Comparative genomics analysis of human sequence variation in the UGT1A gene cluster

Pharmacogenomics Journal

Volumn 6, Issue 1, 2006, Pages 52-62

  Maitland, M L ^a   Grimsley, C ^a,c   Kuttab Boulos, H ^a   Witonsky, D ^a   Kasza, K E ^a   Yang, L ^b   Roe, B A ^b   Di Rienzo, A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c Parkland College   (United States)

Author keywords

Conserved sequence; Genetic polymorphism; Glucuronosyltransferase; Irinotecan; Natural selection; Phenotype

Indexed keywords

GLUCURONOSYLTRANSFERASE;

AFRICAN AMERICAN; ARTICLE; ASIAN; CLUSTER ANALYSIS; COMPUTER ANALYSIS; CONTROLLED STUDY; DRUG METABOLISM; EUROPEAN AMERICAN; GENE CLUSTER; GENE FREQUENCY; GENE SEQUENCE; GENETIC CODE; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOMICS; HUMAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; RAT; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

AFRICAN CONTINENTAL ANCESTRY GROUP; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; BASE SEQUENCE; DOGS; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENE FREQUENCY; GLUCURONOSYLTRANSFERASE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PAPIO; RATS; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; VARIATION (GENETICS);

EID: 31044454137     PISSN: 1470269X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.tpj.6500351     Document Type: Article

References (87)

1. Tukey RH, Strassburg CP. Human UDP-glucuronosyltransferases: Metabolism, expression, and disease. Annu Rev Pharmacol Toxicol 2000; 40: 581-616.
2. Mackenzie PI, Walter Bock K, Burchell B, Guillemette C, Ikushiro SI, Iyanagi T et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics 2005; 15: 677-685.
3. Gong QH, Cho JW, Huang T, Potter C, Gholami N, Basu NK et al. Thirteen UDPglucuronosyltransferase genes are encoded at the human UGT1 gene complex locus. Pharmacogenetics 2001; 11: 357-368.
4. Zhang T, Haws P, Wu Q. Multiple variable first exons: A mechanism for cell- and tissue-specific gene regulation. Genome Res 2004; 14: 79-89.
5. Arias I. Chronic unconjugated hyperbilirubinemia without overt signs of hemolysis in adolescents and adults. J Clin Invest 1962; 41: 2233-2245.
6. Arias I, Gartner L, Cohen M, Ezzer J, Levi A. Chronic nonhemolytic unconjugated hyperbilirubinemia with glucuronosyl transferase deficiency: Clinical, biochemical, pharmacologic, and genetic evidence for heterogeneity. Am J Med 1969; 47: 395-409.
7. Crigler J, Najjar V. Congenital familial non-hemolytic jaundice with kernicterus. Pediatrics 1952; 10: 169-180.
8. Bosma PJ, Chowdhury JR, Bakker C, Gantla S, de Boer A, Oostra BA et al. The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1 in Gilbert's syndrome. N Engl J Med 1995; 333: 1171-1175.
9. Kadakol A, Ghosh SS, Sappal BS, Sharma G, Chowdhury JR, Chowdhury NR. Genetic lesions of bilirubin uridine-diphosphoglucuronate glucuronosyltransferase (UGT1A1) causing Crigler-Najjar and Gilbert syndromes: Correlation of genotype to phenotype. Hum Mutat 2000; 16: 297-306.
10. Ki CS, Lee KA, Lee SY, Kim HJ, Cho SS, Park JH et al. Haplotype structure of the UDP-glucuronosyltransferase 1A1 (UGT1A1) gene and its relationship to serum total bilirubin concentration in a male Korean population. Clin Chem 2003; 49: 2078-2081.
11. Sugatani J, Yamakawa K, Yoshinari K, Machida T, Takagi H, Mori M et al. Identification of a defect in the UGT1A1 gene promoter and its association with hyperbilirubinemia. Biochem Biophys Res Commun 2002; 292: 492-497.
12. Lin JP, Cupples LA, Wilson PW, Heard-Costa N, O'Donnell CJ. Evidence for a gene influencing serum bilirubin on chromosome 2q telomere: A genomewide scan in the Framingham study. Am J Hum Genet 2003; 72: 1029-1034.
13. Kaplan M, Renbaum P, Levy-Lahad E, Hammerman C, Lahad A, Beutler E. Gilbert syndrome and glucose-6-phosphate dehydrogenase deficiency: A dose-dependent genetic interaction crucial to neonatal hyperbilirubinemia. Proc Natl Acad Sci USA 1997; 94: 12128-12132.
14. Haverfield EV, McKenzie CA, Forrester T, Bouzekri N, Harding R, Serjeant G et al. UGT1A1 variation and gallstone formation in sickle cell disease. Blood 2005; 105: 968-972.
15. Beutler E, Gelbart T, Demina A. Racial variability in the UDP-glucuronosyltransferase 1 (UGT1A1) promoter: A balanced polymorphism for regulation of bilirubin metabolism? Proc Natl Acad Sci USA 1998; 95: 8170-8174.
16. Gupta E, Lestingi TM, Mick R, Ramirez J, Vokes EE, Ratain MJ. Metabolic fate of irinotecan in humans: Correlation of glucuronidation with diarrhea. Cancer Res 1994; 54: 3723-3725.
17. Gupta E, Mick R, Ramirez J, Wang X, Lestingi TM, Vokes EE et al. Pharmacokinetic and pharmacodynamic evaluation of the topoisomerase inhibitor irinotecan in cancer patients. J Clin Oncol 1997; 15: 1502-1510.
18. Meyerhardt JA, Kwok A, Ratain MJ, McGovren JP, Fuchs CS. Relationship of baseline serum bilirubin to efficacy and toxicity of single-agent irinotecan in patients with metastatic colorectal cancer. J Clin Oncol 2004; 22: 1439-1446.
19. Iyer L, King CD, Whitington PF, Green MD, Roy SK, Tephly TR et al. Genetic predisposition to the metabolism of irinotecan (CPT-11). Role of uridine diphosphate glucuronosyltransferase isoform 1A1 in the glucuronidation of its active metabolite (SN-38) in human liver microsomes. J Clin Invest 1998; 101: 847-854.
20. Iyer L, Hall D, Das S, Mortell MA, Ramirez J, Kim S et al. Phenotype-genotype correlation of in vitro SN-38 (active metabolite of irinotecan) and bilirubin glucuronidation in human liver tissue with UGT1A1 promoter polymorphism. Clin Pharmacol Ther 1999; 65: 576-582.
21. Gagne JF, Montminy V, Belanger P, Journault K, Gaucher G, Guillemette C. Common human UGT1A polymorphisms and the altered metabolism of irinotecan active metabolite 7-ethyl-10-hydroxycamptothecin (SN-38). Mol Pharmacol 2002; 62: 608-617.
22. Iyer L, Das S, Janisch L, Wen M, Ramirez J, Karrison T et al. UGT1A1*28 polymorphism as a determinant of irinotecan disposition and toxicity. Pharmacogenomics J 2002; 2: 43-47.
23. Innocenti F, Undevia SD, Iyer L, Chen PX, Das S, Kocherginsky M et al. Genetic variants in the UDP-glucuronosyltransferase 1A1 gene predict the risk of severe neutropenia of irinotecan. J Clin Oncol 2004; 22: 1382-1388.
24. Ando Y, Saka H, Ando M, Sawa T, Muro K, Ueoka H et al. Polymorphisms of UDP-glucuronosyltransferase gene and irinotecan toxicity: A pharmacogenetic analysis. Cancer Res 2000; 60: 6921-6926.
25. Sai K, Saeki M, Saito Y, Ozawa S, Katori N, Jinno H et al. UGT1A1 haplotypes associated with reduced glucuronidation and increased serum bilirubin in irinotecan-administered Japanese patients with cancer. Clin Pharmacol Ther 2004; 75: 501-515.
26. Ratain MJ. Irinotecan dosing: Does the CPT in CPT-11 stand for 'Can't Predict Toxicity'? J Clin Oncol 2002; 20: 7-8.
27. Danoff TM, Campbell DA, McCarthy LC, Lewis KF, Repasch MH, Saunders AM et al. A Gilbert's syndrome UGT1A1 variant confers susceptibility to tranilast-induced hyperbilirubinemia. Pharmacogenomics J 2004; 4: 49-53.
28. Xu CF, Lewis KF, Yeo AJ, McCarthy LC, Maguire MF, Anwar Z et al. Identification of a pharmacogenetic effect by linkage disequilibrium mapping. Pharmacogenomics J 2004; 4: 374-378.
29. Shu Y, Leabman MK, Feng B, Mangravite LM, Huang CC, Stryke D et al. Evolutionary conservation predicts function of variants of the human organic cation transporter, OCT1. Proc Natl Acad Sci USA 2003; 100: 5902-5907.
30. Leabman MK, Huang CC, DeYoung J, Carlson EJ, Taylor TR, de la Cruz M et al. Natural variation in human membrane transporter genes reveals evolutionary and functional constraints. Proc Natl Acad Sci USA 2003; 100: 5896-5901.
31. Botstein D, Risch N. Discovering genotypes underlying human phenotypes: past successes for mendelian disease, future approaches for complex disease. Nat Genet 2003; 33(Suppl): 228-237.
32. Monaghan G, Ryan M, Seddon R, Hume R, Burchell B. Genetic variation in bilirubin UPD-glucuronosyltransferase gene promoter and Gilbert's syndrome. Lancet 1996; 347: 578-581.
33. Springer MS, Murphy WJ, Eizirik E, O'Brien SJ. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc Natl Acad Sci USA 2003; 100: 1056-1061.
34. Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J et al. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol 1998; 9: 585-598.
35. Sugatani J, Kojima H, Ueda A, Kakizaki S, Yoshinari K, Gong QH et al. The phenobarbital response enhancer module in the human bilirubin UDP-glucuronosyltransferase UGT1A1 gene and regulation by the nuclear receptor CAR. Hepatology 2001; 33: 1232-1238.
36. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123: 585-595.
37. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975; 7: 256-276.
38. Miller MP, Kumar S. Understanding human disease mutations through the use of interspecific genetic variation. Hum Mol Genet 2001; 10: 2319-2328.
39. Halushka MK, Fan JB, Bentley K, Hsie L, Shen N, Weder A et al. Patterns of single-nucleotide polymorphisms in candidate genes for blood-pressure homeostasis. Nat Genet 1999; 22: 239-247.
40. Fay JC, Wyckoff GJ, Wu CI. Positive and negative selection on the human genome. Genetics 2001; 158: 1227-1234.
41. Cargill M, Altshuler D, Ireland J, Sklar P, Ardlie K, Patil N et al. Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nat Genet 1999; 22: 231-238.
42. Cohen JC, Kiss RS, Pertsemlidis A, Marcel YL, McPherson R, Hobbs HH. Multiple rare alleles contribute to low plasma levels of HDL cholesterol. Science 2004; 305: 869-872.
43. Wen G, Mahata SK, Cadman P, Mahata M, Ghosh S, Mahapatra NR et al. Both rare and common polymorphisms contribute functional variation at CHGA, a regulator of catecholamine physiology. Am J Hum Genet 2004; 74: 197-207.
44. Nebert DW, Vesell ES. Advances in pharmacogenomics and individualized drug therapy: Exciting challenges that lie ahead. Eur J Pharmacol 2004; 500: 267.
45. Iwai M, Maruo Y, Ito M, Yamamoto K, Sato H, Takeuchi Y. Six novel UDP-glucuronosyltransferase (UGT1A3) polymorphisms with varying activity. J Hum Genet 2004; 49: 123-128.
46. Ng PC, Henikoff S. SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 2003; 31: 3812-3814.
47. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001; 11: 863-874.
48. Ng PC, Henikoff S. Accounting for human polymorphisms predicted to affect protein function. Genome Res 2002; 12: 436-446.
49. Zhu Y, Spitz MR, Amos CI, Lin J, Schabath MB, Wu X. An evolutionary perspective on single-nucleotide polymorphism screening in molecular cancer epidemiology. Cancer Res 2004; 64: 2251-2257.
50. Yamamoto K, Soeda Y, Kamisako T, Hosaka H, Fukano M, Sato H et al. Analysis of bilirubin uridine 5′-diphosphate (UDP)-glucuronosyltransferase gene mutations in seven patients with Crigler-Najjar syndrome type II. J Hum Genet 1998; 43: 111-114.
51. Yamamoto K, Sato H, Fujiyama Y, Doida Y, Bamba T. Contribution of two missense mutations (G71R and Y486D) of the bilirubin UDP glycosyltransferase (UGT1A1) gene to phenotypes of Gilbert's syndrome and Crigler-Najjar syndrome type II. Biochim Biophys Acta 1998; 1406: 267-273.
52. Saeki M, Saito Y, Jinno H, Tohkin M, Kurose K, Kaniwa N et al. Comprehensive UGT1A1 genotyping in a Japanese population by Pyrosequencing. Clin Chem 2003; 49: 1182-1185.
53. Sato H, Adachi Y, Koiwai O. The genetic basis of Gilbert's syndrome. Lancet 1996; 347: 557-558.
54. Soeda Y, Yamamoto K, Adachi Y, Hori T, Aono S, Koiwai O et al. Predicted homozygous mis-sense mutation in Gilbert's syndrome. Lancet 1995; 346: 1494.
55. Kadakol A, Sappal BS, Ghosh SS, Lowenheim M, Chowdhury A, Chowdhury S et al. Interaction of coding region mutations and the Gilbert-type promoter abnormality of the UGT1A1 gene causes moderate degrees of unconjugated hyperbilirubinaemia and may lead to neonatal kernicterus. J Med Genet 2001; 38: 244-249.
56. Aono S, Adachi Y, Uyama E, Yamada Y, Keino H, Nanno T et al. Analysis of genes for bilirubin UDP-glucuronosyltransferase in Gilbert's syndrome. Lancet 1995; 345: 958-959.
57. Akaba K, Kimura T, Sasaki A, Tanabe S, Wakabayashi T, Hiroi M et al. Neonatal hyperbilirubinemia and a common mutation of the bilirubin uridine diphosphate-glucuronosyltransferase gene in Japanese. J Hum Genet 1999; 44: 22-25.
58. Strassburg CP, Oldhafer K, Manns MP, Tukey RH. Differential expression of the UGT1A locus in human liver, biliary, and gastric tissue: identification of UGT1A7 and UGT1A10 transcripts in extrahepatic tissue. Mol Pharmacol 1997; 52: 212-220.
59. Frisse L, Hudson RR, Bartoszewicz A, Wall JD, Donfack J, Di Rienzo A. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet 2001; 69: 831-843.
60. Reich DE, Cargill M, Bolk S, Ireland J, Sabeti PC, Richter DJ et al. Linkage disequilibrium in the human genome. Nature 2001; 411: 199-204.
61. Sawyer SL, Mukherjee N, Pakstis AJ, Feuk L, Kidd JR, Brookes AJ et al. Linkage disequilibrium patterns vary substantially among populations. Eur J Hum Genet 2005; 13: 677-686.
62. Justice R. NDA 20-571/S-024/S-027/S-028. Department of Health and Human Services 2005.
63. Holmes Jr DR, Savage M, LaBlanche J-M, Grip L, Serruys PW, Fitzgerald P et al. Results of prevention of REStenosis with tranilast and its outcomes (PRESTO) trial. Circulation 2002; 106: 1243-1250.
64. Roses AD. Pharmacogenetics and drug development: The path to safer and more effective drugs. Nat Rev Genet 2004; 5: 645-656.
65. Hall D, Ybazeta G, Destro-Bisol G, Petzl-Erler ML, Di Rienzo A. Variability at the uridine diphosphate glucuronosyltransferase 1A1 promoter in human populations and primates. Pharmacogenetics 1999; 9: 591-599.
66. Innocenti F, Grimsley C, Das S, Ramirez J, Cheng C, Kuttab-Boulos H et al. Haplotype structure of the UDP-glucuronosyltransferase 1A1 promoter in different ethnic groups. Pharmacogenetics 2002; 12: 725-733.
67. Bigler J, Whitton J, Lampe JW, Fosdick L, Bostick RM, Potter JD. CYP2C9 and UGT1A6 genotypes modulate the protective effect of aspirin on colon adenoma risk. Cancer Res 2001; 61: 3566-3569.
68. Chan AT, Tranah GJ, Giovannucci EL, Hunter DJ, Fuchs CS. Genetic variants in the UGT1A6 enzyme, aspirin use, and the risk of colorectal adenoma. J Natl Cancer Inst 2005; 97: 457-460.
69. Ockenga J, Vogel A, Teich N, Keim V, Manns MP, Strassburg CP. UDP glucuronosyltransferase (UGT1A7) gene polymorphisms increase the risk of chronic pancreatitis and pancreatic cancer. Gastroenterology 2003; 124: 1802-1808.
70. van der Logt EMJ, Bergevoet SM, Roelofs HMJ, van Hooijdonk Z, te Morsche RHM, Wobbes T et al. Genetic polymorphisms in UDP-glucuronosyltransferases and glutathione S-transferases and colorectal cancer risk. Corcinogenesis 2004; 25: 2407-2415.
71. Verlaan M, te Morsche RH, Pap A, Laheij RJ, Jansen JB, Peters WH et al. Functional polymorphisms of UDP-glucuronosyltransferases 1A1, 1A6 and 1A8 are not involved in chronic pancreatitis. Pharmacogenetics 2004; 14: 351-357.
72. Wang Y, Kato N, Hoshida Y, Otsuka M, Taniguchi H, Moriyama M et al. UDP-glucuronosyltransferase 1A7 genetic polymorphisms are associated with hepatocellular carcinoma in Japanese patients with hepatitis C virus infection. Clin Cancer Res 2004; 10: 2441-2446.
73. Zheng Z, Park JY, Guillemette C, Schantz SP, Lazarus P. Tobacco carcinogen-detoxifying enzyme UGT1A7 and its association with orolaryngeal cancer risk. J Natl Cancer Inst 2001; 93: 1411-1418.
74. Hinds DA, Stuve LL, Nilsen GB, Halperin E, Eskin E, Ballinger DG et al. Whole-genome patterns of common DNA variation in three human populations. Science 2005; 307: 1072-1079.
75. Nebert DW. Polymorphisms in drug-metabolizing enzymes: What is their clinical relevance and why do they exist? Am J Hum Genet 1997; 60: 265-271.
76. Roe B. Shotgun library construction for DNA sequencing in Methods in Molecular Biology. In: Stodolski M, Stodolski M (eds). Library Construction, Physical Mapping, and Sequencing. Human Press Inc.: Totowa, NJ, 2004 pp 171-187.
77. Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, Smit A et al. MultiPipMaker and supporting tools: Alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 2003; 31: 3518-3524.
78. Nickerson DA, Tobe VO, Taylor SL. PolyPhred: Automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res 1997; 25: 2745-2751.
79. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED et al. LAGAN and Multi-LAGAN: Efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 2003; 13: 721-731.
80. Hill WG. Estimation of linkage disequilibrium in randomly mating populations. Heredity 1974; 33: 229-239.
81. Strassburg CP, Vogel A, Kneip S, Tukey RH, Manns MP. Polymorphisms of the human UDP-glucuronosyltransferase (UGT) 1A7 gene in colorectal cancer. Gut 2002; 50: 851-856.
82. Vogel A, Kneip S, Barut A, Ehmer U, Tukey RH, Manns MP et al. Genetic link of hepatocellular carcinoma with polymorphisms of the UDP-glucuronosyltransferase UGT1A7 gene. Gastroenterology 2001; 121: 1136-1144.
83. Aono S, Yamada Y, Keino H, Hanada N, Nakagawa T, Sasaoka Y et al. Identification of defect in the genes for bilirubin UDP-glucuronosyltransferase in a patient with Crigler-Najjar syndrome type II. Biochem Biophys Res Commun 1993; 197: 1239-1244.
84. Huang C-S, Chang P-F, Huang M-J, Chen E-S, Chen W-C. Glucose-6-phosphate dehydrogenase deficiency, the UDP-glucuronosyl transferase 1A1 gene, and neonatal hyperbilirubinemia. Gastroenterology 2002; 123: 127.
85. Koiwai O, Nishizawa M, Hasada K, Aono S, Adachi Y, Mamiya N et al. Gilbert's syndrome is caused by a heterozygous missense mutation in the gene for bilirubin UDP-glucuronosyltransferase. Hum Mol Genet 1995; 4: 1183-1186.
86. Maruo Y, Nishizawa K, Sato H, Doida Y, Shimada M. Association of neonatal hyperbilirubinemia with bilirubin UDP-glucuronosyltransferase polymorphism. Pediatrics 1999; 103: 1224-1227.
87. Takeuchi K, Kobayashi Y, Tamaki S, Ishihara T, Maruo Y, Araki J et al. Genetic polymorphisms of bilirubin uridine diphosphate-glucuronosyltransferase gene in Japanese patients with Crigler-Najjar syndrome or Gilbert's syndrome as well as in healthy Japanese subjects. J Gastroenterol Hepatol 2004; 19: 1023-1028.