Associations between ABCB1/MDR1 gene polymorphisms and Crohn's disease: A gene-wide study in a pediatric population

Inflammatory Bowel Diseases

Volumn 15, Issue 6, 2009, Pages 900-908

  Krupoves, Alfreda ^a,b   Seidman, Ernest G ^c   Mack, David ^d   Israel, David ^e   Morgan, Kenneth ^f   Lambrette, Philippe ^a   Costea, Irina ^a,b   Deslandres, Colette ^a   Grimard, Guy ^g   Law, Liliane ^a   Levy, Emile ^a,b   Amre, Devendra K ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^d CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^e BC CHILDREN S HOSPITAL   (Canada)

^f Research Centre of the University   (Canada)

^g UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Clinical phenotypes; Crohn's disease; Genetics; Pediatrics

Indexed keywords

CYTOSINE; DNA; MULTIDRUG RESISTANCE PROTEIN 1; THYMINE;

ARTICLE; CHILD; CONTROLLED STUDY; CROHN DISEASE; FEMALE; GENE FREQUENCY; GENE FUNCTION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; HAPLOTYPE MAP; HUMAN; MAJOR CLINICAL STUDY; MALE; NUCLEIC ACID BASE SUBSTITUTION; POPULATION BASED CASE CONTROL STUDY; PRIORITY JOURNAL; SCHOOL CHILD; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; CHILD; CROHN DISEASE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOMICS; HAPLOTYPES; HUMANS; MALE; P-GLYCOPROTEIN; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS; YOUNG ADULT;

EID: 67650246375     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20849     Document Type: Article

References (67)

1. Bernstein CN, Blanchard JF, Rawsthorne P, et al. Epidemiology of Crohn's disease and ulcerative colitis in a central Canadian province: a population-based study. Am J Epidemiol. 1999;149:916-924.
2. Bernstein CN, Wajda A, Svenson LW, et al. The epidemiology of inflammatory bowel disease in Canada: a population-based study. Am J Gastroenterol. 2006;101:1559-1568.
3. Vermeire S, Wild G, Kocher K, et al. CARD15 genetic variation in a Quebec population: prevalence, genotype-phenotype relationship, and haplotype structure. Am J Hum Genet. 2002;71:74-83.
4. Cuthbert AP, Fisher SA, Mirza MM, et al. The contribution of NOD2 gene mutations to the risk and site of disease in inflammatory bowel disease. Gastroenterology. 2002;122:867-874.
5. Duerr RH, Taylor KD, Brant SR, et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science. 2006; 314:1461-1463.
6. Oliver J, Rueda B, Lopez-Nevot MA, et al. Replication of an association between IL23R gene polymorphism with inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5:977-981.
7. Baldassano RN, Bradfield JP, Monos DS, et al. Association of the T300A non-synonymous variant of the ATG16L1 gene with susceptibility to paediatric Crohn's disease. Gut. 2007;56:1171-1173.
8. Baldassano RN, Bradfield JP, Monos DS, et al. Association of variants of the interleukin-23 receptor gene with susceptibility to pediatric Crohn's disease. Clin Gastroenterol Hepatol. 2007;5:972-976.
9. Xavier RJ, Huett A, Rioux JD. Autophagy as an important process in gut homeostasis and Crohn's disease pathogenesis. Gut. 2008; 57:717-720.
10. Satsangi J, Parkes M, Louis E, et al. Two stage genome-wide search in inflammatory bowel disease provides evidence for susceptibility loci on chromosomes 3, 7 and 12. Nat Genet. 1996;14:199-202.
11. van Heel DA, Fisher SA, Kirby A, et al. Inflammatory bowel disease susceptibility loci defined by genome scan meta-analysis of 1952 affected relative pairs. Hum Mol Genet. 2004;13:763-770.
12. Thiebaut F, Tsuruo T, Hamada H, et al. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci U S A. 1987;84:7735-7738.
13. Fojo AT, Ueda K, Slamon DJ, et al. Expression of a multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci U S A. 1987;84: 265-269.
14. Borst P, Elferink RO. Mammalian ABC transporters in health and disease. Annu Rev Biochem. 2002;71:537-592.
15. Panwala CM, Jones JC, Viney JL. A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, MDR1a, spontaneously develop colitis. J Immunol. 1998;161:5733-5744.
16. Hoffmeyer S, Burk O, von RO, et al. Functional polymorphisms of the human multidrug-resistance gene: multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci U S A. 2000;97:3473-3478.
17. Ishikawa T, Onishi Y, Hirano H, et al. Pharmacogenomics of drug transporters: a new approach to functional analysis of the genetic polymorphisms of ABCB1 (P-glycoprotein/MDR1). Biol Pharm Bull. 2004; 27:939-948.
18. Kim RB, Leake BF, Chod EF, et al. Identification of functionally variant MDR1 alleles among European Americans and African Americans. Clin Pharmacol Ther. 2001;70:189-199.
19. Tanabe M, Ieiri I, Nagata N, et al. Expression of P-glycoprotein in human placenta: relation to genetic polymorphism of the multidrug resistance (MDR)-1 gene. J Pharmacol Exp Ther. 2001;297:1137-1143.
20. Brant SR, Panhuysen CI, Nicolae D, et al. MDR1 Ala893 polymorphism is associated with inflammatory bowel disease. Am J Hum Genet. 2003; 73:1282-1292.
21. Potocnik U, Ferkolj I, Glavac D, et al. Polymorphisms in multidrug resistance 1 (MDR1) gene are associated with refractory Crohn disease and ulcerative colitis. Genes Immun. 2004;5:530-539.
22. Urcelay E, Mendoza JL, Martin MC, et al. MDR1 gene: susceptibility in Spanish Crohn's disease and ulcerative colitis patients. Inflamm Bowel Dis. 2006;12:33-37.
23. Schwab M, Schaeffeler E, Marx C, et al. Association between the C3435T MDR1 gene polymorphism and susceptibility for ulcerative colitis. Gastroenterology. 2003;124:26-33.
24. Palmieri O, Latiano A, Valvano R, et al. Multidrug resistance 1 gene polymorphisms are not associated with inflammatory bowel disease and response to therapy in Italian patients. Aliment Pharmacol Ther. 2005; 22:1129-1138.
25. Ho GT, Nimmo ER, Tenesa A, et al. Allelic variations of the multidrug resistance gene determine susceptibility and disease behavior in ulcerative colitis. Gastroenterology. 2005;128:288-296.
26. Ho GT, Soranzo N, Nimmo ER, et al. ABCB1/MDR1 gene determines susceptibility and phenotype in ulcerative colitis: discrimination of critical variants using a gene-wide haplotype tagging approach. Hum Mol Genet. 2006;15:797-805.
27. Croucher PJ, Mascheretti S, Foelsch UR, et al. Lack of association between the C3435T MDR1 gene polymorphism and inflammatory bowel disease in two independent Northern European populations. Gastroenterology. 2003;125:1919-1920.
28. Ardizzone S, Maconi G, Bianchi V, et al. Multidrug resistance 1 gene polymorphism and susceptibility to inflammatory bowel disease. Inflamm Bowel Dis. 2007;13:516-523.
29. De Iudicibus S, Stocco G, Martelossi S, et al. Association of BclI polymorphism of the glucocorticoid receptor gene locus with response to glucocorticoids in inflammatory bowel disease. Gut. 2007; 56:1319-a.
30. Oostenbrug LE, Dijkstra G, Nolte IM, et al. Absence of association between the multidrug resistance (MDR1) gene and inflammatory bowel disease. Scand J Gastroenterol. 2006;41:1174-1182.
31. Soranzo N, Cavalleri GL, Weale ME, et al. Identifying candidate causal variants responsible for altered activity of the ABCB1 multidrug resistance gene. Genome Res. 2004;14:1333-1344.
32. Biank V, Brodekel U, Kugadmm S. Pediatric inflammatory bowel disease: Clinical and molecular genetics. Inflamm Bowel Dis. 2007; 13: 1430-1438.
33. Mack DR, Langton C, Markowitz J, et al. Laboratory values for children with newly diagnosed inflammatory bowel disease. Pediatrics. 2007; 119:1113-1119.
34. Cucchiara S, Latiano A, Palmieri O, et al. Polymorphisms of tumor necrosis factor-alpha but not MDR1 influence response to medical therapy in pediatric-onset inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2007;44:171-179.
35. Lennard-Jones JE. Classification of inflammatory bowel disease. Scand J Gastroenterol Suppl. 1989;170:2-6.
36. Sands BE. From symptom to diagnosis: clinical distinctions among various forms of intestinal inflammation. Gastroenterology. 2004;126: 1518-1532.
37. Satsangi J, Silverberg MS, Vermeire S, et al. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 2006;55:749-753.
38. Carlson CS, Eberle MA, Rieder MJ, et al. Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibriurn. Am J Hum Genet. 2004;74:106-120.
39. Barrett JC, Fry B, Maller J, et al. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005;21:263-265.
40. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach for multiple testing. J R Star Soc Ser B. 1995;57:289-300.
41. Benjamini Y, Yekutieli. Quantitative trait loci analysis using the false discovery rate. Genetics. 2005;171:783-790.
42. Annese V, Valvano MR, Palmieri O, et al. Multidrug resistance 1 gene in inflammatory bowel disease: a rneta-analysis. World J Gastroenterol. 2006;12:3636-3644.
43. Onnie CM, Fisher SA, Pattni R, et al. Associllitions of allelic variants of the multidrug resistance gene (ABCB1 or MDR1) and inflammatory bowel disease and their effects on disease behavior: a case-control and meta-analysis study. Inflamn: Bowel Dis. 2006;12:263-271.
44. Siegsmund M, Brinkmann U, Schaffeler E, et al. Association of the P-glycoprotein transporter MDR1C3435T polymorphism with the susceptibility to renal epithelial tumors. J Am Sac Nephrol. 2002;13:1847-1854.
45. Miller KL, Kelsey KT, Wiencke M et al. The C3435T polymorphism of MDR1 and susceptibility to adult glioma. Neuroepidemiology. 2005; 25:85-90.
46. Rodriguez Novoa S, Barreiro P, Rendon A, et al. Plasma levels of atazanavir and the risk of hyperbilimbine are predicted by the 3435C[rarr]T polymorphism at die multidrrg resistance gene 1. Clin Infect Dis. 2006;42:291-295.
47. Pawlik A, Wrzesniewska J, Fiedorowicz-Fabrycy I, et al. The MDR1 3435 polymorphism in patients with rheumatoid arthritis. Int J Clin Pharmacol Ther. 2004;42:496-503.
48. Jamroziak K, Mlynarski W, Balcerczak E, et al. Functional C3435T polymorphism of MDR1 gene: an impact on genetic susceptibility and clinical outcome of childhood acute lymphoblastic leukemia. Eur J Haematol. 2004;72:314-321.
49. Kimchi-Sarfaty C, Oh JM, Kim IW, et al. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science. 2007;315:525-528.
50. Kroetz DL, Pauli-Magnus C, Hodges LM, et al. Sequence diversity and haplotype structure in the himan ABCB1 (MDR1, multildrug resistance transporter) gene. Pharmacogenetics. 2003;13:481-494.
51. Salama NN, Yang Z, Bui T, et al. MDR1 hiplotypes significantly minimize intracellular uptake and trarl P-gp substrate transport in recombinant LLC-PK1 cells. J Pharm Sci. 2006;95:2293-2308.
52. Zhu D, Taguchi-Nakarnura H, Goto M, et al. Influence of single-nucleotide polymorphisms in the multidrug resistance-1 gene on the cellular export of nelfinavir and its clinical implication-for highly active antiretroviral therapy. Antivir Ther. 2004; 9:929-935.
53. de Ridder L, Weersma RK, Dijkstra G, et al. Genetic susceptibility has a more important role in pediatric-onset Crohn's disease than in adult-onset Crohn's disease. Inflamm Bowel Dis. 2007;13:1083-1092.
54. Van Limbergen J, Russell M Drummond HE, et al. Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology. 2008;135:1114-1122.
55. Levine A, Kugathasan S, Annese V, et al. Pediatric onset Crohn's colitis is characterized by genotype-dependent age-related susceptibility. Inflamm Bowel Dis. 2007;13:1509-1515.
56. Paul T, Birnbaum A, Pal DK, et al. Distinct plienotype of easly childhood inflammatory bowel disease. J Clin Gastroenterol. 2006;40:583-586.
57. Fisher SA, Tremelling M, Anderson CA, et al. Genetic determinants of ulcerative colitis include the ECM1 locus and five loci implicated in Crohn's disease. Nat Genet. 2008;40:710-712.
58. Franke A, Balschun T, Karlsen TH, et al. Replication of signals from recent studies of Crohn's disease identifies previously unknown disease loci for ulcerative colitis. Nat Genet. 2008;40:713-715.
59. Satsangi J, Grootscholten C, Holt H, et al. Clinl patterns of familial inflammatory bowel disease. Gut. 1996;38:738-741.
60. Amre DK, Mack DR, Israel D, et al. Investigation of associations between the pregnane-X-receptor gene (NR1I2) and Crohn's disease in Canadian children using a gene-wide haplotype-based approach. Inflamm Bowel Dis. 2008; 14:1214-1218.
61. Wootton PT, Drenos F, Cooper JA, et al. Tagging-SNP haplotype analysis of the secretory PLA2IIa gene PLA2G2A shows strong association with serum levels of sPLA2IIa: results from the UDACS study. Hum Mol Genet. 2006;15:355-361.
62. Singh SB, Davis AS, Taylor GA, et al. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science. 2006;313:1438-1441.
63. Xu Y, Jagannath C, Liu XD, et al. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity. 2007;27:135-144.
64. Peterson N, Guthery S, Denson L, et al. Genetic variants in the autophagy pathway contribute to paediatric Crohn's disease. Gut. 2008;57: 1336-1337.
65. Arme DK, Mack DR, Morgan K, et al. Autophagy gene ATG16L1 but not IRGM is associated with Crohn's disease in Canadian children. Inflanim Bowel Dis. 2008 (in press).
66. Buda G, Orciuolo E, Maggini V, et al. MDR1 modulates apoptosis in CD34+ leukemic cells. Ann Hematol. 2008;87:1017-1018.
67. Mizutani T, Masuda M, Nakai E, et al. Genuine functions of P-glycoprotein (ABCB1). Curr Drug Metab. 2008;9:167-174.