Acyclovir is a substrate for the human breast cancer resistance protein (BCRP/ABCG2): Implications for renal tubular transport and acyclovir-induced nephrotoxicity

Canadian Journal of Physiology and Pharmacology

Volumn 89, Issue 9, 2011, Pages 675-680

  Gunness, Patrina ^a,b   Aleksa, Katarina ^a,c   Koren, Gideon ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Acyclovir; BCRP ABCG2; HEK293; In vitro; Renal

Indexed keywords

ACICLOVIR; BREAST CANCER RESISTANCE PROTEIN; FUMITREMORGIN C;

ARTICLE; CELL STRAIN HEK293; DRUG ACCUMULATION; DRUG INDUCED DISEASE; DRUG TRANSPORT; EMBRYO; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY TUBULE; NEPHROTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACUTE KIDNEY INJURY; ACYCLOVIR; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL LINE, TRANSFORMED; FEMALE; HEK293 CELLS; HUMANS; KIDNEY; KIDNEY TUBULES; NEOPLASM PROTEINS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 80051982645     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/y11-045     Document Type: Article

References (39)

1. Ahmad, T., Simmonds, M., McIver, A.G., and McGraw, M.E. 1994. Reversible renal failure in renal transplant patients receiving oral acyclovir prophylaxis. Pediatr. Nephrol. 8(4): 489-491. doi:10. 1007/BF00856544. PMID:7947045.
2. Allen, J.D., Brinkhuis, R.F., Wijnholds, J., and Schinkel, A.H. 1999. The mouse Bcrp1/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res. 59(17): 4237-4241. PMID:10485464.
3. Allikmets, R., Schriml, L.M., Hutchinson, A., Romano-Spica, V., and Dean, M. 1998. A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Res. 58(23): 5337-5339. PMID:9850061.
4. Bachmeier, C.J., Trickler, W.J., and Miller, D.W. 2006. Comparison of drug efflux transport kinetics in various blood-brain barrier models. Drug Metab. Dispos. 34(6): 998-1003. PMID:16554372.
5. Bianchetti, M.G., Roduit, C., and Oetliker, O.H. 1991. Acyclovirinduced renal failure: course and risk factors. Pediatr. Nephrol. 5(2): 238-239. doi:10.1007/BF01095963. PMID:2031844.
6. Brigden, D., Rosling, A.E., and Woods, N.C. 1982. Renal function after acyclovir intravenous injection. Am. J. Med. 73(1A): 182-185. doi:10.1016/0002-9343(82)90087-0. PMID:6285711.
7. Brown, C.D., Sayer, R., Windass, A.S., Haslam, I.S., De Broe, M.E., D'Haese, P.C., and Verhulst, A. 2008. Characterisation of human tubular cell monolayers as a model of proximal tubular xenobiotic handling. Toxicol. Appl. Pharmacol. 233(3): 428-438. doi:10. 1016/j.taap.2008.09.018. PMID:18930752.
8. Chou, J.W., Yong, C., and Wootton, S.H. 2008. Case 2: rash, fever and headache.... first, do no harm. Paediatr. Child Health, 13(1): 49-52. PMID:19119354.
9. Cusatis, G., Gregorc, V., Li, J., Spreafico, A., Ingersoll, R.G., Verweij, J., et al. 2006. Pharmacogenetics of ABCG2 and adverse reactions to gefitinib. J. Natl. Cancer Inst. 98(23): 1739-1742. doi:10.1093/jnci/djj469. PMID:17148776.
10. Dean, M., Rzhetsky, A., and Allikmets, R. 2001. The human ATPbinding cassette (ABC) transporter superfamily. Genome Res. 11(7): 1156-1166. doi:10.1101/gr.GR-1649R. PMID:11435397.
11. Doyle, L.A., Yang, W., Abruzzo, L.V., Krogmann, T., Gao, Y., Rishi, A.K., and Ross, D.D. 1998. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. U.S. A. 95(26): 15665-15670. doi:10.1073/pnas.95.26.15665. PMID: 9861027.
12. Genc, G., Ozkaya, O., Acikgoz, Y., Yapici, O., Bek, K., Gulnar Sensoy, S., and Ozyurek, E. 2010. Acute renal failure with acyclovir treatment in a child with leukemia. Drug Chem. Toxicol. 33(2): 217-219. doi:10.3109/01480540903311076. PMID:20307148.
13. González-Lobato, L., Real, R., Prieto, J.G., Alvarez, A.I., and Merino, G. 2010. Differential inhibition of murine Bcrp1/Abcg2 and human BCRP/ABCG2 by the mycotoxin fumitremorgin C. Eur. J. Pharmacol. 644(1-3): 41-48. doi:10.1016/j.ejphar.2010.07. 016. PMID:20655304.
14. Gunness, P., Aleksa, K., Kosuge, K., Ito, S., and Koren, G. 2010. Comparison of the novel HK-2 human renal proximal tubular cell line with the standard LLC-PK1 cell line in studying drug-induced nephrotoxicity. Can. J. Physiol. Pharmacol. 88(4): 448-455. doi:10.1139/Y10-023. PMID:20555413.
15. Hintz, M., Connor, J.D., Spector, S.A., Blum, M.R., Keeney, R.E., and Yeager, A.S. 1982. Neonatal acyclovir pharmacokinetics in patients with herpes virus infections. Am. J. Med. 73(1A): 210-214. doi:10.1016/0002-9343(82)90093-6. PMID:6285713.
16. Huls, M., Brown, C.D., Windass, A.S., Sayer, R., van den Heuvel, J. J., Heemskerk, S., et al. 2008. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int. 73(2): 220-225. doi:10.1038/ sj.ki.5002645. PMID:17978814.
17. Jonker, J.W., Merino, G., Musters, S., van Herwaarden, A.E., Bolscher, E., Wagenaar, E., et al. 2005. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat. Med. 11(2): 127-129. doi:10.1038/nm1186. PMID:15685169.
18. Keeney, R.E., Kirk, L.E., and Bridgen, D. 1982. Acyclovir tolerance in humans. Am. J. Med. 73(1A): 176-181. doi:10.1016/0002-9343(82)90086-9. PMID:6285709.
19. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227(5259): 680-685. doi:10.1038/227680a0. PMID:5432063.
20. 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(3): 216-237. doi:10.1016/j.taap.2004.10.012. PMID:15845415.
21. Lyon, A.W., Mansoor, A., and Trotter, M.J. 2002. Urinary gems: acyclovir crystalluria. Arch. Pathol. Lab. Med. 126(6): 753-754. PMID:12087974.
22. Maeda, K., and Sugiyama, Y. 2008. Impact of genetic polymorphisms of transporters on the pharmacokinetic, pharmacodynamic and toxicological properties of anionic drugs. Drug Metab. Pharmacokinet. 23(4): 223-235. doi:10.2133/dmpk.23.223. PMID: 18762709.
23. Maliepaard, M., Scheffer, G.L., Faneyte, I.F., van Gastelen, M.A., Pijnenborg, A.C., Schinkel, A.H., et al. 2001. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res. 61(8): 3458-3464. PMID:11309308.
24. Mao, Q., and Unadkat, J.D. 2005. Role of the breast cancer resistance protein (ABCG2) in drug transport. AAPS J. 7(1): E118-E133. doi:10.1208/aapsj070112. PMID:16146333.
25. Mason, W.J., and Nickols, H.H. 2008. Images in clinical medicine. Crystalluria from acyclovir use. N. Engl. J. Med. 358(13): e14. doi:10.1056/NEJMicm066726. PMID:18367732.
26. Millipore. 2007. RIPA buffer: preparation of modified radioimmunoprecipitation (RIPA) buffer. Available from http://www.millipore.com/userguides/tech1/mcproto402 [accessed 1 August 2008].
27. Morisaki, K., Robey, R.W., Ozvegy-Laczka, C., Honjo, Y., Polgar, O., Steadman, K., et al. 2005. Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother. Pharmacol. 56(2): 161-172. doi:10.1007/s00280-004-0931-x. PMID:15838659.
28. Ozvegy, C.T., Litman, T., Szakács, G., Nagy, Z., Bates, S., Váradi, A., and Sarkadi, B. 2001. Functional characterization of the human multidrug transporter, ABCG2, expressed in insect cells. Biochem. Biophys. Res. Commun. 285(1): 111-117. doi:10.1006/bbrc.2001. 5130. PMID:11437380.
29. Peterslund, N.A., Larsen, M.L., and Mygind, H. 1988. Acyclovir crystalluria. Scand. J. Infect. Dis. 20(2): 225-228. doi:10.3109/ 00365548809032442. PMID:3041563.
30. Pollex, E.K., Anger, G., Hutson, J., Koren, G., and Piquette-Miller, M. 2010. Breast cancer resistance protein (BCRP)-mediated glyburide transport: effect of the C421A/Q141K BCRP singlenucleotide polymorphism. Drug Metab. Dispos. 38(5): 740-744. doi:10.1124/dmd.109.030791. PMID:20159988.
31. Robey, R.W., To, K.K., Polgar, O., Dohse, M., Fetsch, P., Dean, M., and Bates, S.E. 2009. ABCG2: a perspective. Adv. Drug Deliv. Rev. 61(1): 3-13. doi:10.1016/j.addr.2008.11.003. PMID:19135109.
32. Rocchi, E., Khodjakov, A., Volk, E.L., Yang, C.H., Litman, T., Bates, S.E., and Schneider, E. 2000. The product of the ABC halftransporter gene ABCG2 (BCRP/MXR/ABCP) is expressed in the plasma membrane. Biochem. Biophys. Res. Commun. 271(1): 42-46. doi:10.1006/bbrc.2000.2590. PMID:10777678.
33. Sawyer, M.H., Webb, D.E., Balow, J.E., and Straus, S.E. 1988. Acyclovir-induced renal failure. Clinical course and histology. Am. J. Med. 84(6): 1067-1071. doi:10.1016/0002-9343(88) 90313-0. PMID:3376977.
34. Sparreboom, A., Gelderblom, H., Marsh, S., Ahluwalia, R., Obach, R., Principe, P., et al. 2004. Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype. Clin. Pharmacol. Ther. 76(1): 38-44. doi:10.1016/j.clpt.2004.03.003. PMID:15229462.
35. Towbin, H., Staehelin, T., and Gordon, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S.A. 76(9): 4350-4354. doi:10.1073/pnas.76.9.4350. PMID: 388439.
36. Vachvanichsanong, P., Patamasucon, P., Malagon, M., and Moore, E. S. 1995. Acute renal failure in a child associated with acyclovir. Pediatr. Nephrol. 9(3): 346-347. doi:10.1007/BF02254206. PMID:7632529.
37. Vomiero, G., Carpenter, B., Robb, I., and Filler, G. 2002. Combination of ceftriaxone and acyclovir-an underestimated nephrotoxic potential? Pediatr. Nephrol. 17(8): 633-637. doi:10. 1007/s00467-002-0867-5. PMID:12185472.
38. Yamasaki, Y., Ieiri, I., Kusuhara, H., Sasaki, T., Kimura, M., Tabuchi, H., et al. 2008. Pharmacogenetic characterization of sulfasalazine disposition based on NAT2 and ABCG2 (BCRP) gene polymorphisms in humans. Clin. Pharmacol. Ther. 84(1): 95-103. doi:10.1038/sj.clpt.6100459. PMID:18167504.
39. Zhang, W., Yu, B.N., He, Y.J., Fan, L., Li, Q., Liu, Z.Q., et al. 2006. Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin. Chim. Acta, 373(1-2): 99-103. doi:10.1016/j.cca.2006.05.010. PMID:16784736.