Gender-stratified analysis of DLG5 R30Q in 4707 patients with Crohn disease and 4973 controls from 12 Caucasian cohorts

Journal of Medical Genetics

Volumn 45, Issue 1, 2008, Pages 36-42

  Browning, B L ^a,b   Annese, V ^j   Barclay, M L ^c,d   Bingham, S A ^e   Brand, S ^f   Buning C ^g   Castro, M ^h   Cucchiara, S ⁱ   Dallapiccola, B ^j   Drummond, H ^k   Ferguson, L R ^a,b   Ferraris, A ^j   Fisher, S A ^l   Gearry, R B ^c,d   Glas, J ^f   Henckaerts, L ^m   Huebner, C ^a,b   Knafelz, D ^h   Lakatos, L ⁿ   Lakatos, P L ^o   Latiano, A ^j   Liu, X ^p,q   Mathew, C ^l   Muller Myhsok B ^r   Newman, W G ^s   Nimmo, E R ^k   Noble, C L ^k   Palmieri, O ^j   Parkes, M ^t   Petermann, I ^a,b   Rutgeerts, P ^m   Satsangi, J ^k   Shelling, A N ^a,b   Siminovitch, K A ^p,q   Torok H P ^f   Tremelling, M ^t   Vermeire, S ^m   Valvano, M R ^j   Witt, H ^g   more..

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b Nutrigenomics New Zealand   (New Zealand)

^c CHRISTCHURCH HOSPITAL   (New Zealand)

^d UNIVERSITY OF OTAGO   (New Zealand)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF MUNICH   (Germany)

^g CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^h BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

ⁱ SAPIENZA UNIVERSITY OF ROME   (Italy)

^j CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^k UNIVERSITY OF EDINBURGH   (United Kingdom)

^l KING'S COLLEGE LONDON   (United Kingdom)

^m UNIVERSITY HOSPITALS LEUVEN   (Belgium)

ⁿ Csolnoky F Province Hospital   (Hungary)

^o SEMMELWEIS UNIVERSITY   (Hungary)

^p UNIVERSITY OF TORONTO   (Canada)

^q MOUNT SINAI HOSPITAL   (Canada)

^r MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^s UNIVERSITY OF MANCHESTER   (United Kingdom)

^t ADDENBROOKE S HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAUCASIAN; COHORT ANALYSIS; CONTROLLED STUDY; CROHN DISEASE; FEMALE; GENE FREQUENCY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RISK; SEX DIFFERENCE; ALLELE; CASE CONTROL STUDY; ETHNOLOGY; GENETIC PREDISPOSITION; GENETICS; LETTER;

DLG5 PROTEIN, HUMAN; MEMBRANE PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALLELES; CASE-CONTROL STUDIES; CROHN DISEASE; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; MALE; MEMBRANE PROTEINS; ODDS RATIO; SEX FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 38349113447     PISSN: 00222593     EISSN: None     Source Type: Journal    
DOI: 10.1136/jmg.2007.050773     Document Type: Article

References (49)

1. Orholm M, Munkholm P, Langholz E, Nielsen OH, Sorensen TI, Binder V. Familial occurrence of inflammatory bowel disease. N Engl J Med 1991;324:84-8.
2. Meucci G, Vecchi M, Torgano G, Arrigoni M, Prada A, Rocca F, Curzio M, Pera A, de Franchis R. Familial aggregation of inflammatory bowel disease in northern Italy: a multicenter study. The Gruppo di Studio per le Malattie Infiammatorie Intestinali (IBD Study Group). Gastroenterology 1992;103:514-19.
3. Probert CS, Jayanthi V, Hughes AO, Thompson JR, Wicks AC, Mayberry JF. Prevalence and family risk of ulcerative colitis and Crohn's disease: an epidemiological study among Europeans and south Asians in Leicestershire. Gut 1993;34:1547-51.
4. Orholm M, Binder V, Sorensen TI, Rasmussen LP, Kyvik KO. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scand J Gastroenterol 2000;35:1075-81.
5. Mathew CG, Lewis CM. Genetics of inflammatory bowel disease: progress and prospects. Hum Mol Genet 2004;13(suppl.):R161-8.
6. van Heel DA, Fisher SA, Kirby A, Daly MJ, Rioux JD, Lewis CM. Inflammatory bowel disease susceptibility loci defined by genome scan meta-analysis of 1952 affected relative pairs. Hum Mol Genet 2004;13:763-70.
7. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Almer S, Tysk C, O'Morain CA, Gassull M, Binder V, Finkel Y, Cortot A, Modigliani R, Laurent-Puig P, Gower-Rousseau C, Macry J, Colombel JF, Sahbatou M, Thomas G. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001;411:599-603.
8. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, Achkar JP, Brant SR, Bayless TM, Kirschner BS, Hanauer SB, Nunez G, Cho JH. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001;411:603-6.
9. Economou M, Trikalinos TA, Loizou KT, Tsianos EV, Ioannidis JP. Differential effects of NOD2 variants on Crohn's disease risk and phenotype in diverse populations: a metaanalysis. Am J Gastroenterol 2004;99:2393-404.
10. Rioux JD, Daly MJ, Silverberg MS, Lindblad K, Steinhart H, Cohen Z, Delmonte T, Kocher K, Miller K, Guschwan S, Kulbokas EJ, O'Leary S, Winchester E, Dewar K, Green T, Stone V, Chow C, Cohen A, Langelier D, Lapointe G, Gaudet D, Faith J, Branco N, Bull SB, McLeod RS, Griffiths AM, Bitton A, Greenberg GR, Land er ES, Siminovitch KA, Hudson TJ. Genetic variation in the 5q31 cytokine gene cluster confers susceptibility to Crohn disease. Nat Genet 2001;29:223-8.
11. Mirza MM, Fisher SA, King K, Cuthbert AP, Hampe J, Sand erson J, Mansfield J, Donaldson P, Macpherson AJ, Forbes A, Schreiber S, Lewis CM, Mathew CG. Genetic evidence for interaction of the 5q31 cytokine locus and the CARD15 gene in Crohn disease. Am J Hum Genet 2003;72:1018-22.
12. Fisher SA, Hampe J, Onnie CM, Daly MJ, Curley C, Purcell S, Sand erson J, Mansfield J, Annese V, Forbes A, Lewis CM, Schreiber S, Rioux JD, Mathew CG. Direct or indirect association in a complex disease: the role of SLC22A4 and SLC22A5 functional variants in Crohn disease. Hum Mutat 2006;27:778-785.
13. Silverberg MS, Duerr RH, Brant SR, Bromfield G, Datta LW, Jani N, Kane SV, Rotter JI, Philip Schumm L, Hillary Steinhart A, Taylor KD, Yang H, Cho JH, Rioux JD, Daly MJ. Refined genomic localization and ethnic differences observed for the IBD5 association with Crohn's disease. Eur J Hum Genet 2007;15:328-35.
14. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ, Steinhart AH, Abraham C, Regueiro M, Griffiths A, Dassopoulos T, Bitton A, Yang H, Targan S, Datta LW, Kistner EO, Schumm LP, Lee AT, Gregersen PK, Barmada MM, Rotter JI, Nicolae DL, Cho JH. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006;314:1461-3.
15. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K, Albrecht M, Mayr G, De La Vega FM, Briggs J, Gunther S, Prescott NJ, Onnie CM, Hasler R, Sipos B, Folsch UR, Lengauer T, Platzer M, Mathew CG, Krawczak M, Schreiber S. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 2007;39:207-211.
16. Libioulle C, Louis E, Hansoul S, Sand or C, Farnir F, Franchimont D, Vermeire S, Dewit O, de Vos M, Dixon A, Demarche B, Gut I, Heath S, Foglio M, Liang L, Laukens D, Mni M, Zelenika D, Van Gossum A, Rutgeerts P, Belaiche J, Lathrop M, Georges M. Novel crohn disease locus identified by genome-wide association maps to a gene desert on 5p13.1 and modulates expression of PTGER4. PLoS Genet 2007;3:e58.
17. Parkes M, Barrett JC, Prescott NJ, Tremelling M, Anderson CA, Fisher SA, Roberts RG, Nimmo ER, Cummings FR, Soars D, Drummond H, Lees CW, Khawaja SA, Bagnall R, Burke DA, Todhunter CE, Ahmad T, Onnie CM, McArdle W, Strachan D, Bethel G, Bryan C, Lewis CM, Deloukas P, Forbes A, Sand erson J, Jewell DP, Satsangi J, Mansfield JC, Cardon L, Mathew CG. Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat Genet 2007;39:830-2.
18. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A, Green T, Kuballa P, Barmada MM, Datta LW, Shugart YY, Griffiths AM, Targan SR, Ippoliti AF, Bernard EJ, Mei L, Nicolae DL, Regueiro M, Schumm LP, Steinhart AH, Rotter JI, Duerr RH, Cho JH, Daly MJ, Brant SR. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007;39:596-604.
19. The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007;447:661-78.
20. Stoll M, Corneliussen B, Costello CM, Waetzig GH, Mellgard B, Koch WA, Rosenstiel P, Albrecht M, Croucher PJ, Seegert D, Nikolaus S, Hampe J, Lengauer T, Pierrou S, Foelsch UR, Mathew CG, Lagerstrom-Fermer M, Schreiber S. Genetic variation in DLG5 is associated with inflammatory bowel disease. Nat Genet 2004;36:476-80.
21. Daly MJ, Pearce AV, Farwell L, Fisher SA, Latiano A, Prescott NJ, Forbes A, Mansfield J, Sand erson J, Langelier D, Cohen A, Bitton A, Wild G, Lewis CM, Annese V, Mathew CG, Rioux JD. Association of DLG5 R30Q variant with inflammatory bowel disease. Eur J Hum Genet 2005;13:835-9.
22. Noble CL, Nimmo ER, Drummond H, Smith L, Arnott ID, Satsangi J. DLG5 variants do not influence susceptibility to inflammatory bowel disease in the Scottish population. Gut 2005;54:1416-20.
23. Török HP, Glas J, Tonenchi L, Lohse P, Muller-Myhsok B, Limbersky O, Neugebauer C, Schnitzler F, Seiderer J, Tillack C, Brand S, Brunnler G, Jagiello P, Epplen JT, Griga T, Klein W, Schiemann U, Folwaczny M, Ochsenkuhn T, Folwaczny C. Polymorphisms in the DLG5 and OCTN cation transporter genes in Crohn's disease. Gut 2005;54:1421-7.
24. Vermeire S, Pierik M, Hlavaty T, Claessens G, van Schuerbeeck N, Joossens S, Ferrante M, Henckaerts L, Bueno de Mesquita M, Vlietinck R, Rutgeerts P. Association of organic cation transporter risk haplotype with perianal penetrating Crohn's disease but not with susceptibility to IBD. Gastroenterology 2005;129:1845-53.
25. Büning C, Geerdts L, Fiedler T, Gentz E, Pitre G, Reuter W, Luck W, Buhner S, Molnar T, Nagy F, Lonovics J, Dignass A, Land t O, Nickel R, Genschel J, Lochs H, Schmidt HH, Witt H. DLG5 variants in inflammatory bowel disease. Am J Gastroenterol 2006;101:786-92.
26. Ferraris A, Torres B, Knafelz D, Barabino A, Lionetti P, de Angelis GL, Iacono G, Papadatou B, D'Amato G, Di Ciommo V, Dallapiccola B, Castro M. Relationship between CARD15, SLC22A4/5 and DLG5 polymorphisms and early-onset inflammatory bowel diseases: an Italian multicentric study. Inflamm Bowel Dis 2006;12:355-61.
27. Lakatos PL, Fischer S, Claes K, Kovacs A, Molnar T, Altorjay I, Demeter P, Tulassay Z, Palatka K, Papp M, Rutgeerts P, Szalay F, Papp J, Vermeire S, Lakatos L. DLG5 R30Q is not associated with IBD in Hungarian IBD patients but predicts clinical response to steroids in Crohn's disease. Inflamm Bowel Dis 2006;12:362-8.
28. Medici V, Mascheretti S, Croucher PJ, Stoll M, Hampe J, Grebe J, Sturniolo GC, Solberg C, Jahnsen J, Moum B, Schreiber S, Vatn MH. Extreme heterogeneity in CARD15 and DLG5 Crohn disease-associated polymorphisms between German and Norwegian populations. Eur J Hum Genet 2006;1:459-68.
29. Newman WG, Gu X, Wintle RF, Liu X, van Oene M, Amos CI, Siminovitch KA. DLG5 variants contribute to Crohn disease risk in a Canadian population. Hum Mutat 2006;27:353-8.
30. Tremelling M, Waller S, Bredin F, Greenfield S, Parkes M. Genetic variants in TNF-alpha but not DLG5 are associated with inflammatory bowel disease in a large United Kingdom cohort. Inflamm Bowel Dis 2006;12:178-84.
31. Biank V, Friedrichs F, Babusukumar U, Wang T, Stoll M, Broeckel U, Kugathasan S. DLG5 R30Q variant is a female-specific protective factor in pediatric onset Crohn's disease. Am J Gastroenterol 2007;102:391- 8.
32. Cucchiara S, Latiano A, Palmieri O, Staiano AM, D'Inca R, Guariso G, Vieni G, Rutigliano V, Borrelli O, Valvano MR, Annese V. Role of CARD15, DLG5 and OCTN genes polymorphisms in children with inflammatory bowel diseases. World J Gastroenterol 2007;13:1221-9.
33. Pearce AV, Fisher SA, Prescott NJ, Onnie CM, Pattni R, Green P, Forbes A, Mansfield J, Sand erson J, Schreiber S, Lewis CM, Mathew CG. Investigation of association of the DLG5 gene with phenotypes of inflammatory bowel disease in the British population. Int J Colorectal Dis 2007;22:419-24.
34. Browning BL, Huebner C, Petermann I, Demmers P, McCulloch A, Gearry RB, Barclay ML, Shelling AN, Ferguson LR. Association of DLG5 variants with inflammatory bowel disease in the New Zealand Caucasian population and meta-analysis of the DLG5 R30Q variant. Inflamm Bowel Dis 2007;13:1069-76.
35. Friedrichs F, Brescianini S, Annese V, Latiano A, Berger K, Kugathasan S, Broeckel U, Nikolaus S, Daly MJ, Schreiber S, Rioux JD, Stoll M. Evidence of transmission ratio distortion of DLG5 R30Q variant in general and implication of an association with Crohn disease in men. Hum Genet 2006;119:305-11.
36. Yamazaki K, Takazoe M, Tanaka T, Ichimori T, Saito S, Iida A, Onouchi Y, Hata A, Nakamura Y. Association analysis of SLC22A4, SLC22A5 and DLG5 in Japanese patients with Crohn disease. J Hum Genet 2004;49:664-8.
37. The International HapMap Consortium. A haplotype map of the human genome. Nature 2005;437:1299-320.
38. de Ridder L, Weersma RK, Dijkstra G, van der Steege G, Benninga MA, Nolte IM, Taminiau JA, Hommes DW, Stokkers PC. Genetic susceptibility has a more important role in pediatric-onset Crohn's disease than in adult-onset Crohn's disease. Inflamm Bowel Dis 2007;13:1083-92.
39. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2006.
40. Cochran WG. The combination of estimates from different experiments. Biometrics 1954;10:101-129.
41. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58.
42. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88.
43. Wigginton JE, Cutler DJ, Abecasis GR. A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet 2005;76:887-93.
44. Binder V. Epidemiology of IBD during the twentieth century: an integrated view. Best Pract Res Clin Gastroenterol 2004;18:463-79.
45. Gunderson KL, Kuhn KM, Steemers FJ, Ng P, Murray SS, Shen R. Whole-genome genotyping of haplotype tag single nucleotide polymorphisms. Pharmacogenomics 2006;7:641-8.
46. Corrao G, Tragnone A, Caprilli R, Trallori G, Papi C, Andreoli A, Di Paolo M, Riegler G, Rigo GP, Ferrau O, Mansi C, Ingrosso M, Valpiani D. Risk of inflammatory bowel disease attributable to smoking, oral contraception and breastfeeding in Italy: a nationwide case-control study. Cooperative Investigators of the Italian Group for the Study of the Colon and the Rectum (GISC). Int J Epidemiol 1998;27:397-404.
47. Garcia Rodriguez LA, Gonzalez-Perez A, Johansson S, Walland er MA. Risk factors for inflammatory bowel disease in the general population. Aliment Pharmacol Ther 2005;22:309-15.
48. Purmonen S, Ahola TM, Pennanen P, Aksenov N, Zhuang YH, Tuohimaa P, Ylikomi T. HDLG5/KIAA0583, encoding a MAGUK-family protein, is a primary progesterone target gene in breast cancer cells. Int J Cancer 2002;102:1-6.
49. Logan RF. Inflammatory bowel disease incidence: up, down or unchanged? Gut 1998;42:309-11.