Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells

Cancer Research

Volumn 59, Issue 1, 1999, Pages 175-182

  Kool, Marcel ^a   Van Der Linden, Marcel ^a   De Haas, Marcel ^a   Baas, Frank ^b   Borst, Piet ^a,c  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c Division of Tumor Biology   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; DNA SEQUENCE; GENE AMPLIFICATION; GENE EXPRESSION; GENE LOCATION; HUMAN; HUMAN CELL; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE; DRUG RESISTANCE, MULTIPLE; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; ORGAN SPECIFICITY; SEQUENCE ALIGNMENT;

EID: 0032893268     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Gottesman, M. M., and Pastan, I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem., 62: 385-427, 1993.
2. Loe, D. W., Deeley, R. G., and Cole, S. P. C. Biology of the multidrug resistance-associated protein, MRP. Eur. J. Cancer. 32A: 945-957, 1996.
3. 4 and structurally related conjugates. J. Biol. Chem., 269: 27807-27810, 1994.
4. Jedlitschky, G., Leier, I., Buchholz, U., Barnouin, K., Kurz, G., and Keppler, D. Transport of glutathione, glucuronate, and sulfate conjugate by the MRP gene-encoded conjugate export pump. Cancer Res., 56: 988-994, 1996.
5. Loe, D. W., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. ATP-dependent 17 β-estradiol 17-(β-D-glucuronide) transport by multidrug resistance protein (MRP). J. Biol. Chem., 271: 9683-9689, 1996.
6. 4 and chemotherapeutic agents in membrane vesicles. J. Biol. Chem., 271: 675-9682, 1996.
7. Zaman, G. J. R., Cnubben, N. H. P., van Bladeren, P. J., Evers, R., and Borst, P. Transport of the glutathione conjugate of ethacrynic acid by the human multidrug resistance protein MRP. FEBS Lett., 391: 126-130, 1996.
8. Cole, S. P. C., Sparks, K. E., Fraser, K., Loe, D. W., Grant, C. E., Wilson, G. M., and Deeley, R. G. Pharmacological characterization of multidrug resistant MRP-transfecled human tumor cells. Cancer Res., 54: 5902-5910, 1994.
9. Zaman, G. J. R., Flens, M. J., van Leusden, M. R., de Haas, M., Mulder, H. S., Lankelma, J., Pinedo, H. M., Scheper, R. J., Baas, F., Broxterman, H. J., and Borst, P. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl Acad. Sci., USA, 91: 8822-8826, 1994.
10. Taniguchi, K., Wada, M., Kohno, K., Nakamura, T., Kawabe, T., Kawakami, M., Kagotani, K., Okumura, K., Akiyama, S-i., and Kuwano, M. 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, 1996.
11. Kool, M., de Haas, M., Scheffer, G. L., Scheper, R. J., Van Eijk, M. J. T., Juijn, J. A., Baas, F., and Borst, P. 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, 1997.
12. Koike, K., Kawabe, T., Tanaka, T., Toh, S., Uchiumi, T., Wada, M., Akiyama, S., Ono, M., and Kuwano, M. A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res., 57: 5475-5479, 1997.
13. Evers, R., Kool, M., van Deemter, L., Janssen, H., Calafat, J., Oomen, L. C. J. M., Paulusma, C. C., Oude Elferink, R. P. J., Baas, F., Schinkel, A. H., and Borst, P. Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J. Clin. Invest., 101: 1310-1319, 1998.
14. Klughauer, N., and Hofmann, F. Primary structure of a novel ABC transporter with a chromosomal localization on the band encoding the multidrug resistance-associated protein. FEBS Lett., 391: 61-65, 1996.
15. Izquierdo, M. A., Neefjes, J. J., Mathari, A. E. L., Flens, M. J., Scheffer, G. L., and Scheper, R. J. Overexpression of the ABC transporter TAP in multidrug resistant human cancer cell lines. Br. J. Cancer, 74: 1961-1967, 1996.
16. O'Neill, G. M., Peters, G. B., Harvie, R. M., MacKenzie, H. B., Henness, S., and Davey, R. A. Amplification and expression of the ABC transporters ARA and MRP in a series of multidrug-resistant leukaemia sublines. Br. J. Cancer, 77: 2076-2080, 1998.
17. Longhurst, T. J., O'Neill, G. M., Harvie, R. M., and Davey, R. A. 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, 1996.
18. Laing, N. M., Belinsky, M. G., Kruh, G. D., Bell, D. W., Boyd, J. T., Barone, L., Testa, J. R., and Tew, K. D. Amplification of the ATP-binding cassette 2 transporter gene is functionally linked with enhanced efflux of estramustine in ovarian carcinoma cells. Cancer Res., 58: 1332-1337, 1998.
19. Oude Elferink, R. P. J., Meijer, D. K. F., Kuipers, F., Jansen, P. L. M., Groen, A. K., and Groothuis, G. M. M. Hepatobiliary secretion of organic compounds: molecular mechanisms of membrane transport. Biochim. Biophys. Acta. 1241: 215-268, 1995.
20. Keppler, D., Leier, I., and Jedlitschky, G. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol. Chem., 378: 787-791, 1997.
21. Masuda, M., I'izuka, Y., Yamazaki, M., Nishigaki, R., Kato, Y., Ni'inuma, K., Suzuki, H., and Sugiyama, Y. Methotrexate is excreted into the bile by canalicular multispecific organic anion transporter in rats. Cancer Res., 57: 3506-3510, 1997.
22. Chu, X. Y., Kato, Y., and Sugiyama, Y. Multiplicity of biliary excretion mechanism for irinotecan, CPT-11, and its metabolites in rats. Cancer Res., 57: 1934-1938, 1997.
23. Lennon, G. G., Auffray, C., Polymeropoulos, M., and Soares, M. B. The I. M. A. G. E. consortium: an integrated molecular analysis of genomes and their expression. Genomics, 33: 151-152, 1996.
24. Devereux, J., Haeberli, P., and Smithies, O. A. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res., 12: 387-395, 1984.
25. Sambrook, J., Fritch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual. Cold spring Harbor, NY: Cold Spring Harbor Laboratory, 1989.
26. Chomczynski, P., and Sacchi, N. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987.
27. Zaman, G. J. R., Versantvoort, C. H. M., Smit, J. J. M., Eijdems, E. W. H. M., de Haas, M., Smith, A. J., Broxterman, H. J., Mulder, N. H., de Vries, E. G. E., Baas, F., and Borst, P. Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res., 53: 1747-1750, 1993.
28. Zinn, K., Dimiao, D., and Maniatis, T. Identification of twodistinct regulatory regions adjacent to the human β-interferon gene. Cell, 34: 865-879, 1983.
29. Baas, F., Jongsma, A. P. M., Broxterman, H. J., Arceci, R. J., Housman, D., Scheffer, G. L., Riethorst, A., van Groenigen, M., Nieuwint, A. W. M., and Joenje, H. Non-P-glycoprotein mediated mechanism for multidrug resistance precedes P-glycoprotein expression during in vitro selection for doxorubicin resistance in a human lung cancer cell line. Cancer Res., 50: 5392-5398, 1990.
30. Enoch, T., Zinn, K., and Maniatis, T. Activation of the human β-interferon gene requires an interferon inducible factor. Mol. Cell. Biol., 6: 801-810, 1986.
31. Miller, S. A., Dykes, D. D., and Polesky, H. F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res., 16: 1215, 1988.
32. Cole, S. P. C., Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C., Stewart, A. J., Kurz, E. U., Duncan, A. M. V., and Deeley, R. G. Overexpression of a transporter gene in a multidrug resistant human lung cancer cell line. Science (Washington DC), 258: 1650-1654, 1992.
33. Paulusma, C. C.. Kool, M., Bosma, P. J., Scheffer, G. L., ter Borg, F., Scheper, R. J., Tytgat, G. N. J., Borst, P., Baas, F., and Oude Elferink, R. P. J. A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome. Hepatology, 25: 1539-1542, 1997.
34. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res., 54: 357-361, 1994.
35. Hirohashi, T., Suzuki, H., Ito, K., Ogawa, K., Kume, K., Shimizu, T., and Sugiyama, Y. Hepatic expression of multidrug resistance-associated protein-like proteins maintained in Eisai hyperbilirubinemic rats. Mol. Pharmacol., 53: 1068-1075, 1998.
36. Hipfner, D. R., Almquist, K. C., Leslie, E. M., Gerlach, J. H., Grant, C. E., Deeley, R. G., and Cole, S. P. C. Membrane topology of the multidrug resistance protein (MRP). J. Biol. Chem., 272: 23623-23630, 1997.
37. Kast, C., and Gros, P. Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immunofluorescence. Science (Washington DC), 272: 26479-26487, 1997.
38. Kast, C., and Gros, P. Epitope insertion favors a six transmembrane domain model for the carboxy-terminal portion of the multidrug resistance-associated protein. Biochemistry, 37: 2305-2313, 1998.
39. Davey, R. A., Longhurst, T. J., Davey, M. W., Belov, L., Harvie, R. M., Hancox, D., and Wheeler, H. Drug resistance mechanisms and MRP expression in response to epirubicin treatment in a human leukaemia cell line. Leuk. Res., 19: 275-282, 1995.
40. Boguski, M. S., Lowe, T. M., and Tolstoshev, C. M. dbEST-database for "expressed sequence tags." Nat. Genet., 4: 332-333, 1993.
41. Barrand, M. A., Heppel-Parton, A. C., Wright, K. A., Rabbitts, P. H., and Twentyman, P. R. A 190-kilodalton protein overexpressed in non-P-glycoprotein-containing multidrug-resistant cells and its relationship to the MRP gene. J. Natl Cancer Inst., 86: 110-117, 1994.
42. Eijdems, E. W. H. M., de Haas, M., Coco-Martin, J. M., Ottenheim, C. P., Zaman, G. J. R., Dauwerse, H. G., Breuning, M. H., Twentyman, P. R., Borst, P., and Baas, F. Mechanisms of MRP overexpression in four human lung cancer cell lines and analysis of the MRP amplicon. Int. J. Cancer, 60: 676-684, 1995.
43. Krishnamachary, N., Ma, L., Zheng, L., Safa, A. R., and Center, M. S. Analysis of MRP expression and function in HL60 cells isolated for resistance to Adriamycin. Oncol. Res., 6: 119-127, 1994.
44. Decottignies, A., and Goffeau, A. Complete inventory of the yeast ABC proteins. Nat. Genet., 15: 137-144, 1997.
45. Broeks, A., Gerrard, B., Allikmets, R., Dean, M., and Plasterk, R. H. A. Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J., 15: 6132-6143, 1996.
46. Tommasini, R., Vogt, E., Schmid, J., Fromentau, M., Amrhein, N., and Martinoia, E. Differential expression of genes coding for ABC transporters after treatment of Arabidopsis thaliana with xenobiotics. FEBS Lett., 411: 206-210, 1997.
47. Lu, Y. P., Li, Z. S., Drozdowicz, Y. M., Hortensteiner, S., and Martinoia, E. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell, 10: 267-282, 1998.
48. Lu, Y. P., Li, Z. S., and Rea, P. A. AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc. Natl Acad. Sci. USA, 94; 8243-8248, 1997.
49. Tommasini, R., Evers, R., Vogt, E., Mornet, C., Zaman, G. J. R., Schinkel, A. H., Borst, P., and Martinoia, E. The human multidrug resistance-associated protein functionally complements the yeast cadmium resistance factor 1. Proc. Natl Acad. Sci. USA, 93: 6743-6748, 1996.
50. Muller, M., Meijer, C., Zaman, G. J. R., Borst, P., Scheper, R. J., Mulder, N. H., de Vries, E. G. E., and Jansen, P. L. M. Overexpression of the gene encoding the multidrug resistance associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc. Natl Acad. Sci. USA, 91: 13033-13037, 1994.
51. Li, Z. S., Szcypka, M. S., Lu, Y. P., Thiele, D. J., and Rea, P. A. The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem., 271: 6509-6517, 1996.
52. Cui, Z., Hirata, D., Tsuchiya, E., Osada, H., and Miyakawa, T. The multidrug resistance-associated protein (MRP) subfamily (Ysr1/Yor1) of Saccharomyces cerevisiae is important for the tolerance to a broad range of organic anions. J. Biol. Chem., 271: 14712-14716, 1996.
53. Katzmann, D. J., Hallstrom, T. C., Voet, M., Wysock, W., Golin, J., Volckaert, G., and Moye-Rowley, W. S. Expression of an ATP-binding cassette transporter-encoding gene (YORI) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol., 15: 6875-6883, 1995.
54. Szcypka, M. S., Wemmie, J. A., Moye-Rowley, W. S., and Thiele, D. J. A yeast metal resistance protein similar to cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem., 269: 22853-22857, 1994.