A Promoter Variant Within the Aryl Hydrocarbon Receptor Gene Is Associated with an Epithelial Barrier Defect in Smokers with Crohn's Disease

Inflammatory Bowel Diseases

Volumn 22, Issue 10, 2016, Pages 2356-2368

  Prager, Matthias ^a   Büttner, Janine ^a   Grunert, Philip ^a   Ellinghaus, David ^b   Büning, Carsten ^a,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c Krankenhaus Waldfriede   (Germany)

Author keywords

AHR; aryl hydrocarbon receptor; Crohn's disease; intestinal permeability; smoking; ulcerative colitis

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; AHR PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR;

ADULT; ARTICLE; CASE CONTROL STUDY; COHORT ANALYSIS; COLON BIOPSY; CONTROLLED STUDY; CROHN DISEASE; EXON; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; INTESTINE MUCOSA PERMEABILITY; INTRON; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE STUDY; REAL TIME POLYMERASE CHAIN REACTION; SMOKING HABIT; ULCERATIVE COLITIS; ADOLESCENT; COLON; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENETICS; GENOTYPE; INTESTINE MUCOSA; PATHOLOGY; PERMEABILITY; PHENOTYPE; SEQUENCE ANALYSIS; SMOKING; YOUNG ADULT;

ADOLESCENT; ADULT; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CASE-CONTROL STUDIES; COLON; CROHN DISEASE; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOTYPE; HUMANS; INTESTINAL MUCOSA; MALE; PERMEABILITY; PHENOTYPE; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ARYL HYDROCARBON; SEQUENCE ANALYSIS; SMOKING; YOUNG ADULT;

EID: 84988660530     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000910     Document Type: Article

References (60)

1. Higuchi LM, Khalili H, Chan AT, et al. A prospective study of cigarette smoking and the risk of inflammatory bowel disease in women. Am J Gastroenterol. 2012;107:1399-1406
2. Mahid SS, Minor KS, Soto RE, et al. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006;81:1462-1471
3. Breuer-Katschinski BD, Hollander N, Goebell H. Effect of cigarette smoking on the course of Crohn's disease. Eur J Gastroenterol Hepatol. 1996;8:225-228
4. Cosnes J. Smoking, physical activity, nutrition and lifestyle: environmental factors and their impact on IBD. Dig Dis. 2010;28:411-417
5. Louis E, Michel V, Hugot JP, et al. Early development of stricturing or penetrating pattern in Crohn's disease is influenced by disease location, number of flares, and smoking but not by NOD2/CARD15 genotype. Gut. 2003;52:552-557
6. Picco MF, Bayless TM. Tobacco consumption and disease duration are associated with fistulizing and stricturing behaviors in the first 8 years of Crohn's disease. Am J Gastroenterol. 2003;98:363-368
7. Cottone M, Rosselli M, Orlando A, et al. Smoking habits and recurrence in Crohn's disease. Gastroenterology. 1994;106:643-648
8. Sutherland LR, Ramcharan S, Bryant H, et al. Effect of cigarette smoking on recurrence of Crohn's disease. Gastroenterology. 1990;98:1123-1128
9. Monteleone I, MacDonald TT, Pallone F, et al. The aryl hydrocarbon receptor in inflammatory bowel disease: linking the environment to disease pathogenesis. Curr Opin Gastroenterol. 2012;28:310-313
10. Gu YZ, Hogenesch JB, Bradfield CA. The PAS superfamily: sensors of environmental and developmental signals. Annu Review Pharmacol Toxicol. 2000;40:519-561
11. Kerkvliet NI. Recent advances in understanding the mechanisms of TCDD immunotoxicity. Int Immunopharmacol. 2002;2:277-291
12. Beischlag TV, Luis Morales J, Hollingshead BD, et al. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr. 2008;18:207-250
13. Gambier N, Marteau JB, Batt AM, et al. Interaction between CYP1A1 T3801C and AHR G1661A polymorphisms according to smoking status on blood pressure in the Stanislas cohort. J Hypertens. 2006;24: 2199-2205
14. Huang S, Shui X, He Y, et al. AhR expression and polymorphisms are associated with risk of coronary arterial disease in Chinese population. Sci Rep. 2015;5:8022
15. Liu JZ, van Sommeren S, Huang H, et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet. 2015;47:979-986
16. Hollander D, Vadheim CM, Brettholz E, et al. Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann Intern Med. 1986;105:883-885
17. Beadsmoore C, Cheow HK, Szczepura K, et al. Healthy passive cigarette smokers have increased pulmonary alveolar permeability. Nucl Med Commun. 2007;28:75-77
18. Jones JG, Minty BD, Lawler P, et al. Increased alveolar epithelial permeability in cigarette smokers. Lancet. 1980;1:66-68
19. Dignass A, Eliakim R, Magro F, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 1: definitions and diagnosis. J Crohn's Colitis. 2012;6:965-990
20. Van Assche G, Dignass A, Panes J, et al. The second European evidencebased Consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis. J Crohn's Colitis. 2010;4:7-27
21. Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(suppl ):5A-36A
22. Buhner S, Reese I, Kuehl F, et al. Pseudoallergic reactions in chronic urticaria are associated with altered gastroduodenal permeability. Allergy. 2004;59:1118-1123
23. Wyatt J, Vogelsang H, Hubl W, et al. Intestinal permeability and the prediction of relapse in Crohn's disease. Lancet. 1993;341:1437-1439
24. Buhner S, Buning C, Genschel J, et al. Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation? Gut. 2006;55:342-347
25. Prager M, Durmus T, Buttner J, et al. Myosin IXb variants and their pivotal role in maintaining the intestinal barrier: a study in Crohn's disease. Scand J Gastroenterol. 2014;49:1191-1200
26. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res. 2001;11:863-874
27. Adzhubei IA, Schmidt S, Peshkin L, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7: 248-249
28. Heinemeyer T, Wingender E, Reuter I, et al. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res. 1998; 26:362-367
29. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74
30. Consortium G. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science. 2015;348:648-660
31. Kheradpour P, Kellis M. Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments. Nucleic Acids Res. 2014;42:2976-2987
32. Kundaje A, Meuleman W, Ernst J, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518:317-330
33. Ward LD, Kellis M. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Nucleic Acids Res. 2012;40:D930-D934
34. Berger MF, Philippakis AA, Qureshi AM, et al. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol. 2006;24:1429-1435
35. Badis G, Berger MF, Philippakis AA, et al. Diversity and complexity in DNA recognition by transcription factors. Science. 2009;324:1720-1723
36. Berger MF, Badis G, Gehrke AR, et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell. 2008;133:1266-1276
37. Touzet H, Varre JS. Efficient and accurate P-value computation for Position Weight Matrices. Algorithms Mol Biol. 2007;2:15
38. Cauchi S, Stucker I, Solas C, et al. Polymorphisms of human aryl hydrocarbon receptor (AhR) gene in a French population: relationship with CYP1A1 inducibility and lung cancer. Carcinogenesis. 2001;22: 1819-1824
39. Bamias G, Goukos D, Laoudi E, et al. Comparative study of candidate housekeeping genes for quantification of target gene messenger RNA expression by real-time PCR in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2013;19:2840-2847
40. Kim JH, Kim H, Lee KY, et al. Aryl hydrocarbon receptor gene polymorphisms affect lung cancer risk. Lung Cancer. 2007;56:9-15
41. Perez-Morales R, Mendez-Ramirez I, Moreno-Macias H, et al. Genetic susceptibility to lung cancer based on candidate genes in a sample from the Mexican Mestizo population: a case-control study. Lung. 2014;192: 167-173
42. Moorthy B, Chu C, Carlin DJ. Polycyclic aromatic hydrocarbons: from metabolism to lung cancer. Toxicol Sci. 2015;145:5-15
43. Zuo L, Li Y, Wang H, et al. Cigarette smoking is associated with intestinal barrier dysfunction in the small intestine but not in the large intestine of mice. J Crohn's Colitis. 2014;8:1710-1722
44. Kevans D, Turpin W, Madsen K, et al. Determinants of intestinal permeability in healthy first-degree relatives of individuals with Crohn's disease. Inflamm Bowel Dis. 2015;21:879-887
45. Blomquist L, Bark T, Hedenborg G, et al. Evaluation of the lactulose/ mannitol and 51Cr-ethylenediaminetetraacetic acid/14C-mannitol methods for intestinal permeability. Scand J Gastroenterol. 1997;32: 805-812
46. Prytz H, Benoni C, Tagesson C. Does smoking tighten the gut? Scand J Gastroenterol. 1989;24:1084-1088
47. Suenaert P, Bulteel V, Den Hond E, et al. The effects of smoking and indomethacin on small intestinal permeability. Aliment Pharmacol Ther. 2000;14:819-822
48. Quintana FJ, Basso AS, Iglesias AH, et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature. 2008;453: 65-71
49. Brand S. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut. 2009;58:1152-1167
50. Feng Y, Teitelbaum DH. Tumour necrosis factor-induced loss of intestinal barrier function requires TNFR1 and TNFR2 signalling in a mouse model of total parenteral nutrition. J Physiol. 2013;591:3709-3723
51. Ma TY, Iwamoto GK, Hoa NT, et al. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol. 2004;286: G367-G376
52. Amasheh M, Fromm A, Krug SM, et al. TNFalpha-induced and berberineantagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkappaB signaling. J Cell Sci. 2010;123:4145-4155
53. Prager M, Buttner J, Haas V, et al. The JAK2 variant rs10758669 in Crohn's disease: altering the intestinal barrier as one mechanism of action. Int J Colorectal Dis. 2012;27:565-573
54. McCole DF. IBD candidate genes and intestinal barrier regulation. Inflamm Bowel Dis. 2014;20:1829-1849
55. Benoni C, Prytz H. Effects of smoking on the urine excretion of oral 51Cr EDTA in ulcerative colitis. Gut. 1998;42:656-658
56. Kasai A, Hiramatsu N, Hayakawa K, et al. High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing. Cancer Res. 2006;66:7143-7150
57. Kitamura M, Kasai A. Cigarette smoke as a trigger for the dioxin receptormediated signaling pathway. Cancer Lett. 2007;252:184-194
58. Tian Y, Rabson AB, Gallo MA. Ah receptor and NF-kappaB interactions: mechanisms and physiological implications. Chem Biol Interact. 2002; 141:97-115
59. Tian Y. Ah receptor and NF-kappaB interplay on the stage of epigenome. Biochem Pharmacol. 2009;77:670-680
60. Arsenescu R, Arsenescu V, Zhong J, et al. Role of the xenobiotic receptor in inflammatory bowel disease. Inflamm Bowel Dis. 2011;17:1149-1162