The potential impact of drug transporters on nucleoside-analog-based antiviral chemotherapy

Antiviral Research

Volumn 62, Issue 1, 2004, Pages 1-7

  Borst, P ^a   Balzarini, J ^b   Ono, N ^a   Reid, G ^c   De Vries, H ^a   Wielinga, P ^a   Wijnholds, J ^d   Zelcer, N ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

ABC transporters; Aryloxyalaninylphosphoramidate of ddA 5 monophosphate (ddAMP); Cf1093; cGMP; cPr PMEDAP; Cyclic nucleotides; Cyclopropyl PMEDAP; Guanosine 3 ,5 cyclic monophosphate; MRPs; Nucleoside analogs; Oral drug availability

Indexed keywords

ABACAVIR; ABC TRANSPORTER; ADEFOVIR; ANTIVIRUS AGENT; BREAST CANCER RESISTANCE PROTEIN; CALGRANULIN; CLADRIBINE; DIDANOSINE; FLOXURIDINE; FLUOROURACIL; GANCICLOVIR; GLYCOPROTEIN P; MERCAPTOPURINE; 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 9; NUCLEOSIDE DERIVATIVE; PURINE NUCLEOSIDE DERIVATIVE; PYRIMIDINE NUCLEOSIDE DERIVATIVE; STAVUDINE; TIOGUANINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; ZALCITABINE; ZIDOVUDINE;

BINDING AFFINITY; CELL LINE; CONCENTRATION RESPONSE; DRUG ACCUMULATION; DRUG RESISTANCE; DRUG TRANSPORT; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANTIVIRAL AGENTS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE, VIRAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NUCLEOSIDES; NUCLEOTIDES, CYCLIC;

EID: 1542509357     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2003.11.002     Document Type: Review

References (52)

1. Adachi M., Reid G., Schuetz J.D. Therapeutic and biological importance of getting nucleotides out of cells: a case for the ABC transporters, MRP4 and 5. Adv. Drug Deliv. Rev. 54:2002a;1333-1342.
2. Adachi M., Sampath J., Lan L.-B., Sun D., Hargrove P., Flatley R.M., Tatum A., Ziegelmeier M.Z., Wezeman M., Matherly L.H., Drake R.R., Schuetz J.D. Expression of MRP4 confers resistance to ganciclovir and compromises bystander cell killing. J. Biol. Chem. 277:2002b;38998-39004.
3. Bakos E., Evers R., Sinkó E., Váradi A., Borst P., Sarkadi B. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 57:2000;760-768.
4. Balzarini J., Hao Z., Herdewijn P., Johns D.G., De Clercq E. Intracellular metabolism and mechanism of anti-retrovirus action of 9-(2-phosphonylmethoxyethyl)adenine, a potent anti-human immunodeficiency virus compound. Proc. Natl. Acad. Sci. U.S.A. 88:1991;1499-1503.
5. Balzarini J., Karlsson A., Aquaro S., Perno C.F., Cahard D., Naesens L., De Clercq E., McGuigan C. Mechanism of anti-HIV action of masked alaninyl D4T-MP derivatives. Proc. Natl. Acad. Sci. U.S.A. 93:1996;7295-7299.
6. Bera T.K., Lee S., Salvatore G., Lee B., Pastan I. 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. 7:2001;509-516.
7. Bera T.K., Iavarone C., Kumar V., Lee S., Lee B., Pastan I. MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc. Natl. Acad. Sci. U.S.A. 99:2002;6997-7002.
8. Bódó A., Bakos E., Szeri F., Váradi A., Sarkadi B. Differential modulation of the human liver conjugate transporters MRP2 and MRP3 by bile acids and organic anions. J. Biol. Chem. 278:2003;23529-23537.
9. Borst, P., Oude Elferink, R., 2002. Mammalian ABC transporters in health and disease. In: Richardson, C.C., Kornberg, R., Raetz, C.H.R., Thorstensen, K. (Eds.), Annual Review of Biochemistry. Science, California, pp. 537-592.
10. Borst P., Evers R., Kool M., Wijnholds J. The multidrug resistance protein family. Biochim. Biophys. Acta. 1461:1999;347-357.
11. Borst P., Evers R., Kool M., Wijnholds J. A family of drug transporters, the MRP's. J. Natl. Cancer Inst. 92:2000;1295-1302.
12. Borst, P., Reid, G., Saeki, T., Wielinga, P., Zelcer, N., 2003. The multidrug resistance proteins 3-7. In: Holland, I.B., Kuchler, K., Higgins, C.F., Cole, S.P.C. (Eds.), ABC Proteins: From Bacteria to Man. Elsevier, London, pp. 445-458.
13. Chen Z.-S., Lee K., Kruh G.D. Transport of cyclic nucleotides and estradiol 17-β-D-glucuronide by multidrug resistance protein 4: resistance to 6-mercaptopurine and 6-thioguanine. J. Biol. Chem. 276:2001;33747-33754.
14. Chen Z.S., Robey R.W., Belinsky M.G., Shchaveleva I., Ren X.Q., Sugimoto Y., Ross D.D., Bates S.E., Kruh G.D. Transport of methotrexate, methotrexate polyglutamates, and 17beta-estradiol 17-(beta-D-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res. 63:2003;4048-4054.
15. Cihlar T., Lin D.C., Pritchard J.B., Fuller M.D., Mendel D.B., Sweet D.H. The antiviral nucleotide analogs cidofovir and adefovir are novel substrates for human and rat renal organic anion transporter 1. Mol. Pharmacol. 56:1999;570-580.
16. Dantzig, A.H., Pratt, S.E., Shepard, R.L., 2003. MRP5 confers resistance to 5-FU and transports a phosphorylated metabolite of 5-FU. Proc. Am. Assoc. Cancer Res. 44 (March) (#3696).
17. Davidson, J.D., Ma, L., Iverson, P.W., Lesoon, A., Jin, S., Horwitz, L., Gallery, M., Slapak, C.A., 2002. Human Multi-drug Resistance Protein 5 (MRP5) confers resistance to gemcitabine. Proc. Am. Assoc. Cancer Res. 43 (March) (#3868).
18. Dietrich C.G., De Waart D.R., Ottenhoff R., Schoots I.G., Elferink R.P. Increased bioavailability of the food-derived carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine in MRP2-deficient rats. Mol. Pharmacol. 59:2001a;974-980.
19. Dietrich C.G., De Waart D.R., Ottenhoff R., Bootsma A.H., Van Gennip A.H., Elferink R.P. MRP2-deficiency in the ratimpairs biliary and intestinal excretion and influences metabolism and sipositionof the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo. Carcinogenesis. 22:2001b;805-811.
20. Dietrich C.G., Ottenhoff R., De Waart D.R., Oude Elferink R.P.J. Role of MRP2 and GSH in intrahepatic cycling of toxins. Toxicology. 167:2001c;73-81.
21. Evers R., Zaman G.J.R., Van Deemter L., Jansen H., Calafat J., Oomen L.C.J.M., Oude Elferink R.P.J., Borst P., Schinkel A.H. Basolateral localization and export activity of the human multidrug resistance-associated protein (MRP) in polarized pig kidney cells. J. Clin. Invest. 97:1996;1211-1218.
22. Guo Y., Kotova E., Chen Z.-S., Lee K., Hopper-Borge E., Belinsky M.G., Kruh G.D. 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. 278:2003;29509-29514.
23. Holland, I.B., Kuchler, K., Higgins, C., Cole, S. (Eds.), 2003. ABC Proteins: From Bacteria to Man. Elsevier, London, 647 pp.
24. Huisman M.T., Smit J.W., Schinkel A.H. Significance of P-glycoprotein for the pharmacology and clinical use of HIV protease inhibitors. AIDS. 14:2000;237-242.
25. Huisman M.T., Smit J.W., Crommentuyn K.M., Zelcer N., Wiltshire H.R., Beijnen J.H., Schinkel A.H. Multidrug resistance protein 2 (MRP2) transports HIV protease inhibitors, and transport can be enhanced by other drugs. AIDS. 16:2002;2295-2301.
26. Jedlitschky G., Keppler D. Transport of leukotriene C4 and structurally related conjugates. Vitam. Horm. 64:2002;153-184.
27. Jedlitschky G., Burchell B., Keppler D. The multidrug resistance protein 5 (MRP5) functions as an ATP-dependent export pump for cyclic nucleotides. J. Biol. Chem. 275:2000;30069-30074.
28. Johnson D.R., Finch R.A., Lin Z.P., Zeiss C.J., Sartorelli A.C. The pharmacological phenotype of combined multidrug-resistance mdr1a/1b- and mrp1-deficient mice. Cancer Res. 61:2001;1469-1476.
29. Kruh G.D., Zeng H., Rea P.A., Liu G., Chen Z.S., Lee K., Belinsky M.G. MRP subfamily transporters and resistance to anticancer agents. J. Bioenerg. Biomembr. 33:2001;493-501.
30. Lai L., Tan T.M.C. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem. J. 361:2002;497-503.
31. Lorico A., Rappa G., Flavell R.A., Sartorelli A.C. Double knockout of the MRP gene leads to increased drug sensitivity in vivo. Cancer Res. 56:1996;5351-5355.
32. Lorico A., Rappa G., Finch R.A., Yang D., Flavell R.A., Sartorelli A.C. Disruption of the murine MRP (Multidrug Resistance Protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res. 57:1997;5238-5242.
33. Oude Elferink R.P.J., Tytgat G.N.J., Groen A.K. The role of mdr2 P-glycoprotein in hepatobiliary lipid transport. FASEB J. 11:1997;19-28.
34. Potschka H., Fedrowitz M., Loscher W. Multidrug resistance protein MRP2 contributes to blood-brain barrier function and restricts antiepileptic drug activity. J. Pharmacol. Exp. Ther. 306:2003;124-131.
35. Reid G., Wielinga P., Zelcer N., De Haas M., Van Deemter L., Wijnholds J., Balzarini J., Borst P. Characterization of the transport of nucleoside analogue drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol. Pharmacol. 63:2003a;1102.
36. Reid G., Wielinga P., Zelcer N., Van der Heijden I., Kuil A., Borst P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by NSAIDs. Proc. Natl. Acad. Sci. U.S.A. 100:2003b;9244-9249.
37. Schinkel A.H., Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Deliv. Rev. 55:2003;3-29.
38. Schuetz J.D., Connelly M.C., Sun D., Paibir S.G., Flynn P.M., Srinivas R.V., Kumar A., Fridland A. MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat. Med. 5:1999;1048-1051.
39. Shimizu H., Taniguchi K., Hippou Y., Hayashizaki Y., Aburatani H., Ishikawa T. Characterization of the mouse ABcc12 gene and its transcript encoding an ATP-binding transporter, an orthologue of human ABCC12. Gene. 310:2003;17-28.
40. Suzuki M., Suzuki H., Sugimoto Y., Sugiyama Y. ABCG2 transports sulfated conjugates of steroids and xenobiotics. J. Biol. Chem. 278:2003;22644-22649.
41. Tammur J., Prades C., Arnould I., Rzhetsky A., Hutchinson A., Adachi M., Schuetz J.D., Swoboda K.J., Ptacek L.J., Rosier M., Dean M., Allikmets R. Two new genes from the human ATP-binding cassette transporter superfamily, ABCC11 and ABCC12, tandemly duplicated on chromosome 16q12. Gene. 273:2001;89-96.
42. Volk E.L., Farley K.M., Wu Y., Li F., Robey R.W., Schneider E. Overexpression of wild-type breast cancer resistance protein mediates methotrexate resistance. Cancer Res. 62:2002;5035-5040.
43. Wielinga P.R., Reid G., Challa E.E., Van der Heijden I., Van Deemter L., De Haas M., Mol C., Kuil A.J., Groeneveld E., Schuetz J.D., Brouwer C., De Abreu R.A., Wijnholds J., Beijnen J.H., Borst P. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol. Pharmacol. 62:2002;1321-1332.
44. Wielinga P.R., Van der Heijden I., Reid G., Beijnen J.H., Wijnholds J., Borst P. Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J. Biol. Chem. 278:2003;17664-17671.
45. Wijnholds J., Evers R., van Leusden M.R., Mol C.A.A.M., Zaman G.J.R., Mayer U., Beijnen J., Van der Valk M., Krimpenfort P., Borst P. Increased sensitivity to anticancer drugs and decreased inflammatory response in mice lacking MRP. Nat. Med. 11:1997;1275-1279.
46. Wijnholds J., Scheffer G.L., Van der Valk M., Beijnen J.H., Scheper R.J., Borst P. Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J. Exp. Med. 188:1998;797-808.
47. Wijnholds, J., Mol, C.A.A.M., Scheffer, G.L., Scheper, R.J., Borst, P., 1999. Multidrug resistance protein 5, a candidate multispecific organic anion transporter. Proc. Am. Assoc. Cancer Res. 40 (March) (#2088).
48. Wijnholds J., De Lange E.C.M., Scheffer G.L., Van den Berg D.J., Mol C.A.A.M., Van der Valk M., Schinkel A.H., Scheper R.J., Breimer D.J., Borst P. Multidrug-resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J. Clin. Invest. 105:2000a;279-285.
49. Wijnholds J., Mol C.A.A.M., Van Deemter L., De Haas M., Scheffer G.L., Baas F., Beijnen J.H., Scheper R.J., Hatse S., De Clercq E., Balzarini J., Borst P. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleoside analogs. Proc. Natl. Acad. Sci. U.S.A. 97:2000b;7476-7481.
50. Yabuuchi H., Shimizu H., Takayanagi S., Ishikawa T. Multiple splicing variants of two new human ATP-binding cassette transporters, ABCC11 and ABCC12. Biochem. Biophys. Res. Commun. 288:2001;933-939.
51. Zelcer N., Huisman M.T., Reid G., Wielinga P.R., Breedveld P., Kuil A., Knipscheer P., Schellens J.H., Schinkel A.H., Borst P. Evidence for two interacting ligand-binding sites in human MRP2 (ATP binding cassette C2). J. Biol. Chem. 278:2003a;23538-23544.
52. Zelcer N., Reid G., Wielinga P., Kuil A., Van der Heijden I., Schuetz J.D., Borst P. Steroid and bile acid-conjugates are substrates of human MRP4 (ABCC4). J. Biol. Chem. 371:2003b;361-367.