Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases

FEBS Journal

Volumn 278, Issue 18, 2011, Pages 3226-3245

  Chen, Zhe Sheng ^a   Tiwari, Amit K ^a  

^a ST JOHN'S UNIVERSITY   (United States)

Author keywords

ABCC transporters; cancer chemotherapy; cyclic nucleotides; Dubin Johnson syndrome; genetic diseases; GS X efflux pump; leukotriene C4; multidrug resistance; multiple resistance protein; Pseudoxanthoma elasticum

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER C; ADENOSINE TRIPHOSPHATE; ANION; ANTINEOPLASTIC AGENT; CYCLIC AMP; DRUG METABOLITE; LEUKOTRIENE C4; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; MULTIDRUG RESISTANCE PROTEIN 7; MULTIDRUG RESISTANCE PROTEIN 8; MULTIDRUG RESISTANCE PROTEIN 9; UNCLASSIFIED DRUG;

CANCER CELL; CANCER CHEMOTHERAPY; DRUG DISPOSITION; DRUG ELIMINATION; DRUG TRANSPORT; DUBIN JOHNSON SYNDROME; GENE MUTATION; GENETIC DISORDER; HEPATOBILIARY SYSTEM; HUMAN; MEMBRANE TRANSPORT; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PSEUDOXANTHOMA ELASTICUM; REVIEW; URINARY EXCRETION;

ANIMALS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; GENETIC DISEASES, INBORN; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; NEOPLASMS; PROTEIN ISOFORMS;

EID: 80052449326     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08235.x     Document Type: Review

References (193)

1. Dean M, &, Allikmets R, (2001) Complete characterization of the human ABC gene family. J Bioenerg Biomembr 33, 475-479.
2. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, &, Deeley RG, (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654.
3. Deeley RG, Westlake C, &, Cole SP, (2006) Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86, 849-899.
4. Slot AJ, Molinkski SV, &, Cole SPC, (2011) Mammalian multidrug resistance proteins (MRPs). Essays Biochem 50, doi:.
5. Borst P, Evers R, Kool M, &, Wijnholds J, (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92, 1295-1302.
6. Hollenstein K, Dawson RJ, &, Locher KP, (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17, 412-418.
7. Linton KJ, &, Higgins CF, (2007) Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch 453, 555-567.
8. Qin L, Zheng J, Grant CE, Jia Z, Cole SP, &, Deeley RG, (2008) Residues responsible for the asymmetric function of the nucleotide binding domains of multidrug resistance protein 1. Biochemistry 47, 13952-13965.
9. Leslie EM, Deeley RG, &, Cole SP, (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204, 216-237.
10. Cole SP, &, Deeley RG, (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 27, 438-446.
11. Wijnholds J, Evers R, van Leusden MR, Mol CA, Zaman GJ, Mayer U, Beijnen JH, van der Valk M, Krimpenfort P, &, Borst P, (1997) Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking the multidrug resistance-associated protein. Nat Med 3, 1275-1279.
12. Wijnholds J, Scheffer GL, van der Valk M, van der Valk P, Beijnen JH, Scheper RJ, &, Borst P, (1998) Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J Exp Med 188, 797-808.
13. Lorico A, Rappa G, Finch RA, Yang D, Flavell RA, &, Sartorelli AC, (1997) Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res 57, 5238-5242.
14. Leier I, Jedlitschky G, Buchholz U, Cole SP, Deeley RG, &, Keppler D, (1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 269, 27807-27810.
15. Samuelsson B, Dahlen SE, Lindgren JA, Rouzer CA, &, Serhan CN, (1987) Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 237, 1171-1176.
16. Ishikawa T, (1992) The ATP-dependent glutathione S-conjugate export pump. Trends Biochem Sci 17, 463-468.
17. Leslie EM, Ito K, Upadhyaya P, Hecht SS, Deeley RG, &, Cole SP, (2001) Transport of the beta-O-glucuronide conjugate of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) by the multidrug resistance protein 1 (MRP1). Requirement for glutathione or a non-sulfur-containing analog. J Biol Chem 276, 27846-27854.
18. Zhang DW, Cole SP, &, Deeley RG, (2001) Identification of an amino acid residue in multidrug resistance protein 1 critical for conferring resistance to anthracyclines. J Biol Chem 276, 13231-13239.
19. Leier I, Jedlitschky G, Buchholz U, Center M, Cole SP, Deeley RG, &, Keppler D, (1996) ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem J 314 (Pt 2), 433-437.
20. Krause MS, Oliveira LP Jr, Silveira EM, Vianna DR, Rossato JS, Almeida BS, Rodrigues MF, Fernandes AJ, Costa JA, Curi R, et al. (2007) MRP1/GS-X pump ATPase expression: is this the explanation for the cytoprotection of the heart against oxidative stress-induced redox imbalance in comparison to skeletal muscle cells? Cell Biochem Funct 25, 23-32.
21. Loe DW, Deeley RG, &, Cole SP, (2000) Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 293, 530-538.
22. Leslie EM, Deeley RG, &, Cole SP, (2003) Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab Dispos 31, 11-15.
23. 4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 271, 9675-9682.
24. Mao Q, Deeley RG, &, Cole SP, (2000) Functional reconstitution of substrate transport by purified multidrug resistance protein MRP1 (ABCC1) in phospholipid vesicles. J Biol Chem 275, 34166-34172.
25. Qian YM, Song WC, Cui H, Cole SP, &, Deeley RG, (2001) Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem 276, 6404-6411.
26. Leslie EM, Bowers RJ, Deeley RG, &, Cole SP, (2003) Structural requirements for functional interaction of glutathione tripeptide analogs with the human multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 304, 643-653.
27. Deeley RG, &, Cole SP, (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 580, 1103-1111.
28. Iram SH, &, Cole SP, (2011) Expression and function of human MRP1 (ABCC1) is dependent on amino acids in cytoplasmic loop 5 and its interface with nucleotide binding domain 2. J Biol Chem 286, 7202-7213.
29. Tiwari AK, Sodani K, Dai CL, Ashby CR Jr, &, Chen ZS, (2011) Revisiting the ABCs of multidrug resistance in cancer chemotherapy. Curr Pharm Biotechnol 12, 570-594.
30. Loe DW, Deeley RG, &, Cole SP, (1998) Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res 58, 5130-5136.
31. Hegedus T, Orfi L, Seprodi A, Varadi A, Sarkadi B, &, Keri G, (2002) Interaction of tyrosine kinase inhibitors with the human multidrug transporter proteins, MDR1 and MRP1. Biochim Biophys Acta 1587, 318-325.
32. Nooter K, Westerman AM, Flens MJ, Zaman GJ, Scheper RJ, van Wingerden KE, Burger H, Oostrum R, Boersma T, Sonneveld P, et al. (1995) Expression of the multidrug resistance-associated protein (MRP) gene in human cancers. Clin Cancer Res 1, 1301-1310.
33. Burger H, Foekens JA, Look MP, Meijer-van Gelder ME, Klijn JG, Wiemer EA, Stoter G, &, Nooter K, (2003) RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clin Cancer Res 9, 827-836.
34. Buchler M, Konig J, Brom M, Kartenbeck J, Spring H, Horie T, &, 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.
35. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, &, Oude Elferink RP, (1996) Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271, 1126-1128.
36. Taniguchi K, Wada M, Kohno K, Nakamura T, Kawabe T, Kawakami M, Kagotani K, Okumura K, Akiyama S, &, 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.
37. Fritz F, Chen J, Hayes P, &, Sirotnak FM, (2000) Molecular cloning of the murine cMOAT ATPase. Biochim Biophys Acta 1492, 531-536.
38. Conrad S, Viertelhaus A, Orzechowski A, Hoogstraate J, Gjellan K, Schrenk D, &, Kauffmann HM, (2001) Sequencing and tissue distribution of the canine MRP2 gene compared with MRP1 and MDR1. Toxicology 156, 81-91.
39. Nies AT, &, Keppler D, (2007) The apical conjugate efflux pump ABCC2 (MRP2). Pflugers Arch 453, 643-659.
40. Paulusma CC, Kool M, Bosma PJ, Scheffer GL, ter Borg F, Scheper RJ, Tytgat GN, Borst P, Baas F, &, Oude Elferink RP, (1997) A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome. Hepatology 25, 1539-1542.
41. Schaub TP, Kartenbeck J, Konig J, Vogel O, Witzgall R, Kriz W, &, Keppler D, (1997) Expression of the conjugate export pump encoded by the mrp2 gene in the apical membrane of kidney proximal tubules. J Am Soc Nephrol 8, 1213-1221.
42. Mottino AD, Hoffman T, Jennes L, Cao J, &, Vore M, (2001) Expression of multidrug resistance-associated protein 2 in small intestine from pregnant and postpartum rats. Am J Physiol Gastrointest Liver Physiol 280, G1261-G1273.
43. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJ, Juijn JA, Baas F, &, 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.
44. Rost D, Konig J, Weiss G, Klar E, Stremmel W, &, Keppler D, (2001) Expression and localization of the multidrug resistance proteins MRP2 and MRP3 in human gallbladder epithelia. Gastroenterology 121, 1203-1208.
45. St-Pierre MV, Serrano MA, Macias RI, Dubs U, Hoechli M, Lauper U, Meier PJ, &, Marin JJ, (2000) Expression of members of the multidrug resistance protein family in human term placenta. Am J Physiol Regul Integr Comp Physiol 279, R1495-R1503.
46. Konig J, Nies AT, Cui Y, Leier I, &, Keppler D, (1999) Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1461, 377-394.
47. Evers R, de Haas M, Sparidans R, Beijnen J, Wielinga PR, Lankelma J, &, Borst P, (2000) Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br J Cancer 83, 375-383.
48. 4 by the human canalicular multispecific organic anion transporter (cMOAT/MRP2). FEBS Lett 456, 327-331.
49. Chu XY, Strauss JR, Mariano MA, Li J, Newton DJ, Cai X, Wang RW, Yabut J, Hartley DP, Evans DC, et al. (2006) Characterization of mice lacking the multidrug resistance protein MRP2 (ABCC2). J Pharmacol Exp Ther 317, 579-589.
50. Ishizuka H, Konno K, Shiina T, Naganuma H, Nishimura K, Ito K, Suzuki H, &, Sugiyama Y, (1999) Species differences in the transport activity for organic anions across the bile canalicular membrane. J Pharmacol Exp Ther 290, 1324-1330.
51. Ninomiya M, Ito K, &, Horie T, (2005) Functional analysis of dog multidrug resistance-associated protein 2 (Mrp2) in comparison with rat Mrp2. Drug Metab Dispos 33, 225-232.
52. Xiong H, Turner KC, Ward ES, Jansen PL, &, Brouwer KL, (2000) Altered hepatobiliary disposition of acetaminophen glucuronide in isolated perfused livers from multidrug resistance-associated protein 2-deficient TR(-) rats. J Pharmacol Exp Ther 295, 512-518.
53. Tanaka H, Sano N, &, Takikawa H, (2003) Biliary excretion of phenolphthalein sulfate in rats. Pharmacology 68, 177-182.
54. Patel NJ, Zamek-Gliszczynski MJ, Zhang P, Han YH, Jansen PL, Meier PJ, Stieger B, &, Brouwer KL, (2003) Phenobarbital alters hepatic Mrp2 function by direct and indirect interactions. Mol Pharmacol 64, 154-159.
55. Zamek-Gliszczynski MJ, Hoffmaster KA, Humphreys JE, Tian X, Nezasa K, &, Brouwer KL, (2006) Differential involvement of Mrp2 (Abcc2) and Bcrp (Abcg2) in biliary excretion of 4-methylumbelliferyl glucuronide and sulfate in the rat. J Pharmacol Exp Ther 319, 459-467.
56. Kim HS, Min YD, &, Choi CH, (2001) Double-edged sword of chemosensitizer: increase of multidrug resistance protein (MRP) in leukemic cells by an MRP inhibitor probenecid. Biochem Biophys Res Commun 283, 64-71.
57. Chen ZS, Kawabe T, Ono M, Aoki S, Sumizawa T, Furukawa T, Uchiumi T, Wada M, Kuwano M, &, Akiyama SI, (1999) Effect of multidrug resistance-reversing agents on transporting activity of human canalicular multispecific organic anion transporter. Mol Pharmacol 56, 1219-1228.
58. Roy U, Chakravarty G, Honer Zu Bentrup K, &, Mondal D, (2009) Montelukast is a potent and durable inhibitor of multidrug resistance protein 2-mediated efflux of taxol and saquinavir. Biol Pharm Bull 32, 2002-2009.
59. Asakura E, Nakayama H, Sugie M, Zhao YL, Nadai M, Kitaichi K, Shimizu A, Miyoshi M, Takagi K, &, Hasegawa T, (2004) Azithromycin reverses anticancer drug resistance and modifies hepatobiliary excretion of doxorubicin in rats. Eur J Pharmacol 484, 333-339.
60. Payen L, Courtois A, Campion JP, Guillouzo A, &, Fardel O, (2000) Characterization and inhibition by a wide range of xenobiotics of organic anion excretion by primary human hepatocytes. Biochem Pharmacol 60, 1967-1975.
61. Kwatra D, Vadlapatla RK, Vadlapudi AD, Pal D, &, Mitra AK, (2010) Interaction of gatifloxacin with efflux transporters: a possible mechanism for drug resistance. Int J Pharm 395, 114-121.
62. Bandler PE, Westlake CJ, Grant CE, Cole SP, &, Deeley RG, (2008) Identification of regions required for apical membrane localization of human multidrug resistance protein 2. Mol Pharmacol 74, 9-19.
63. Kikuchi S, Hata M, Fukumoto K, Yamane Y, Matsui T, Tamura A, Yonemura S, Yamagishi H, Keppler D, &, Tsukita S, (2002) Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat Genet 31, 320-325.
64. Wang W, Soroka CJ, Mennone A, Rahner C, Harry K, Pypaert M, &, Boyer JL, (2006) Radixin is required to maintain apical canalicular membrane structure and function in rat hepatocytes. Gastroenterology 131, 878-884.
65. Ryu S, Kawabe T, Nada S, &, Yamaguchi A, (2000) Identification of basic residues involved in drug export function of human multidrug resistance-associated protein 2. J Biol Chem 275, 39617-39624.
66. Haimeur A, Conseil G, Deeley RG, &, Cole SP, (2004) Mutations of charged amino acids in or near the transmembrane helices of the second membrane spanning domain differentially affect the substrate specificity and transport activity of the multidrug resistance protein MRP1 (ABCC1). Mol Pharmacol 65, 1375-1385.
67. Ito K, Oleschuk CJ, Westlake C, Vasa MZ, Deeley RG, &, Cole SP, (2001) Mutation of Trp1254 in the multispecific organic anion transporter, multidrug resistance protein 2 (MRP2) (ABCC2), alters substrate specificity and results in loss of methotrexate transport activity. J Biol Chem 276, 38108-38114.
68. Zelcer N, Huisman MT, Reid G, Wielinga P, Breedveld P, Kuil A, Knipscheer P, Schellens JH, Schinkel AH, &, Borst P, (2003) Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). J Biol Chem 278, 23538-23544.
69. Narasaki F, Oka M, Nakano R, Ikeda K, Fukuda M, Nakamura T, Soda H, Nakagawa M, Kuwano M, &, Kohno S, (1997) Human canalicular multispecific organic anion transporter (cMOAT) is expressed in human lung, gastric, and colorectal cancer cells. Biochem Biophys Res Commun 240, 606-611.
70. Sandusky GE, Mintze KS, Pratt SE, &, Dantzig AH, (2002) Expression of multidrug resistance-associated protein 2 (MRP2) in normal human tissues and carcinomas using tissue microarrays. Histopathology 41, 65-74.
71. van der Kolk DM, de Vries EG, Koning JA, van den Berg E, Muller M, &, Vellenga E, (1998) Activity and expression of the multidrug resistance proteins MRP1 and MRP2 in acute myeloid leukemia cells, tumor cell lines, and normal hematopoietic CD34 + peripheral blood cells. Clin Cancer Res 4, 1727-1736.
72. Cui Y, Konig J, Buchholz JK, Spring H, Leier I, &, 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.
73. Chu XY, Kato Y, Niinuma K, Sudo KI, Hakusui H, &, Sugiyama Y, (1997) Multispecific organic anion transporter is responsible for the biliary excretion of the camptothecin derivative irinotecan and its metabolites in rats. J Pharmacol Exp Ther 281, 304-314.
74. Huisman MT, Chhatta AA, van Tellingen O, Beijnen JH, &, Schinkel AH, (2005) MRP2 (ABCC2) transports taxanes and confers paclitaxel resistance and both processes are stimulated by probenecid. Int J Cancer 116, 824-829.
75. Korita PV, Wakai T, Shirai Y, Matsuda Y, Sakata J, Takamura M, Yano M, Sanpei A, Aoyagi Y, Hatakeyama K, et al. (2010) Multidrug resistance-associated protein 2 determines the efficacy of cisplatin in patients with hepatocellular carcinoma. Oncol Rep 23, 965-972.
76. Dubin IN, &, Johnson FB, (1954) Chronic idiopathic jaundice with unidentified pigment in liver cells; a new clinicopathologic entity with a report of 12 cases. Medicine (Baltimore) 33, 155-197.
77. Kartenbeck J, Leuschner U, Mayer R, &, Keppler D, (1996) Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome. Hepatology 23, 1061-1066.
78. Wada M, Toh S, Taniguchi K, Nakamura T, Uchiumi T, Kohno K, Yoshida I, Kimura A, Sakisaka S, Adachi Y, et al. (1998) Mutations in the canilicular multispecific organic anion transporter (cMOAT) gene, a novel ABC transporter, in patients with hyperbilirubinemia II/Dubin-Johnson syndrome. Hum Mol Genet 7, 203-207.
79. Toh S, Wada M, Uchiumi T, Inokuchi A, Makino Y, Horie Y, Adachi Y, Sakisaka S, &, 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.
80. Lee JH, Chen HL, Ni YH, Hsu HY, &, Chang MH, (2006) Neonatal Dubin-Johnson syndrome: long-term follow-up and MRP2 mutations study. Pediatr Res 59, 584-589.
81. Kanda D, Takagi H, Kawahara Y, Yata Y, Takakusagi T, Hatanaka T, Yoshinaga T, Iesaki K, Kashiwabara K, Higuchi T, et al. (2009) Novel large-scale deletion (whole exon 7) in the ABCC2 gene in a patient with the Dubin-Johnson syndrome. Drug Metab Pharmacokinet 24, 464-468.
82. Jansen PL, Peters WH, &, Lamers WH, (1985) Hereditary chronic conjugated hyperbilirubinemia in mutant rats caused by defective hepatic anion transport. Hepatology 5, 573-579.
83. Hosokawa S, Tagaya O, Mikami T, Nozaki Y, Kawaguchi A, Yamatsu K, &, Shamoto M, (1992) A new rat mutant with chronic conjugated hyperbilirubinemia and renal glomerular lesions. Lab Anim Sci 42, 27-34.
84. Hirohashi T, Suzuki H, Ito K, Ogawa K, Kume K, Shimizu T, &, Sugiyama Y, (1998) Hepatic expression of multidrug resistance-associated protein-like proteins maintained in eisai hyperbilirubinemic rats. Mol Pharmacol 53, 1068-1075.
85. Kiuchi Y, Suzuki H, Hirohashi T, Tyson CA, &, Sugiyama Y, (1998) cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett 433, 149-152.
86. Belinsky MG, Bain LJ, Balsara BB, Testa JR, &, Kruh GD, (1998) Characterization of MOAT-C and MOAT-D, new members of the MRP/cMOAT subfamily of transporter proteins. J Natl Cancer Inst 90, 1735-1741.
87. Kool M, van der Linden M, de Haas M, Scheffer GL, de Vree JM, Smith AJ, Jansen G, Peters GJ, Ponne N, Scheper RJ, et al. (1999) MRP3, an organic anion transporter able to transport anti-cancer drugs. Proc Natl Acad Sci USA 96, 6914-6919.
88. Konig J, Rost D, Cui Y, &, Keppler D, (1999) Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology 29, 1156-1163.
89. Rost D, Mahner S, Sugiyama Y, &, Stremmel W, (2002) Expression and localization of the multidrug resistance-associated protein 3 in rat small and large intestine. Am J Physiol Gastrointest Liver Physiol 282, G720-G726.
90. Borst P, Zelcer N, &, van de Wetering K, (2006) MRP2 and 3 in health and disease. Cancer Lett 234, 51-61.
91. Scheffer GL, Kool M, de Haas M, de Vree JM, Pijnenborg AC, Bosman DK, Elferink RP, van der Valk P, Borst P, &, Scheper RJ, (2002) Tissue distribution and induction of human multidrug resistant protein 3. Lab Invest 82, 193-201.
92. Kubo K, Sekine S, &, Saito M, (2009) Compensatory expression of MRP3 in the livers of MRP2-deficient EHBRs is promoted by DHA intake. Biosci Biotechnol Biochem 73, 2432-2438.
93. Soroka CJ, Lee JM, Azzaroli F, &, Boyer JL, (2001) Cellular localization and up-regulation of multidrug resistance-associated protein 3 in hepatocytes and cholangiocytes during obstructive cholestasis in rat liver. Hepatology 33, 783-791.
94. Belinsky MG, Dawson PA, Shchaveleva I, Bain LJ, Wang R, Ling V, Chen ZS, Grinberg A, Westphal H, Klein-Szanto A, et al. (2005) Analysis of the in vivo functions of Mrp3. Mol Pharmacol 68, 160-168.
95. Zelcer N, van de Wetering K, de Waart R, Scheffer GL, Marschall HU, Wielinga PR, Kuil A, Kunne C, Smith A, van der Valk M, et al. (2006) Mice lacking Mrp3 (Abcc3) have normal bile salt transport, but altered hepatic transport of endogenous glucuronides. J Hepatol 44, 768-775.
96. Zelcer N, van de Wetering K, Hillebrand M, Sarton E, Kuil A, Wielinga PR, Tephly T, Dahan A, Beijnen JH, &, Borst P, (2005) Mice lacking multidrug resistance protein 3 show altered morphine pharmacokinetics and morphine-6-glucuronide antinociception. Proc Natl Acad Sci USA 102, 7274-7279.
97. Steinbach D, Lengemann J, Voigt A, Hermann J, Zintl F, &, Sauerbrey A, (2003) Response to chemotherapy and expression of the genes encoding the multidrug resistance-associated proteins MRP2, MRP3, MRP4, MRP5, and SMRP in childhood acute myeloid leukemia. Clin Cancer Res 9, 1083-1086.
98. Borst P, de Wolf C, &, van de Wetering K, (2007) Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 453, 661-673.
99. Zelcer N, Saeki T, Reid G, Beijnen JH, &, Borst P, (2001) Characterization of drug transport by the human multidrug resistance protein 3 (ABCC3). J Biol Chem 276, 46400-46407.
100. Hirohashi T, Suzuki H, &, Sugiyama Y, (1999) Characterization of the transport properties of cloned rat multidrug resistance-associated protein 3 (MRP3). J Biol Chem 274, 15181-15185.
101. Lagas JS, Fan L, Wagenaar E, Vlaming ML, van Tellingen O, Beijnen JH, &, Schinkel AH, (2010) P-glycoprotein (P-gp/Abcb1), Abcc2, and Abcc3 determine the pharmacokinetics of etoposide. Clin Cancer Res 16, 130-140.
102. Nies AT, Konig J, Pfannschmidt M, Klar E, Hofmann WJ, &, Keppler D, (2001) Expression of the multidrug resistance proteins MRP2 and MRP3 in human hepatocellular carcinoma. Int J Cancer 94, 492-499.
103. Ohishi Y, Oda Y, Uchiumi T, Kobayashi H, Hirakawa T, Miyamoto S, Kinukawa N, Nakano H, Kuwano M, &, Tsuneyoshi M, (2002) ATP-binding cassette superfamily transporter gene expression in human primary ovarian carcinoma. Clin Cancer Res 8, 3767-3775.
104. Plasschaert SL, de Bont ES, Boezen M, vander Kolk DM, Daenen SM, Faber KN, Kamps WA, de Vries EG, &, Vellenga E, (2005) Expression of multidrug resistance-associated proteins predicts prognosis in childhood and adult acute lymphoblastic leukemia. Clin Cancer Res 11, 8661-8668.
105. Benderra Z, Faussat AM, Sayada L, Perrot JY, Tang R, Chaoui D, Morjani H, Marzac C, Marie JP, &, Legrand O, (2005) MRP3, BCRP, and P-glycoprotein activities are prognostic factors in adult acute myeloid leukemia. Clin Cancer Res 11, 7764-7772.
106. Schuetz JD, Connelly MC, Sun D, Paibir SG, Flynn PM, Srinivas RV, Kumar A, &, Fridland A, (1999) MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat Med 5, 1048-1051.
107. Russel FG, Koenderink JB, &, Masereeuw R, (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29, 200-207.
108. Nies AT, Jedlitschky G, Konig J, Herold-Mende C, Steiner HH, Schmitt HP, &, Keppler D, (2004) Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129, 349-360.
109. + exchanger regulatory factor 1 increases expression and function of multidrug resistance protein 4. Cancer Res 68, 4802-4809.
110. Hoque MT, Conseil G, &, Cole SP, (2009) Involvement of NHERF1 in apical membrane localization of MRP4 in polarized kidney cells. Biochem Biophys Res Commun 379, 60-64.
111. Kruh GD, Belinsky MG, Gallo JM, &, Lee K, (2007) Physiological and pharmacological functions of Mrp2, Mrp3 and Mrp4 as determined from recent studies on gene-disrupted mice. Cancer Metastasis Rev 26, 5-14.
112. Fletcher JI, Haber M, Henderson MJ, &, Norris MD, (2010) ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 10, 147-156.
113. Ho LL, Kench JG, Handelsman DJ, Scheffer GL, Stricker PD, Grygiel JG, Sutherland RL, Henshall SM, Allen JD, &, Horvath LG, (2008) Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer. Prostate 68, 1421-1429.
114. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, Du G, Mercer KE, Zhuang Y, Panetta JC, Johnston B, et al. (2004) Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24, 7612-7621.
115. Hasegawa M, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, &, Sugiyama Y, (2007) Multidrug resistance-associated protein 4 is involved in the urinary excretion of hydrochlorothiazide and furosemide. J Am Soc Nephrol 18, 37-45.
116. Ci L, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, &, Sugiyama Y, (2007) Involvement of MRP4 (ABCC4) in the luminal efflux of ceftizoxime and cefazolin in the kidney. Mol Pharmacol 71, 1591-1597.
117. El-Sheikh AA, Masereeuw R, &, Russel FG, (2008) Mechanisms of renal anionic drug transport. Eur J Pharmacol 585, 245-255.
118. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, &, Borst P, (2003) Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63, 1094-1103.
119. Reid G, Wielinga P, Zelcer N, van der Heijden I, Kuil A, de Haas M, Wijnholds J, &, 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.
120. Krishnamurthy P, Schwab M, Takenaka K, Nachagari D, Morgan J, Leslie M, Du W, Boyd K, Cheok M, Nakauchi H, et al. (2008) Transporter-mediated protection against thiopurine-induced hematopoietic toxicity. Cancer Res 68, 4983-4989.
121. van Aubel RA, Smeets PH, Peters JG, Bindels RJ, &, Russel FG, (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.
122. Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, Jalink K, Li M, Nelson DJ, Schuetz JD, et al. (2007) Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131, 940-951.
123. Rius M, Thon WF, Keppler D, &, Nies AT, (2005) Prostanoid transport by multidrug resistance protein 4 (MRP4/ABCC4) localized in tissues of the human urogenital tract. J Urol 174, 2409-2414.
124. Hanaka H, Pawelzik SC, Johnsen JI, Rakonjac M, Terawaki K, Rasmuson A, Sveinbjornsson B, Schumacher MC, Hamberg M, Samuelsson B, et al. (2009) Microsomal prostaglandin E synthase 1 determines tumor growth in vivo of prostate and lung cancer cells. Proc Natl Acad Sci USA 106, 18757-18762.
125. Rius M, Hummel-Eisenbeiss J, &, Keppler D, (2008) ATP-dependent transport of leukotrienes B4 and C4 by the multidrug resistance protein ABCC4 (MRP4). J Pharmacol Exp Ther 324, 86-94.
126. Jedlitschky G, Cattaneo M, Lubenow LE, Rosskopf D, Lecchi A, Artoni A, Motta G, Niessen J, Kroemer HK, &, Greinacher A, (2010) Role of MRP4 (ABCC4) in platelet adenine nucleotide-storage: evidence from patients with delta-storage pool deficiencies. Am J Pathol 176, 1097-1103.
127. Chen ZS, Lee K, Walther S, Raftogianis RB, Kuwano M, Zeng H, &, Kruh GD, (2002) Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res 62, 3144-3150.
128. Wielinga PR, Reid G, Challa EE, van der Heijden I, van Deemter L, de Haas M, Mol C, Kuil AJ, Groeneveld E, Schuetz JD, et al. (2002) Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharmacol 62, 1321-1331.
129. Wijnholds J, Mol CA, van Deemter L, de Haas M, Scheffer GL, Baas F, Beijnen JH, Scheper RJ, Hatse S, De Clercq E, et al. (2000) Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc Natl Acad Sci USA 97, 7476-7481.
130. McAleer MA, Breen MA, White NL, &, Matthews N, (1999) pABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J Biol Chem 274, 23541-23548.
131. Dazert P, Meissner K, Vogelgesang S, Heydrich B, Eckel L, Bohm M, Warzok R, Kerb R, Brinkmann U, Schaeffeler E, et al. (2003) Expression and localization of the multidrug resistance protein 5 (MRP5/ABCC5), a cellular export pump for cyclic nucleotides, in human heart. Am J Pathol 163, 1567-1577.
132. Calatozzolo C, Gelati M, Ciusani E, Sciacca FL, Pollo B, Cajola L, Marras C, Silvani A, Vitellaro-Zuccarello L, Croci D, et al. (2005) Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5 and GST-pi in human glioma. J Neurooncol 74, 113-121.
133. Karla PK, Quinn TL, Herndon BL, Thomas P, Pal D, &, Mitra A, (2009) Expression of multidrug resistance associated protein 5 (MRP5) on cornea and its role in drug efflux. J Ocul Pharmacol Ther 25, 121-132.
134. Nies AT, Spring H, Thon WF, Keppler D, &, Jedlitschky G, (2002) Immunolocalization of multidrug resistance protein 5 in the human genitourinary system. J Urol 167, 2271-2275.
135. Meyer Zu Schwabedissen HE, Grube M, Heydrich B, Linnemann K, Fusch C, Kroemer HK, &, Jedlitschky G, (2005) Expression, localization, and function of MRP5 (ABCC5), a transporter for cyclic nucleotides, in human placenta and cultured human trophoblasts: effects of gestational age and cellular differentiation. Am J Pathol 166, 39-48.
136. Jedlitschky G, Burchell B, &, Keppler D, (2000) The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J Biol Chem 275, 30069-30074.
137. Wu CP, Woodcock H, Hladky SB, &, Barrand MA, (2005) cGMP (guanosine 3â,5â-cyclic monophosphate) transport across human erythrocyte membranes. Biochem Pharmacol 69, 1257-1262.
138. Chen ZS, Guo Y, Belinsky MG, Kotova E, &, Kruh GD, (2005) Transport of bile acids, sulfated steroids, estradiol 17-beta-d-glucuronide, and leukotriene C4 by human multidrug resistance protein 8 (ABCC11). Mol Pharmacol 67, 545-557.
139. Andric SA, Kostic TS, &, Stojilkovic SS, (2006) Contribution of multidrug resistance protein MRP5 in control of cyclic guanosine 5â-monophosphate intracellular signaling in anterior pituitary cells. Endocrinology 147, 3435-3445.
140. Boadu E, &, Sager G, (2004) Reconstitution of ATP-dependent cGMP transport into proteoliposomes by membrane proteins from human erythrocytes. Scand J Clin Lab Invest 64, 41-48.
141. Xu HL, Gavrilyuk V, Wolde HM, Baughman VL, &, Pelligrino DA, (2004) Regulation of rat pial arteriolar smooth muscle relaxation in vivo through multidrug resistance protein 5-mediated cGMP efflux. Am J Physiol Heart Circ Physiol 286, H2020-H2027.
142. Oguri T, Isobe T, Suzuki T, Nishio K, Fujiwara Y, Katoh O, &, Yamakido M, (2000) Increased expression of the MRP5 gene is associated with
143. Hagmann W, Jesnowski R, Faissner R, Guo C, &, Lohr JM, (2009) ATP-binding cassette C transporters in human pancreatic carcinoma cell lines. Upregulation in 5-fluorouracil-resistant cells. Pancreatology 9, 136-144.
144. Yoshida M, Suzuki T, Komiya T, Hatashita E, Nishio K, Kazuhiko N, &, Fukuoka M, (2001) Induction of MRP5 and SMRP mRNA by adriamycin exposure and its overexpression in human lung cancer cells resistant to adriamycin. Int J Cancer 94, 432-437.
145. Pratt S, Shepard RL, Kandasamy RA, Johnston PA, Perry W III, &, Dantzig AH, (2005) The multidrug resistance protein 5 (ABCC5) confers resistance to 5-fluorouracil and transports its monophosphorylated metabolites. Mol Cancer Ther 4, 855-863.
146. Wielinga P, Hooijberg JH, Gunnarsdottir S, Kathmann I, Reid G, Zelcer N, van der Born K, de Haas M, van der Heijden I, Kaspers G, et al. (2005) The human multidrug resistance protein MRP5 transports folates and can mediate cellular resistance against antifolates. Cancer Res 65, 4425-4430.
147. Longhurst TJ, O'Neill GM, Harvie RM, &, Davey RA, (1996) The anthracycline resistance-associated (ara) gene, a novel gene associated with multidrug resistance in a human leukaemia cell line. Br J Cancer 74, 1331-1335.
148. Kool M, van der Linden M, de Haas M, Baas F, &, Borst P, (1999) Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 59, 175-182.
149. Scheffer GL, Hu X, Pijnenborg AC, Wijnholds J, Bergen AA, &, Scheper RJ, (2002) MRP6 (ABCC6) detection in normal human tissues and tumors. Lab Invest 82, 515-518.
150. Boraldi F, Quaglino D, Croce MA, Garcia Fernandez MI, Tiozzo R, Gheduzzi D, Bacchelli B, &, Pasquali Ronchetti I, (2003) Multidrug resistance protein-6 (MRP6) in human dermal fibroblasts. Comparison between cells from normal subjects and from Pseudoxanthoma elasticum patients. Matrix Biol 22, 491-500.
151. Belinsky MG, Chen ZS, Shchaveleva I, Zeng H, &, Kruh GD, (2002) Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 62, 6172-6177.
152. Ilias A, Urban Z, Seidl TL, Le Saux O, Sinko E, Boyd CD, Sarkadi B, &, Varadi A, (2002) Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 277, 16860-16867.
153. Bergen AA, Plomp AS, Schuurman EJ, Terry S, Breuning M, Dauwerse H, Swart J, Kool M, van Soest S, Baas F, et al. (2000) Mutations in ABCC6 cause pseudoxanthoma elasticum. Nat Genet 25, 228-231.
154. Le Saux O, Urban Z, Tschuch C, Csiszar K, Bacchelli B, Quaglino D, Pasquali-Ronchetti I, Pope FM, Richards A, Terry S, et al. (2000) Mutations in a gene encoding an ABC transporter cause pseudoxanthoma elasticum. Nat Genet 25, 223-227.
155. Ringpfeil F, Lebwohl MG, Christiano AM, &, Uitto J, (2000) Pseudoxanthoma elasticum: mutations in the MRP6 gene encoding a transmembrane ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 97, 6001-6006.
156. Struk B, Cai L, Zach S, Ji W, Chung J, Lumsden A, Stumm M, Huber M, Schaen L, Kim CA, et al. (2000) Mutations of the gene encoding the transmembrane transporter protein ABC-C6 cause pseudoxanthoma elasticum. J Mol Med 78, 282-286.
157. Li Q, Jiang Q, Pfendner E, Varadi A, &, Uitto J, (2009) Pseudoxanthoma elasticum: clinical phenotypes, molecular genetics and putative pathomechanisms. Exp Dermatol 18, 1-11.
158. Gheduzzi D, Sammarco R, Quaglino D, Bercovitch L, Terry S, Taylor W, &, Ronchetti IP, (2003) Extracutaneous ultrastructural alterations in pseudoxanthoma elasticum. Ultrastruct Pathol 27, 375-384.
159. Gorgels TG, Hu X, Scheffer GL, van der Wal AC, Toonstra J, de Jong PT, van Kuppevelt TH, Levelt CN, de Wolf A, Loves WJ, et al. (2005) Disruption of Abcc6 in the mouse: novel insight in the pathogenesis of pseudoxanthoma elasticum. Hum Mol Genet 14, 1763-1773.
160. Klement JF, Matsuzaki Y, Jiang QJ, Terlizzi J, Choi HY, Fujimoto N, Li K, Pulkkinen L, Birk DE, Sundberg JP, et al. (2005) Targeted ablation of the abcc6 gene results in ectopic mineralization of connective tissues. Mol Cell Biol 25, 8299-8310.
161. Jiang Q, &, Uitto J, (2006) Pseudoxanthoma elasticum: a metabolic disease? J Invest Dermatol 126, 1440-1441.
162. Uitto J, Pulkkinen L, &, Ringpfeil F, (2001) Molecular genetics of pseudoxanthoma elasticum: a metabolic disorder at the environment-genome interface? Trends Mol Med 7, 13-17.
163. Jahnen-Dechent W, Schinke T, Trindl A, Muller-Esterl W, Sablitzky F, Kaiser S, &, Blessing M, (1997) Cloning and targeted deletion of the mouse fetuin gene. J Biol Chem 272, 31496-31503.
164. Liaw L, Birk DE, Ballas CB, Whitsitt JS, Davidson JM, &, Hogan BL, (1998) Altered wound healing in mice lacking a functional osteopontin gene (spp1). J Clin Invest 101, 1468-1478.
165. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR, &, Karsenty G, (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386, 78-81.
166. Borst P, van de Wetering K, &, Schlingemann R, (2008) Does the absence of ABCC6 (multidrug resistance protein 6) in patients with Pseudoxanthoma elasticum prevent the liver from providing sufficient vitamin K to the periphery? Cell Cycle 7, 1575-1579.
167. Hu X, Plomp A, Wijnholds J, Ten Brink J, van Soest S, van den Born LI, Leys A, Peek R, de Jong PT, &, Bergen AA, (2003) ABCC6/MRP6 mutations: further insight into the molecular pathology of pseudoxanthoma elasticum. Eur J Hum Genet 11, 215-224.
168. Le Saux O, Beck K, Sachsinger C, Silvestri C, Treiber C, Goring HH, Johnson EW, De Paepe A, Pope FM, Pasquali-Ronchetti I, et al. (2001) A spectrum of ABCC6 mutations is responsible for pseudoxanthoma elasticum. Am J Hum Genet 69, 749-764.
169. Hopper E, Belinsky MG, Zeng H, Tosolini A, Testa JR, &, Kruh GD, (2001) Analysis of the structure and expression pattern of MRP7 (ABCC10), a new member of the MRP subfamily. Cancer Lett 162, 181-191.
170. Kao HH, Chang MS, Cheng JF, &, Huang JD, (2003) Genomic structure, gene expression, and promoter analysis of human multidrug resistance-associated protein 7. J Biomed Sci 10, 98-110.
171. Kruh GD, Guo Y, Hopper-Borge E, Belinsky MG, &, Chen ZS, (2007) ABCC10, ABCC11, and ABCC12. Pflugers Arch 453, 675-684.
172. Chen ZS, Hopper-Borge E, Belinsky MG, Shchaveleva I, Kotova E, &, Kruh GD, (2003) Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 63, 351-358.
173. Hopper-Borge E, Chen ZS, Shchaveleva I, Belinsky MG, &, Kruh GD, (2004) Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 64, 4927-4930.
174. Hopper-Borge E, Xu X, Shen T, Shi Z, Chen ZS, &, Kruh GD, (2009) Human multidrug resistance protein 7 (ABCC10) is a resistance factor for nucleoside analogues and epothilone B. Cancer Res 69, 178-184.
175. Naramoto H, Uematsu T, Uchihashi T, Doto R, Matsuura T, Usui Y, Uematsu S, Li X, Takahashi M, Yamaoka M, et al. (2007) Multidrug resistance-associated protein 7 expression is involved in cross-resistance to docetaxel in salivary gland adenocarcinoma cell lines. Int J Oncol 30, 393-401.
176. Oguri T, Ozasa H, Uemura T, Bessho Y, Miyazaki M, Maeno K, Maeda H, Sato S, &, Ueda R, (2008) MRP7/ABCC10 expression is a predictive biomarker for the resistance to paclitaxel in non-small cell lung cancer. Mol Cancer Ther 7, 1150-1155.
177. Bessho Y, Oguri T, Ozasa H, Uemura T, Sakamoto H, Miyazaki M, Maeno K, Sato S, &, Ueda R, (2009) ABCC10/MRP7 is associated with vinorelbine resistance in non-small cell lung cancer. Oncol Rep 21, 263-268.
178. Bera TK, Lee S, Salvatore G, Lee B, &, 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.
179. Yabuuchi H, Shimizu H, Takayanagi S, &, Ishikawa T, (2001) Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem Biophys Res Commun 288, 933-939.
180. Tammur J, Prades C, Arnould I, Rzhetsky A, Hutchinson A, Adachi M, Schuetz JD, Swoboda KJ, Ptacek LJ, Rosier M, et al. (2001) Two new genes from the human ATP-binding cassette transporter superfamily, ABCC11 and ABCC12, tandemly duplicated on chromosome 16q12. Gene 273, 89-96.
181. Bortfeld M, Rius M, Konig J, Herold-Mende C, Nies AT, &, Keppler D, (2006) Human multidrug resistance protein 8 (MRP8/ABCC11), an apical efflux pump for steroid sulfates, is an axonal protein of the CNS and peripheral nervous system. Neuroscience 137, 1247-1257.
182. Guo Y, Kotova E, Chen ZS, Lee K, Hopper-Borge E, Belinsky MG, &, Kruh GD, (2003) MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2â,3â- dideoxycytidine and 9â-(2â-phosphonylmethoxyethyl)adenine. J Biol Chem 278, 29509-29514.
183. Guo Y, Kock K, Ritter CA, Chen ZS, Grube M, Jedlitschky G, Illmer T, Ayres M, Beck JF, Siegmund W, et al. (2009) Expression of ABCC-type nucleotide exporters in blasts of adult acute myeloid leukemia: relation to long-term survival. Clin Cancer Res 15, 1762-1769.
184. 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.
185. Toyoda Y, Sakurai A, Mitani Y, Nakashima M, Yoshiura K, Nakagawa H, Sakai Y, Ota I, Lezhava A, Hayashizaki Y, et al. (2009) Earwax, osmidrosis, and breast cancer: why does one SNP (538G > A) in the human ABC transporter ABCC11 gene determine earwax type? FASEB J 23, 2001-2013.
186. Petrakis NL, (1971) Cerumen genetics and human breast cancer. Science 173, 347-349.
187. Yoo WM, Pae NS, Lee SJ, Roh TS, Chung S, &, Tark KC, (2006) Endoscopy-assisted ultrasonic surgical aspiration of axillary osmidrosis: a retrospective review of 896 consecutive patients from 1998 to 2004. J Plast Reconstr Aesthet Surg 59, 978-982.
188. Miura K, Yoshiura K, Miura S, Shimada T, Yamasaki K, Yoshida A, Nakayama D, Shibata Y, Niikawa N, &, Masuzaki H, (2007) A strong association between human earwax-type and apocrine colostrum secretion from the mammary gland. Hum Genet 121, 631-633.
189. Bera TK, Iavarone C, Kumar V, Lee S, Lee B, &, 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.
190. Shimizu H, Taniguchi H, Hippo Y, Hayashizaki Y, Aburatani H, &, Ishikawa T, (2003) Characterization of the mouse Abcc12 gene and its transcript encoding an ATP-binding cassette transporter, an orthologue of human ABCC12. Gene 310, 17-28.
191. Maher JM, Slitt AL, Cherrington NJ, Cheng X, &, Klaassen CD, (2005) Tissue distribution and hepatic and renal ontogeny of the multidrug resistance-associated protein (Mrp) family in mice. Drug Metab Dispos 33, 947-955.
192. Augustine LM, Markelewicz RJ Jr, Boekelheide K, &, Cherrington NJ, (2005) Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab Dispos 33, 182-189.
193. Ono N, Van der Heijden I, Scheffer GL, Van de Wetering K, Van Deemter E, De Haas M, Boerke A, Gadella BM, De Rooij DG, Neefjes JJ, et al. (2007) Multidrug resistance-associated protein 9 (ABCC12) is present in mouse and boar sperm. Biochem J 406, 31-40.