Prevalence of Clinically Relevant UGT1A Alleles and Haplotypes in African Populations

Annals of Human Genetics

Volumn 75, Issue 2, 2011, Pages 236-246

  Horsfall, Laura J ^a   Zeitlyn, David ^b   Tarekegn, Ayele ^a   Bekele, Endashaw ^c   Thomas, Mark G ^a,d   Bradman, Neil ^a   Swallow, Dallas M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ADDIS ABABA UNIVERSITY   (Ethiopia)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

Allele frequency; Bilirubin; Drug metabolism; Haplotype diversity; Population structure; UDP glucuronosyltransferase 1A1; UDP glucuronosyltransferase 1A7; UGT1A gene complex

Indexed keywords

GLUCURONOSYLTRANSFERASE 1A1; IRINOTECAN;

AFRICA; ALLELE; ARTICLE; ETHNIC GROUP; GENE FREQUENCY; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; HYPERBILIRUBINEMIA; MAJOR CLINICAL STUDY; PREVALENCE; PRIORITY JOURNAL; PROMOTER REGION; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM;

AFRICAN CONTINENTAL ANCESTRY GROUP; GENE FREQUENCY; GENETICS, POPULATION; GLUCURONOSYLTRANSFERASE; HAPLOTYPES; HUMANS; HYPERBILIRUBINEMIA; POLYMORPHISM, SINGLE NUCLEOTIDE; PREVALENCE; PROMOTER REGIONS, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE ANALYSIS, DNA;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 79851496878     PISSN: 00034800     EISSN: 14691809     Source Type: Journal    
DOI: 10.1111/j.1469-1809.2010.00638.x     Document Type: Article

References (44)

1. Beutler, E., Gelbart, T. & Demina, A. (1998) Racial variability in the UDP-glucuronosyltransferase 1 (UGT1A1) promoter: A balanced polymorphism for regulation of bilirubin metabolism? Proc Natl Acad Sci USA 95, 8170-8174.
2. Borlak, J., Thum, T., Landt, O., Erb, K. & Hermann, R. (2000) Molecular diagnosis of a familial nonhemolytic hyperbilirubinemia (Gilbert's syndrome) in healthy subjects. Hepatology 32, 792-795.
3. Bosma, P. J., Chowdhury, J. R., Bakker, C., Gantla, S., De Boer, A., Oostra, B. A., Lindhout, D., Tytgat, G. N., Jansen, P. L. & Oude Elferink, R. P. (1995) The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1 in Gilbert's syndrome. N Engl J Med 333, 1171-1175.
4. Bosma, P. J., Seppen, J., Goldhoorn, B., Bakker, C., Oude Elferink, R. P., Chowdhury, J. R., Chowdhury, N. R. & Jansen, P. L. (1994) Bilirubin UDP-glucuronosyltransferase 1 is the only relevant bilirubin glucuronidating isoform in man. J Biol Chem 269, 17960-17964.
5. Bougouma, A., Ilboudo, P. D., Bonkoungou, P., Sombie, R. & Siko, A. (1999) La maladie de Gilbert chez le Noir Africain: A propos de 4 observations au Centre Hospitalier National de Ouagadougou. Medecine d'Afrique Noire 45, 613-617.
6. Buyukasik, Y., Akman, U., Buyukasik, N. S., Goker, H., Kilicarslan, A., Shorbagi, A. I., Hascelik, G. & Haznedaroglu, I. C. (2008) Evidence for higher red blood cell mass in persons with unconjugated hyperbilirubinemia and Gilbert's syndrome. Am J Med Sci 335, 115-119.
7. Carpenter, S. L., Lieff, S., Howard, T. A., Eggleston, B. & Ware, R. E. (2008) UGT1A1 promoter polymorphisms and the development of hyperbilirubinemia and gallbladder disease in children with sickle cell anemia. Am J Hematol 63, 800-803.
8. Chaar, V., Keclard, L., Diara, J. P., Leturdu, C., Elion, J., Krishnamoorthy, R., Clayton, J. & Romana, M. (2005) Association of UGT1A1 polymorphism with prevalence and age at onset of cholelithiasis in sickle cell anemia. Haematologica 90, 188-199.
9. Cote, J. F., Kirzin, S., Kramar, A., Mosnier, J. F., Diebold, M. D., Soubeyran, I., Thirouard, A. S., Selves, J., Laurent-Puig, P. & Ychou, M. (2007) UGT1A1 polymorphism can predict hematologic toxicity in patients treated with irinotecan. Clin Cancer Res 13, 3269-3275.
10. Danoff, T. M., Campbell, D. A., Mccarthy, L. C., Lewis, K. F., Repasch, M. H., Saunders, A. M., Spurr, N. K., Purvis, I. J., Roses, A. D. & Xu, C. F. (2004) A Gilbert's syndrome UGT1A1 variant confers susceptibility to tranilast-induced hyperbilirubinemia. Pharmacogenomics J 4, 49-53.
11. Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1, 47-50.
12. Gwee, K. A., Koay, E. S. & Kang, J. Y. (1992) The prevalence of isolated unconjugated hyperbilirubinaemia (Gilbert's syndrome) in subjects attending a health screening programme in Singapore. Singapore Med J 33, 588-589.
13. Heeney, M. M., Howard, T. A., Zimmerman, S. A. & Ware, R. E. (2003) UGT1A promoter polymorphisms influence bilirubin response to hydroxyurea therapy in sickle cell anemia. J Lab Clin Med 141, 279-282.
14. Hong, A. L., Huo, D., Kim, H. J., Niu, Q., Fackenthal, D. L., Cummings, S. A., John, E. M., West, D. W., Whittemore, A. S., Das, S. & Olopade, O. I. (2007) UDP-glucuronosyltransferase 1A1 gene polymorphisms and total bilirubin levels in an ethnically diverse cohort of women. Drug Metab Dispos 35, 1254-1261.
15. Hoskins, J. M., Goldberg, R. M., Qu, P., Ibrahim, J. G. & Mcleod, H. L. (2007) UGT1A1*28 genotype and irinotecan-induced neutropenia: Dose matters. J Natl Cancer Inst 99, 1290-1295.
16. Hsieh, T. Y., Shiu, T. Y., Huang, S. M., Lin, H. H., Lee, T. C., Chen, P. J., Chu, H. C., Chang, W. K., Jeng, K. S., Lai, M. M. & Chao, Y. C. (2007) Molecular pathogenesis of Gilbert's syndrome: Decreased TATA-binding protein binding affinity of UGT1A1 gene promoter. Pharmacogenet Genomics 17, 229-236.
17. Innocenti, F., Grimsley, C., Das, S., Ramirez, J., Cheng, C., Kuttab-Boulos, H., Ratain, M. J. & Di Rienzo, A. (2002) Haplotype structure of the UDP-glucuronosyltransferase 1A1 promoter in different ethnic groups. Pharmacogenetics 12, 725-733.
18. Innocenti, F., Liu, W., Chen, P., Desai, A. A., Das, S. & Ratain, M. J. (2005) Haplotypes of variants in the UDP-glucuronosyltransferase1A9 and 1A1 genes. Pharmacogenet Genomics 15, 295-301.
19. Innocenti, F., Undevia, S. D., Iyer, L., Chen, P. X., Das, S., Kocherginsky, M., Karrison, T., Janisch, L., Ramirez, J., Rudin, C. M., Vokes, E. E. & Ratain, M. J. (2004) Genetic variants in the UDP-glucuronosyltransferase 1A1 gene predict the risk of severe neutropenia of irinotecan. J Clin Oncol 22, 1382-1388.
20. Kaplan, M., Slusher, T., Renbaum, P., Essiet, D. F., Pam, S., Levy-Lahad, E. & Hammerman, C. (2008) (TA)n UDP-glucuronosyltransferase 1A1 promoter polymorphism in Nigerian neonates. Pediatr Res 63, 109-111.
21. Kohle, C., Mohrle, B., Munzel, P. A., Schwab, M., Wernet, D., Badary, O. A. & Bock, K. W. (2003) Frequent co-occurrence of the TATA box mutation associated with Gilbert's syndrome (UGT1A1*28) with other polymorphisms of the UDP-glucuronosyltransferase-1 locus (UGT1A6*2 and UGT1A7*3) in Caucasians and Egyptians. Biochem Pharmacol 65, 1521-1527.
22. Kornberg, A. (1942) Latent liver disease in persons recovered from catarrhal jaundice and in otherwise normal medical students as revealed by the bilirubin excretion test. J Clin Invest 21, 299-308.
23. Kumar, S., Guha, M., Choubey, V., Maity, P., Srivastava, K., Puri, S. K. & Bandyopadhyay, U. (2008) Bilirubin inhibits Plasmodium falciparum growth through the generation of reactive oxygen species. Free Radic Biol Med 44, 602-613.
24. Lampe, J. W., Bigler, J., Horner, N. K. & Potter, J. D. (1999) UDP-glucuronosyltransferase (UGT1A1*28 and UGT1A6*2) polymorphisms in Caucasians and Asians: Relationships to serum bilirubin concentrations. Pharmacogenetics 9, 341-349.
25. Lankisch, T., Moebius, U., Wehmeier, M., Behrens, G., Manns, M., Schmidt, R. & Strassburg, C. (2006) Gilbert's disease and atazanavir: From phenotype to UDP-glucuronosyltransferase haplotype. Hepatology 44, 1324-1332.
26. Lankisch, T. O., Behrens, G., Ehmer, U., Mobius, U., Rockstroh, J., Wehmeier, M., Kalthoff, S., Freiberg, N., Manns, M. P., Schmidt, R. E. & Strassburg, C. P. (2009) Gilbert's syndrome and hyperbilirubinemia in protease inhibitor therapy-an extended haplotype of genetic variants increases risk in indinavir treatment. J Hepatol 50, 1010-1018.
27. Lankisch, T. O., Schulz, C., Zwingers, T., Erichsen, T. J., Manns, M. P., Heinemann, V. & Strassburg, C. P. (2008) Gilbert's Syndrome and irinotecan toxicity: Combination with UDP-glucuronosyltransferase 1A7 variants increases risk. Cancer Epidemiol Biomarkers Prev 17, 695-701.
28. Lin, J. P., O'Donnell, C. J., Schwaiger, J. P., Cupples, L. A., Lingenhel, A., Hunt, S. C., Yang, S. & Kronenberg, F. (2006) Association between the UGT1A1*28 allele, bilirubin levels, and coronary heart disease in the Framingham Heart Study. Circulation 114, 1476-1481.
29. McPhee, F., Caldera, P., Bemis, G., Mcdonagh, A., Kuntz, I. & Craik, C. (1996) Bile pigments as HIV-1 protease inhibitors and their effects on HIV-1 viral maturation and infectivity in vitro. Biochem J 320(Pt 2), 681-686.
30. Menard, V., Girard, H., Harvey, M., Perusse, L. & Guillemette, C. (2009) Analysis of inherited genetic variations at the UGT1 locus in the French-Canadian population. Hum Mutat 30, 677-687.
31. Najib, F. (1937) Defensive role of bilirubinemia in pneumococcal infection. The Lancet 229, 505-506.
32. New Drug Application 20-571 - Final label - UGT1A1 Camptosar-®(irinotecan HCl).
33. Novotny, L. & Vitek, L. (2003) Inverse relationship between serum bilirubin and atherosclerosis in men: A meta-analysis of published studies. Exp Biol Med (Maywood) 228, 568-571.
34. Odeberg, J. M., Andrade, J., Holmberg, K., Hoglund, P., Malmqvist, U. & Odeberg, J. (2006) UGT1A polymorphisms in a Swedish cohort and a human diversity panel, and the relation to bilirubin plasma levels in males and females. Eur J Clin Pharmacol 62, 829-837.
35. Owens, D. & Evans, J. (1975) Population studies on Gilbert's syndrome. J Med Genet 12, 152-156.
36. Passon, R. G., Howard, T. A., Zimmerman, S. A., Schultz, W. H. & Ware, R. E. (2001) Influence of bilirubin uridine diphosphate-glucuronosyltransferase 1A promoter polymorphisms on serum bilirubin levels and cholelithiasis in children with sickle cell anemia. J Pediatr Hematol Oncol 23, 448-451.
37. Premawardhena, A., Fisher, C. A., Liu, Y. T., Verma, I. C., De Silva, S., Arambepola, M., Clegg, J. B. & Weatherall, D. J. (2003) The global distribution of length polymorphisms of the promoters of the glucuronosyltransferase 1 gene (UGT1A1): Hematologic and evolutionary implications. Blood Cells Mol Dis 31, 98-101.
38. Rodriguez-Novoa, S., Martin-Carbonero, L., Barreiro, P., Gonzalez-Pardo, G., Jimenez-Nacher, I., Gonzalez-Lahoz, J. & Soriano, V. (2007) Genetic factors influencing atazanavir plasma concentrations and the risk of severe hyperbilirubinemia. Aids 21, 41-46.
39. Sampietro, M., Lupica, L., Perrero, L., Romano, R., Molteni, V. & Fiorelli, G. (1998) TATA-box mutant in the promoter of the uridine diphosphate glucuronosyltransferase gene in Italian patients with Gilbert's syndrome. Ital J Gastroenterol Hepatol 30, 194-198.
40. Stocker, R., Yamamoto, Y., Mcdonagh, A. F., Glazer, A. N. & Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046.
41. Temme, E. H., Zhang, J., Schouten, E. G. & Kesteloot, H. (2001) Serum bilirubin and 10-year mortality risk in a Belgian population. Cancer Causes Control 12, 887-894.
42. Veeramah, K. R., Thomas, M. G., Weale, M. E., Zeitlyn, D., Tarekegn, A., Bekele, E., Mendell, N. R., Shephard, E. A., Bradman, N. & Phillips, I. R. (2008) The potentially deleterious functional variant flavin-containing monooxygenase 2*1 is at high frequency throughout sub-Saharan Africa. Pharmacogenet Genomics 18, 877-886.
43. Zhang, D., Chando, T., Everett, D., Patten, C., Dehal, S. & Humphreys, W. (2005) In vitro inhibition of UDP glucuronosyltransferases by atazanavir and other HIV protease inhibitors and the relationship of this property to in vivo bilirubin glucuronidation. Drug Metab Dispos 33, 1729-1739.
44. Zucker, S. D., Horn, P. S. & Sherman, K. E. (2004) Serum bilirubin levels in the U.S. population: Gender effect and inverse correlation with colorectal cancer. Hepatology 40, 827-835.