Multidrug resistance and pharmacological protection mediated by the breast cancer resistance protein (BCRP/ABCG2)

Molecular Cancer Therapeutics

Volumn 1, Issue 6, 2002, Pages 427-434

  Allen, John D ^a   Schinkel, Alfred H ^b  

^a CENTENARY INSTITUTE   (Australia)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; TUMOR PROTEIN;

BREAST TUMOR; DRUG RESISTANCE; HUMAN; METABOLISM; MULTIDRUG RESISTANCE; REVIEW;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BREAST NEOPLASMS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASM PROTEINS;

EID: 0001744641     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: None     Document Type: Short Survey

References (59)

1. Higgins, C. F. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol., 8: 67-113, 1992. (Pubitemid 23000992)
2. Juliano, R. L., and Ling, V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta, 455: 152-162, 1976.
3. Chen, C. J., Chin, J. E., Ueda, K., Clark, D. P., Pastan, I., Gottesman, M. M., and Roninson, I. B. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell, 47: 381-389, 1986. (Pubitemid 17210152)
4. Gros, P., Croop, J., and Housman, D. Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell, 47: 371-380, 1986. (Pubitemid 17210151)
5. Cole, S. P. C., Bhardway, 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 (Wash. DC), 258: 1650-1654, 1992. (Pubitemid 23012438)
6. Gottesman, M. M., and Pastan, I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem., 62: 385-427, 1993. (Pubitemid 23237876)
7. Paulusma, C. C., Bosma, P. J., Zaman, G. J., Bakker, C. T., Otter, M., Scheffer, G. L., Scheper, R. J., Borst, P., Oude Elferink, R. P. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science (Wash. DC), 271: 1126-1128, 1996. (Pubitemid 26075228)
8. Schinkel, A. H. The physiological function of drug-transporting P-glycoproteins. Semin. Cancer Biol., 8: 161-170, 1997. (Pubitemid 28041013)
9. Wijnholds, J., Evers, R., Van Leusden, M. R., Mol, C. A. A. M., Zaman, G. J. R., Mayer, U., Beijnen, J. H., Van der Valk, M., Krimpenfort, P., Berns, A., and Borst, P. Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking MRP. Nat. Med., 3: 1275-1279, 1997. (Pubitemid 27508831)
10. Hipfner, D. R., Deeley, R. G., and Cole, S. P. C. Structural, mechanistic, and clinical aspects of MRP1. Biochim. Biophys. Acta, 1461: 359-376, 1999.
11. König, J., Nies, A. T., Cui, Y., Leier, I., and Keppler, D. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim. Biophys. Acta, 1461: 377-394, 1999.
12. Borst, P., Evers, R., Kool, M., and Wijnholds, J. A family of drug transporters: the multidrug resistance-associated proteins. J. Natl. Cancer Inst., 92: 1295-1302, 2000. (Pubitemid 30662093)
13. Doyle, L. A., Yang, W., Abruzzo, L. V., Krogmann, T., Gao, Y., Rishi, A. K., and Ross, D. D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA, 95: 15665-15670, 1998. (Pubitemid 29018757)
14. Chen, Y-N., Mickley, L. A., Schwartz, A. M., Acton, E. M., Hwang, J., and Fojo, T. Characterization of adriamycin-resistant human breast cancer cells which display overexpression of a novel resistance-related membrane protein. J. Biol. Chem., 265: 10073-10080, 1990.
15. Lee, J. S., Scala, S., Matsumoto, Y., Dickstein, B., Robey, R., Zhan, Z., Altenberg, G., and Bates, S. E. Reduced drug accumulation and multidrug resistance in human breast cancer cells without associated P-glycoprotein or MRP overexpression. J. Cell Biochem., 65: 513-526, 1997. (Pubitemid 27240917)
16. Özvegy, C., Litman, T., Szakacs, G., Nagy, Z., Bates, S., Varadi, A., and Sarkadi, B. Functional characterization of the human multidrug transporter, abcg2, expressed in insect cells. Biochem. Biophys. Res. Commun., 285: 111-117, 2001. (Pubitemid 32912517)
17. Miyake, K., Mickley, L., Litman, T., Zhan, Z., Robey, R., Cristensen, B., Brangi, M., Greenberger, L., Dean, M., Fojo, T., and Bates S. E. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res., 59: 8-13, 1999. (Pubitemid 29062946)
18. Allikmets, R., Schriml, L. M., Hutchinson, A., Romano-Spica, V., and Dean, M. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res., 58: 5337-5339, 1998. (Pubitemid 28551112)
19. Allen, J. D., Brinkhuis, R. F., Wijnholds, J., and Schinkel, A. H. The mouse Bcrp/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res., 59: 4237-4241, 1999. (Pubitemid 29418735)
20. Bailey-Dell, K. J., Hassel, B., Doyle, L. A., and Ross, D. D. Promoter characterization and genomic organization of the human breast cancer resistance protein (ATP-binding cassette transporter G2) gene. Biochim. Biophys. Acta, 1520: 234-241, 2001. (Pubitemid 32868794)
21. Knutsen, T., Rao, V. K., Ried, T., Mickley, L., Schneider, E., Miyake, K., Ghadimi, B. M., Padilla-Nash, H., Pack, S., Greenberger, L., Cowan, K., Dean, M., Fojo, T., and Bates, S. Amplification of 4q21-q22 and the MXR gene in independently derived mitoxantrone-resistant cell lines. Genes Chromosomes Cancer, 27: 110-116, 2000.
22. Ewart, G. D., and Howells, A. J. ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster. In: S. Ambudkar and M. M. Gottesman (eds.), Methods in Enzymology, Vol. 292, pp. 213-224. San Diego, CA: Academic Press, Inc., 1998. (Pubitemid 29343889)
23. Honjo, Y., Hrycyna, C. A., Robey, R. W., Medina-Pérez, W. Y., Yan, Q-W., van de Laar, A., Litman, T., Dean, M., and Bates, S. E. Acquired mutations in the MXR/BCRP/ABCP gene alter substrate specificity in MXR/BCRP/ABCP-overexpressing cells. Cancer Res., 61: 6635-6639, 2001. (Pubitemid 32896477)
24. Kage, K., Tsukahara, S., Sugiyama, T., Asada, S., Ishikawa, E., Tsuruo, T., and Sugimoto, Y. Dominant-negative inhibition of breast cancer resistance protein as drug efflux pump through the inhibition of S-S homodimerization. Int. J. Cancer, 97: 626-630, 2002. (Pubitemid 34087801)
25. Mickley, L., Jain, P., Miyake, K., Schriml, L. M., Rao, K., Fojo, T., Bates, S., and Dean, M. An ATP-binding cassette gene (ABCG3) closely related to the multidrug resistance transporter ABCG2 (MXR/ABCP) has an unusual ATP-binding domain. Mamm. Genome, 12: 86-88, 2001. (Pubitemid 32127977)
26. Scheffer, G. L., Maliepaard, M., Pijnenborg, A. C. L. M., van Gastelen, M. A., de Jong, M. C., Schroeijers, A. B., van der Kolk, D. M., Allen, J. D., Ross, D. D., van der Valk, P., Dalton, W. S., Schellens, J. H. M., and Scheper, R. J. Breast cancer resistance protein is localized at the plasma membrane in mitoxantrone- and topotecan-resistant cell lines. Cancer Res., 60: 2589-2593, 2000. (Pubitemid 30318229)
27. Rocchi, E., Khodjakov, A., Volk, E. L., Yang, C-H., Litman, T., Bates, S. E., and Schneider, E. The product of the ABC half-transporter gene ABCG2 (BCRP/MXR/ABCP) is expressed in the plasma membrane. Biochem. Biophys. Res. Comm., 271: 42-46, 2000. (Pubitemid 30444853)
28. Maliepaard, M., Scheffer, G. L., Faneyte, I. F., van Gastelen, M. A., Pijnenborg, A. C. L. M., Schinkel, A. H., van de Vijver, M. J., Scheper, R. J., and Schellens, J. H. M. Subcellular localization and distribution of the breast cancer resistance protein in normal human tissues. Cancer Res., 61: 3458-3464, 2001. (Pubitemid 32695041)
29. Jonker, J. W., Smit, J. W., Brinkhuis, R. F., Maliepaard, M., Beijnen, J. H., Schellens, J. H. M., and Schinkel, A. H. Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J. Natl. Cancer Inst., 92: 1651-1656, 2000.
30. Litman, T., Brangi, M., Hudson, E., Fetsch, P., Abati, A., Ross, D. D., Miyake, K., Resau, J. H., and Bates, S. E. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J. Cell Sci., 113: 2011-2021, 2000. (Pubitemid 30386505)
31. Ross, D. D., Yang, W., Abruzzo, L. V., Dalton, W. S., Schneider, E., Lage, H., Dietel, M., Greenberger, L., Cole, S. P. C., and Doyle, L. A. Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J. Natl. Cancer Inst., 91: 429-433, 1999. (Pubitemid 29128278)
32. Maliepaard, M., van Gastelen, M. A., de Jong, L. A., Pluim, D., van Waardenburg, R. C. A. M., Ruevekamp-Helmers, M. C., Floot, B. J. G., and Schellens, J. H. M. Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res., 59: 4559-4563, 1999. (Pubitemid 29428958)
33. Kawabata, S., Oka, M., Shiozawa, K., Tsukamoto, K., Nakatomi, K., Soda, H., Fukuda, M., Ikegami, Y., Sugahara, K., Yamada, Y., Kamihira, S., Doyle, L. A., Ross, D. D., and Kohno, S. Breast cancer resistance protein directly confers SN-38 resistance of lung cancer cells. Biochem. Biophys. Res. Comm., 280: 1216-1223, 2001. (Pubitemid 32917772)
34. Robey, R. W., Medina-Perez, W. Y, Nishiyama, K., Lahusen, T., Miyake, K., Litman, T., Senderowicz, A. M., Ross, D. D., and Bates, S. E. Overexpression of the ATP-binding cassette half-transporter, ABCG2 (MXR/BCRP/ABCP1), in flavopiridol-resistant human breast cancer cells. Clin. Cancer Res., 7: 145-152, 2001. (Pubitemid 32110217)
35. Komatani, H., Kotani, H., Hara, Y., Nakagawa, R., Matsumoto, M., Arakawa, H., and Nishimura, S. Identification of breast cancer resistance protein/mitoxantrone resistance/placenta-specific, ATP-binding cassette transporter as a transporter of NB-506 and J-107088, topoisomerase I inhibitors with an indolocarbazole structure. Cancer Res., 61: 2827-2832, 2001. (Pubitemid 32691919)
36. Hazlehurst, L. A., Foley, N. E., Gleason-Guzman, M. C., Hacker, M. P., Cress, A. E., Greenberger, L. M., De Jong, M. C., and Dalton, W. S. Multiple mechanisms confer drug resistance to mitoxantrone in the human 8226 myeloma cell line. Cancer Res., 59: 1021-1028, 1999. (Pubitemid 29135961)
37. Rabindran, S. K., Ross, D. D., Doyle, L. A., Yang, W., and Greenberger, L. M. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res., 60: 47-50, 2000. (Pubitemid 30058728)
38. Robey, R. W., Honjo, Y., van de Laar, A., Miyake, K., Regis, J. T., Litman, T., and Bates, S. E. A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim. Biophys. Acta, 1512: 171-182, 2001. (Pubitemid 32530764)
39. Brangi, M., Litman, T., Ciotti, M., Nishiyama, K., Kohlhagen, G., Takimoto, C., Robey, R., Pommier, Y., Fojo, T., and Bates, S. E. Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR), and potential for glucuronidation in MXR-expressing cells. Cancer Res., 59: 5938-5946, 1999. (Pubitemid 30004955)
40. Rabindran, S. K., He, H., Singh, M., Brown, E., Collins, K. I., Annable, T., and Greenberger, L. M. Reversal of a novel multidrug resistance mechanism in human colon carcinoma cells by fumitremorgin C. Cancer Res., 58: 5850-5858, 1998. (Pubitemid 29006428)
41. Slapak, C. A., Mizunuma, M., and Kufe, D. W. Expression of the multidrug resistance associated protein and P-glycoprotein in doxorubicin-selected human myeloid leukemia cells. Blood, 84: 3113-3121, 1994.
42. Choi, K. H., Chen, C. J., Kriegler, M., and Roninson, I. B. An altered pattern of cross-resistance in multidrug-resistant human cells results from spontaneous mutations in the mdr1 (P-glycoprotein) gene. Cell, 53: 519-529, 1988.
43. Stride, B. D., Grant, C. E., Loe, D. W., Hipfner, D. R., Cole, S. P. C., and Deeley, R. G. Pharmacological characterization of the murine and human orthologs of multidrug-resistance protein in transfected human embryonic kidney cells. Mol. Pharmacol., 52: 344-353, 1997. (Pubitemid 27412958)
44. Volk, E. L., Rohde, K., Rhee, M., McGuire, J. J., Doyle, L. A., Ross, D. D., and Schneider, E. Methotrexate cross-resistance in a mitoxantrone-selected multidrug-resistant MCF7 breast cancer cell line is attributable to enhanced energy-dependent drug efflux. Cancer Res., 60: 3514-3521, 2000. (Pubitemid 30482171)
45. Sikic, B. I. Modulation of multidrug resistance: a paradigm for translational clinical research. Oncology (Huntingt.), 13: 183-187, 1999.
46. Huisman, M. T., Smit, J. W., and Schinkel, A. H. Significance of P-glycoprotein for the pharmacology and clinical use of HIV protease inhibitors. AIDS, 14: 237-242, 2000. (Pubitemid 30132917)
47. De Bruin, M., Miyake, K., Litman, T., Robey, R., and Bates, S. E. Reversal of drug resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR. Cancer Lett., 146: 117-126, 1999. (Pubitemid 29492880)
48. Hyafil, F., Vergely, C., Du Vigneaud, P., and Grand-Perret, T. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res., 53: 4595-4602, 1993. (Pubitemid 23304385)
49. Malingré, M. M., Beijnen, J. H., Rosing, H., Koopman, F. J., Jewell, R. C., Paul, E. M., Ten Bokkel Huinink, W. W., and Schellens, J. H. M. Co-administration of GF120918 significantly increases the systemic exposure to oral paclitaxel in cancer patients. Br. J. Cancer., 84: 42-47, 2001. (Pubitemid 32102502)
50. He, H., Rabindran, S. G., Greenberger, L. M., and Carter, G. T. Fumitremorgin C analogs that reverse mitoxantrone resistance in human colon carcinoma cells. Med. Chem. Res., 9: 424-437, 1999. (Pubitemid 30056762)
51. Van Loevezijn, A., Allen, J. D., Schinkel, A. H., and Koomen, G-J. Inhibition of BCRP-mediated drug efflux by fumitremorgin-type indolyl diketopiperazines. Biorgan. Med. Chem. Lett., 11: 29-32, 2001. (Pubitemid 32006117)
52. Erlichman, C., Boerner, S. A., Hallgren, C. G, Spieker, R., Wang, X-Y., James, C. D., Scheffer, G. L., Maliepaard, M., Ross, D. D., Bible, K. C., Kaufmann, S. H. The HER tyrosine kinase inhibitor CI1033 enhances cytotoxicity of 7-ethyl-10-hydroxycamptothecin and topotecan by inhibiting breast cancer resistance protein-mediated drug efflux. Cancer Res., 61: 739-748, 2001. (Pubitemid 32128641)
53. Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A-M., Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H., and Sorrentino, B. P. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med., 7: 1028-1034, 2001. (Pubitemid 32937383)
54. Taipalensuu, J., Törnblom, H., Lindberg, G., Einarsson, C., Sjöqvist, F., Melhus, H., Garberg, P., Sjöström, B., Lundgren, B., and Artursson, P. Correlation of gene expression of ten drug efflux proteins of the human ATP-binding cassette transporter family in normal human jejunum and in human intestinal epithelial Caco-2 cell monolayers. J. Pharmacol. Exp. Ther., 299: 164-170, 2001. (Pubitemid 32905131)
55. Scharenberg, C. W., Harkey, M. A., and Torok-Storb, B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood, 99: 507-512, 2002. (Pubitemid 34533085)
56. Allen, J. D., Brinkhuis, R. F., van Deemter, L., Wijnholds, J., and Schinkel, A. H. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res., 60: 5761-5766, 2000.
57. Ross, D. D., Karp, J. E., Chen, T. T., and Doyle, L. A. Expression of breast cancer resistance protein in blast cells from patients with acute leukemia. Blood, 96: 365-368, 2000. (Pubitemid 30456496)
58. Sargent, J. M., Williamsom, C. J., Maliepaard, M., Elgie, A. W., Scheper, R. J., and Taylor, C. G. Breast cancer resistance protein expression and resistance to daunorubicin in blast cells from patients with acute myeloid leukaemia. Br. J. Haematol., 115: 257-262, 2001. (Pubitemid 34203486)
59. Kanzaki, A., Toi, M., Nakayama, K., Bando, H., Mutoh, M., Uchida, T., Fukumoto, M., and Takebayashi, Y. Expression of multidrug resistance-related transporters in human breast carcinoma. Jpn. J. Cancer Res., 92: 452-458, 2001. (Pubitemid 32427782)