Pharmacogenomics of human multidrug resistance associated proteins

Current Pharmacogenomics and Personalized Medicine

Volumn 6, Issue 2, 2008, Pages 134-149

  Zhou, Shu Feng ^a   Fulcher, Jana ^b  

^a RMIT UNIVERSITY   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

7 ETHYL 10 HYDROXYCAMPTOTHECIN; ADEFOVIR; AMINO ACID DERIVATIVE; ANTINEOPLASTIC AGENT; CAMPTOTHECIN DERIVATIVE; CISPLATIN; CYCLOPHOSPHAMIDE; DICLOFENAC; DOXORUBICIN; ETOPOSIDE; FLUCYTOSINE DEOXYRIBOSIDE; FLUOROURACIL; GANCICLOVIR; INDOMETACIN; IRINOTECAN; MERCAPTOPURINE; METHOTREXATE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; PARACETAMOL; SULFINPYRAZONE; TAXANE DERIVATIVE; UNINDEXED DRUG; VERAPAMIL; VINCRISTINE; XENOBIOTIC AGENT; ZIDOVUDINE DERIVATIVE;

CANCER RESISTANCE; CARDIOTOXICITY; DRUG EFFICACY; DRUG METABOLISM; DRUG PENETRATION; DRUG SAFETY; DRUG TRANSPORT; ENZYME SUBSTRATE; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; LIVER TOXICITY; MALIGNANT NEOPLASTIC DISEASE; MULTIDRUG RESISTANCE; NONHUMAN; PHARMACEUTICAL CARE; PHARMACOGENOMICS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 67649354458     PISSN: 18756921     EISSN: 18756913     Source Type: Journal    
DOI: 10.2174/1875692110806020134     Document Type: Review

References (111)

1. Anderson, P. L.; Lamba, J.; Aquilante, C. L.; Schuetz, E. and Fletcher, C. V. (2006) Pharmacogenetic characteristics of indinavir, zidovudine, and lamivudine therapy in HIV-infected adults: a pilot study. J. Acquir. Immune Defic. Syndr. 42, 441-449.
2. Bartosz, G.; Konig, J.; Keppler, D. and Hagmann, W. (1998) Human mast cells secreting leukotriene C4 express the MRP1 gene-encoded conjugate export pump. Biol. Chem. 379, 1121-1126.
3. Belinsky, M. G.; Chen, Z. S.; Shchaveleva, I.; Zeng, H. and Kruh, G. D. (2002) Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res. 62, 6172-6177.
4. Bera, T. K.; Iavarone, C.; Kumar, V.; Lee, S.; Lee, B. and Pastan, I. (2002) MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc. Natl. Acad. Sci. USA 99, 6997-7002.
5. Bera, T. K.; Lee, S.; Salvatore, G.; Lee, B. and Pastan, I. (2001) MRP8, a new member of ABC transporter superfamily, identified by EST database mining and gene prediction program, is highly expressed in breast cancer. Mol. Med. 7, 509-516.
6. Bergen, A. A.; Plomp, A. S.; Hu, X.; de Jong, P. T. and Gorgels, T. G. (2007) ABCC6 and pseudoxanthoma elasticum. Pflugers Arch. 453, 685-691.
7. Bohan, A.; Chen, W. S.; Denson, L. A.; Held, M. A. and Boyer, J. L. (2003) Tumor necrosis factor alpha-dependent up-regulation of Lrh-1 and Mrp3(Abcc3) reduces liver injury in obstructive cholestasis. J. Biol. Chem. 278, 36688-36698.
8. Borst, P.; Evers, R.; Kool, M. and Wijnholds, J. (2000) A family of drug transporters: the multidrug resistance-associated proteins. J. Natl. Cancer Inst. 92, 1295-1302.
9. Buchler, M.; Konig, J.; Brom, M.; Kartenbeck, J.; Spring, H.; Horie, T. and Keppler, D. (1996) cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J. Biol. Chem. 271, 15091-15098.
10. Cai, L.; Lumsden, A.; Guenther, U. P.; Neldner, S. A.; Zach, S.; Knoblauch, H.; Ramesar, R.; Hohl, D.; Callen, D. F.; Neldner, K. H.; Lindpaintner, K.; Richards, R. I. and Struk, B. (2001) A novel Q378X mutation exists in the transmembrane transporter protein ABCC6 and its pseudogene: implications for mutation analysis in pseudoxanthoma elasticum. J. Mol. Med. 79, 536-546.
11. Cascorbi, I. (2006) Role of pharmacogenetics of ATP-binding cassette transporters in the pharmacokinetics of drugs. Pharmacol. Ther. 112, 457-473.
12. Chassaing, N.; Martin, L.; Calvas, P.; Le Bert, M. and Hovnanian, A. (2005) Pseudoxanthoma elasticum: a clinical, pathophysiological and genetic update including 11 novel ABCC6 mutations. J. Med. Genet. 42, 881-892.
13. Chassaing, N.; Martin, L.; Mazereeuw, J.; Barrie, L.; Nizard, S.; Bonafe, J. L.; Calvas, P. and Hovnanian, A. (2004) Novel ABCC6 mutations in pseudoxanthoma elasticum. J. Invest. Dermatol. 122, 608-613.
14. Choi, J. H.; Ahn, B. M.; Yi, J.; Lee, J. H.; Lee, J. H.; Nam, S. W.; Chon, C. Y.; Han, K. H.; Ahn, S. H.; Jang, I. J.; Cho, J. Y.; Suh, Y.; Cho, M. O.; Lee, J. E.; Kim, K. H. and Lee, M. G. (2007) MRP2 haplotypes confer differential susceptibility to toxic liver injury. Pharmacogenet. Genomics 17, 403-415.
15. Choudhuri, S.; Cherrington, N. J.; Li, N. and Klaassen, C. D. (2003) Constitutive expression of various xenobiotic and endobiotic transporter mRNAs in the choroid plexus of rats. Drug Metab. Dispos. 31, 1337-1345.
16. Choudhuri, S. and Klaassen, C. D. (2006) Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int. J. Toxicol. 25, 231-259.
17. Cole, S. P.; Bhardwaj, G.; Gerlach, J. H.; Mackie, J. E.; Grant, C. E.; Almquist, K. C.; Stewart, A. J.; Kurz, E. U.; Duncan, A. M. and Deeley, R. G. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654.
18. 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.
19. 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.
20. Conseil, G.; Deeley, R. G. and Cole, S. P. (2005) Polymorphisms of MRP1 (ABCC1) and related ATP-dependent drug transporters. Pharmacogenet. Genomics 15, 523-533.
21. Couture, L.; Nash, J. A. and Turgeon, J. (2006) The ATP-binding cassette transporters and their implication in drug disposition: a special look at the heart. Pharmacol. Rev. 58, 244-258.
22. Cui, Y.; Konig, J.; Buchholz, J. K.; Spring, H.; Leier, I. and Keppler, D. (1999) Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. 55, 929-937.
23. Daly, A. K.; Aithal, G. P.; Leathart, J. B.; Swainsbury, R. A.; Dang, T. S. and Day, C. P. (2007) Genetic susceptibility to diclofenac-induced hepatotoxicity: contribution of UGT2B7, CYP2C8, and ABCC2 genotypes. Gastroenterology 132, 272-281.
24. Eichelbaum, M.; Ingelman-Sundberg, M. and Evans, W. E. (2006) Pharmacogenomics and individualized drug therapy. Annu. Rev. Med. 57, 119-137.
25. Evans, W. E. and Johnson, J. A. (2001) Pharmacogenomics: the inherited basis for interindividual differences in drug response. Annu. Rev. Genom. Human Genet. 2, 9-39.
26. Fukushima-Uesaka, H.; Saito, Y.; Maekawa, K.; Hasegawa, R.; Suzuki, K.; Yanagawa, T.; Kajio, H.; Kuzuya, N.; Noda, M.; Yasuda, K.; Tohkin, M. and Sawada, J. (2007a) Genetic variations of the ABC transporter gene ABCC3 in a Japanese population. Drug Metab. Pharmacokinet. 22, 129-135.
27. Fukushima-Uesaka, H.; Saito, Y.; Tohkin, M.; Maekawa, K.; Hasegawa, R.; Kawamoto, M.; Kamatani, N.; Suzuki, K.; Yanagawa, T.; Kajio, H.; Kuzuya, N.; Yasuda, K. and Sawada, J. (2007b) Genetic variations and haplotype structures of the ABC transporter gene ABCC1 in a Japanese population. Drug Metab. Pharmacokinet. 22, 48-60.
28. Gerloff, T. (2004) Impact of genetic polymorphisms in transmembrane carrier-systems on drug and xenobiotic distribution. Naunyn Schmiedebergs Arch. Pharmacol. 369, 69-77.
29. Germain, D. P.; Remones, V.; Perdu, J. and Jeunemaitre, X. (2000) Identification of two polymorphisms (c189G>C; c190T>C) in exon 2 of the human MRP6 gene (ABCC6) by screening of Pseudoxanthoma elasticum patients: possible sequence correction? Hum. Mutat. 16, 449.
30. Gheduzzi, D.; Guidetti, R.; Anzivino, C.; Tarugi, P.; Di Leo, E.; Quaglino, D. and Ronchetti, I. P. (2004) ABCC6 mutations in Italian families affected by pseudoxanthoma elasticum (PXE). Hum. Mutat. 24, 438-439.
31. Gorgels, T. G.; Hu, X.; Scheffer, G. L.; van der Wal, A. C.; Toonstra, J.; de Jong, P. T.; van Kuppevelt, T. H.; Levelt, C. N.; de Wolf, A.; Loves, W. J.; Scheper, R. J.; Peek, R. and Bergen, A. A. (2005) Disruption of Abcc6 in the mouse: novel insight in the pathogenesis of pseudoxanthoma elasticum. Hum. Mol. Genet. 14, 1763-1773.
32. Gradhand, U.; Lang, T.; Schaeffeler, E.; Glaeser, H.; Tegude, H.; Klein, K.; Fritz, P.; Jedlitschky, G.; Kroemer, H. K.; Bachmakov, I.; Anwald, B.; Kerb, R.; Zanger, U. M.; Eichelbaum, M.; Schwab, M. and Fromm, M. F. (2008) Variability in human hepatic MRP4 expression: influence of cholestasis and genotype. Pharmacogenomics J. 8, 42-52.
33. 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.
34. Guo, Y.; Kotova, E.; Chen, Z. S.; Lee, K.; Hopper-Borge, E.; Belinsky, M. G. and Kruh, G. D. (2003) MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2′,3′-dideoxycytidine and 9′-(2′-phosphonylmethoxyethyl)adenine. J. Biol. Chem. 278, 29509-29514.
35. 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.
36. Hipfner, D. R.; Deeley, R. G. and Cole, S. P. (1999) Structural, mechanistic and clinical aspects of MRP1. Biochim. Biophys. Acta 1461, 359-376.
37. Hirohashi, T.; Suzuki, H. and Sugiyama, Y. (1999) Characterization of the transport properties of cloned rat multidrug resistance-associated protein 3 (MRP3). J. Biol. Chem. 274, 15181-15185.
38. Hitzl, M.; Klein, K.; Zanger, U. M.; Fritz, P.; Nussler, A. K.; Neuhaus, P. and Fromm, M. F. (2003) Influence of omeprazole on multidrug resistance protein 3 expression in human liver. J. Pharmacol. Exp. Ther. 304, 524-530.
39. Hooijberg, J. H.; Broxterman, H. J.; Kool, M.; Assaraf, Y. G.; Peters, G. J.; Noordhuis, P.; Scheper, R. J.; Borst, P.; Pinedo, H. M. and Jansen, G. (1999) Antifolate resistance mediated by the multidrug resistance proteins MRP1 and MRP2. Cancer Res. 59, 2532-2535.
40. Hopper-Borge, E.; Chen, Z. S.; Shchaveleva, I.; Belinsky, M. G. and Kruh, G. D. (2004) Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res. 64, 4927-4930.
41. Hopper, E.; Belinsky, M. G.; Zeng, H.; Tosolini, A.; Testa, J. R. and Kruh, G. D. (2001) Analysis of the structure and expression pattern of MRP7 (ABCC10), a new member of the MRP subfamily. Cancer Lett. 162, 181-191.
42. Huang, Y. (2007) Pharmacogenetics/genomics of membrane transporters in cancer chemotherapy. Cancer Metastasis Rev. 26, 183-201.
43. Hulot, J. S.; Villard, E.; Maguy, A.; Morel, V.; Mir, L.; Tostivint, I.; William-Faltaos, D.; Fernandez, C.; Hatem, S.; Deray, G.; Komajda, M.; Leblond, V. and Lechat, P. (2005) A mutation in the drug transporter gene ABCC2 associated with impaired methotrexate elimination. Pharmacogenet. Genomics 15, 277-285.
44. Hyde, S. C.; Emsley, P.; Hartshorn, M. J.; Mimmack, M. M.; Gileadi, U.; Pearce, S. R.; Gallagher, M. P.; Gill, D. R.; Hubbard, R. E. and Higgins, C. F. (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346, 362-365.
45. Imaoka, T.; Kusuhara, H.; Adachi, M.; Schuetz, J. D.; Takeuchi, K. and Sugiyama, Y. (2007) Functional involvement of multidrug resistance-associated protein 4 (MRP4/ABCC4) in the renal elimination of the antiviral drugs adefovir and tenofovir. Mol. Pharmacol. 71, 619-627.
46. 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. and 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.
47. Inokuchi, A.; Hinoshita, E.; Iwamoto, Y.; Kohno, K.; Kuwano, M. and Uchiumi, T. (2001) Enhanced expression of the human multidrug resistance protein 3 by bile salt in human enterocytes. A transcriptional control of a plausible bile acid transporter. J. Biol. Chem. 276, 46822-46829.
48. Ito, S.; Ieiri, I.; Tanabe, M.; Suzuki, A.; Higuchi, S. and Otsubo, K. (2001) Polymorphism of the ABC transporter genes, MDR1, MRP1 and MRP2/ cMOAT, in healthy Japanese subjects. Pharmacogenetics 11, 175-184.
49. Itoda, M.; Saito, Y.; Soyama, A.; Saeki, M.; Murayama, N.; Ishida, S.; Sai, K.; Nagano, M.; Suzuki, H.; Sugiyama, Y.; Ozawa, S. and Sawada Ji, J. (2002) Polymorphisms in the ABCC2 (cMOAT/MRP2) gene found in 72 established cell lines derived from Japanese individuals: an association between single nucleotide polymorphisms in the 5′-untranslated region and exon 28. Drug Metab. Dispos. 30, 363-364.
50. Izzedine, H.; Hulot, J. S.; Villard, E.; Goyenvalle, C.; Dominguez, S.; Ghosn, J.; Valantin, M. A.; Lechat, P. and Deray, A. G. (2006) Association between ABCC2 gene haplotypes and tenofovir-induced proximal tubulopathy. J. Infect. Dis. 194, 1481-1491.
51. Koike, K.; Kawabe, T.; Tanaka, T.; Toh, S.; Uchiumi, T.; Wada, M.; Akiyama, S.; Ono, M. and Kuwano, M. (1997) A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res. 57, 5475-5479.
52. Kool, M.; de Haas, M.; Scheffer, G. L.; Scheper, R. J.; van Eijk, M. J.; Juijn, J. A.; Baas, F. and Borst, P. (1997) Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57, 3537-3547.
53. Kool, M.; van der Linden, M.; de Haas, M.; Baas, F. and Borst, P. (1999a) Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res. 59, 175-182.
54. Kool, M.; van der Linden, M.; de Haas, M.; Scheffer, G. L.; de Vree, J. M.; Smith, A. J.; Jansen, G.; Peters, G. J.; Ponne, N.; Scheper, R. J.; Elferink, R. P.; Baas, F. and Borst, P. (1999b) MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc. Natl. Acad. Sci. USA 96, 6914-6919.
55. Kruh, G. D. and Belinsky, M. G. (2003) The MRP family of drug efflux pumps. Oncogene 22, 7537-7552.
56. Kruh, G. D.; Belinsky, M. G.; Gallo, J. M. and Lee, K. (2007a) Physiological and pharmacological functions of Mrp2, Mrp3 and Mrp4 as determined from recent studies on gene-disrupted mice. Cancer Metastasis Rev. 26, 5-14.
57. Kruh, G. D.; Gaughan, K. T.; Godwin, A. and Chan, A. (1995) Expression pattern of MRP in human tissues and adult solid tumor cell lines. J. Natl. Cancer Inst. 87, 1256-1258.
58. Kruh, G. D.; Guo, Y.; Hopper-Borge, E.; Belinsky, M. G. and Chen, Z. S. (2007b) ABCC10, ABCC11, and ABCC12. Pflugers Arch. 453, 675-684.
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. Lee, K.; Belinsky, M. G.; Bell, D. W.; Testa, J. R. and Kruh, G. D. (1998) Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/canalicular multispecific organic anion transporter-related transporter. Cancer Res. 58, 2741-2747.
61. Lee, Y. M.; Cui, Y.; Konig, J.; Risch, A.; Jager, B.; Drings, P.; Bartsch, H.; Keppler, D. and Nies, A. T. (2004) Identification and functional characterization of the natural variant MRP3-Arg1297His of human multidrug resistance protein 3 (MRP3/ABCC3). Pharmacogenetics 14, 213-223.
62. Leggas, M.; Adachi, M.; Scheffer, G. L.; Sun, D.; Wielinga, P.; Du, G.; Mercer, K. E.; Zhuang, Y.; Panetta, J. C.; Johnston, B.; Scheper, R. J.; Stewart, C. F. and Schuetz, J. D. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol. Cell Biol. 24, 7612-7621.
63. Leschziner, G.; Zabaneh, D.; Pirmohamed, M.; Owen, A.; Rogers, J.; Coffey, A. J.; Balding, D. J.; Bentley, D. B. and Johnson, M. R. (2006) Exon sequencing and high resolution haplotype analysis of ABC transporter genes implicated in drug resistance. Pharmacogenet. Genomics 16, 439-450.
64. Leslie, E. M.; Deeley, R. G. and Cole, S. P. (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204, 216-237.
65. Leslie, E. M.; Letourneau, I. J.; Deeley, R. G. and Cole, S. P. (2003) Functional and structural consequences of cysteine substitutions in the NH2 proximal region of the human multidrug resistance protein 1 (MRP1/ ABCC1). Biochemistry 42, 5214-5224.
66. 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.
67. Lockhart, A. C.; Tirona, R. G. and Kim, R. B. (2003) Pharmacogenetics of ATP-binding cassette transporters in cancer and chemotherapy. Mol. Cancer Ther. 2, 685-698.
68. Machida, I.; Wakusawa, S.; Sanae, F.; Hayashi, H.; Kusakabe, A.; Ninomiya, H.; Yano, M. and Yoshioka, K. (2005) Mutational analysis of the MRP2 gene and long-term follow-up of Dubin-Johnson syndrome in Japan. J. Gastroenterol. 40, 366-370.
69. Maekawa, K.; Itoda, M.; Sai, K.; Saito, Y.; Kaniwa, N.; Shirao, K.; Hamaguchi, T.; Kunitoh, H.; Yamamoto, N.; Tamura, T.; Minami, H.; Kubota, K.; Ohtsu, A.; Yoshida, T.; Saijo, N.; Kamatani, N.; Ozawa, S. and Sawada, J. (2006) Genetic variation and haplotype structure of the ABC transporter gene ABCG2 in a Japanese population. Drug Metab. Pharmacokinet. 21, 109-121.
70. Manautou, J. E.; de Waart, D. R.; Kunne, C.; Zelcer, N.; Goedken, M.; Borst, P. and Elferink, R. O. (2005) Altered disposition of acetaminophen in mice with a disruption of the Mrp3 gene. Hepatology 42, 1091-1098.
71. Matsunaga, S.; Asano, T.; Tsutsuda-Asano, A. and Fukunaga, Y. (2006) Indomethacin overcomes doxorubicin resistance with inhibiting multi-drug resistance protein 1 (MRP1). Cancer Chemother. Pharmacol. 58, 348-353.
72. Matsuzaki, Y.; Nakano, A.; Jiang, Q. J.; Pulkkinen, L. and Uitto, J. (2005) Tissue-specific expression of the ABCC6 gene. J. Invest. Dermatol. 125, 900-905.
73. Meloni, I.; Rubegni, P.; De Aloe, G.; Bruttini, M.; Pianigiani, E.; Cusano, R.; Seri, M.; Mondillo, S.; Federico, A.; Bardelli, A. M.; Andreassi, L.; Fimiani, M. and Renieri, A. (2001) Pseudoxanthoma elasticum: Point mutations in the ABCC6 gene and a large deletion including also ABCC1 and MYH11. Hum. Mutat. 18, 85.
74. Moriya, Y.; Nakamura, T.; Horinouchi, M.; Sakaeda, T.; Tamura, T.; Aoyama, N.; Shirakawa, T.; Gotoh, A.; Fujimoto, S.; Matsuo, M.; Kasuga, M. and Okumura, K. (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.
75. Naesens, M.; Kuypers, D. R.; Verbeke, K. and Vanrenterghem, Y. (2006) Multidrug resistance protein 2 genetic polymorphisms influence mycophenolic acid exposure in renal allograft recipients. Transplantation 82, 1074-1084.
76. Nezasa, K.; Tian, X.; Zamek-Gliszczynski, M. J.; Patel, N. J.; Raub, T. J. and Brouwer, K. L. (2006) Altered hepatobiliary disposition of 5 (and 6)-carboxy-2′,7′-dichlorofluorescein in Abcg2 (Bcrp1) and Abcc2 (Mrp2) knockout mice. Drug Metab. Dispos. 34, 718-723.
77. Oguri, T.; Isobe, T.; Suzuki, T.; Nishio, K.; Fujiwara, Y.; Katoh, O. and Yamakido, M. (2000) Increased expression of the MRP5 gene is associated with exposure to platinum drugs in lung cancer. Int. J. Cancer 86, 95-100.
78. 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.
79. Paulusma, C. C.; Kool, M.; Bosma, P. J.; Scheffer, G. L.; ter Borg, F.; Scheper, R. J.; Tytgat, G. N.; Borst, P.; Baas, F. and Oude Elferink, R. P. (1997) A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome. Hepatology 25, 1539-1542.
80. Perdu, J. and Germain, D. P. (2001) Identification of novel polymorphisms in the pM5 and MRP1 (ABCC1) genes at locus 16p13.1 and exclusion of both genes as responsible for pseudoxanthoma elasticum. Hum. Mutat. 17, 74-75.
81. Pulkkinen, L.; Nakano, A.; Ringpfeil, F. and Uitto, J. (2001) Identification of ABCC6 pseudogenes on human chromosome 16p: implications for mutation detection in pseudoxanthoma elasticum. Hum. Genet. 109, 356-365.
82. Reid, G.; Wielinga, P.; Zelcer, N.; van der Heijden, I.; Kuil, A.; de Haas, M.; Wijnholds, J. and Borst, P. (2003) The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl. Acad. Sci. USA 100, 9244-9249.
83. Rius, M.; Nies, A. T.; Hummel-Eisenbeiss, J.; Jedlitschky, G. and Keppler, D. (2003) Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38, 374-384.
84. Robbiani, D. F.; Finch, R. A.; Jager, D.; Muller, W. A.; Sartorelli, A. C. and Randolph, G. J. (2000) The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3beta, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103, 757-768.
85. Saito, S.; Iida, A.; Sekine, A.; Miura, Y.; Ogawa, C.; Kawauchi, S.; Higuchi, S. and Nakamura, Y. (2002) Identification of 779 genetic variations in eight genes encoding members of the ATP-binding cassette, subfamily C (ABCC/MRP/CFTR. J. Hum. Genet. 47, 147-171.
86. Schneider, E.; Yamazaki, H.; Sinha, B. K. and Cowan, K. H. (1995) Buthionine sulphoximine-mediated sensitisation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer 71, 738-743.
87. Schuetz, J. D.; Connelly, M. C.; Sun, D. X.; Paibir, S. G.; Flynn, P. M.; Srinivas, R. V.; Kumar, A. and Fridland, A. (1999) MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat. Med. 5, 1048-1051.
88. Sparreboom, A.; Danesi, R.; Ando, Y.; Chan, J. and Figg, W. D. (2003) Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Resist. Updat. 6, 71-84.
89. Sridhar, R.; Dwivedi, C.; Anderson, J.; Baker, P. B.; Sharma, H. M.; Desai, P. and Engineer, F. N. (1992) Effects of verapamil on the acute toxicity of doxorubicin in vivo. J. Natl. Cancer Inst. 84, 1653-1660.
90. Suzuki, H. and Sugiyama, Y. (2002) Single nucleotide polymorphisms in multidrug resistance associated protein 2 (MRP2/ABCC2): its impact on drug disposition. Adv. Drug Deliv. Rev. 54, 1311-1331.
91. Taniguchi, K.; Wada, M.; Kohno, K.; Nakamura, T.; Kawabe, T.; Kawakami, M.; Kagotani, K.; Okumura, K.; Akiyama, S. and Kuwano, M. (1996) A human canalicular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation. Cancer Res. 56, 4124-4129.
92. Teng, S.; Jekerle, V. and Piquette-Miller, M. (2003) Induction of ABCC3 (MRP3) by pregnane X receptor activators. Drug Metab. Dispos. 31, 1296-1299.
93. Tian, Q.; Zhang, J.; Chan, E.; Duan, W. and Zhou, S. F. (2005) Multidrug resistance proteins (MRPs) and implication in drug development. Drug Dev. Res. 51, 1-18.
94. Toh, S.; Wada, M.; Uchiumi, T.; Inokuchi, A.; Makino, Y.; Horie, Y.; Adachi, Y.; Sakisaka, S. and Kuwano, M. (1999) Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome. Am. J. Hum. Genet. 64, 739-746.
95. van Aubel, R. A.; Smeets, P. H.; Peters, J. G.; Bindels, R. J. and Russel, F. G. (2002) The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 13, 595-603.
96. Van Aubel, R. A.; Smeets, P. H.; van den Heuvel, J. J. and Russel, F. G. (2005) Human organic anion transporter MRP4 (ABCC4) is an efflux pump for the purine end metabolite urate with multiple allosteric substrate binding sites. Am. J. Physiol. Renal Physiol. 288, F327-F333.
97. Versantvoort, C. H.; Broxterman, H. J.; Bagrij, T.; Scheper, R. J. and Twentyman, P. R. (1995) Regulation by glutathione of drug transport in multidrug-resistant human lung tumour cell lines overexpressing multidrug resistance-associated protein. Br. J. Cancer 72, 82-89.
98. Wang, H.; Hao, B.; Zhou, K.; Chen, X.; Wu, S.; Zhou, G.; Zhu, Y. and He, F. (2004) Linkage disequilibrium and haplotype architecture for two ABC transporter genes (ABCC1 and ABCG2) in Chinese population: implications for pharmacogenomic association studies. Ann. Hum. Genet. 68, 563-573.
99. Wang, Z.; Sew, P. H.; Ambrose, H.; Ryan, S.; Chong, S. S.; Lee, E. J. and Lee, C. G. (2006) Nucleotide sequence analyses of the MRP1 gene in four populations suggest negative selection on its coding region. BMC Genomics 7, 111.
100. 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.
101. Wielinga, P. R.; van der Heijden, I.; Reid, G.; Beijnen, J. H.; Wijnholds, J. and Borst, P. (2003) Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J. Biol. Chem. 278, 17664-17671.
102. Wijnholds, J.; deLange, E. C.; Scheffer, G. L.; van den Berg, D. J.; Mol, C. A.; van der Valk, M.; Schinkel, A. H.; Scheper, R. J.; Breimer, D. D. and Borst, P. (2000a) Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J. Clin. Invest. 105, 279-285.
103. Wijnholds, J.; Mol, C. A.; van Deemter, L.; de Haas, M.; Scheffer, G. L.; Baas, F.; Beijnen, J. H.; Scheper, R. J.; Hatse, S.; De Clercq, E.; Balzarini, J. and Borst, P. (2000b) Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. USA 97, 7476-7481.
104. Yabuuchi, H.; Shimizu, H.; Takayanagi, S. and Ishikawa, T. (2001) Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem. Biophys. Res. Commun. 288, 933-939.
105. Yu, X. Q.; Xue, C. C.; Wang, G. and Zhou, S. F. (2007) Multidrug resistance associated proteins as determining factors of pharmacokinetics and pharmacodynamics of drugs. Curr. Drug Metab. 8, 787-802.
106. 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.
107. Zelcer, N.; Reid, G.; Wielinga, P.; Kuil, A.; van der Heijden, I.; Schuetz, J. D. and Borst, P. (2003) Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem. J. 371, 361-367.
108. Zelcer, N.; Saeki, T.; Reid, G.; Beijnen, J. H. and Borst, P. (2001) Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J. Biol. Chem. 276, 46400-46407.
109. Zelcer, N.; van de Wetering, K.; de Waart, R.; Scheffer, G. L.; Marschall, H. U.; Wielinga, P. R.; Kuil, A.; Kunne, C.; Smith, A.; van der Valk, M.; Wijnholds, J.; Elferink, R. O. and Borst, P. (2006) Mice lacking Mrp3 (Abcc3) have normal bile salt transport, but altered hepatic transport of endogenous glucuronides. J. Hepatol. 44, 768-775.
110. Zeng, H.; Bain, L. J.; Belinsky, M. G. and Kruh, G. D. (1999) Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents. Cancer Res. 59, 5964-5967.
111. Zhang, D. W.; Cole, S. P. and Deeley, R. G. (2001) Identification of a non-conserved amino acid residue in multidrug resistance protein 1 important for determining substrate specificity: evidence for functional interaction between transmembrane helices 14 and 17. J. Biol. Chem. 276, 34966-34974.