Promoter methylation of the MGAT3 and BACH2 genes correlates with the composition of the immunoglobulin G glycome in inflammatory bowel disease

Clinical Epigenetics

Volumn 10, Issue 1, 2018, Pages

  Klasić, Marija ^a   Markulin, Dora ^a   Vojta, Aleksandar ^a   Samaržija, Ivana ^a   Biruš, Ivan ^a   Dobrinić, Paula ^a   Ventham, Nicholas T ^b   Trbojević Akmačić, Irena ^c   Šimurina, Mirna ^c   Štambuk, Jerko ^c   Razdorov, Genadij ^c   Kennedy, Nicholas A ^b,e   Satsangi, Jack ^b,j   Dias, Ana M ^f   Pinho, Salome ^f   Annese, Vito ^g   Latiano, Anna ^h   D'Inca, Renata ⁱ   Lauc, Gordan ^c,d   Zoldoš, Vlatka ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^d UNIVERSITY OF ZAGREB   (Croatia)

^e UNIVERSITY OF EXETER   (United Kingdom)

^f UNIVERSITY OF PORTO   (Portugal)

^g CAREGGI UNIVERSITY HOSPITAL   (Italy)

^h IRCCS CSS Hospital   (Italy)

ⁱ UNIVERSITY OF PADOVA   (Italy)

^j UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; CD19 ANTIGEN; IMMUNOGLOBULIN G; N ACETYLGLUCOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE III; UNCLASSIFIED DRUG; BACH2 PROTEIN, HUMAN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BETA-1,4-MANNOSYL-GLYCOPROTEIN BETA-1,4-N-ACETYLGLUCOSAMINYLTRANSFERASE; GLYCOSYLATED IGG; POLYSACCHARIDE;

ARTICLE; B LYMPHOCYTE; BACH2 GENE; CD3+ T LYMPHOCYTE; CELL ISOLATION; COHORT ANALYSIS; COLON BIOPSY; CONTROLLED STUDY; CORRELATIONAL STUDY; CROHN DISEASE; DNA METHYLATION; ENZYME ACTIVITY; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IKZF1 GENE; IL6ST GENE; INFLAMMATORY BOWEL DISEASE; LAMB1 GENE; MAJOR CLINICAL STUDY; MGAT3 GENE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROSPECTIVE STUDY; PYROSEQUENCING; SIALYLATION; ULCERATIVE COLITIS; CASE CONTROL STUDY; DNA SEQUENCE; FEMALE; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; MALE; METABOLISM;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CASE-CONTROL STUDIES; COLITIS, ULCERATIVE; CROHN DISEASE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; IMMUNOGLOBULIN G; INFLAMMATORY BOWEL DISEASES; MALE; N-ACETYLGLUCOSAMINYLTRANSFERASES; POLYSACCHARIDES; PROMOTER REGIONS, GENETIC; PROSPECTIVE STUDIES; SEQUENCE ANALYSIS, DNA;

EID: 85048033567     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-018-0507-y     Document Type: Article

References (70)

1. Burisch J, Pedersen N, Čuković-Čavka S, Brinar M, Kaimakliotis I, Duricova D, Shonová O, Vind I, Avnstrøm S, Thorsgaard N, et al. East-West gradient in the incidence of inflammatory bowel disease in Europe: the ECCO-EpiCom inception cohort. Gut. 2013;63:588-97.
2. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-34.
3. Anderson CA, Boucher G, Lees CW, Franke A, D'Amato M, Taylor KD, Lee JC, Goyette P, Imielinski M, Latiano A, et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet. 2011;43:246-52.
4. Franke A, Balschun T, Sina C, Ellinghaus D, Häsler R, Mayr G, Albrecht M, Wittig M, Buchert E, Nikolaus S, et al. Genome-wide association study for ulcerative colitis identifies risk loci at 7q22 and 22q13 (IL17REL). Nat Genet. 2010;42:292-4.
5. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Lees CW, Balschun T, Lee J, Roberts R, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet. 2010;42:1118-25.
6. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-24.
7. Liu JZ, van Sommeren S, Huang H, Ng SC, Alberts R, Takahashi A, Ripke S, Lee JC, Jostins L, Shah T, et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet. 2015;47:979-86.
8. Bonaz BL, Bernstein CN. Brain-gut interactions in inflammatory bowel disease. Gastroenterology. 2013;144:36-49.
9. Pituch-Zdanowska A, Banaszkiewicz A, Albrecht P. The role of dietary fibre in inflammatory bowel disease. Gastroenterol Rev. 2015;3:135-41.
10. Rubin DT, Hanauer SB. Smoking and inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2000;12:855-62.
11. McDermott E, Ryan EJ, Tosetto M, Gibson D, Burrage J, Keegan D, Byrne K, Crowe E, Sexton G, Malone K, et al. DNA methylation profiling in inflammatory bowel disease provides new insights into disease pathogenesis. J Crohn's Colitis. 2015;10:77-86.
12. Nimmo ER, Prendergast JG, Aldhous MC, Kennedy NA, Henderson P, Drummond HE, Ramsahoye BH, Wilson DC, Semple CA, Satsangi J. 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;18:889-99.
13. Ventham NT, Kennedy NA, Adams AT, Kalla R, Heath S, O'Leary KR, Drummond H, Consortium IB, Consortium IC, Wilson DC, et al: Integrative epigenome-wide analysis demonstrates that DNA methylation may mediate genetic risk in inflammatory bowel disease. Nat Commun 2016, 7:13507.
14. Low D. DNA methylation in inflammatory bowel disease and beyond. World J Gastroenterol. 2013;19:5238.
15. Ventham NT, Kennedy NA, Nimmo ER, Satsangi J. Beyond gene discovery in inflammatory bowel disease: the emerging role of epigenetics. Gastroenterology. 2013;145:293-308.
16. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484-92.
17. Ambatipudi S, Cuenin C, Hernandez-Vargas H, Ghantous A, Le Calvez-Kelm F, Kaaks R, Barrdahl M, Boeing H, Aleksandrova K, Trichopoulou A, et al. Tobacco smoking-associated genome-wide DNA methylation changes in the EPIC study. Epigenomics. 2016;8:599-618.
18. Barrès R, Yan J, Egan B, Treebak Jonas T, Rasmussen M, Fritz T, Caidahl K, Krook A, O'Gorman Donal J, Zierath Juleen R. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15:405-11.
19. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336:489-93.
20. Symonds ME, Sebert SP, Budge H. The impact of diet during early life and its contribution to later disease: critical checkpoints in development and their long-term consequences for metabolic health. Proc Nutr Soc. 2009;68:416.
21. Vaissiere T, Hung RJ, Zaridze D, Moukeria A, Cuenin C, Fasolo V, Ferro G, Paliwal A, Hainaut P, Brennan P, et al. Quantitative analysis of DNA methylation profiles in lung cancer identifies aberrant DNA methylation of specific genes and its association with gender and cancer risk factors. Cancer Res. 2009;69:243-52.
22. Milagro FI, Mansego ML, De Miguel C, Martinez JA. Dietary factors, epigenetic modifications and obesity outcomes: progresses and perspectives. Mol Asp Med. 2013;34:782-812.
23. Adams AT, Kennedy NA, Hansen R, Ventham NT, O'Leary KR, Drummond HE, Noble CL, El-Omar E, Russell RK, Wilson DC, et al. Two-stage genome-wide methylation profiling in childhood-onset Crohn's disease implicates epigenetic alterations at the VMP1/MIR21 and HLA loci. Inflamm Bowel Dis. 2014;20:1784-93.
24. Cooke J, Zhang H, Greger L, Silva A-L, Massey D, Dawson C, Metz A, Ibrahim A, Parkes M. Mucosal genome-wide methylation changes in inflammatory bowel disease. Inflamm Bowel Dis. 2012;18:2128-37.
25. Harris RA, Nagy-Szakal D, Mir SAV, Frank E, Szigeti, Kaplan JL, Bronsky J, Opekun A, Ferry GD, Winter H, Kellermayer R. DNA methylation-associated colonic mucosal immune and defense responses in treatment-naïve pediatric ulcerative colitis. Epigenetics. 2014;9:1131-7.
26. Karatzas PS, Gazouli M, Safioleas M, Mantzaris GJ. DNA methylation changes in inflammatory bowel disease. Ann Gastroenterol. 2014;27:125-32.
27. Hart GW, Copeland RJ. Glycomics hits the big time. Cell. 2010;143:672-6.
28. Böhm S, Kao D, Nimmerjahn F. Sweet and sour: the role of glycosylation for the anti-inflammatory activity of immunoglobulin G. In: Fc Receptors. Basel: Springer International Publishing; 2014. p. 393-417. 393-417.
29. Kaneko Y. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313:670-3.
30. National Research Council (U.S.). Committee on Assessing the Importance and Impact of Glycomics and Glycosciences., National Research Council (U.S.). Board on Chemical Sciences and Technology., National Research Council (U.S.). Board on Life Sciences.: Transforming glycoscience: a roadmap for the future. Washington, D.C.: National Academies Press; 2012.
31. Stowell SR, Ju T, Cummings RD. Protein glycosylation in cancer. Annu Rev Pathol: Mech Dis. 2015;10:473-510.
32. Horvat T, Deželjin M, Redžić I, Barišić D, Herak Bosnar M, Lauc G, Zoldoš V. Reversibility of membrane N-Glycome of HeLa cells upon treatment with epigenetic inhibitors. PLoS One. 2013;8:e54672.
33. Horvat T, Mužinić A, Barišić D, Bosnar MH, Zoldoš V. Epigenetic modulation of the HeLa cell membrane N-glycome. Biochim Biophys Acta Gen Subj. 2012;1820:1412-9.
34. Horvat T, Zoldoš V, Lauc G. Evolutional and clinical implications of the epigenetic regulation of protein glycosylation. Clin Epigenetics. 2011;2:425-32.
35. Klasić M, Krištić J, Korać P, Horvat T, Markulin D, Vojta A, Reiding KR, Wuhrer M, Lauc G, Zoldoš V. DNA hypomethylation upregulates expression of the MGAT3 gene in HepG2 cells and leads to changes in N-glycosylation of secreted glycoproteins. Sci Rep. 2016;6:24363.
36. Saldova R, Dempsey E, Pérez-Garay M, Mariño K, Watson JA, Blanco-Fernández A, Struwe WB, Harvey DJ, Madden SF, Peracaula R, et al. 5-AZA-2'-deoxycytidine induced demethylation influences N-glycosylation of secreted glycoproteins in ovarian cancer. Epigenetics. 2011;6:1362-72.
37. Vojta A, Samaržija I, Bočkor L, Zoldoš V. Glyco-genes change expression in cancer through aberrant methylation. Biochim Biophys Acta Gen Subj. 2016;1860:1776-85.
38. Zoldoš V, Horvat T, Novokmet M, Cuenin C, Mužinić A, Pučić M, Huffman JE, Gornik O, Polašek O, Campbell H, et al. Epigenetic silencing of HNF1A associates with changes in the composition of the human plasma N-glycome. Epigenetics. 2012;7:164-72.
39. Theodoratou E, Campbell H, Ventham NT, Kolarich D, Pučić-Baković M, Zoldoš V, Fernandes D, Pemberton IK, Rudan I, Kennedy NA, et al. The role of glycosylation in IBD. Nat Rev Gastroenterol Hepatol. 2014;11(10):588-600.
40. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol. 2007;25:21-50.
41. Miyahara K, Nouso K, Saito S, Hiraoka S, Harada K, Takahashi S, Morimoto Y, Kobayashi S, Ikeda F, Miyake Y, et al. Serum glycan markers for evaluation of disease activity and prediction of clinical course in patients with ulcerative colitis. PLoS One. 2013;8:e74861.
42. Shinzaki S, Iijima H, Nakagawa T, Egawa S, Nakajima S, Ishii S, Irie T, Kakiuchi Y, Nishida T, Yasumaru M, et al. IgG oligosaccharide alterations are a novel diagnostic marker for disease activity and the clinical course of inflammatory bowel disease. Am J Gastroenterol. 2008;103:1173-81.
43. Trbojevic Akmacic I, Ventham NT, Theodoratou E, Vuckovic F, Kennedy NA, Kristic J, Nimmo ER, Kalla R, Drummond H, Stambuk J, et al. Inflammatory bowel disease associates with proinflammatory potential of the immunoglobulin G glycome. Inflamm Bowel Dis. 2015;21:1237-47.
44. Plomp R, Ruhaak LR, Uh HW, Reiding KR, Selman M, Houwing-Duistermaat JJ, Slagboom PE, Beekman M, Wuhrer M. Subclass-specific IgG glycosylation is associated with markers of inflammation and metabolic health. Sci Rep. 2017;7:12325.
45. Schwab I, Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat Rev Immunol. 2013;13:176-89.
46. Simurina M, de Haan N, Vuckovic F, Kennedy NA, Stambuk J, Falck D, Trbojevic-Akmacic I, Clerc F, Razdorov G, Khon A, et al: Glycosylation of immunoglobulin G associates with clinical features of inflammatory bowel diseases. Gastroenterology. 2018;154(5):1320-1333.e10.
47. Barrett JC, Lee JC, Lees CW, Prescott NJ, Anderson CA, Phillips A, Wesley E, Parnell K, Zhang H, Drummond H, et al. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet. 2009;41:1330-4.
48. McGovern DPB, Jones MR, Taylor KD, Marciante K, Yan X, Dubinsky M, Ippoliti A, Vasiliauskas E, Berel D, Derkowski C, et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 2010;19:3468-76.
49. Lauc G, Huffman JE, Pucic M, Zgaga L, Adamczyk B, Muzinic A, Novokmet M, Polasek O, Gornik O, Kristic J, et al. Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet. 2013;9:e1003225.
50. Dias AM, Dourado J, Lago P, Cabral J, Marcos-Pinto R, Salgueiro P, Almeida CR, Carvalho S, Fonseca S, Lima M, et al. Dysregulation of T cell receptor N-glycosylation: a molecular mechanism involved in ulcerative colitis. Hum Mol Genet. 2014;23:2416-27.
51. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlen SE, Greco D, Soderhall C, Scheynius A, Kere J. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One. 2012;7:e41361.
52. Krištić J, Zoldoš V, Lauc G. Complex genetics of protein N-glycosylation. In: Endo T, Seeberger PH, Hart GW, Wong C-H, Taniguchi N, editors. Glycoscience: biology and medicine. Tokyo: Springer Japan; 2014. p. 1-7.
53. Stewart SK, Morris TJ, Guilhamon P, Bulstrode H, Bachman M, Balasubramanian S, Beck S. oxBS-450K: a method for analysing hydroxymethylation using 450K BeadChips. Methods. 2015;72:9-15.
54. Kroeze LI, Aslanyan MG, van Rooij A, Koorenhof-Scheele TN, Massop M, Carell T, Boezeman JB, Marie JP, Halkes CJ, de Witte T, et al. Characterization of acute myeloid leukemia based on levels of global hydroxymethylation. Blood. 2014;124:1110-8.
55. Sanchez-Guerra M, Zheng Y, Osorio-Yanez C, Zhong J, Chervona Y, Wang S, Chang D, McCracken JP, Diaz A, Bertazzi PA, et al. Effects of particulate matter exposure on blood 5-hydroxymethylation: results from the Beijing truck driver air pollution study. Epigenetics. 2015;10:633-42.
56. Yu M, Hon GC, Szulwach KE, Song CX, Zhang L, Kim A, Li X, Dai Q, Shen Y, Park B, et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell. 2012;149:1368-80.
57. Pucic M, Knezevic A, Vidic J, Adamczyk B, Novokmet M, Polasek O, Gornik O, Supraha-Goreta S, Wormald MR, Redzic I, et al. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics. 2011;M111(010090):10.
58. Trbojevic-Akmacic I, Ugrina I, Lauc G. Comparative analysis and validation of different steps in glycomics studies. Methods Enzymol. 2017;586:37-55.
59. Selman MH, Derks RJ, Bondt A, Palmblad M, Schoenmaker B, Koeleman CA, van de Geijn FE, Dolhain RJ, Deelder AM, Wuhrer M. Fc specific IgG glycosylation profiling by robust nano-reverse phase HPLC-MS using a sheath-flow ESI sprayer interface. J Proteome. 2012;75:1318-29.
60. Jansen BC, Falck D, de Haan N, Hipgrave Ederveen AL, Razdorov G, Lauc G, Wuhrer M. LaCyTools: a targeted liquid chromatography-mass spectrometry data processing package for relative quantitation of glycopeptides. J Proteome Res. 2016;15:2198-210.
61. Fujii S, Nishiura T, Nishikawa A, Miura R, Taniguchi N. Structural heterogeneity of sugar chains in immunoglobulin G. Conformation of immunoglobulin G molecule and substrate specificities of glycosyltransferases. J Biol Chem. 1990;265:6009-18.
62. Igarashi K, Ochiai K, Itoh-Nakadai A, Muto A. Orchestration of plasma cell differentiation by Bach2 and its gene regulatory network. Immunol Rev. 2014;261:116-25.
63. Kuwahara M, Suzuki J, Tofukuji S, Yamada T, Kanoh M, Matsumoto A, Maruyama S, Kometani K, Kurosaki T, Ohara O, et al. The Menin-Bach2 axis is critical for regulating CD4 T-cell senescence and cytokine homeostasis. Nat Commun. 2014;5:3555.
64. Dekkers G, Plomp R, Koeleman CA, Visser R, von Horsten HH, Sandig V, Rispens T, Wuhrer M, Vidarsson G. Multi-level glyco-engineering techniques to generate IgG with defined Fc-glycans. Sci Rep. 2016;6:36964.
65. Chu X, Pan C-M, Zhao S-X, Liang J, Gao G-Q, Zhang X-M, Yuan G-Y, Li C-G, Xue L-Q, Shen M, et al. A genome-wide association study identifies two new risk loci for Graves' disease. Nat Genet. 2011;43:897-901.
66. Dubois PCA, Trynka G, Franke L, Hunt KA, Romanos J, Curtotti A, Zhernakova A, Heap GAR, Ádány R, Aromaa A, et al. Multiple common variants for celiac disease influencing immune gene expression. Nat Genet. 2010;42:295-302.
67. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, Freeman C, Hunt SE, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature. 2011;476:214-9.
68. Macdonald TT, Monteleone G. Immunity, inflammation, and allergy in the gut. Science. 2005;307:1920-5.
69. Vossenkamper A, Hundsrucker C, Page K, van Maurik A, Sanders TJ, Stagg AJ, Das L, MacDonald TT. A CD3-specific antibody reduces cytokine production and alters phosphoprotein profiles in intestinal tissues from patients with inflammatory bowel disease. Gastroenterology. 2014;147:172-83.
70. Jaffe AE, Irizarry RA. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014;15:R31.