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

Volumn 20, Issue 10, 2014, Pages 1784-1793

  Adams, Alex T ^a   Kennedy, Nicholas A ^a   Hansen, Richard ^b   Ventham, Nicholas T ^a   O'Leary, Kate R ^a   Drummond, Hazel E ^a   Noble, Colin L ^a   El Omar, Emad ^b   Russell, Richard K ^c   Wilson, David C ^d   Nimmo, Elaine R ^a   Hold, Georgina L ^b   Satsangi, Jack ^a  

^a WESTERN GENERAL HOSPITAL   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c ROYAL HOSPITAL FOR SICK CHILDREN   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Crohn's disease; Epigenetics; MIR21

Indexed keywords

MICRORNA 21; BIOLOGICAL MARKER; HLA ANTIGEN; MEMBRANE PROTEIN; MICRORNA; MIRN21 MICRORNA, HUMAN; VMP1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; CPG ISLAND; CROHN DISEASE; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE LOCUS; GENETIC ASSOCIATION; HLA SYSTEM; HUMAN; HUMAN TISSUE; INTESTINE MUCOSA; LEUKOCYTE; PRIORITY JOURNAL; PYROSEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; ADULT; CASE CONTROL STUDY; CHILD; COMPARATIVE STUDY; FEMALE; FOLLOW UP; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMAN GENOME; MALE; PROGNOSIS;

ADULT; BIOMARKERS; CASE-CONTROL STUDIES; CHILD; CROHN DISEASE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FOLLOW-UP STUDIES; GENETIC PREDISPOSITION TO DISEASE; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HLA ANTIGENS; HUMANS; MALE; MEMBRANE PROTEINS; MICRORNAS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS;

EID: 84922385890     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000179     Document Type: Article

References (71)

1. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-124.
2. Henderson P, Wilson DC. The rising incidence of paediatric-onset inflammatory bowel disease. Arch Dis Child. 2012;97:585-586.
3. Benchimol EI, Fortinsky KJ, Gozdyra P, et al. Epidemiology of pediatric inflammatory bowel disease: a systematic review of international trends. Inflamm Bowel Dis. 2011;17:423-439.
4. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46.e42-54.e42; quiz e30.
5. Burisch J, Munkholm P. Inflammatory bowel disease epidemiology. Curr Opin Gastroenterol. 2013;29:357-362.
6. Hold GL. Western lifestyle: a "master" manipulator of the intestinal microbiota? Gut. 2014;63:5-6.
7. Hansen R, Russell RK, Reiff C, et al. Microbiota of de-novo pediatric IBD: increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn's but not in ulcerative colitis. Am J Gastroenterol. 2012;107:1913-1922.
8. Relton CL, Davey Smith G. Epigenetic epidemiology of common complex disease: prospects for prediction, prevention, and treatment. PLoS Med. 2010;7:e1000356.
9. Rakyan VK, Down TA, Balding DJ, et al. Epigenome-wide association studies for common human diseases. Nat Rev Genet. 2011;12:529-541.
10. Ventham NT, Kennedy NA, Nimmo ER, et al. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology. 2013;145:293-308.
11. Liu Y, Aryee MJ, Padyukov L, et al. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat Biotechnol. 2013;31:142-147.
12. Huynh JL, Garg P, Thin TH, et al. Epigenome-wide differences in pathology-free regions of multiple sclerosis-affected brains. Nat Neurosci. 2014;17:121-130.
13. Bell CG, Finer S, Lindgren CM, et al. Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus. PLoS One. 2010;5:e14040.
14. Dick KJ, Nelson CP, Tsaprouni L, et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet. 2014;383:1990-1998.
15. Breitling LP, Yang R, Korn B, et al. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet. 2011;88:450-457.
16. Lam LL, Emberly E, Fraser HB, et al. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci U S A. 2012;109(suppl 2):17253-17260.
17. Kellermayer R. Epigenetics and the developmental origins of inflammatory bowel diseases. Can J Gastroenterol. 2012;26:909-915.
18. Bell JT, Tsai PC, Yang TP, et al. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet. 2012;8:e1002629.
19. Stadler MB, Murr R, Burger L, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature. 2011;480:490-495.
20. Gutierrez-Arcelus M, Lappalainen T, Montgomery SB, et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife (Cambridge). 2013;2:e00523.
21. Hansen R, Berry SH, Mukhopadhya I, et al. The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease: the BISCUIT study. PLoS One. 2013;8:e58825.
22. Van Limbergen J, Russell RK, Drummond HE, et al. Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology. 2008;135:1114-1122.
23. Bibikova M, Barnes B, Tsan C, et al. High density DNA methylation array with single CpG site resolution. Genomics. 2011;98:288-295.
24. Abecasis GR, Auton A, Brooks LD, et al. An integrated map of genetic variation from 1, 092 human genomes. Nature. 2012;491:56-65.
25. Du P, Kibbe WA, Lin SM. Lumi: a pipeline for processing Illumina microarray. Bioinformatics. 2008;24:1547-1548.
26. Marabita F, Almgren M, Lindholm ME, et al. An evaluation of analysis pipelines for DNA methylation profiling using the Illumina HumanMethylation450 BeadChip platform. Epigenetics. 2013;8:333-346.
27. Teschendorff AE, Marabita F, Lechner M, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics. 2013;29:189-196.
28. Leek JT, Storey JD. Capturing heterogeneity in gene expression studies by surrogate variable analysis. PLoS Genet. 2007;3:1724-1735.
29. Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86.
30. Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, et al, eds. Bioinformatics and Computational Biology Solutions Using {R} and Bioconductor. New York, NY: Springer; 2005:397-420.
31. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57:289-300.
32. Morris TJ, Butcher LM, Feber A, et al. ChAMP: 450k chip analysis methylation pipeline. Bioinformatics. 2014;30:428-430.
33. Li Y, Zhu J, Tian G, et al. The DNA methylome of human peripheral blood mononuclear cells. PLoS Biol. 2010;8:e1000533.
34. Noble CL, Abbas AR, Cornelius J, et al. Regional variation in gene expression in the healthy colon is dysregulated in ulcerative colitis. Gut. 2008;57:1398-1405.
35. Venables WN, Ripley BD. Modern Applied Statistics with S. 4th ed. New York, NY: Springer; 2002.
36. Young MD, Wakefield MJ, Smyth GK, et al. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11:R14.
37. Geeleher P, Hartnett L, Egan LJ, et al. Gene-set analysis is severely biased when applied to genome-wide methylation data. Bioinformatics. 2013;29:1851-1857.
38. Nimmo ER, Prendergast JG, Aldhous MC, et al. Genome-wide methylation profiling in Crohn's disease identifies altered epigenetic regulation of key host defense mechanisms including the Th17 pathway. Inflamm Bowel Dis. 2012;18:889-899.
39. Calvo-Garrido J, Carilla-Latorre S, Escalante R. Vacuole membrane protein 1, autophagy and much more. Autophagy. 2008;4:835-837.
40. Kang R, Zeh HJ, Lotze MT, et al. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18:571-580.
41. Molejon MI, Ropolo A, Re AL, et al. The VMP1-Beclin 1 interaction regulates autophagy induction. Sci Rep. 2013;3:1055.
42. Kanaan Z, Rai SN, Eichenberger MR, et al. Plasma miR-21: a potential diagnostic marker of colorectal cancer. Ann Surg. 2012;256:544-551.
43. Good PJ, Guyer MS, Kamholz S, et al. The ENCODE (ENCyclopedia of DNA elements) project. Science. 2004;306:636-640.
44. Lu TX, Hartner J, Lim EJ, et al. MicroRNA-21 limits in vivo immune response-mediated activation of the IL-12/IFN-gamma pathway, Th1 polarization, and the severity of delayed-type hypersensitivity. J Immunol. 2011;187:3362-3373.
45. Chang CC, Zhang QY, Liu Z, et al. Downregulation of inflammatory microRNAs by Ig-like transcript 3 is essential for the differentiation of human CD8 (+) T suppressor cells. J Immunol. 2012;188:3042-3052.
46. Sawant DV, Wu H, Kaplan MH, et al. The Bcl6 target gene microRNA-21 promotes Th2 differentiation by a T cell intrinsic pathway. Mol Immunol. 2013;54:435-442.
47. Ludwig K, Fassan M, Mescoli C, et al. PDCD4/miR-21 dysregulation in inflammatory bowel disease-associated carcinogenesis. Virchows Arch. 2013;462:57-63.
48. Wu F, Zikusoka M, Trindade A, et al. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624-1635.e24.
49. Wu F, Zhang S, Dassopoulos T, et al. Identification of microRNAs associated with ileal and colonic Crohn's disease. Inflamm Bowel Dis. 2010;16:1729-1738.
50. Shi C, Liang Y, Yang J, et al. MicroRNA-21 knockout improve the survival rate in DSS induced fatal colitis through protecting against inflammation and tissue injury. PLoS One. 2013;8:e66814.
51. Chuang AY, Chuang JC, Zhai Z, et al. NOD2 expression is regulated by microRNAs in Colonic epithelial HCT116 cells. Inflamm Bowel Dis. 2014;20:126-135.
52. Chen Y, Wang C, Liu Y, et al. miR-122 targets NOD2 to decrease intestinal epithelial cell injury in Crohn's disease. Biochem Biophys Res Commun. 2013;438:133-139.
53. Brain O, Owens BMJ, Pichulik T, et al. The intracellular sensor NOD2 induces microRNA-29 expression in human dendritic cells to limit IL-23 release. Immunity. 2013;39:521-536.
54. Nguyen HTT, Dalmasso G, Müller S, et al. Crohn's disease-associated adherent invasive escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology. 2014;146:508-519.
55. Lu C, Chen J, Xu HG, et al. MIR106B and MIR93 prevent removal of bacteria from epithelial cells by disrupting ATG16L1-mediated autophagy. Gastroenterology. 2014;146:188-199.
56. Griffiths-Jones S, Saini HK, Van Dongen S, et al. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36:D154-D158.
57. Suzuki A, Hanada T, Mitsuyama K, et al. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J Exp Med. 2001;193:471-481.
58. Carow B, Rottenberg ME. SOCS3, a major regulator of infection and inflammation. Front Immunol. 2014;5:58.
59. Maillard MH, Bega H, Uhlig HH, et al. Toll-interacting protein modulates colitis susceptibility in mice. Inflamm Bowel Dis. 2014;20:660-670.
60. Zhao Y, Bjørbaek C, Weremowicz S, et al. RSK3 encodes a novel pp90rsk isoform with a unique N-terminal sequence: growth factorstimulated kinase function and nuclear translocation. Mol Cell Biol. 1995;15:4353-4363.
61. Grützmann R, Molnar B, Pilarsky C, et al. Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS One. 2008;3:e3759.
62. Church TR, Wandell M, Lofton-Day C, et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014;63:317-325.
63. Harris RA, Nagy-Szakal D, Pedersen N, et al. Genome-wide peripheral blood leukocyte DNA methylation microarrays identified a single association with inflammatory bowel diseases. Inflamm Bowel Dis. 2012;2399:1-8.
64. Hawkey CJ. Stem cells as treatment in inflammatory bowel disease. Dig Dis. 2012;30(suppl 3):134-139.
65. Callaway E. Epigenomics starts to make its mark. Nature. 2014;508:22.
66. Reinius LE, Acevedo N, Joerink M, et al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One. 2012;7:e41361.
67. Houseman EA, Molitor J, Marsit CJ. Reference-free cell mixture adjustments in analysis of DNA methylation data. Bioinformatics. 2014;30:1431-1439.
68. Hugot JP, Laurent-Puig P, Gower-Rousseau C, et al. Mapping of a susceptibility locus for Crohn's disease on chromosome 16. Nature. 1996;379:821-823.
69. Satsangi J, Parkes M, Louis E, et al. Two stage genome-wide search in inflammatory bowel disease provides evidence for susceptibility loci on chromosomes 3, 7 and 12. Nat Genet. 1996;14:199-202.
70. Satsangi J, Welsh KI, Bunce M, et al. Contribution of genes of the major histocompatibility complex to susceptibility and disease phenotype in inflammatory bowel disease. Lancet. 1996;347:1212-1217.
71. Cooke J, Zhang H, Greger L, et al. Mucosal genome-wide methylation changes in inflammatory bowel disease. Inflamm Bowel Dis. 2012;18:2128-2137.