Epigenetic Changes in Chronic Inflammatory Diseases

Advances in Protein Chemistry and Structural Biology

Volumn 106, Issue , 2017, Pages 139-189

  Fogel, O ^a,b   Richard Miceli, C ^a,c   Tost, J ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

Behcet's disease; Crohn's disease; DNA methylation; Epigenetics; EWAS; Histone modifications; Inflammatory bowel disease; Psoriasis; Spondyloarthritis; Ulcerative colitis

Indexed keywords

DNA; HISTONE; RESTRICTION ENDONUCLEASE; UNTRANSLATED RNA;

B LYMPHOCYTE; CHRONIC DISEASE; DISEASE PREDISPOSITION; DNA METHYLATION; DYSBIOSIS; EPIGENETICS; GENETIC VARIATION; HISTONE MODIFICATION; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATORY BOWEL DISEASE; INFLAMMATORY DISEASE; INTESTINE FLORA; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; PATHOPHYSIOLOGY; PROTEIN PROCESSING; PSORIASIS; RESTRICTION MAPPING; SPONDYLARTHRITIS; T LYMPHOCYTE; GENETIC EPIGENESIS; GENETICS; INFLAMMATION;

CHRONIC DISEASE; EPIGENESIS, GENETIC; HUMANS; INFLAMMATION;

EID: 85006003432     PISSN: 18761623     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.apcsb.2016.09.003     Document Type: Chapter

References (193)

1. Abhishek, S., Palamadai Krishnan, S., Epidermal differentiation complex: A review on its epigenetic regulation and potential drug targets. Cell Journal 18:1 (2016), 1–6.
2. Absher, D.M., Li, X., Waite, L.L., 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 Genetics, 9(8), 2013, e1003678, 10.1371/journal.pgen.1003678.
3. Adams, D., Altucci, L., Antonarakis, S.E., Ballesteros, J., Beck, S., Bird, A., et al. BLUEPRINT to decode the epigenetic signature written in blood. Nature Biotechnology 30:3 (2012), 224–226, 10.1038/nbt.2153.
4. Adams, A.T., Kennedy, N.A., Hansen, R., Ventham, N.T., O'Leary, K.R., Drummond, H.E., et al. Two-stage genome-wide methylation profiling in childhood-onset Crohn's disease implicates epigenetic alterations at the VMP1/MIR21 and HLA loci. Inflammatory Bowel Diseases 20:10 (2014), 1784–1793, 10.1097/MIB.0000000000000179.
5. Ahmadi, A., Polyak, S., Draganov, P.V., Colorectal cancer surveillance in inflammatory bowel disease: The search continues. World Journal of Gastroenterology 15:1 (2009), 61–66.
6. Ahuja, N., Li, Q., Mohan, A.L., Baylin, S.B., Issa, J.P., Aging and DNA methylation in colorectal mucosa and cancer. Cancer Research 58:23 (1998), 5489–5494.
7. Alegria-Torres, J.A., Baccarelli, A., Bollati, V., Epigenetics and lifestyle. Epigenomics 3:3 (2011), 267–277, 10.2217/epi.11.22.
8. Allan, R.S., The epigenetic mechanisms that underlie health and disease. Immunology and Cell Biology 93:3 (2015), 224–225, 10.1038/icb.2015.8.
9. Ansel, K.M., Djuretic, I., Tanasa, B., Rao, A., Regulation of Th2 differentiation and Il4 locus accessibility. Annual Review of Immunology 24 (2006), 607–656, 10.1146/annurev.immunol.23.021704.115821.
10. Ansel, K.M., Lee, D.U., Rao, A., An epigenetic view of helper T cell differentiation. Nature Immunology 4:7 (2003), 616–623, 10.1038/ni0703-616.
11. Azarschab, P., Porschen, R., Gregor, M., Blin, N., Holzmann, K., Epigenetic control of the E-cadherin gene (CDH1) by CpG methylation in colectomy samples of patients with ulcerative colitis. Genes, Chromosomes & Cancer 35:2 (2002), 121–126, 10.1002/gcc.10101.
12. Bai, A.H., Wu, W.K., Xu, L., Wong, S.H., Go, M.Y., Chan, A.W., et al. Dysregulated lysine acetyltransferase 2B promotes inflammatory bowel disease pathogenesis through transcriptional repression of interleukin-10. Journal of Crohn's & Colitis 10:6 (2016), 726–734, 10.1093/ecco-jcc/jjw020.
13. Balasa, A., Gathungu, G., Kisfali, P., Smith, E.O., Cho, J.H., Melegh, B., et al. Assessment of DNA methylation at the interferon regulatory factor 5 (IRF5) promoter region in inflammatory bowel diseases. International Journal of Colorectal Disease 25:5 (2010), 553–556, 10.1007/s00384-010-0874-0.
14. Ballestar, E., Epigenetics lessons from twins: Prospects for autoimmune disease. Clinical Reviews in Allergy & Immunology 39:1 (2010), 30–41, 10.1007/s12016-009-8168-4.
15. Bao, Y., Cao, X., Epigenetic control of B cell development and B-cell-related immune disorders. Clinical Reviews in Allergy & Immunology 50:3 (2016), 301–311, 10.1007/s12016-015-8494-7.
16. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., et al. High-resolution profiling of histone methylations in the human genome. Cell 129:4 (2007), 823–837.
17. Baylin, S.B., Jones, P.A., A decade of exploring the cancer epigenome—Biological and translational implications. Nature Reviews. Cancer 11:10 (2011), 726–734, 10.1038/nrc3130.
18. Berni Canani, R., Di Costanzo, M., Leone, L., The epigenetic effects of butyrate: Potential therapeutic implications for clinical practice. Clinical Epigenetics, 4(1), 2012, 4, 10.1186/1868-7083-4-4.
19. Bibikova, M., Le, J., Barnes, B., Saedinia-Melnyk, S., Zhou, L., Shen, R., et al. Genome-wide DNA methylation profiling using Infinium((R)) assay. Epigenomics 1:1 (2009), 177–200, 10.2217/epi.09.14.
20. Bird, A., DNA methylation patterns and epigenetic memory. Genes & Development 16:1 (2002), 6–21.
21. Blander, J.M., Death in the intestinal epithelium-basic biology and implications for inflammatory bowel disease. The FEBS Journal 283:14 (2016), 2720–2730, 10.1111/febs.13771.
22. Blueprint Consortium, Quantitative comparison of DNA methylation assays for biomarker development and clinical applications. Nature Biotechnology 34:7 (2016), 726–737, 10.1038/nbt.3605.
23. Bock, C., Tomazou, E.M., Brinkman, A.B., Muller, F., Simmer, F., Gu, H., et al. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nature Biotechnology 28:10 (2010), 1106–1114, 10.1038/nbt.1681 nbt.1681 [pii].
24. Borno, S.T., Fischer, A., Kerick, M., Falth, M., Laible, M., Brase, J.C., et al. Genome-wide DNA methylation events in TMPRSS2-ERG fusion-negative prostate cancers implicate an EZH2-dependent mechanism with miR-26a hypermethylation. Cancer Discovery 2:11 (2012), 1024–1035, 10.1158/2159-8290.CD-12-0041.
25. Bowcock, A.M., The genetics of psoriasis and autoimmunity. Annual Review of Genomics and Human Genetics 6 (2005), 93–122, 10.1146/annurev.genom.6.080604.162324.
26. Brandtzaeg, P., Update on mucosal immunoglobulin A in gastrointestinal disease. Current Opinion in Gastroenterology 26:6 (2010), 554–563, 10.1097/MOG.0b013e32833dccf8.
27. Brandtzaeg, P., Carlsen, H.S., Halstensen, T.S., The B-cell system in inflammatory bowel disease. Advances in Experimental Medicine and Biology 579 (2006), 149–167, 10.1007/0-387-33778-4_10.
28. Brinkman, A.B., Simmer, F., Ma, K., Kaan, A., Zhu, J., Stunnenberg, H.G., Whole-genome DNA methylation profiling using MethylCap-seq. Methods 52:3 (2010), 232–236, 10.1016/j.ymeth.2010.06.012 S1046-2023(10)00166-0 [pii].
29. Campan, M., Moffitt, M., Houshdaran, S., Shen, H., Widschwendter, M., Daxenbichler, G., et al. Genome-scale screen for DNA methylation-based detection markers for ovarian cancer. PLoS One, 6(12), 2011, e28141, 10.1371/journal.pone.0028141 PONE-D-11-08732 [pii].
30. Cavazza, A., Miccio, A., Romano, O., Petiti, L., Malagoli Tagliazucchi, G., Peano, C., et al. Dynamic transcriptional and epigenetic regulation of human epidermal Keratinocyte differentiation. Stem Cell Reports 6:4 (2016), 618–632, 10.1016/j.stemcr.2016.03.003.
31. Chapman, C.G., Pekow, J., The emerging role of miRNAs in inflammatory bowel disease: A review. Therapeutic Advances in Gastroenterology 8:1 (2015), 4–22, 10.1177/1756283X14547360.
32. Chen, M., Chen, Z.Q., Cui, P.G., Yao, X., Li, Y.M., Li, A.S., et al. The methylation pattern of p16INK4a gene promoter in psoriatic epidermis and its clinical significance. The British Journal of Dermatology 158:5 (2008), 987–993, 10.1111/j.1365-2133.2008.08505.x.
33. Choi, B., Kim, H.A., Suh, C.H., Byun, H.O., Jung, J.Y., Sohn, S., The relevance of miRNA-21 in HSV-induced inflammation in a mouse model. International Journal of Molecular Sciences 16:4 (2015), 7413–7427, 10.3390/ijms16047413.
34. Cohn, S.M., Roth, K.A., Birkenmeier, E.H., Gordon, J.I., Temporal and spatial patterns of transgene expression in aging adult mice provide insights about the origins, organization, and differentiation of the intestinal epithelium. Proceedings of the National Academy of Sciences of the United States of America 88:3 (1991), 1034–1038.
35. Cooke, J., Zhang, H., Greger, L., Silva, A.L., Massey, D., Dawson, C., et al. Mucosal genome-wide methylation changes in inflammatory bowel disease. Inflammatory Bowel Diseases 18:11 (2012), 2128–2137, 10.1002/ibd.22942.
36. Cortese, R., Lu, L., Yu, Y., Ruden, D., Claud, E.C., Epigenome–microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease. Epigenetics 11:3 (2016), 205–215, 10.1080/15592294.2016.1155011.
37. Cottrell, S.E., Distler, J., Goodman, N.S., Mooney, S.H., Kluth, A., Olek, A., et al. A real-time PCR assay for DNA-methylation using methylation-specific blockers. Nucleic Acids Research, 32(1), 2004, e10.
38. Couturier-Maillard, A., Secher, T., Rehman, A., Normand, S., De Arcangelis, A., Haesler, R., et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. The Journal of Clinical Investigation 123:2 (2013), 700–711, 10.1172/JCI62236.
39. de Zoeten, E.F., Wang, L., Sai, H., Dillmann, W.H., Hancock, W.W., Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 138:2 (2010), 583–594, 10.1053/j.gastro.2009.10.037.
40. Deng, X., Su, Y., Wu, H., Wu, R., Zhang, P., Dai, Y., et al. The role of microRNAs in autoimmune diseases with skin involvement. Scandinavian Journal of Immunology 81:3 (2015), 153–165, 10.1111/sji.12261.
41. Djuretic, I.M., Levanon, D., Negreanu, V., Groner, Y., Rao, A., Ansel, K.M., Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nature Immunology 8:2 (2007), 145–153, 10.1038/ni1424.
42. Eads, C.A., Danenberg, K.D., Kawakami, K., Saltz, L.B., Blake, C., Shibata, D., et al. MethyLight: A high-throughput assay to measure DNA methylation. Nucleic Acids Research, 28(8), 2000, e32.
43. Ehrich, M., Nelson, M.R., Stanssens, P., Zabeau, M., Liloglou, T., Xinarianos, G., et al. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America 102:44 (2005), 15785–15790.
44. Ekbom, A., Helmick, C., Zack, M., Adami, H.O., Ulcerative colitis and colorectal cancer. A population-based study. The New England Journal of Medicine 323:18 (1990), 1228–1233, 10.1056/NEJM199011013231802.
45. Ekman, A.K., Enerback, C., Lack of preclinical support for the efficacy of histone deacetylase inhibitors in the treatment of psoriasis. The British Journal of Dermatology 174:2 (2016), 424–426, 10.1111/bjd.14021.
46. Ellinghaus, D., Bethune, J., Petersen, B.S., Franke, A., The genetics of Crohn's disease and ulcerative colitis—Status quo and beyond. Scandinavian Journal of Gastroenterology 50:1 (2015), 13–23, 10.3109/00365521.2014.990507.
47. Farh, K.K., Marson, A., Zhu, J., Kleinewietfeld, M., Housley, W.J., Beik, S., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 518:7539 (2015), 337–343, 10.1038/nature13835.
48. Fleischer, T., Frigessi, A., Johnson, K.C., Edvardsen, H., Touleimat, N., Klajic, J., et al. Genome-wide DNA methylation profiles in progression to in situ and invasive carcinoma of the breast with impact on gene transcription and prognosis. Genome Biology, 15(8), 2014, 435, 10.1186/PREACCEPT-2333349012841587.
49. Fleisher, A.S., Esteller, M., Harpaz, N., Leytin, A., Rashid, A., Xu, Y., et al. Microsatellite instability in inflammatory bowel disease-associated neoplastic lesions is associated with hypermethylation and diminished expression of the DNA mismatch repair gene, hMLH1. Cancer Research 60:17 (2000), 4864–4868.
50. Fofanova, T.Y., Petrosino, J.F., Kellermayer, R., Microbiome–epigenome interactions and the environmental origins of inflammatory bowel diseases. Journal of Pediatric Gastroenterology and Nutrition 62:2 (2016), 208–219, 10.1097/MPG.0000000000000950.
51. Franke, A., McGovern, D.P., Barrett, J.C., Wang, K., Radford-Smith, G.L., Ahmad, T., et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nature Genetics 42:12 (2010), 1118–1125, 10.1038/ng.717.
52. Frommer, M., McDonald, L.E., Millar, D.S., Collis, C.M., Watt, F., Grigg, G.W., et al. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proceedings of the National Academy of Sciences of the United States of America 89:5 (1992), 1827–1831.
53. Gerstein, M.B., Kundaje, A., Hariharan, M., Landt, S.G., Yan, K.K., Cheng, C., et al. Architecture of the human regulatory network derived from ENCODE data. Nature 489:7414 (2012), 91–100, 10.1038/nature11245.
54. Gervin, K., Vigeland, M.D., Mattingsdal, M., Hammero, M., Nygard, H., Olsen, A.O., et al. DNA methylation and gene expression changes in monozygotic twins discordant for psoriasis: Identification of epigenetically dysregulated genes. PLoS Genetics, 8(1), 2012, e1002454, 10.1371/journal.pgen.1002454.
55. Gilmour, D.S., Lis, J.T., Detecting protein–DNA interactions in vivo: Distribution of RNA polymerase on specific bacterial genes. Proceedings of the National Academy of Sciences of the United States of America 81:14 (1984), 4275–4279.
56. Glauben, R., Batra, A., Fedke, I., Zeitz, M., Lehr, H.A., Leoni, F., et al. Histone hyperacetylation is associated with amelioration of experimental colitis in mice. Journal of Immunology 176:8 (2006), 5015–5022.
57. Globisch, D., Munzel, M., Muller, M., Michalakis, S., Wagner, M., Koch, S., et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One, 5(12), 2010, e15367, 10.1371/journal.pone.0015367.
58. Gloria, L., Cravo, M., Pinto, A., de Sousa, L.S., Chaves, P., Leitao, C.N., et al. DNA hypomethylation and proliferative activity are increased in the rectal mucosa of patients with long-standing ulcerative colitis. Cancer 78:11 (1996), 2300–2306.
59. Gonsky, R., Deem, R.L., Targan, S.R., Distinct methylation of IFNG in the gut. Journal of Interferon & Cytokine Research 29:7 (2009), 407–414, 10.1089/jir.2008.0109.
60. Gordon, S., Martinez, F.O., Alternative activation of macrophages: Mechanism and functions. Immunity 32:5 (2010), 593–604, 10.1016/j.immuni.2010.05.007.
61. Grjibovski, A.M., Olsen, A.O., Magnus, P., Harris, J.R., Psoriasis in Norwegian twins: Contribution of genetic and environmental effects. Journal of the European Academy of Dermatology and Venereology 21:10 (2007), 1337–1343, 10.1111/j.1468-3083.2007.02268.x.
62. Gu, X., Nylander, E., Coates, P.J., Fahraeus, R., Nylander, K., Correlation between reversal of DNA methylation and clinical symptoms in psoriatic epidermis following narrow-band UVB phototherapy. The Journal of Investigative Dermatology 135:8 (2015), 2077–2083, 10.1038/jid.2015.128.
63. Guo, H., Zhu, P., Guo, F., Li, X., Wu, X., Fan, X., et al. Profiling DNA methylome landscapes of mammalian cells with single-cell reduced-representation bisulfite sequencing. Nature Protocols 10:5 (2015), 645–659, 10.1038/nprot.2015.039.
64. Guttman-Yassky, E., Suarez-Farinas, M., Chiricozzi, A., Nograles, K.E., Shemer, A., Fuentes-Duculan, J., et al. Broad defects in epidermal cornification in atopic dermatitis identified through genomic analysis. The Journal of Allergy and Clinical Immunology 124:6 (2009), 1235–1244, 10.1016/j.jaci.2009.09.031 e1258.
65. Han, J., Park, S.G., Bae, J.B., Choi, J., Lyu, J.M., Park, S.H., et al. The characteristics of genome-wide DNA methylation in naive CD4 + T cells of patients with psoriasis or atopic dermatitis. Biochemical and Biophysical Research Communications 422:1 (2012), 157–163, 10.1016/j.bbrc.2012.04.128.
66. Harris, R.A., Nagy-Szakal, D., Mir, S.A., Frank, E., Szigeti, R., Kaplan, J.L., et al. DNA methylation-associated colonic mucosal immune and defense responses in treatment-naive pediatric ulcerative colitis. Epigenetics 9:8 (2014), 1131–1137, 10.4161/epi.29446.
67. Harris, R.A., Nagy-Szakal, D., Pedersen, N., Opekun, A., Bronsky, J., Munkholm, P., et al. Genome-wide peripheral blood leukocyte DNA methylation microarrays identified a single association with inflammatory bowel diseases. Inflammatory Bowel Diseases 18:12 (2012), 2334–2341, 10.1002/ibd.22956.
68. Harris, R.A., Shah, R., Hollister, E.B., Tronstad, R.R., Hovdenak, N., Szigeti, R., et al. Colonic mucosal epigenome and microbiome development in children and adolescents. Journal of Immunology Research, 2016, 2016, 10.1155/2016/9170162 Art. ID 9170162.
69. Hasler, R., Feng, Z., Backdahl, L., Spehlmann, M.E., Franke, A., Teschendorff, A., et al. A functional methylome map of ulcerative colitis. Genome Research 22:11 (2012), 2130–2137, 10.1101/gr.138347.112.
70. Hawkes, J.E., Nguyen, G.H., Fujita, M., Florell, S.R., Callis Duffin, K., Krueger, G.G., et al. microRNAs in psoriasis. The Journal of Investigative Dermatology 136:2 (2016), 365–371, 10.1038/JID.2015.409.
71. 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. Proceedings of the National Academy of Sciences of the United States of America 93:18 (1996), 9821–9826.
72. Hoehe, M.R., Kopke, K., Wendel, B., Rohde, K., Flachmeier, C., Kidd, K.K., et al. Sequence variability and candidate gene analysis in complex disease: Association of mu opioid receptor gene variation with substance dependence. Human Molecular Genetics 9:19 (2000), 2895–2908.
73. Hoeksema, M.A., Laan, L.C., Postma, J.J., Cummings, R.D., de Winther, M.P., Dijkstra, C.D., et al. Treatment with Trichuris suis soluble products during monocyte-to-macrophage differentiation reduces inflammatory responses through epigenetic remodeling. The FASEB Journal 30:8 (2016), 2826–2836, 10.1096/fj.201600343R.
74. Hoeksema, M.A., Stoger, J.L., de Winther, M.P., Molecular pathways regulating macrophage polarization: Implications for atherosclerosis. Current Atherosclerosis Reports 14:3 (2012), 254–263, 10.1007/s11883-012-0240-5.
75. Hou, J.K., Abraham, B., El-Serag, H., Dietary intake and risk of developing inflammatory bowel disease: A systematic review of the literature. The American Journal of Gastroenterology 106:4 (2011), 563–573, 10.1038/ajg.2011.44.
76. Hou, R., Yin, G., An, P., Wang, C., Liu, R., Yang, Y., et al. DNA methylation of dermal MSCs in psoriasis: Identification of epigenetically dysregulated genes. Journal of Dermatological Science 72:2 (2013), 103–109, 10.1016/j.jdermsci.2013.07.002.
77. Houseman, E.A., Accomando, W.P., Koestler, D.C., Christensen, B.C., Marsit, C.J., Nelson, H.H., et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics, 13, 2012, 86, 10.1186/1471-2105-13-86.
78. Houseman, E.A., Kile, M.L., Christiani, D.C., Ince, T.A., Kelsey, K.T., Marsit, C.J., Reference-free deconvolution of DNA methylation data and mediation by cell composition effects. BMC Bioinformatics, 17, 2016, 259, 10.1186/s12859-016-1140-4.
79. Hsieh, C.J., Klump, B., Holzmann, K., Borchard, F., Gregor, M., Porschen, R., Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis. Cancer Research 58:17 (1998), 3942–3945.
80. Hughes, T., Ture-Ozdemir, F., Alibaz-Oner, F., Coit, P., Direskeneli, H., Sawalha, A.H., Epigenome-wide scan identifies a treatment-responsive pattern of altered DNA methylation among cytoskeletal remodeling genes in monocytes and CD4 + T cells from patients with Behcet's disease. Arthritis & Rheumatology 66:6 (2014), 1648–1658, 10.1002/art.38409.
81. Issa, J.P., Epigenetic variation and human disease. The Journal of Nutrition 132:8 Suppl. (2002), 2388S–2392S.
82. Issa, J.P., Ahuja, N., Toyota, M., Bronner, M.P., Brentnall, T.A., Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Research 61:9 (2001), 3573–3577.
83. Jaenisch, R., Bird, A., Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetics 33:Suppl. (2003), 245–254.
84. Jiang, Y., Wang, L., Role of histone deacetylase 3 in ankylosing spondylitis via negative feedback loop with microRNA-130a and enhancement of tumor necrosis factor-1alpha expression in peripheral blood mononuclear cells. Molecular Medicine Reports 13:1 (2016), 35–40, 10.3892/mmr.2015.4494.
85. Jung, M., Kadam, S., Xiong, W., Rauch, T.A., Jin, S.G., Pfeifer, G.P., MIRA-seq for DNA methylation analysis of CpG islands. Epigenomics 7:5 (2015), 695–706, 10.2217/epi.15.33.
86. Kalla, R., Ventham, N.T., Kennedy, N.A., Quintana, J.F., Nimmo, E.R., Buck, A.H., et al. MicroRNAs: New players in IBD. Gut 64:3 (2015), 504–517, 10.1136/gutjnl-2014-307891.
87. Kang, K., Bae, J.H., Han, K., Kim, E.S., Kim, T.O., Yi, J.M., A genome-wide methylation approach identifies a new hypermethylated gene panel in ulcerative colitis. International Journal of Molecular Sciences, 17(8), 2016, e1291, 10.3390/ijms17081291.
88. Karatzas, P.S., Mantzaris, G.J., Safioleas, M., Gazouli, M., DNA methylation profile of genes involved in inflammation and autoimmunity in inflammatory bowel disease. Medicine (Baltimore), 93(28), 2014, e309, 10.1097/MD.0000000000000309.
89. Karczewski J., Dobrowolska A., Rychlewska-Hanczewska A. and Adamski Z. (2016). New insights into the role of T cells in pathogenesis of psoriasis and psoriatic arthritis, Autoimmunity, 1–16, http://dx.doi.org/10.3109/08916934.2016.1166214, in press.
90. Katsurano, M., Niwa, T., Yasui, Y., Shigematsu, Y., Yamashita, S., Takeshima, H., et al. Early-stage formation of an epigenetic field defect in a mouse colitis model, and non-essential roles of T- and B-cells in DNA methylation induction. Oncogene 31:3 (2012), 342–351, 10.1038/onc.2011.241.
91. Kellermayer, R., Epigenetics and the developmental origins of inflammatory bowel diseases. Canadian Journal of Gastroenterology 26:12 (2012), 909–915.
92. Kellermayer, R., Balasa, A., Zhang, W., Lee, S., Mirza, S., Chakravarty, A., et al. Epigenetic maturation in colonic mucosa continues beyond infancy in mice. Human Molecular Genetics 19:11 (2010), 2168–2176, 10.1093/hmg/ddq095.
93. Kiernan, R., Bres, V., Ng, R.W., Coudart, M.P., El Messaoudi, S., Sardet, C., et al. Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65. The Journal of Biological Chemistry 278:4 (2003), 2758–2766, 10.1074/jbc.M209572200.
94. Koizumi, K., Alonso, S., Miyaki, Y., Okada, S., Ogura, H., Shiiya, N., et al. Array-based identification of common DNA methylation alterations in ulcerative colitis. International Journal of Oncology 40:4 (2012), 983–994, 10.3892/ijo.2011.1283.
95. Kominsky, D.J., Keely, S., MacManus, C.F., Glover, L.E., Scully, M., Collins, C.B., et al. An endogenously anti-inflammatory role for methylation in mucosal inflammation identified through metabolite profiling. Journal of Immunology 186:11 (2011), 6505–6514, 10.4049/jimmunol.1002805.
96. Korbie, D., Lin, E., Wall, D., Nair, S.S., Stirzaker, C., Clark, S.J., et al. Multiplex bisulfite PCR resequencing of clinical FFPE DNA. Clinical Epigenetics, 7(1), 2015, 28, 10.1186/s13148-015-0067-3.
97. Kraiczy, J., Nayak, K., Ross, A., Raine, T., Mak, T.N., Gasparetto, M., et al. Assessing DNA methylation in the developing human intestinal epithelium: Potential link to inflammatory bowel disease. Mucosal Immunology 9:3 (2016), 647–658, 10.1038/mi.2015.88.
98. Kriaucionis, S., Heintz, N., The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324:5929 (2009), 929–930, 10.1126/science.1169786 1169786 [pii].
99. Kugathasan, S., Amre, D., Inflammatory bowel disease—Environmental modification and genetic determinants. Pediatric Clinics of North America 53:4 (2006), 727–749, 10.1016/j.pcl.2006.05.009.
100. Ladd-Acosta, C., Epigenetic signatures as biomarkers of exposure. Current Environmental Health Reports 2:2 (2015), 117–125, 10.1007/s40572-015-0051-2.
101. Lai, N.S., Chou, J.L., Chen, G.C., Liu, S.Q., Lu, M.C., Chan, M.W., Association between cytokines and methylation of SOCS-1 in serum of patients with ankylosing spondylitis. Molecular Biology Reports 41:6 (2014), 3773–3780, 10.1007/s11033-014-3242-2.
102. Law, J.A., Jacobsen, S.E., Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews. Genetics 11:3 (2010), 204–220, 10.1038/nrg2719.
103. Lee, J., Hong, E.C., Jeong, H., Hwang, J.W., Kim, H., Bae, E.K., et al. A novel histone deacetylase 6-selective inhibitor suppresses synovial inflammation and joint destruction in a collagen antibody-induced arthritis mouse model. International Journal of Rheumatic Diseases 18:5 (2015), 514–523, 10.1111/1756-185X.12501.
104. Li, M., Liu, X., Sun, X., Wang, Z., Guo, W., Hu, F., et al. Therapeutic effects of NK-HDAC-1, a novel histone deacetylase inhibitor, on collagen-induced arthritis through the induction of apoptosis of fibroblast-like synoviocytes. Inflammation 36:4 (2013), 888–896, 10.1007/s10753-013-9616-0.
105. Li, Q., Suzuki, M., Wendt, J., Patterson, N., Eichten, S.R., Hermanson, P.J., et al. Post-conversion targeted capture of modified cytosines in mammalian and plant genomes. Nucleic Acids Research, 43(12), 2015, e81, 10.1093/nar/gkv244.
106. Li, Z., Wong, S.H., Shen, J., Chan, M.T., Wu, W.K., The role of MicroRNAS in Ankylosing Spondylitis. Medicine (Baltimore), 95(14), 2016, e3325, 10.1097/MD.0000000000003325.
107. Lin, Z., Hegarty, J.P., Cappel, J.A., Yu, W., Chen, X., Faber, P., et al. Identification of disease-associated DNA methylation in intestinal tissues from patients with inflammatory bowel disease. Clinical Genetics 80:1 (2011), 59–67, 10.1111/j.1399-0004.2010.01546.x.
108. Lin, Z., Hegarty, J.P., Yu, W., Cappel, J.A., Chen, X., Faber, P.W., et al. Identification of disease-associated DNA methylation in B cells from Crohn's disease and ulcerative colitis patients. Digestive Diseases and Sciences 57:12 (2012), 3145–3153, 10.1007/s10620-012-2288-z.
109. Liu, H.P., Cao, A.T., Feng, T., Li, Q., Zhang, W., Yao, S., et al. TGF-beta converts Th1 cells into Th17 cells through stimulation of Runx1 expression. European Journal of Immunology 45:4 (2015), 1010–1018, 10.1002/eji.201444726.
110. Lo Sasso, G., Menzies, K.J., Mottis, A., Piersigilli, A., Perino, A., Yamamoto, H., et al. SIRT2 deficiency modulates macrophage polarization and susceptibility to experimental colitis. PLoS One, 9(7), 2014, e103573, 10.1371/journal.pone.0103573.
111. Lobaton, T., Azuara, D., Rodriguez-Moranta, F., Loayza, C., Sanjuan, X., de Oca, J., et al. Relationship between methylation and colonic inflammation in inflammatory bowel disease. World Journal of Gastroenterology 20:30 (2014), 10591–10598, 10.3748/wjg.v20.i30.10591.
112. Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63:8 (2014), 1275–1283, 10.1136/gutjnl-2013-304833.
113. Maeda, T., Guan, J.Z., Higuchi, Y., Oyama, J., Makino, N., Aging-related alterations of subtelomeric methylation in sarcoidosis patients. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 64:7 (2009), 752–760, 10.1093/gerona/glp049.
114. Marques-Rocha, J.L., Samblas, M., Milagro, F.I., Bressan, J., Martinez, J.A., Marti, A., Noncoding RNAs, cytokines, and inflammation-related diseases. The FASEB Journal 29:9 (2015), 3595–3611, 10.1096/fj.14-260323.
115. Masser, D.R., Berg, A.S., Freeman, W.M., Focused, high accuracy 5-methylcytosine quantitation with base resolution by benchtop next-generation sequencing. Epigenetics & Chromatin, 6(1), 2013, 33, 10.1186/1756-8935-6-33.
116. Meissner, A., Gnirke, A., Bell, G.W., Ramsahoye, B., Lander, E.S., Jaenisch, R., Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Research 33:18 (2005), 5868–5877, 10.1093/nar/gki901.
117. Miceli-Richard, C., Wang-Renault, S.F., 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 Sjogren's syndrome. Annals of the Rheumatic Diseases 75:5 (2016), 933–940, 10.1136/annrheumdis-2014-206998.
118. Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:7153 (2007), 553–560.
119. Mischke, M., Plosch, T., The gut microbiota and their metabolites: Potential implications for the host epigenome. Advances in Experimental Medicine and Biology 902 (2016), 33–44, 10.1007/978-3-319-31248-4_3.
120. Miura, F., Enomoto, Y., Dairiki, R., Ito, T., Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Research, 40(17), 2012, e136, 10.1093/nar/gks454.
121. Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R.S., Bhan, A.K., Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16:2 (2002), 219–230.
122. Moran, S., Arribas, C., Esteller, M., Validation of a DNA methylation microarray for 850,000 CpG sites of the human genome enriched in enhancer sequences. Epigenomics 8:3 (2016), 389–399, 10.2217/epi.15.114.
123. Mullican, S.E., Gaddis, C.A., Alenghat, T., Nair, M.G., Giacomin, P.R., Everett, L.J., et al. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes & Development 25:23 (2011), 2480–2488, 10.1101/gad.175950.111.
124. Nielsen, H.M., Tost, J., Epigenetic changes in inflammatory and autoimmune diseases. Sub-Cellular Biochemistry 61 (2012), 455–478, 10.1007/978-94-007-4525-4_20.
125. Nimmo, E.R., Prendergast, J.G., Aldhous, M.C., Kennedy, N.A., Henderson, P., Drummond, H.E., et al. Genome-wide methylation profiling in Crohn's disease identifies altered epigenetic regulation of key host defense mechanisms including the Th17 pathway. Inflammatory Bowel Diseases 18:5 (2012), 889–899, 10.1002/ibd.21912.
126. Noronha, A.M., Liang, Y., Hetzel, J.T., Hasturk, H., Kantarci, A., Stucchi, A., et al. Hyperactivated B cells in human inflammatory bowel disease. Journal of Leukocyte Biology 86:4 (2009), 1007–1016, 10.1189/jlb.0309203.
127. Northrop, J.K., Thomas, R.M., Wells, A.D., Shen, H., Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells. Journal of Immunology 177:2 (2006), 1062–1069.
128. Oakes, C.C., La Salle, S., Robaire, B., Trasler, J.M., Evaluation of a quantitative DNA methylation analysis technique using methylation-sensitive/dependent restriction enzymes and real-time PCR. Epigenetics 1:3 (2006), 146–152.
129. Park, G.T., Han, J., Park, S.G., Kim, S., Kim, T.Y., DNA methylation analysis of CD4 + T cells in patients with psoriasis. Archives of Dermatological Research 306:3 (2014), 259–268, 10.1007/s00403-013-1432-8.
130. Planell, N., Lozano, J.J., Mora-Buch, R., Masamunt, M.C., Jimeno, M., Ordas, I., et al. Transcriptional analysis of the intestinal mucosa of patients with ulcerative colitis in remission reveals lasting epithelial cell alterations. Gut 62:7 (2013), 967–976, 10.1136/gutjnl-2012-303333.
131. Qi, J., Hou, S., Zhang, Q., Liao, D., Wei, L., Fang, J., et al. A functional variant of pre-miRNA-196a2 confers risk for Behcet's disease but not for Vogt–Koyanagi–Harada syndrome or AAU in ankylosing spondylitis. Human Genetics 132:12 (2013), 1395–1404, 10.1007/s00439-013-1346-8.
132. Qi, J., Yang, Y., Hou, S., Qiao, Y., Wang, Q., Yu, H., et al. Increased Notch pathway activation in Behcet's disease. Rheumatology (Oxford) 53:5 (2014), 810–820, 10.1093/rheumatology/ket438.
133. Reilly, C.M., Thomas, M., Gogal, R. Jr., Olgun, S., Santo, A., Sodhi, R., et al. The histone deacetylase inhibitor trichostatin A upregulates regulatory T cells and modulates autoimmunity in NZB/WF1 mice. Journal of Autoimmunity 31:2 (2008), 123–130, 10.1016/j.jaut.2008.04.020.
134. Reveille, J.D., Genetics of spondyloarthritis—Beyond the MHC. Nature Reviews. Rheumatology 8:5 (2012), 296–304, 10.1038/nrrheum.2012.41.
135. Roadmap Epigenomics, C., Kundaje, A., Meuleman, W., Ernst, J., Bilenky, M., Yen, A., et al. Integrative analysis of 111 reference human epigenomes. Nature 518:7539 (2015), 317–330, 10.1038/nature14248.
136. Roberson, E.D., Liu, Y., Ryan, C., Joyce, C.E., Duan, S., Cao, L., et al. A subset of methylated CpG sites differentiate psoriatic from normal skin. The Journal of Investigative Dermatology 132:3 Pt. 1 (2012), 583–592, 10.1038/jid.2011.348.
137. Roberts A.R., Vecellio M., Chen L., Ridley A., Cortes A., Knight J.C., et al. (2016). An ankylosing spondylitis-associated genetic variant in the IL23R-IL12RB2 intergenic region modulates enhancer activity and is associated with increased Th1-cell differentiation, Annals of the Rheumatic Diseases, http://dx.doi.org/10.1136/annrheumdis-2015-208640, in press.
138. Ronn, T., Ling, C., DNA methylation as a diagnostic and therapeutic target in the battle against Type 2 diabetes. Epigenomics 7:3 (2015), 451–460, 10.2217/epi.15.7.
139. Ruchusatsawat, K., Wongpiyabovorn, J., Shuangshoti, S., Hirankarn, N., Mutirangura, A., SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. Journal of Molecular Medicine (Berlin, Germany) 84:2 (2006), 175–182, 10.1007/s00109-005-0020-6.
140. Ruzov, A., Tsenkina, Y., Serio, A., Dudnakova, T., Fletcher, J., Bai, Y., et al. Lineage-specific distribution of high levels of genomic 5-hydroxymethylcytosine in mammalian development. Cell Research 21:9 (2011), 1332–1342, 10.1038/cr.2011.113.
141. Saito, S., Kato, J., Hiraoka, S., Horii, J., Suzuki, H., Higashi, R., et al. DNA methylation of colon mucosa in ulcerative colitis patients: Correlation with inflammatory status. Inflammatory Bowel Diseases 17:9 (2011), 1955–1965, 10.1002/ibd.21573.
142. Samuel N., Wilson G., Lemire M., Id Said B., Lou Y., Li W., et al., (2016). Genome-wide DNA methylation analysis reveals epigenetic dysregulation of MicroRNA-34A in TP53-associated cancer susceptibility, Journal of Clinical Oncology, http://dx.doi.org/10.1200/JCO.2016.67.6940, in press.
143. Sandoval, J., Heyn, H., Moran, S., Serra-Musach, J., Pujana, M.A., Bibikova, M., et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 6:6 (2011), 692–702 doi:16196 [pii].
144. Santourlidis, S., Graffmann, N., Christ, J., Uhrberg, M., Lineage-specific transition of histone signatures in the killer cell Ig-like receptor locus from hematopoietic progenitor to NK cells. Journal of Immunology 180:1 (2008), 418–425.
145. Sato, F., Harpaz, N., Shibata, D., Xu, Y., Yin, J., Mori, Y., et al. Hypermethylation of the p14(ARF) gene in ulcerative colitis-associated colorectal carcinogenesis. Cancer Research 62:4 (2002), 1148–1151.
146. Sato, F., Shibata, D., Harpaz, N., Xu, Y., Yin, J., Mori, Y., et al. Aberrant methylation of the HPP1 gene in ulcerative colitis-associated colorectal carcinoma. Cancer Research 62:23 (2002), 6820–6822.
147. Scarpa, M., Stylianou, E., Epigenetics: Concepts and relevance to IBD pathogenesis. Inflammatory Bowel Diseases 18:10 (2012), 1982–1996, 10.1002/ibd.22934.
148. Schlums, H., Cichocki, F., Tesi, B., Theorell, J., Beziat, V., Holmes, T.D., et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 42:3 (2015), 443–456, 10.1016/j.immuni.2015.02.008.
149. Schultz, M.D., He, Y., Whitaker, J.W., Hariharan, M., Mukamel, E.A., Leung, D., et al. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature 523:7559 (2015), 212–216, 10.1038/nature14465.
150. Shen, L., Du, J., Xia, Y., Tan, Z., Fu, Y., Yang, Q., et al. Genome-wide landscape of DNA methylomes and their relationship with mRNA and miRNA transcriptomes in oxidative and glycolytic skeletal muscles. Scientific Reports, 6, 2016, 32186, 10.1038/srep32186.
151. Shen, L., Kondo, Y., Guo, Y., Zhang, J., Zhang, L., Ahmed, S., et al. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genetics 3:10 (2007), 2023–2036.
152. Smith, P.J., Levine, A.P., Dunne, J., Guilhamon, P., Turmaine, M., Sewell, G.W., et al. Mucosal transcriptomics implicates under expression of BRINP3 in the pathogenesis of ulcerative colitis. Inflammatory Bowel Diseases 20:10 (2014), 1802–1812, 10.1097/MIB.0000000000000169.
153. Subramaniam, R., Mizoguchi, A., Mizoguchi, E., Mechanistic roles of epithelial and immune cell signaling during the development of colitis-associated cancer. Cancer Research Frontiers 2:1 (2016), 1–21, 10.17980/2016.1.
154. Tahara, T., Shibata, T., Nakamura, M., Yamashita, H., Yoshioka, D., Okubo, M., et al. Promoter methylation of protease-activated receptor (PAR2) is associated with severe clinical phenotypes of ulcerative colitis (UC). Clinical and Experimental Medicine 9:2 (2009), 125–130, 10.1007/s10238-008-0025-x.
155. Tahara, T., Shibata, T., Nakamura, M., Yamashita, H., Yoshioka, D., Okubo, M., et al. Effect of MDR1 gene promoter methylation in patients with ulcerative colitis. International Journal of Molecular Medicine 23:4 (2009), 521–527.
156. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:5929 (2009), 930–935, 10.1126/science.1170116 1170116 [pii].
157. Taiwo, O., Wilson, G.A., Morris, T., Seisenberger, S., Reik, W., Pearce, D., et al. Methylome analysis using MeDIP-seq with low DNA concentrations. Nature Protocols 7:4 (2012), 617–636, 10.1038/nprot.2012.012.
158. Tost, J., Methods for the genome-wide and gene-specific analysis of DNA methylation levels and patterns. Tost, J., (eds.) Epigenetics, 2008, Horizon Scientific Press, Norwich, 63–104.
159. Tost, J., DNA methylation: An introduction to the biology and the disease-associated changes of a promising biomarker. Molecular Biotechnology 44:1 (2010), 71–81, 10.1007/s12033-009-9216-2.
160. Tost, J., Engineering of the epigenome: Synthetic biology to define functional causality and develop innovative therapies. Epigenomics 8:2 (2016), 153–156, 10.2217/epi.15.112.
161. Tost, J., Follow the trace of death: Methylation analysis of cell-free DNA for clinical applications in non-cancerous diseases. Epigenomics 8 (2016), 1169–1172, 10.2217/epi-2016-0080.
162. Tost, J., Gut, I.G., DNA methylation analysis by pyrosequencing. Nature Protocols 2:9 (2007), 2265–2275.
163. Toussirot, E., Abbas, W., Khan, K.A., Tissot, M., Jeudy, A., Baud, L., et al. Imbalance between HAT and HDAC activities in the PBMCs of patients with ankylosing spondylitis or rheumatoid arthritis and influence of HDAC inhibitors on TNF alpha production. PLoS One, 8(8), 2013, e70939, 10.1371/journal.pone.0070939.
164. Tovar-Castillo, L.E., Cancino-Diaz, J.C., Garcia-Vazquez, F., Cancino-Gomez, F.G., Leon-Dorantes, G., Blancas-Gonzalez, F., et al. Under-expression of VHL and over-expression of HDAC-1, HIF-1alpha, LL-37, and IAP-2 in affected skin biopsies of patients with psoriasis. International Journal of Dermatology 46:3 (2007), 239–246, 10.1111/j.1365-4632.2006.02962.x.
165. Tsaprouni, L.G., Ito, K., Powell, J.J., Adcock, I.M., Punchard, N., Differential patterns of histone acetylation in inflammatory bowel diseases. Journal of Inflammation (London, England), 8(1), 2011, 1, 10.1186/1476-9255-8-1.
166. Tschurtschenthaler, M., Kachroo, P., Heinsen, F.A., Adolph, T.E., Ruhlemann, M.C., Klughammer, J., et al. Paternal chronic colitis causes epigenetic inheritance of susceptibility to colitis. Scientific Reports, 6, 2016, 31640, 10.1038/srep31640.
167. Ueno, A., Ghosh, A., Hung, D., Li, J., Jijon, H., Th17 plasticity and its changes associated with inflammatory bowel disease. World Journal of Gastroenterology 21:43 (2015), 12283–12295, 10.3748/wjg.v21.i43.12283.
168. Urich, M.A., Nery, J.R., Lister, R., Schmitz, R.J., Ecker, J.R., MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing. Nature Protocols 10:3 (2015), 475–483, 10.1038/nprot.2014.114.
169. Van den Bossche, J., Neele, A.E., Hoeksema, M.A., de Winther, M.P., Macrophage polarization: The epigenetic point of view. Current Opinion in Lipidology 25:5 (2014), 367–373, 10.1097/MOL.0000000000000109.
170. van Rooij, E., The art of microRNA research. Circulation Research 108:2 (2011), 219–234, 10.1161/CIRCRESAHA.110.227496.
171. Vecellio, M., Roberts, A.R., Cohen, C.J., Cortes, A., Knight, J.C., Bowness, P., et al. The genetic association of RUNX3 with ankylosing spondylitis can be explained by allele-specific effects on IRF4 recruitment that alter gene expression. Annals of the Rheumatic Diseases 75:8 (2016), 1534–1540, 10.1136/annrheumdis-2015-207490.
172. Vernia, P., Annese, V., Bresci, G., d'Albasio, G., D'Inca, R., Giaccari, S., et al. Topical butyrate improves efficacy of 5-ASA in refractory distal ulcerative colitis: Results of a multicentre trial. European Journal of Clinical Investigation 33:3 (2003), 244–248.
173. Voelter-Mahlknecht, S., Epigenetic associations in relation to cardiovascular prevention and therapeutics. Clinical Epigenetics, 8, 2016, 4, 10.1186/s13148-016-0170-0.
174. Wang, F.Y., Arisawa, T., Tahara, T., Takahama, K., Watanabe, M., Hirata, I., et al. Aberrant DNA methylation in ulcerative colitis without neoplasia. Hepato-Gastroenterology 55:81 (2008), 62–65.
175. Wendling, D., Delattre, E., Abbas, W., Guillot, X., Toussirot, E., Herbein, G., Sirt-1 activity in PBMC from patients with spondyloarthritis. Joint, Bone, Spine 82:3 (2015), 210–211, 10.1016/j.jbspin.2014.10.002.
176. Wheeler, J.M., Kim, H.C., Efstathiou, J.A., Ilyas, M., Mortensen, N.J., Bodmer, W.F., Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer. Gut 48:3 (2001), 367–371.
177. White, C.A., Pone, E.J., Lam, T., Tat, C., Hayama, K.L., Li, G., et al. Histone deacetylase inhibitors upregulate B cell microRNAs that silence AID and Blimp-1 expression for epigenetic modulation of antibody and autoantibody responses. Journal of Immunology 193:12 (2014), 5933–5950, 10.4049/jimmunol.1401702.
178. Wilson, T.J., Jobim, M., Jobim, L.F., Portela, P., Salim, P.H., Rosito, M.A., et al. Study of killer immunoglobulin-like receptor genes and human leukocyte antigens class I ligands in a Caucasian Brazilian population with Crohn's disease and ulcerative colitis. Human Immunology 71:3 (2010), 293–297, 10.1016/j.humimm.2009.12.006.
179. Wojdacz, T.K., Dobrovic, A., Hansen, L.L., Methylation-sensitive high-resolution melting. Nature Protocols 3:12 (2008), 1903–1908, 10.1038/nprot.2008.191 nprot.2008.191 [pii].
180. Xia, J., Zhang, W., MicroRNAs in normal and psoriatic skin. Physiological Genomics 46:4 (2014), 113–122, 10.1152/physiolgenomics.00157.2013.
181. Yadav, P.K., Chen, C., Liu, Z., Potential role of NK cells in the pathogenesis of inflammatory bowel disease. Journal of Biomedicine & Biotechnology, 2011, 2011, 348530, 10.1155/2011/348530.
182. Yamamoto, F., Yamamoto, M., A DNA microarray-based methylation-sensitive (MS)-AFLP hybridization method for genetic and epigenetic analyses. Molecular Genetics and Genomics 271:6 (2004), 678–686.
183. Yu, L., Chibnik, L.B., Srivastava, G.P., Pochet, N., Yang, J., Xu, J., et al. Association of brain DNA methylation in SORL1, ABCA7, HLA-DRB5, SLC24A4, and BIN1 with pathological diagnosis of Alzheimer disease. Journal of the American Medical Association Neurology 72:1 (2015), 15–24, 10.1001/jamaneurol.2014.3049.
184. Yuksel, S., Kucukazman, S.O., Karatas, G.S., Ozturk, M.A., Prombhul, S., Hirankarn, N., Methylation status of Alu and LINE-1 interspersed repetitive sequences in Behcet's disease patients. BioMed Research International, 2016, 2016, 1393089, 10.1155/2016/1393089.
185. Zan, H., Casali, P., Epigenetics of peripheral B-cell differentiation and the antibody response. Frontiers in Immunology, 6, 2015, 631, 10.3389/fimmu.2015.00631.
186. Zawada, A.M., Schneider, J.S., Michel, A.I., Rogacev, K.S., Hummel, B., Krezdorn, N., et al. DNA methylation profiling reveals differences in the 3 human monocyte subsets and identifies uremia to induce DNA methylation changes during differentiation. Epigenetics 11:4 (2016), 259–272, 10.1080/15592294.2016.1158363.
187. Zhang, T., Cooper, S., Brockdorff, N., The interplay of histone modifications—Writers that read. EMBO Reports 16:11 (2015), 1467–1481, 10.15252/embr.201540945.
188. Zhang, P., Su, Y., Chen, H., Zhao, M., Lu, Q., Abnormal DNA methylation in skin lesions and PBMCs of patients with psoriasis vulgaris. Journal of Dermatological Science 60:1 (2010), 40–42, 10.1016/j.jdermsci.2010.07.011.
189. Zhang, P., Su, Y., Zhao, M., Huang, W., Lu, Q., Abnormal histone modifications in PBMCs from patients with psoriasis vulgaris. European Journal of Dermatology 21:4 (2011), 552–557, 10.1684/ejd.2011.1383.
190. Zhang, K., Zhang, R., Li, X., Yin, G., Niu, X., Promoter methylation status of p15 and p21 genes in HPP-CFCs of bone marrow of patients with psoriasis. European Journal of Dermatology 19:2 (2009), 141–146, 10.1684/ejd.2008.0618.
191. Zhang, P., Zhao, M., Liang, G., Yin, G., Huang, D., Su, F., et al. Whole-genome DNA methylation in skin lesions from patients with psoriasis vulgaris. Journal of Autoimmunity 41 (2013), 17–24, 10.1016/j.jaut.2013.01.001.
192. Zhang, Q., Zhao, K., Shen, Q., Han, Y., Gu, Y., Li, X., et al. Tet2 is required to resolve inflammation by recruiting Hdac2 to specifically repress IL-6. Nature 525:7569 (2015), 389–393, 10.1038/nature15252.
193. Zhou, F., Wang, W., Shen, C., Li, H., Zuo, X., Zheng, X., et al. Epigenome-wide association analysis identified nine skin DNA methylation loci for psoriasis. The Journal of Investigative Dermatology 136:4 (2016), 779–787, 10.1016/j.jid.2015.12.029.