Intestinal DMBT1 expression is modulated by Crohn's disease-associated IL23R variants and by a DMBT1 variant which influences binding of the transcription factors CREB1 and ATF-2

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Diegelmann, Julia ^a,b   Czamara, Darina ^c,d   Le Bras, Emmanuelle ^a   Zimmermann, Eva ^b   Olszak, Torsten ^a,e   Bedynek, Andrea ^b   Göke, Burkhard ^a   Franke, Andre ^f   Glas, Jürgen ^a,b,g   Brand, Stephan ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^d Germany 3 Munich Cluster for Systems Neurology   (Germany)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f UNIVERSITY OF KIEL   (Germany)

^g RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOPROTEIN; INTERLEUKIN 22; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 27; PROTEIN DMBT1; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ALLELE; ARTICLE; BINDING SITE; CASE CONTROL STUDY; CONTROLLED STUDY; CROHN DISEASE; DISEASE PREDISPOSITION; DMBT1 GENE; DNA BINDING; EPISTASIS; EPITHELIUM CELL; FEMALE; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC TRANSFECTION; GENETIC VARIABILITY; HAPLOTYPE; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IL23R GENE; IL27 GENE; IN VITRO STUDY; INTESTINE EPITHELIUM; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NOD2 GENE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; VERY ELDERLY; YOUNG ADULT;

ACTIVATING TRANSCRIPTION FACTOR 2; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BASE SEQUENCE; BINDING SITES; CASE-CONTROL STUDIES; CROHN DISEASE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EPISTASIS, GENETIC; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTERLEUKINS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECEPTORS, INTERLEUKIN; SEQUENCE ANALYSIS, DNA; TRANSCRIPTIONAL ACTIVATION; YOUNG ADULT;

EID: 84892384785     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077773     Document Type: Article

References (51)

1. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, et al. (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
2. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, et al. (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
3. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, et al. (2007) A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 39: 207-211.
4. Glas J, Konrad A, Schmechel S, Dambacher J, Seiderer J, et al. (2008) The ATG16L1 gene variants rs2241879 and rs2241880 (T300A) are strongly associated with susceptibility to Crohn's disease in the German population. Am J Gastroenterol 103: 682-691.
5. Parkes M, Barrett JC, Prescott NJ, Tremelling M, Anderson CA, et al. (2007) Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat Genet 39: 830-832.
6. Glas J, Seiderer J, Bues S, Stallhofer J, Fries C, et al. (2013) IRGM variants and susceptibility to inflammatory bowel disease in the German population PLoS One 8: e54338.
7. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, et al. (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314: 1461-1463.
8. Glas J, Seiderer J, Wetzke M, Konrad A, Török HP, et al. (2007) rs1004819 is the main disease-associated IL23R variant in German Crohn's disease patients: combined analysis of IL23R, CARD15, and OCTN1/2 variants. PLoS One 2: e819.
9. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, et al. (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491: 119-124.
10. Glas J, Stallhofer J, Ripke S, Wetzke M, Pfennig S, et al. (2009) Novel genetic risk markers for ulcerative colitis in the IL2/IL21 region are in epistasis with IL23R and suggest a common genetic background for ulcerative colitis and celiac disease. Am J Gastroenterol 104: 1737-1744.
11. Loimaranta V, Hytonen J, Pulliainen AT, Sharma A, Tenovuo J, et al. (2009) Leucine-rich repeats of bacterial surface proteins serve as common pattern recognition motifs of human scavenger receptor gp340. J Biol Chem 284: 18614-18623.
12. Rosenstiel P, Sina C, End C, Renner M, Lyer S, et al. (2007) Regulation of DMBT1 via NOD2 and TLR4 in intestinal epithelial cells modulates bacterial recognition and invasion. J Immunol 178: 8203-8211.
13. Edwards AM, Manetti AG, Falugi F, Zingaretti C, Capo S, et al. (2008) Scavenger receptor gp340 aggregates group A streptococci by binding pili. Mol Microbiol 68: 1378-1394.
14. Holmskov U, Lawson P, Teisner B, Tornoe I, Willis AC, et al. (1997) Isolation and characterization of a new member of the scavenger receptor superfamily, glycoprotein-340 (gp-340), as a lung surfactant protein-D binding molecule. J Biol Chem 272: 13743-13749.
15. Bikker FJ, Ligtenberg AJ, Nazmi K, Veerman EC, van't Hof W, et al. (2002) Identification of the bacteria-binding peptide domain on salivary agglutinin (gp-340/DMBT1), a member of the scavenger receptor cysteine-rich superfamily. J Biol Chem 277: 32109-32115.
16. End C, Bikker F, Renner M, Bergmann G, Lyer S, et al. (2009) DMBT1 functions as pattern-recognition molecule for poly-sulfated and poly-phosphorylated ligands. Eur J Immunol 39: 833-842.
17. Brand S, Staudinger T, Schnitzler F, Pfennig S, Hofbauer K, et al. (2005) The role of Toll-like receptor 4 Asp299Gly and Thr399Ile polymorphisms and CARD15/NOD2 mutations in the susceptibility and phenotype of Crohn's disease. Inflamm Bowel Dis 11: 645-652.
18. De Jager PL, Franchimont D, Waliszewska A, Bitton A, Cohen A, et al. (2007) The role of the Toll receptor pathway in susceptibility to inflammatory bowel diseases. Genes Immun 8: 387-397.
19. De Lisle RC, Xu W, Roe BA, Ziemer D (2008) Effects of Muclin (Dmbt1) deficiency on the gastrointestinal system. Am J Physiol Gastrointest Liver Physiol 294: G717-727.
20. Renner M, Bergmann G, Krebs I, End C, Lyer S, et al. (2007) DMBT1 confers mucosal protection in vivo and a deletion variant is associated with Crohn's disease. Gastroenterology 133: 1499-1509.
21. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, et al. (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A 110: 3507-3512.
22. Fukui H, Sekikawa A, Tanaka H, Fujimori Y, Katake Y, et al. (2011) DMBT1 is a novel gene induced by IL-22 in ulcerative colitis. Inflamm Bowel Dis 17: 1177-1188.
23. Diegelmann J, Olszak T, Göke B, Blumberg RS, Brand S (2012) A novel role for interleukin-27 (IL-27) as mediator of intestinal epithelial barrier protection mediated via differential signal transducer and activator of transcription (STAT) protein signaling and induction of antibacterial and anti-inflammatory proteins. J Biol Chem 287: 286-298.
24. Cayatte C, Joyce-Shaikh B, Vega F, Boniface K, Grein J, et al. (2012) Biomarkers of therapeutic response in the IL-23 pathway in inflammatory bowel disease. Clin Transl Gastroenterol 3: e10.
25. Dambacher J, Beigel F, Seiderer J, Haller D, Goeke B, et al. (2007) Interleukin 31 mediates MAP kinase and STAT1/3 activation in intestinal epithelial cells and its expression is upregulated in inflammatory bowel disease. Gut 56: 1257-1265.
26. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, et al. (1998) Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 26: 362-367.
27. Dignam JD, Lebovitz RM, Roeder RG (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475-1489.
28. Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, et al. (2005) 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 19 Suppl A: 5-36.
29. Seiderer J, Brand S, Herrmann KA, Schnitzler F, Hatz R, et al. (2006) Predictive value of the CARD15 variant 1007fs for the diagnosis of intestinal stenoses and the need for surgery in Crohn's disease in clinical practice: results of a prospective study. Inflamm Bowel Dis 12: 1114-1121.
30. Seiderer J, Schnitzler F, Brand S, Staudinger T, Pfennig S, et al. (2006) Homozygosity for the CARD15 frameshift mutation 1007fs is predictive of early onset of Crohn's disease with ileal stenosis, entero-enteral fistulas, and frequent need for surgical intervention with high risk of re-stenosis. Scand J Gastroenterol 41: 1421-1432.
31. Schnitzler F, Brand S, Staudinger T, Pfennig S, Hofbauer K, et al. (2006) Eight novel CARD15 variants detected by DNA sequence analysis of the CARD15 gene in 111 patients with inflammatory bowel disease. Immunogenetics 58: 99-106.
32. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, et al. (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 42: 1118-1125.
33. Glas J, Seiderer J, Tillack C, Pfennig S, Beigel F, et al. (2010) The NOD2 single nucleotide polymorphisms rs2066843 and rs2076756 are novel and common Crohn's disease susceptibility gene variants. PLoS One 5: e14466.
34. Schmechel S, Konrad A, Diegelmann J, Glas J, Wetzke M, et al. (2008) Linking genetic susceptibility to Crohn's disease with Th17 cell function: IL-22 serum levels are increased in Crohn's disease and correlate with disease activity and IL23R genotype status. Inflamm Bowel Dis 14: 204-212.
35. Brand S, Beigel F, Olszak T, Zitzmann K, Eichhorst ST, et al. (2006) IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am J Physiol Gastrointest Liver Physiol 290: G827-838.
36. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, et al. (2006) Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 203: 2271-2279.
37. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, et al. (2004) IL-22 increases the innate immunity of tissues. Immunity 21: 241-254.
38. Andoh A, Zhang Z, Inatomi O, Fujino S, Deguchi Y, et al. (2005) Interleukin-22, a member of the IL-10 subfamily, induces inflammatory responses in colonic subepithelial myofibroblasts. Gastroenterology 129: 969-984.
39. Diveu C, McGeachy MJ, Boniface K, Stumhofer JS, Sathe M, et al. (2009) IL-27 blocks RORc expression to inhibit lineage commitment of Th17 cells. J Immunol 182: 5748-5756.
40. Imielinski M, Baldassano RN, Griffiths A, Russell RK, Annese V, et al. (2009) Common variants at five new loci associated with early-onset inflammatory bowel disease. Nat Genet 41: 1335-1340.
41. Jürgens M, Laubender RP, Hartl F, Weidinger M, Seiderer J, et al. (2010) Disease activity, ANCA, and IL23R genotype status determine early response to infliximab in patients with ulcerative colitis. Am J Gastroenterol 105: 1811- 1819.
42. Barrett JC, Hansoul S, Nicolae DL, Cho JH, Duerr RH, et al. (2008) Genomewide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 40: 955-962.
43. Anderson CA, Boucher G, Lees CW, Franke A, D'Amato M, et al. (2011) Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 43: 246-252.
44. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, et al. (2007) Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 39: 596-604.
45. Glas J, Seiderer J, Pasciuto G, Tillack C, Diegelmann J, et al. (2009) rs224136 on chromosome 10q21.1 and variants in PHOX2B, NCF4, and FAM92B are not major genetic risk factors for susceptibility to Crohn's disease in the German population. Am J Gastroenterol 104: 665-672.
46. Stoll M, Corneliussen B, Costello CM, Waetzig GH, Mellgard B, et al. (2004) Genetic variation in DLG5 is associated with inflammatory bowel disease. Nat Genet 36: 476-480.
47. Browning BL, Annese V, Barclay ML, Bingham SA, Brand S, et al. (2008) Gender-stratified analysis of DLG5 R30Q in 4707 patients with Crohn disease and 4973 controls from 12 Caucasian cohorts. J Med Genet 45: 36-42.
48. Dinu I, Mahasirimongkol S, Liu Q, Yanai H, Sharaf Eldin N, et al. (2012) SNPSNP interactions discovered by logic regression explain Crohn's disease genetics. PLoS One 7: e43035.
49. Sotelo J, Esposito D, Duhagon MA, Banfield K, Mehalko J, et al. (2010) Long-range enhancers on 8 q24 regulate c-Myc. Proc Natl Acad Sci U S A 107: 3001-3005.
50. Ong CT, Corces VG (2011) Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet 12: 283-293.
51. Wen AY, Sakamoto KM, Miller LS (2010) The role of the transcription factor CREB in immune function. J Immunol 185: 6413-6419.