Genetic Analysis of Innate Immunity in Crohn's Disease and Ulcerative Colitis Identifies Two Susceptibility Loci Harboring CARD9 and IL18RAP

American Journal of Human Genetics

Volumn 82, Issue 5, 2008, Pages 1202-1210

  Zhernakova, Alexandra ^a   Festen, Eleanora M ^b   Franke, Lude ^a,b   Trynka, Gosia ^b   van Diemen, Cleo C ^b   Monsuur, Alienke J ^a   Bevova, Marianna ^a   Nijmeijer, Rian M ^a   van 't Slot, Ruben ^a   Heijmans, Roel ^c   Boezen, H Marike ^b   van Heel, David A ^d   van Bodegraven, Adriaan A ^c   Stokkers, Pieter C F ^e   Wijmenga, Cisca ^a,b   Crusius, J Bart A ^c   Weersma, Rinse K ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOSOME; CASPASE RECRUITMENT DOMAIN GENE; CONTROLLED STUDY; CROHN DISEASE; DISEASE PREDISPOSITION; ENTERITIS; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE REPLICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC SUSCEPTIBILITY; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN GENOME; IL18RAP GENE; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; ULCERATIVE COLITIS;

CARD SIGNALING ADAPTOR PROTEINS; COLITIS, ULCERATIVE; CROHN DISEASE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNITY, NATURAL; INTERLEUKIN-18 RECEPTOR BETA SUBUNIT; LINKAGE DISEQUILIBRIUM; MALE;

EID: 42749096082     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajhg.2008.03.016     Document Type: Article

References (53)

1. Binder V., Both H., Hansen P.K., Hendriksen C., Kreiner S., and Torp-Pedersen K. Incidence and prevalence of ulcerative colitis and Crohn's disease in the County of Copenhagen, 1962 to 1978. Gastroenterology 83 (1982) 563-568
2. Podolsky D.K. Inflammatory bowel disease. N. Engl. J. Med. 347 (2002) 417-429
3. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., Britton H., Moran T., Karaliuskas R., Duerr R.H., et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411 (2001) 603-606
4. Oostenbrug L.E., Drenth J.P., de Jong D.J., Nolte I.M., Oosterom E., van Dullemen H.M., van der Linde K., te Meerman G.J., van der Steege G., Kleibeuker J.H., and Jansen P.L. Association between Toll-like receptor 4 and inflammatory bowel disease. Inflamm. Bowel Dis. 11 (2005) 567-575
5. De Jager P.L., Franchimont D., Waliszewska A., Bitton A., Cohen A., Langelier D., Belaiche J., Vermeire S., Farwell L., Goris A., et al. The role of the Toll receptor pathway in susceptibility to inflammatory bowel diseases. Genes Immun. 8 (2007) 387-397
6. McGovern D.P., Hysi P., Ahmad T., van Heel D.A., Moffatt M.F., Carey A., Cookson W.O., and Jewell D.P. Association between a complex insertion/deletion polymorphism in NOD1 (CARD4) and susceptibility to inflammatory bowel disease. Hum. Mol. Genet. 14 (2005) 1245-1250
7. Duerr R.H., Taylor K.D., Brant S.R., Rioux J.D., Silverberg M.S., Daly M.J., Steinhart A.H., Abraham C., Regueiro M., Griffiths A., et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314 (2006) 1461-1463
8. Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447 (2007) 661-678
9. Parkes M., Barrett J.C., Prescott N.J., Tremelling M., Anderson C.A., Fisher S.A., Roberts R.G., Nimmo E.R., Cummings F.R., Soars D., et al. Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 39 (2007) 830-832
10. Libioulle C., Louis E., Hansoul S., Sandor C., Farnir F., Franchimont D., Vermeire S., Dewit O., de Vos M., Dixon A., et al. Novel Crohn disease locus identified by genome-wide association maps to a gene desert on 5p13.1 and modulates expression of PTGER4. PLoS Genet 3 (2007) e58
11. Hampe J., Franke A., Rosenstiel P., Till A., Teuber M., Huse K., Albrecht M., Mayr G., De La Vega F.M., Briggs J., et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39 (2007) 207-211
12. Mitchell J.A., Paul-Clark M.J., Clarke G.W., McMaster S.K., and Cartwright N. Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J. Endocrinol. 193 (2007) 323-330
13. Becker C.E., and O'Neill L.A. Inflammasomes in inflammatory disorders: The role of TLRs and their interactions with NLRs. Semin. Immunopathol. 29 (2007) 239-248
14. Fritz J.H., and Girardin S.E. How Toll-like receptors and Nod-like receptors contribute to innate immunity in mammals. J. Endotoxin Res. 11 (2005) 390-394
15. Fritz J.H., Ferrero R.L., Philpott D.J., and Girardin S.E. Nod-like proteins in immunity, inflammation and disease. Nat. Immunol. 7 (2006) 1250-1257
16. Miggin S.M., and O'Neill L.A. New insights into the regulation of TLR signaling. J. Leukoc. Biol. 80 (2006) 220-226
17. Harris G., KuoLee R., and Chen W. Role of Toll-like receptors in health and diseases of gastrointestinal tract. World J. Gastroenterol. 12 (2006) 2149-2160
18. Yamamoto-Furusho J.K., and Podolsky D.K. Innate immunity in inflammatory bowel disease. World J. Gastroenterol. 13 (2007) 5577-5580
19. van Bodegraven A.A., Curley C.R., Hunt K.A., Monsuur A.J., Linskens R.K., Onnie C.M., Crusius J.B., Annese V., Latiano A., Silverberg M.S., et al. Genetic variation in myosin IXB is associated with ulcerative colitis. Gastroenterology 131 (2006) 1768-1774
20. Weersma R.K., Zhernakova A., Nolte I.M., Lefebvre C., Rioux J.D., Mulder F., van Dullemen H.M., Kleibeuker J.H., Wijmenga C., and Dijkstra G. ATG16L1 and IL23R are associated with inflammatory bowel diseases but not with celiac disease in the netherlands. Am. J. Gastroenterol. 103 (2007) 621-627
21. Stokkers P.C., Huibregtse Jr. K., Leegwater A.C., Reitsma P.H., Tytgat G.N., and van Deventer S.J. Analysis of a positional candidate gene for inflammatory bowel disease: NRAMP2. Inflamm. Bowel Dis. 6 (2000) 92-98
22. van Heel D.A., Franke L., Hunt K.A., Gwilliam R., Zhernakova A., Inouye M., Wapenaar M.C., Barnardo M.C., Bethel G., Holmes G.K., et al. A genome-wide association study for celiac disease identifies risk variants in the region harboring IL2 and IL21. Nat. Genet. 39 (2007) 827-829
23. Zhernakova A., Eerligh P., Barrera P., Wesoly J.Z., Huizinga T.W., Roep B.O., Wijmenga C., and Koeleman B.P. CTLA4 is differentially associated with autoimmune diseases in the Dutch population. Hum. Genet. 118 (2005) 58-66
24. Rijcken B., Schouten J.P., Mensinga T.T., Weiss S.T., De Vries K., and Van der Lende R. Factors associated with bronchial responsiveness to histamine in a population sample of adults. Am. Rev. Respir. Dis. 147 (1993) 1447-1453
25. van Diemen C.C., Postma D.S., Vonk J.M., Bruinenberg M., Schouten J.P., and Boezen H.M. A disintegrin and metalloprotease 33 polymorphisms and lung function decline in the general population. Am. J. Respir. Crit. Care Med. 172 (2005) 329-333
26. Glas J., Seiderer J., Wetzke M., Konrad A., Torok H.P., Schmechel S., Tonenchi L., Grassl C., Dambacher J., Pfennig S., et al. 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 (2007) e819
27. Cummings J.R., Ahmad T., Geremia A., Beckly J., Cooney R., Hancock L., Pathan S., Guo C., Cardon L.R., and Jewell D.P. Contribution of the novel inflammatory bowel disease gene IL23R to disease susceptibility and phenotype. Inflamm. Bowel Dis. 13 (2007) 1063-1068
28. Barrett J.C., Fry B., Maller J., and Daly M.J. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21 (2005) 263-265
29. Frazer K.A., Ballinger D.G., Cox D.R., Hinds D.A., Stuve L.L., Gibbs R.A., Belmont J.W., Boudreau A., Hardenbol P., Leal S.M., et al. A second generation human haplotype map of over 3.1 million SNPs. Nature 449 (2007) 851-861
30. Hunt K.A., Zhernakova A., Turner G., Heap G.A., Franke L., Bruinenberg M., Romanos J., Dinesen L.C., Ryan A.W., Panesar D., et al. Newly identified genetic risk variants for celiac disease related to the immune response. Nat. Genet. 40 (2008) 395-402
31. Marchini J., Howie B., Myers S., McVean G., and Donnelly P. A new multipoint method for genome-wide association studies by imputation of genotypes. Nat. Genet. 39 (2007) 906-913
32. Corbaz A., ten Hove T., Herren S., Graber P., Schwartsburd B., Belzer I., Harrison J., Plitz T., Kosco-Vilbois M.H., Kim S.H., et al. IL-18-binding protein expression by endothelial cells and macrophages is up-regulated during active Crohn's disease. J. Immunol. 168 (2002) 3608-3616
33. Reuter B.K., and Pizarro T.T. Commentary: The role of the IL-18 system and other members of the IL-1R/TLR superfamily in innate mucosal immunity and the pathogenesis of inflammatory bowel disease: Friend or foe?. Eur. J. Immunol. 34 (2004) 2347-2355
34. Kanai T., Watanabe M., Okazawa A., Nakamaru K., Okamoto M., Naganuma M., Ishii H., Ikeda M., Kurimoto M., and Hibi T. Interleukin 18 is a potent proliferative factor for intestinal mucosal lymphocytes in Crohn's disease. Gastroenterology 119 (2000) 1514-1523
35. Pizarro T.T., Michie M.H., Bentz M., Woraratanadharm J., Smith Jr. M.F., Foley E., Moskaluk C.A., Bickston S.J., and Cominelli F. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J. Immunol. 162 (1999) 6829-6835
36. Monteleone G., Trapasso F., Parrello T., Biancone L., Stella A., Iuliano R., Luzza F., Fusco A., and Pallone F. Bioactive IL-18 expression is up-regulated in Crohn's disease. J. Immunol. 163 (1999) 143-147
37. Ten Hove T., Corbaz A., Amitai H., Aloni S., Belzer I., Graber P., Drillenburg P., van Deventer S.J., Chvatchko Y., and Te Velde A.A. Blockade of endogenous IL-18 ameliorates TNBS-induced colitis by decreasing local TNF-alpha production in mice. Gastroenterology 121 (2001) 1372-1379
38. Sivakumar P.V., Westrich G.M., Kanaly S., Garka K., Born T.L., Derry J.M., and Viney J.L. Interleukin 18 is a primary mediator of the inflammation associated with dextran sulphate sodium induced colitis: blocking interleukin 18 attenuates intestinal damage. Gut 50 (2002) 812-820
39. Wu C., Sakorafas P., Miller R., McCarthy D., Scesney S., Dixon R., and Ghayur T. IL-18 receptor beta-induced changes in the presentation of IL-18 binding sites affect ligand binding and signal transduction. J. Immunol. 170 (2003) 5571-5577
40. Underhill D.M., and Shimada T. A pair of 9s: It's in the CARDs. Nat. Immunol. 8 (2007) 122-124
41. Colonna M. All roads lead to CARD9. Nat. Immunol. 8 (2007) 554-555
42. Gross O., Gewies A., Finger K., Schafer M., Sparwasser T., Peschel C., Forster I., and Ruland J. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442 (2006) 651-656
43. Hsu Y.M., Zhang Y., You Y., Wang D., Li H., Duramad O., Qin X.F., Dong C., and Lin X. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat. Immunol. 8 (2007) 198-205
44. LeibundGut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., Schweighoffer E., Tybulewicz V., Brown G.D., Ruland J., and Reis e Sousa C. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8 (2007) 630-638
45. Hara H., Ishihara C., Takeuchi A., Imanishi T., Xue L., Morris S.W., Inui M., Takai T., Shibuya A., Saijo S., et al. The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-associated and Toll-like receptors. Nat. Immunol. 8 (2007) 619-629
46. Bertin J., Guo Y., Wang L., Srinivasula S.M., Jacobson M.D., Poyet J.L., Merriam S., Du M.Q., Dyer M.J., Robison K.E., et al. CARD9 is a novel caspase recruitment domain-containing protein that interacts with BCL10/CLAP and activates NF-kappa B. J. Biol. Chem. 275 (2000) 41082-41086
47. Xavier R.J., and Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448 (2007) 427-434
48. McGovern D., and Powrie F. The IL23 axis plays a key role in the pathogenesis of IBD. Gut 56 (2007) 1333-1336
49. Dixon A.L., Liang L., Moffatt M.F., Chen W., Heath S., Wong K.C., Taylor J., Burnett E., Gut I., Farrall M., et al. A genome-wide association study of global gene expression. Nat. Genet. 39 (2007) 1202-1207
50. Moffatt M.F., Kabesch M., Liang L., Dixon A.L., Strachan D., Heath S., Depner M., von Berg A., Bufe A., Rietschel E., et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448 (2007) 470-473
51. Pattingre S., De Vries L., Bauvy C., Chantret I., Cluzeaud F., Ogier-Denis E., Vandewalle A., and Codogno P. The G-protein regulator AGS3 controls an early event during macroautophagy in human intestinal HT-29 cells. J. Biol. Chem. 278 (2003) 20995-21002
52. Mathew C.G. New links to the pathogenesis of Crohn disease provided by genome-wide association scans. Nat. Rev. Genet. 9 (2008) 9-14
53. Neznanov N., Neznanova L., Angres B., and Gudkov A.V. Serologically defined colon cancer antigen 3 is necessary for the presentation of TNF receptor 1 on cell surface. DNA Cell Biol. 24 (2005) 777-785