with rheumatoid arthritis. Ann Rheum Dis 2011, 70(Suppl. 1):i88-91.
53. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004, 5:522-531.
54. Ngalamika O., Zhang Y., Yin H., Zhao M., Gershwin M.E., Lu Q. Epigenetics, autoimmunity and hematologic malignancies: a comprehensive review. J Autoimmun 2012, 39:451-465.
55. Nakasa T., Miyaki S., Okubo A., Hashimoto M., Nishida K., Ochi M., et al. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum 2008, 58:1284-1292.
56. Kobayashi K., Yagasaki M., Harada N., Chichibu K., Hibi T., Yoshida T., et al. Detection of Fcgamma binding protein antigen in human sera and its relation with autoimmune diseases. Immunol Lett 2001, 79:229-235.
57. Nishimoto N., Kishimoto T., Yoshizaki K. Anti-interleukin 6 receptor antibody treatment in rheumatic disease. Ann Rheum Dis 2000, 59(Suppl. 1):i21-i27.
58. Watanabe Y., Takeuchi K., Higa Onaga S., Sato M., Tsujita M., Abe M., et al. Chondroitin sulfate N-acetylgalactosaminyltransferase-1 is required for normal cartilage development. Biochem J 2010, 432:47-55.
59. Sato T., Kudo T., Ikehara Y., Ogawa H., Hirano T., Kiyohara K., et al. Chondroitin sulfate N-acetylgalactosaminyltransferase 1 is necessary for normal endochondral ossification and aggrecan metabolism. J Biol Chem 2011, 286:5803-5812.
60. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., et al. MIF signal transduction initiated by binding to CD74. J Exp Med 2003, 197:1467-1476.
61. Simhadri V.L., Hansen H.P., Simhadri V.R., Reiners K.S., Bessler M., Engert A., et al. A novel role for reciprocal CD30-CD30L signaling in the cross-talk between natural killer and dendritic cells. Biol Chem 2012, 393:101-106.
62. Matsui T., Akahoshi T., Namai R., Hashimoto A., Kurihara Y., Rana M., et al. Selective recruitment of CCR6-expressing cells by increased production of MIP-3 alpha in rheumatoid arthritis. Clin Exp Immunol 2001, 125:155-161.
63. Ospelt C., Mertens J.C., Jungel A., Brentano F., Maciejewska-Rodriguez H., Huber L.C., et al. Inhibition of fibroblast activation protein and dipeptidylpeptidase 4 increases cartilage invasion by rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 2010, 62:1224-1235.
64. Buhligen J., Himmel M., Gebhardt C., Simon J.C., Ziegler W., Averbeck M. Lysophosphatidylcholine-mediated functional inactivation of syndecan-4 results in decreased adhesion and motility of dendritic cells. J Cell Physiol 2010, 225:905-914.
65. Nishimura W.E., Costallat L.T., Fernandes S.R., Conde R.A., Bertolo M.B. Association of HLA-DRB5*01 with protection against cutaneous manifestations of rheumatoid vasculitis in Brazilian patients. Rev Bras Rheumatol 2012, 52:366-374.
66. Griffiths R.J., Smith M.A., Roach M.L., Stock J.L., Stam E.J., Milici A.J., et al. Collagen-induced arthritis is reduced in 5-lipoxygenase-activating protein-deficient mice. J Exp Med 1997, 185:1123-1129.
67. Manzo A., Vitolo B., Humby F., Caporali R., Jarrossay D., Dell'accio F., et al. Mature antigen-experienced T helper cells synthesize and secrete the B cell chemoattractant CXCL13 in the inflammatory environment of the rheumatoid joint. Arthritis Rheum 2008, 58:3377-3387.
68. Pradhan D., Morrow J. The spectrin-ankyrin skeleton controls CD45 surface display and interleukin-2 production. Immunity 2002, 17:303-315.