Signatures of recent positive selection at the ATP-binding cassette drug transporter uperfamily gene loci

Human Molecular Genetics

Volumn 16, Issue 11, 2007, Pages 1367-1380

  Wang, Zihua ^a   Wang, Jingbo ^a   Tantoso, Erwin ^b   Wang, Baoshuang ^c   Tai, Amy Y P ^c   Ooi, London L P J ^c,d   Chong, Samuel S ^a,e   Lee, Caroline G L ^a,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^d SINGAPORE GENERAL HOSPITAL   (Singapore)

^e NATIONAL UNIVERSITY HOSPITAL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER;

ARTICLE; CONTROLLED STUDY; DRUG RESPONSE; DRUG TRANSPORT; GENE DUPLICATION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC IDENTIFICATION; GENOTYPE; HAPLOTYPE; HAPLOTYPE MAP; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PHARMACOGENETICS; PRIORITY JOURNAL; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; UNINDEXED SEQUENCE;

ATP-BINDING CASSETTE TRANSPORTERS; GENE FREQUENCY; GENETIC MARKERS; HUMANS; MULTIGENE FAMILY; SELECTION (GENETICS);

EID: 34447345179     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm087     Document Type: Article

References (80)

1. Weinshilboum, R. (2003) Inheritance and drug response. N. Engl. J. Med., 348, 529-537.
2. Eichelbaum, M., Ingelman-Sundberg, M. and Evans, W.E. (2006) Pharmacogenomics and individualized drug therapy. Annu. Rev. Med., 57, 119-137.
3. Evans, W.E. and McLeod, H.L. (2003) Pharmacogenomics-drug disposition, drug targets, and side effects. N. Engl. J. Med., 348, 538-549.
4. Schmith, V.D., Campbell, D.A., Sehgal, S., Anderson, W.H., Burns, D.K., Middleton, L.T. and Roses, A.D. (2003) Pharmacogenetics and disease genetics of complex diseases. Cell. Mol. Life Sci., 60, 1636-1646.
5. Ishikawa, T., Tsuji, A., Inui, K., Sai, Y., Anzai, N., Wada, M., Endou, H. and Sumino, Y. (2004) The genetic polymorphism of drug transporters: functional analysis approaches. Pharmacogenomics, 5, 67-99.
6. Ross, D.D. and Doyle, L.A. (2004) Mining our ABCs: Pharmacogenomic approach for evaluating transporter function in cancer drug resistance. Cancer Cell., 6, 105-107.
7. Dean, M., Rzhetsky, A. and Allikmets, R. (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res., 11, 1156-1166.
8. Schinkel, A.H. and Jonker, J.W. (2003) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: An overview. Adv. Drug Deliv. Rev., 55, 3-29.
9. Collins, F.S., Brooks, L.D. and Chakravarti, A. (1998) A DNA polymorphism discovery resource for research on human genetic variation. [Erratum (1999) Genome Res., 9, 210.] Genome Res., 8, 1229-1231.
10. Consortium, T.I.H. (2004) Integrating ethics and science in the International HapMap Project. Nat. Rev. Genet., 5, 467-475.
11. Goldstein, D.B., Ahmadi, K.R., Weale, M.E. and Wood, N.W. (2003) Genome scans and candidate gene approaches in the study of common diseases and variable drug responses. Trends Genet., 19, 615-622.
12. Neale, B.M. and Sham, P.C. (2004) The future of association studies: gene-based analysis and replication. Am. J. Hum. Genet., 75, 353-362.
13. Ke, X., Miretti, M.M., Broxholme, J., Hunt, S., Beck, S., Bentley, D.R., Deloukas, P. and Cardon, L.R. (2005) A comparison of tagging methods and their tagging space. Hum. Mol. Genet., 14, 2757-2767.
14. Biswas, S. and Akey, J.M. (2006) Genomic insights into positive selection. Trends Genet., 22, 437-446.
15. Sabeti, P.C., Schaffner, S.F., Fry, B., Lohmueller, J., Varilly, P., Shamovsky, O., Palma, A., Mikkelsen, T.S., Altshuler, D. and Lander, E.S. (2006) Positive natural selection in the human lineage. Science 312, 1614-1620.
16. Wang, E.T., Kodama, G., Baldi, P. and Moyzis, R.K. (2006) Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc. Natl Acad. Sci. USA, 103, 135-140.
17. Voight, B.F., Kudaravalli, S., Wen, X. and Pritchard, J.K. (2006) A map of recent positive selection in the human genome. PLoS Biol., 4 e72.
18. Zhang, C., Bailey, D.K., Awad, T., Liu, G., Xing, G., Cao, M., Valmeekam, V., Retief, J., Matsuzaki, H., Taub, M. et al. (2006) A whole genome long-range haplotype (WGLRH) test for detecting imprints of positive selection in human populations. Bioinformatics, 22, 2122-2128.
19. Walsh, E.C., Sabeti, P., Hutcheson, H.B., Fry, B., Schaffner, S.F., de Bakker, P.I., Varilly, P., Palma, A.A., Roy, J., Cooper, R. et al. (2006) Searching for signals of evolutionary selection in 168 genes related to immune function. Hum. Genet., 119, 92-102.
20. Izagirre, N., Garcia, I., Junquera, C., de la Rua, C. and Alonso, S. (2006) A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol. Biol. Evol., 23, 1697-1706.
21. Akey, J.M., Zhang, G., Zhang, K., Jin, L. and Shriver, M.D. (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Res., 12, 1805-1814.
22. Goddard, K.A., Hopkins, P.J., Hall, J.M. and Witte, J.S. (2000) Linkage disequilibrium and allele-frequency distributions for 114 single-nucleotide polymorphisms in five populations. Am. J. Hum. Genet., 66, 216-234.
23. Hinds, D.A., Stuve, L.L., Nilsen, G.B., Halperin, E., Eskin, E., Ballinger, D.G., Frazer, K.A. and Cox, D.R. (2005) Whole-genome patterns of common DNA variation in three human populations. Science, 307, 1072-1079.
24. Reich, D.E., Cargill, M., Bolk, S., Ireland, J., Sabeti, P.C., Richter, D.J., Lavery, T., Kouyoumjian, R., Farhadian, S.F., Ward, R. et al. (2001) Linkage disequilibrium in the human genome. Nature, 411, 199-204.
25. Tang, K., Wong, L.P., Lee, E.J., Chong, S.S. and Lee, C.G. (2004) Genomic evidence for recent positive selection at the human MDR1 gene locus. Hum. Mol. Genet., 13, 783-797.
26. Gwee, P.C., Tang, K., Sew, P.H., Lee, E.J., Chong, S.S. and Lee, C.G. (2005) Strong linkage disequilibrium at the nucleotide analogue transporter ABCC5 gene locus. Pharmacogenet. Genomics, 15, 91-104.
27. Wang, Z., Wang, B., Tang, K., Lee, E.J., Chong, S.S. and Lee, C.G. (2005) A functional polymorphism within the MRP1 gene locus identified through its genomic signature of positive selection. Hum. Mol. Genet. 14, 2075-2087.
28. Mace, S., Cousin, E., Ricard, S., Genin, E., Spanakis, E., Lafargue-Soubigou, C., Genin, B., Fournel, R., Roche, S., Haussy, G. et al. (2005) ABCA2 is a strong genetic risk factor for early-onset Alzheimer's disease. Neurobiol. Dis., 18, 119-125.
29. Wollmer, M.A., Kapaki, E., Hersberger, M., Muntwyler, J., Brunner, F., Tsolaki, M., Akatsu, H., Kosaka, K., Michikawa, M., Molyva, D. et al. (2006) Ethnicity-dependent genetic association of ABCA2 with sporadic Alzheimer's disease. Am. J. Med. Genet. B Neuropsychiatr. Genet., 141, 534-536.
30. Mack, J.T., Townsend, D.M., Beljanski, V. and Tew, K.D. (2007) The ABCA2 transporter: Intracellular roles in trafficking and metabolism of LDL-derived cholesterol and sterol-related compounds. Curr. Drug. Metab., 8, 47-57.
31. Tang, K., Ngoi, S.M., Gwee, P.C., Chua, J.M.Z., Lee, E.J.D., Chong, S.C. and Lee, C.G.L. (2002) Distinct haplotype profiles and strong linkage disequilibrium at the MDR1 multidrug transporter gene locus in three ethnic Asian populations. Pharmacogenetics, 12, 437-450.
32. Kerb, R. (2006) Implications of genetic polymorphisms in drug transporters for pharmacotherapy. Cancer Lett., 234, 4-33.
33. Lee, C.G., Chong, S.S. and Lee, E.J. (2004) Pharmacogenetics of the Human MDR1 multidrug transporter. Curr Pharmacogenomics, 2, 1-11.
34. Cascorbi, I. (2006) Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacol. Ther., 112, 457-473.
35. Drozdzik, M., Bialecka, M., Mysliwiec, K., Honczarenko, K., Stankiewicz, J. and Sych, Z. (2003) Polymorphism in the P-glycoprotein drug transporter MDR1 gene: A possible link between environmental and genetic factors in Parkinson's disease. Pharmacogenetics, 13, 259-263.
36. Schwab, M., Schaeffeler, E., Marx, C., Fromm, M.F., Kaskas, B., Metzler, J., Stange, E., Herfarth, H., Schoelmerich, J., Gregor, M. et al. (2003) Association between the C3435T MDR1 gene polymorphism and susceptibility for ulcerative colitis. Gastroenterology, 124 26-33.
37. Furuno, T., Landi, M.T., Ceroni, M., Caporaso, N., Bernucci, I., Nappi, G., Martignoni, E., Schaeffeler, E., Eichelbaum, M., Schwab, M. et al. (2002) Expression polymorphism of the blood-brain barrier component P-glycoprotein (MDR1) in relation to Parkinson's disease. Pharmacogenetics, 12, 529-534.
38. Siegsmund, M., Brinkmann, U., Schaffeler, E., Weirich, G., Schwab, M., Eichelbaum, M., Fritz, P., Burk, O., Decker, J., Alken, P. et al. (2002) Association of the P-glycoprotein transporter MDR1(C3435T) polymorphism with the susceptibility to renal epithelial tumors. J. Am. Soc. Nephrol., 13, 1847-1854.
39. van den Heuvel-Eibrink, M.M., Wiemer, E.A., de Boevere, M.J., van der Holt, B., Vossebeld, P.J., Pieters, R. and Sonneveld, P. (2001) MDR1 gene-related clonal selection and P-glycoprotein function and expression in relapsed or refractory acute myeloid leukemia. Blood, 97, 3605-3611.
40. Illmer, T., Schuler, U.S., Thiede, C., Schwarz, U.I., Kim, R.B., Gotthard, S., Freund, D., Schakel, U., Ehninger, G. and Schaich, M. (2002) MDR1 gene polymorphisms affect therapy outcome in acute myeloid leukemia patients. Cancer Res., 62, 4955-4962.
41. Tan, E.K., Drozdzik, M., Bialecka, M., Honczarenko, K., Klodowska-Duda, G., Teo, Y.Y., Tang, K., Wong, L.P., Chong, S.S., Tan, C. et al. (2004) Analysis of MDR1 haplotypes in Parkinson's disease in a white population. Neurosci. Lett., 372, 240-244.
42. Tan, E.K., Chan, D.K.Y., Ng, P.W., Woo, J., Teo, Y.Y., Tang, K., Wong, L.P., Chong, S.S., Tan, C., Shen, H. et al. (2005) MDR1 haplotype (e21/2677T and e26/3435T) modulates risk of Parkinson's Disease. Arch. Neurol., 62, 460-464.
43. Lee, C.G., Tang, K., Cheung, Y.B., Wong, L.P., Tan, C., Shen, H., Zhao, Y., Pavanni, R., Lee, E.J., Wong, M.C. et al. (2004) MDR1, the blood-brain barrier transporter, is associated with Parkinson's disease in ethnic Chinese. J. Med. Genet., 41, e60.
44. Rosmorduc, O., Hermelin, B., Boelle, P.Y., Parc, R., Taboury, J. and Poupon, R. (2003) ABCB4 gene mutation-associated cholelithiasis in adults. Gastroenterology, 125, 452-459.
45. Lang, T., Haberl, M., Jung, D., Drescher, A., Schlagenhaufer, R., Keil, A., Mornhinweg, E., Stieger, B., Kullak-Ublick, G.A. and Kerb, R. (2006) Genetic variability, haplotype structures, and ethnic diversity of hepatic transporters MDR3 (ABCB4) and bile salt export pump (ABCB11). Drug Metab. Dispos., 34, 1582-1599.
46. Jacquemin, E., De Vree, J.M., Cresteil, D., Sokal, E.M., Sturm, E., Dumont, M., Scheffer, G.L., Paul, M., Burdelski, M., Bosma, P.J. et al. (2001) The wide spectrum of multidrug resistance 3 deficiency: from neonatal cholestasis to cirrhosis of adulthood. Gastroenterology 120, 1448-1458.
47. Lang, C., Meier, Y., Stieger, B., Beuers, U., Lang, T., Kerb, R., Kullak-Ublick, G.A., Meier, P.J. and Pauli-Magnus, C. (2007) Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug-induced liver injury. Pharmacogenet. Genomics, 17, 47-60.
48. Eloranta, M.L., Hakli, T., Hiltunen, M., Helisalmi, S., Punnonen, K. and Heinonen, S. (2003) Association of single nucleotide polymorphisms of the bile salt export pump gene with intrahepatic cholestasis of pregnancy. Scand. J. Gastroenterol., 38, 648-652.
49. Conrad, S., Kauffmann, H.M., Ito, K., Deeley, R.G., Cole, S.P. and Schrenk, D. (2001) Identification of human multidrug resistance protein 1 (MRP1) mutations and characterization of a G671V substitution. J. Hum. Genet., 46, 656-663.
50. Oselin, K., Mrozikiewicz, P.M., Gaikovitch, E., Pahkla, R. and Roots, I. (2003) Frequency of MRP1 genetic polymorphisms and their functional significance in Caucasians: Detection of a novel mutation G816A in the human MRP1 gene. Eur. J. Clin. Pharmacol., 59, 347-350.
51. Mathijssen, R.H., Marsh, S., Karlsson, M.O., Xie, R., Baker, S.D., Verweij, J., Sparreboom, A. and McLeod, H.L. (2003) Irinotecan pathway genotype analysis to predict pharmacokinetics. Clin. Cancer Res., 9, 3246-3253.
52. Moriya, Y., Nakamura, T., Horinouchi, M., Sakaeda, T., Tamura, T., Aoyama, N., Shirakawa, T., Gotoh, A., Fujimoto, S., Matsuo, M. et al. (2002) Effects of polymorphisms of MDR1, MRP1 and MRP2 genes on their mRNA expression levels in duodenal enterocytes of healthy Japanese subjects. Biol. Pharm. Bull., 25, 1356-1359.
53. Letourneau, I.J., Deeley, R.G. and Cole, S.P. (2005) Functional characterization of non-synonymous single nucleotide polymorphisms in the gene encoding human multidrug resistance protein 1 (MRP1/ABCC1). Pharmacogenet. Genomics., 15, 647-657.
54. Conrad, S., Kauffmann, H.M., Ito, K., Leslie, E.M., Deeley, R.G., Schrenk, D. and Cole, S.P. (2002) A naturally occurring mutation in MRP1 results in a selective decrease in organic anion transport and in increased doxorubicin resistance. Pharmacogenetics, 12, 321-330.
55. Jensen, L.E., Wall, A.M., Cook, M., Hoess, K., Thorn, C.F., Whitehead, A.S. and Mitchell, L.E. (2004) A common ABCC2 promoter polymorphism is not a determinant of the risk of spina bifida. Birth Defects Res. A Clin. Mol. Teratol., 70, 396-399.
56. Meyer zu Schwabedissen, H.E., Jedlitschky, G., Gratz, M., Haenisch, S., Linnemann, K., Fusch, C., Cascorbi, I. and Kroemer, H.K. (2005) Variable expression of MRP2 (ABCC2) in human placenta: Influence of gestational age and cellular differentiation. Drug Metab. Dispos., 33, 896-904.
57. Haenisch, S., Zimmermann, U., Dazert, E., Wruck, C.J., Dazert, P., Siegmund, S., Kroemer, H.K., Warzok, R.W. and Cascorbi, I. (2007) Influence of polymorphisms of ABCB1 and ABCC2 on mRNA and protein expression in normal and cancerous kidney cortex. Pharmacogenomics J. 7, 56-65.
58. Niemi, M., Arnold, K.A., Backman, J.T., Pasanen, M.K., Godtel-Armbrust, U., Wojnowski, L., Zanger, U.M., Neuvonen, P.J., Eichelbaum, M., Kivisto, K.T. et al. (2006) Association of genetic polymorphism in ABCC2 with hepatic multidrug resistance-associated protein 2 expression and pravastatin pharmacokinetics. Pharmacogenet. Genomics, 16 801-808.
59. Lang, T., Hitzl, M., Burk, O., Mornhinweg, E., Keil, A., Kerb, R., Klein, K., Zanger, U.M., Eichelbaum, M. and Fromm, M.F. (2004) Genetic polymorphisms in the multidrug resistance-associated protein 3 (ABCC3, MRP3) gene and relationship to its mRNA and protein expression in human liver. Pharmacogenetics, 14, 155-164.
60. Gradhand, U., Tegude, H., Burk, O., Eichelbaum, M., Fromm, M.F. and Konig, J. (2007) Functional analysis of the polymorphism - 211C>T in the regulatory region of the human ABCC3 gene. Life Sci., 80, 1490-1494.
61. Doerfel, C., Rump, A., Sauerbrey, A., Gruhn, B., Zintl, F. and Steinbach, D. (2006) In acute leukemia, the polymorphism -211C>T in the promoter region of the multidrug resistance-associated protein 3 (MRP3) does not determine the expression level of the gene. Pharmacogenet. Genomics, 16, 149-150.
62. Wang, J., Near, S., Young, K., Connelly, P.W. and Hegele, R.A. (2001) ABCC6 gene polymorphism associated with variation in plasma lipoproteins. J. Hum. Genet., 46, 699-705.
63. Schulz, V., Hendig, D., Henjakovic, M., Szliska, C., Kleesiek, K. and Gotting, C. (2006) Mutational analysis of the ABCC6 gene and the proximal ABCC6 gene promoter in German patients with pseudoxanthoma elasticum (PXE). Hum. Mutat., 27, 831.
64. Yoshiura, K., Kinoshita, A., Ishida, T., Ninokata, A., Ishikawa, T., Kaname, T., Bannai, M., Tokunaga, K., Sonoda, S., Komaki, R. et al. (2006) A SNP in the ABCC11 gene is the determinant of human earwax type. Nat. Genet., 38, 324-330.
65. Imai, Y., Nakane, M., Kage, K., Tsukahara, S., Ishikawa, E., Tsuruo, T., Miki, Y. and Sugimoto, Y. (2002) C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance. Mol. Cancer Ther., 1, 611-616.
66. Kobayashi, D., Ieiri, I., Hirota, T., Takane, H., Maegawa, S., Kigawa, J., Suzuki, H., Nanba, E., Oshimura, M., Terakawa, N. et al. (2005) Functional assessment of ABCG2 (BCRP) gene polymorphisms to protein expression in human placenta. Drug Metab. Dispos., 33 94-101.
67. Kondo, C., Suzuki, H., Itoda, M., Ozawa, S., Sawada, J., Kobayashi, D., Ieiri, I., Mine, K., Ohtsubo, K. and Sugiyama, Y. (2004) Functional analysis of SNPs variants of BCRP/ABCG2. Pharm. Res., 21, 1895-1903.
68. Mizuarai, S., Aozasa, N. and Kotani, H. (2004) Single nucleotide polymorphisms result in impaired membrane localization and reduced atpase activity in multidrug transporter ABCG2. Int. J. Cancer., 109, 238-246.
69. Morisaki, K., Robey, R.W., Ozvegy-Laczka, C., Honjo, Y., Polgar, O., Steadman, K., Sarkadi, B. and Bates, S.E. (2005) Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother. Pharmacol., 56, 161-172.
70. Sparreboom, A., Loos, W.J., Burger, H., Sissung, T.M., Verweij, J., Figg, W.D., Nooter, K. and Gelderblom, H. (2005) Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol. Ther. 4, 650-658.
71. Sparreboom, A., Gelderblom, H., Marsh, S., Ahluwalia, R., Obach, R., Principe, P., Twelves, C., Verweij, J. and McLeod, H.L. (2004) Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype. Clin. Pharmacol. Ther., 76, 38-44.
72. Gwee, P.C., Tang, K., Chua, J.M., Lee, E.J., Chong, S.S. and Lee, C.G. (2003) Simultaneous genotyping of seven single-nucleotide polymorphisms in the MDR1 gene by single-tube multiplex minisequencing. Clin. Chem. 49, 672-676.
73. Lee, C.G., Ramachandra, M., Jeang, K.T., Martin, M.A., Pastan, I. and Gottesman, M.M. (2000) Effect of ABC transporters on HIV-1 infection: inhibition of virus production by the MDR1 transporter. FASEB J., 14, 516-522.
74. Schwab, M., Eichelbaum, M. and Fromm, M.F. (2003) Genetic polymorphisms of the human mdr1 drug transporter. Annu. Rev. Pharmacol. Toxicol. 43, 285-307.
75. Gendrot, C., Bacq, Y., Brechot, M.C., Lansac, J. and Andres, C. (2003) A second heterozygous MDR3 nonsense mutation associated with intrahepatic cholestasis of pregnancy. J. Med. Genet., 40, e32.
76. Keitel, V., Vogt, C., Haussinger, D. and Kubitz, R. (2006) Combined mutations of canalicular transporter proteins cause severe intrahepatic cholestasis of pregnancy. Gastroenterology, 131, 624-629.
77. Obata, H., Yahata, T., Quan, J., Sekine, M. and Tanaka, K. (2006) Association between single nucleotide polymorphisms of drug resistance-associated genes and response to chemotherapy in advanced ovarian cancer. Anticancer Res., 26, 2227-2232.
78. Hirouchi, M., Suzuki, H., Itoda, M., Ozawa, S., Sawada, J., Ieiri, I., Ohtsubo, K. and Sugiyama, Y. (2004) Characterization of the cellular localization, expression level, and function of SNP variants of MRP2/ABCC2. Pharm. Res., 21, 742-748.
79. Rowe, S.M., Miller, S. and Sorscher, E.J. (2005) Cystic fibrosis. N. Engl. J. Med., 352, 1992-2001.
80. Zamboni, W.C., Ramanathan, R.K., McLeod, H.L., Mani, S., Potter, D.M., Strychor, S., Maruca, L.J., King, C.R., Jung, L.L., Parise, R.A., Egorin, M.J., Davis, T.A. and Marsh, S. (2006) Disposition of 9-nitrocamptothecin and its 9-aminocamptothecin metabolite in relation to ABC transporter genotypes. Invest. New Drugs, 24, 393-401.