DNA methylation-associated colonic mucosal immune and defense responses in treatmentnaïve pediatric ulcerative colitis

Epigenetics

Volumn 9, Issue 8, 2014, Pages 1131-1137

  Harris, R Alan ^a   Nagy Szakal, Dorottya ^b   Mir, Sabina A V ^b   Frank, Eibe ^c   Szigeti, Reka ^a   Kaplan, Jess L ^d   Bronsky, Jiri ^e   Opekun, Antone ^a   Ferry, George D ^b   Winter, Harland ^d   Kellermayer, Richard ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF WAIKATO   (New Zealand)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY HOSPITAL MOTOL   (Czech Republic)

Author keywords

DNA expression; DNA methylation; DNA methylome; Epigenetics; Pediatric inflammatory bowel disease; Treatment na ve; Ulcerative colitis

Indexed keywords

CALGRANULIN B; CD18 ANTIGEN; DNA METHYLTRANSFERASE 1; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 1; MEMBRANE PROTEIN; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SERUM AMYLOID A; SERUM AMYLOID A 1; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; BIOTINYLATION; CHILD; CHILDHOOD DISEASE; CLINICAL ARTICLE; COLON BIOPSY; COLON MUCOSA; COLONOSCOPY; CONTROLLED STUDY; CROHN DISEASE; DNA EXTRACTION; DNA METHYLATION; ENDOSCOPY; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; INFLAMMATION; MALE; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRINCIPAL COMPONENT ANALYSIS; PROTEIN MICROARRAY; PYROSEQUENCING; REMISSION; RNA EXTRACTION; RNA PROCESSING; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; SPECTROPHOTOMETRY; ULCERATIVE COLITIS; CASE CONTROL STUDY; COLON; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; MUCOSAL IMMUNITY; YOUNG ADULT;

ADOLESCENT; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; COLITIS, ULCERATIVE; COLON; CROHN DISEASE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MALE; YOUNG ADULT;

EID: 84905661327     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.29446     Document Type: Article

References (42)

1. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012; 142:46-54, e42, quiz e30; PMID:22001864; http://dx.doi.org/10.1053/j.gastro.2011.10.001
2. Park KT, Bass D. Inflammatory bowel diseaseattributable costs and cost-effective strategies in the United States: a review. Inflamm Bowel Dis 2011; 17:1603-9; PMID:21053357; http://dx.doi. org/10.1002/ibd.21488
3. Benchimol EI, Guttmann A, Griffiths AM, Rabeneck L, Mack DR, Brill H, Howard J, Guan J, To T. Increasing incidence of paediatric inflammatory bowel disease in Ontario, Canada: evidence from health administrative data. Gut 2009; 58:1490-7; PMID:19651626; http://dx.doi.org/10.1136/ gut.2009.188383
4. Abramson O, Durant M, Mow W, Finley A, Kodali P, Wong A, Tavares V, McCroskey E, Liu L, Lewis JD, et al. Incidence, prevalence, and time trends of pediatric inflammatory bowel disease in Northern California, 1996 to 2006. J Pediatr 2010; 157:233, e1; PMID:20400099; http://dx.doi.org/10.1016/j. jpeds.2010.02.024
5. Gupta N, Bostrom AG, Kirschner BS, Ferry GD, Gold BD, Cohen SA, Winter HS, Baldassano RN, Abramson O, Smith T, et al. Incidence of stricturing and penetrating complications of Crohn's disease diagnosed in pediatric patients. Inflamm Bowel Dis 2010; 16:638-44; PMID:19760783; http://dx.doi. org/10.1002/ibd.21099
6. Braegger CP, Ballabeni P, Rogler D, Vavricka SR, Friedt M, Pittet V; Swiss IBD Cohort Study Group. Epidemiology of inflammatory bowel disease: Is there a shift towards onset at a younger age? J Pediatr Gastroenterol Nutr 2011; 53:141-4; PMID:21788753; http://dx.doi.org/10.1097/ MPG.0b013e318218be35
7. Griffiths AM. Specificities of inflammatory bowel disease in childhood. Best Pract Res Clin Gastroenterol 2004; 18:509-23; PMID:15157824; http://dx.doi.org/10.1016/j.bpg.2004.01.002
8. Kappelman MD, Moore KR, Allen JK, Cook SF. Recent trends in the prevalence of Crohn's disease and ulcerative colitis in a commercially insured US population. Dig Dis Sci 2013; 58:519-25; PMID:22926499; http://dx.doi.org/10.1007/ s10620-012-2371-5
9. Rocchi A, Benchimol EI, Bernstein CN, Bitton A, Feagan B, Panaccione R, Glasgow KW, Fernandes A, Ghosh S. Inflammatory bowel disease: a Canadian burden of illness review. Can J Gastroenterol 2012; 26:811-7; PMID:23166905
10. Van Limbergen J, Russell RK, Drummond HE, Aldhous MC, Round NK, Nimmo ER, Smith L, Gillett PM, McGrogan P, Weaver LT, et al. Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology 2008; 135:1114-22; PMID:18725221; http://dx.doi. org/10.1053/j.gastro.2008.06.081
11. Barnett M, Bermingham E, McNabb W, Bassett S, Armstrong K, Rounce J, Roy N. Investigating micronutrients and epigenetic mechanisms in relation to inflammatory bowel disease. Mutat Res 2010; 690:71-80; PMID:20188748; http://dx.doi. org/10.1016/j.mrfmmm.2010.02.006
12. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol 2011; 106:563-73; PMID:21468064; http://dx.doi. org/10.1038/ajg.2011.44
13. Schaible TD, Harris RA, Dowd SE, Smith CW, Kellermayer R. Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet 2011; 20:1687-96; PMID:21296867; http:// dx.doi.org/10.1093/hmg/ddr044
14. Kellermayer R, Balasa A, Zhang W, Lee S, Mirza S, Chakravarty A, Szigeti R, Laritsky E, Tatevian N, Smith CW, et al. Epigenetic maturation in colonic mucosa continues beyond infancy in mice. Hum Mol Genet 2010; 19:2168-76; PMID:20197410; http:// dx.doi.org/10.1093/hmg/ddq095
15. Mir SA, Nagy-Szakal D, Dowd SE, Szigeti RG, Smith CW, Kellermayer R. Prenatal methyl-donor supplementation augments colitis in young adult mice. PLoS One 2013; 8:e73162; PMID:23977377; http://dx.doi.org/10.1371/journal.pone.0073162
16. Lin Z, Hegarty JP, Cappel JA, Yu W, Chen X, Faber P, Wang Y, Kelly AA, Poritz LS, Peterson BZ, et al. Identification of disease-associated DNA methylation in intestinal tissues from patients with inflammatory bowel disease. Clin Genet 2011; 80:59-67; PMID:20950376
17. Kominsky DJ, Keely S, MacManus CF, Glover LE, Scully M, Collins CB, Bowers BE, Campbell EL, Colgan SP. An endogenously anti-inflammatory role for methylation in mucosal inflammation identified through metabolite profiling. J Immunol 2011; 186:6505-14; PMID:21515785; http://dx.doi. org/10.4049/jimmunol.1002805
18. Häsler R, Feng Z, Bäckdahl L, Spehlmann ME, Franke A, Teschendorff A, Rakyan VK, Down TA, Wilson GA, Feber A, et al. A functional methylome map of ulcerative colitis. Genome Res 2012; 22:2130-7; PMID:22826509; http://dx.doi.org/10.1101/ gr.138347.112
19. Turner D, Otley AR, Mack D, Hyams J, de Bruijne J, Uusoue K, Walters TD, Zachos M, Mamula P, Beaton DE, et al. Development, validation, and evaluation of a pediatric ulcerative colitis activity index: a prospective multicenter study. Gastroenterology 2007; 133:423-32; PMID:17681163; http://dx.doi. org/10.1053/j.gastro.2007.05.029
20. Jaffe AE, Murakami P, Lee H, Leek JT, Fallin MD, Feinberg AP, Irizarry RA. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol 2012; 41:200-9; PMID:22422453; http://dx.doi.org/10.1093/ije/ dyr238
21. Kellermayer R. Epigenetics and the developmental origins of inflammatory bowel diseases. Can J Gastroenterol 2012; 26:909-15; PMID:23248794
22. Sandoval J, Heyn H, Moran S, Serra-Musach J, Pujana MA, Bibikova M, Esteller M. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 2011; 6:692-702; PMID:21593595; http://dx.doi.org/10.4161/ epi.6.6.16196
23. Kellermayer R, Mir SA, Nagy-Szakal D, Cox SB, Dowd SE, Kaplan JL, Sun Y, Reddy S, Bronsky J, Winter HS. Microbiota separation and C-reactive protein elevation in treatment-naïve pediatric granulomatous Crohn disease. J Pediatr Gastroenterol Nutr 2012; 55:243-50; PMID:22699834; http:// dx.doi.org/10.1097/MPG.0b013e3182617c16
24. Harris RA, Nagy-Szakal D, Pedersen N, Opekun A, Bronsky J, Munkholm P, Jespersgaard C, Andersen P, Melegh B, Ferry G, et al. Genome-wide peripheral blood leukocyte DNA methylation microarrays identified a single association with inflammatory bowel diseases. Inflamm Bowel Dis 2012; 18:2334-41; PMID:22467598; http://dx.doi.org/10.1002/ ibd.22956
25. Lin Z, Hegarty JP, Yu W, Cappel JA, Chen X, Faber PW, Wang Y, Poritz LS, Fan JB, Koltun WA. Identification of disease-associated DNA methylation in B cells from Crohn's disease and ulcerative colitis patients. Dig Dis Sci 2012; 57:3145-53; PMID:22821069; http://dx.doi.org/10.1007/ s10620-012-2288-z
26. Kellermayer R. Hurdles for epigenetic disease associations from peripheral blood leukocytes. Inflamm Bowel Dis 2013; 19:E66-7; PMID:23314245; http://dx.doi.org/10.1097/ MIB.0b013e318280eca4
27. Jenke AC, Postberg J, Raine T, Nayak KM, Molitor M, Wirth S, Kaser A, Parkes M, Heuschkel RB, Orth V, et al. DNA methylation analysis in the intestinal epithelium-effect of cell separation on gene expression and methylation profile. PLoS One 2013; 8:e55636; PMID:23409010; http://dx.doi.org/10.1371/ journal.pone.0055636
28. Lawrance IC, Fiocchi C, Chakravarti S. Ulcerative colitis and Crohn's disease: distinctive gene expression profiles and novel susceptibility candidate genes. Hum Mol Genet 2001; 10:445-56; PMID:11181568; http://dx.doi.org/10.1093/hmg/10.5.445
29. Xiao YH, Yi H, Tan T, Liang T, Chen ZC, Xiao ZQ. [Analysis of in vitro anti-leukemia effect of 5-aza-2′-deoxycitydine]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2008; 33:344-52; PMID:18460780
30. Schmid M, Fellermann K, Fritz P, Wiedow O, Stange EF, Wehkamp J. Attenuated induction of epithelial and leukocyte serine antiproteases elafin and secretory leukocyte protease inhibitor in Crohn's disease. J Leukoc Biol 2007; 81:907-15; PMID:17200145; http://dx.doi.org/10.1189/jlb.0906581
31. Carey R, Jurickova I, Ballard E, Bonkowski E, Han X, Xu H, Denson LA. Activation of an IL-6:STAT3-dependent transcriptome in pediatric-onset inflammatory bowel disease. Inflamm Bowel Dis 2008; 14:446-57; PMID:18069684; http://dx.doi. org/10.1002/ibd.20342
32. Yang J, Bai W, Niu P, Tian L, Gao A. Aberrant hypomethylated STAT3 was identified as a biomarker of chronic benzene poisoning through integrating DNA methylation and mRNA expression data. Exp Mol Pathol 2014; 96:346-53; PMID:24613686; http://dx.doi.org/10.1016/j.yexmp.2014.02.013
33. Okahara S, Arimura Y, Yabana T, Kobayashi K, Gotoh A, Motoya S, Imamura A, Endo T, Imai K. Inflammatory gene signature in ulcerative colitis with cDNA macroarray analysis. Aliment Pharmacol Ther 2005; 21:1091-7; PMID:15854170; http://dx.doi. org/10.1111/j.1365-2036.2005.02443.x
34. Román J, Planell N, Lozano JJ, Aceituno M, Esteller M, Pontes C, Balsa D, Merlos M, Panés J, Salas A. Evaluation of responsive gene expression as a sensitive and specific biomarker in patients with ulcerative colitis. Inflamm Bowel Dis 2013; 19:221-9; PMID:22605655; http://dx.doi.org/10.1002/ ibd.23020
35. Horii J, Hiraoka S, Kato J, Harada K, Kuwaki K, Fujita H, Toyooka S, Yamamoto K. Age-related methylation in normal colon mucosa differs between the proximal and distal colon in patients who underwent colonoscopy. Clin Biochem 2008; 41:1440-8; PMID:18835263; http://dx.doi. org/10.1016/j.clinbiochem.2008.08.089
36. Wang Y, Devkota S, Musch MW, Jabri B, Nagler C, Antonopoulos DA, Chervonsky A, Chang EB. Regional mucosa-associated microbiota determine physiological expression of TLR2 and TLR4 in murine colon. PLoS One 2010; 5:e13607; PMID:21042588; http://dx.doi.org/10.1371/journal.pone.0013607
37. Lepage P, Häsler R, Spehlmann ME, Rehman A, Zvirbliene A, Begun A, Ott S, Kupcinskas L, Doré J, Raedler A, et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 2011; 141:227-36; PMID:21621540; http://dx.doi. org/10.1053/j.gastro.2011.04.011
38. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003; 23:5293-300; PMID:12861015; http://dx.doi.org/10.1128/ MCB.23.15.5293-5300.2003
39. Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD, Irizarry RA. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics 2014; 30:1363-9; PMID:24478339; http://dx.doi.org/10.1093/ bioinformatics/btu049
40. Smyth GK. Limma: linear models for microarray data. In: R. Gentleman VC, S. Dudoit, R. Irizarry, W. Huber ed. Bioinformatics and Computational Biology Solutions using R and Bioconductor. 2005 ed: Springer, New York, 2005:397-420.
41. Benjamini YHY. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc, B 1995; 57:289-300
42. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004; 20:307-15; PMID:14960456; http://dx.doi.org/10.1093/ bioinformatics/btg405