Organic anion transporting polypeptide (Oatp) 1a1-mediated perfluorooctanoate transport and evidence for a renal reabsorption mechanism of Oatp1a1 in renal elimination of perfluorocarboxylates in rats

Toxicology Letters

Volumn 190, Issue 2, 2009, Pages 163-171

  Yang, Ching Hui ^a   Glover, Kyle P ^a   Han, Xing ^a  

^a DUPONT COMPANY   (United States)

Author keywords

Oatp1a1; Perfluorocarboxylate; Perfluorooctanoate; Perfluorooctanoic acid; PFOA; Tubular reabsorption

Indexed keywords

AURANTIIN; BROMSULFOPHTHALEIN; CARBOXYLIC ACID DERIVATIVE; COMPLEMENTARY DNA; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 1A1; PERFLUORO COMPOUND; PERFLUOROBUTANOATE; PERFLUOROCARBOXYLATE DERIVATIVE; PERFLUORODECANOATE; PERFLUOROHEXANOATE; PERFLUOROOCTANOIC ACID; PERFLUOROPENTANOATE; TAUROCHOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; KIDNEY TUBULE ABSORPTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SEX DIFFERENCE; URINARY EXCRETION;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; BUTYRATES; CARBOXYLIC ACIDS; CHO CELLS; CRICETINAE; CRICETULUS; DATA INTERPRETATION, STATISTICAL; ESTRONE; FLUOROCARBONS; KIDNEY; KINETICS; MALE; NONLINEAR DYNAMICS; OCTANOIC ACIDS; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; PLASMIDS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION;

CITRUS X PARADISI; CRICETULUS GRISEUS; RATTUS;

EID: 69449099763     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2009.07.011     Document Type: Article

References (50)

1. Andersen M.E., Butenhoff J.L., Chang S.C., Farrar D.G., Kennedy Jr. G.L., Lau C., Olsen G.W., Seed J., and Wallace K.B. Perfluoroalkyl acids and related chemistries-toxicokinetics and modes of action. Toxicol. Sci. 102 (2008) 3-14
2. Andersen M.E., Clewell III H.J., Tan Y.M., Butenhoff J.L., and Olsen G.W. Pharmacokinetic modeling of saturable, renal resorption of perfluoroalkylacids in monkeys-probing the determinants of long plasma half-lives. Toxicology 227 (2006) 156-164
3. Anzai N., Jutabha P., Enomoto A., Yokoyama H., Nonoguchi H., Hirata T., Shiraya K., He X., Cha S.H., Takeda M., Miyazaki H., Sakata T., Tomita K., Igarashi T., Kanai Y., and Endou H. Functional characterization of rat organic anion transporter 5 (Slc22a19) at the apical membrane of renal proximal tubules. J. Pharmacol. Exp. Ther. 315 (2005) 534-544
4. Bailey D.G., Dresser G.K., Leake B.F., and Kim R.B. Naringin is a major and selective clinical inhibitor of organic anion-transporting polypeptide 1A2 (OATP1A2) in grapefruit juice. Clin. Pharmacol. Ther. 81 (2007) 495-502
5. Bergwerk A.J., Shi X., Ford A.C., Kanai N., Jacquemin E., Burk R.D., Bai S., Novikoff P.M., Stieger B., Meier P.J., Schuster V.L., and Wolkoff A.W. Immunologic distribution of an organic anion transport protein in rat liver and kidney. Am. J. Physiol. Gastrointest. Liver Physiol. 271 (1996) G231-238
6. Butenhoff J.L., Kennedy Jr. G.L., Hinderliter P.M., Lieder P.H., Jung R., Hansen K.J., Gorman G.S., Noker P.E., and Thomford P.J. Pharmacokinetics of perfluorooctanoate in cynomolgus monkeys. Toxicol. Sci. 82 (2004) 394-406
7. Chang S.C., Das K., Ehresman D.J., Ellefson M.E., Gorman G.S., Hart J.A., Noker P.E., Tan Y.M., Lieder P.H., Lau C., Olsen G.W., and Butenhoff J.L. Comparative pharmacokinetics of perfluorobutyrate in rats, mice, monkeys, and humans and relevance to human exposure via drinking water. Toxicol. Sci. 104 (2008) 40-53
8. Dresser G.K., Bailey D.G., Leake B.F., Schwarz U.I., Dawson P.A., Freeman D.J., and Kim R.B. Fruit juices inhibit organic anion transporting polypeptide-mediated drug uptake to decrease the oral availability of fexofenadine. Clin. Pharmacol. Ther. 71 (2002) 11-20
9. Eckhardt U., Schroeder A., Stieger B., Hochli M., Landmann L., Tynes R., Meier P.J., and Hagenbuch B. Polyspecific substrate uptake by the hepatic organic anion transporter Oatp1 in stably transfected CHO cells. Am. J. Physiol. 276 (1999) G1037-1042
10. Gotoh Y., Kato Y., Stieger B., Meier P.J., and Sugiyama Y. Gender difference in the Oatp1-mediated tubular reabsorption of estradiol 17beta-d-glucuronide in rats. Am. J. Physiol. Endocrinol. Metab. 282 (2002) E1245-1254
11. Han X., Snow T.A., Kemper R.A., and Jepson G.W. Binding of perfluorooctanoic acid to rat and human plasma proteins. Chem. Res. Toxicol. 16 (2003) 775-781
12. Han X., Yang C.H., Snajdr S.I., Nabb D.L., and Mingoia R.T. Uptake of perfluorooctanoate in freshly isolated hepatocytes from male and female rats. Toxicol. Lett. 181 (2008) 81-86
13. Hata S., Wang P., Eftychiou N., Ananthanarayanan M., Batta A., Salen G., Pang K.S., and Wolkoff A.W. Substrate specificities of rat oatp1 and ntcp: implications for hepatic organic anion uptake. Am. J. Physiol. Gastrointest. Liver Physiol. 285 (2003) G829-839
14. Hundley S.G., Sarrif A.M., and Kennedy G.L. Absorption, distribution, and excretion of ammonium perfluorooctanoate (APFO) after oral administration to various species. Drug Chem. Toxicol. 29 (2006) 137-145
15. Jacquemin E., Hagenbuch B., Stieger B., Wolkoff A.W., and Meier P.J. Expression cloning of a rat liver Na(+)-independent organic anion transporter. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 133-137
16. Katakura M., Kudo N., Tsuda M., Hibino Y., Mitsumoto A., and Kawashima Y. Rat organic anion transporter 3 and organic anion transporting polypeptide 1 mediate perfluorooctanoic acid transport. J. Health Sci. 53 (2007) 77-83
17. Kato Y., Kuge K., Kusuhara H., Meier P.J., and Sugiyama Y. Gender difference in the urinary excretion of organic anions in rats. J. Pharmacol. Exp. Ther. 302 (2002) 483-489
18. Kemper, R.A., 2003. Perfluorooctanoic acid: toxicokinetics in the rat. DuPont Haskell Laboratories, Report ID: DuPont-7473, USEPA Administrative Record AR-226.1499.
19. Kennedy Jr. G.L., Butenhoff J.L., Olsen G.W., O'Connor J.C., Seacat A.M., Perkins R.G., Biegel L.B., Murphy S.R., and Farrar D.G. The toxicology of perfluorooctanoate. Crit. Rev. Toxicol. 34 (2004) 351-384
20. Kojima R., Sekine T., Kawachi M., Cha S.H., Suzuki Y., and Endou H. Immunolocalization of multispecific organic anion transporters, OAT1, OAT2, and OAT3, in rat kidney. J. Am. Soc. Nephrol. 13 (2002) 848-857
21. Kouzuki H., Suzuki H., Ito K., Ohashi R., and Sugiyama Y. Contribution of organic anion transporting polypeptide to uptake of its possible substrates into rat hepatocytes. J. Pharmacol. Exp. Ther. 288 (1999) 627-634
22. Kudo N., Katakura M., Sato Y., and Kawashima Y. Sex hormone-regulated renal transport of perfluorooctanoic acid. Chem. Biol. Interact. 139 (2002) 301-316
23. Kudo N., and Kawashima Y. Toxicity and toxicokinetics of perfluorooctanoic acid in humans and animals. J. Toxicol. Sci. 28 (2003) 49-57
24. Kudo N., Suzuki E., Katakura M., Ohmori K., Noshiro R., and Kawashima Y. Comparison of the elimination between perfluorinated fatty acids with different carbon chain length in rats. Chem. Biol. Interact. 134 (2001) 203-216
25. Lau C., Anitole K., Hodes C., Lai D., Pfahles-Hutchens A., and Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol. Sci. 99 (2007) 366-394
26. Lee T.K., Koh A.S., Cui Z., Pierce R.H., and Ballatori N. N-glycosylation controls functional activity of Oatp1, an organic anion transporter. Am. J. Physiol. Gastrointest. Liver Physiol. 285 (2003) G371-381
27. Lee W., and Kim R.B. Transporters and renal drug elimination. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 137-166
28. Leuthold S., Hagenbuch B., Mohebbi N., Wagner C.A., Meier P.J., and Stieger B. Mechanisms of pH-gradient driven transport mediated by organic anion polypeptide transporters. Am. J. Physiol. Cell Physiol. 296 (2009) C570-582
29. Li N., Hartley D.P., Cherrington N.J., and Klaassen C.D. Tissue expression, ontogeny, and inducibility of rat organic anion transporting polypeptide 4. J. Pharmacol. Exp. Ther. 301 (2002) 551-560
30. Ljubojevic M., Balen D., Breljak D., Kusan M., Anzai N., Bahn A., Burckhardt G., and Sabolic I. Renal expression of organic anion transporter OAT2 in rats and mice is regulated by sex hormones. Am. J. Physiol. Renal Physiol. 292 (2007) F361-372
31. Ljubojevic M., Herak-Kramberger C.M., Hagos Y., Bahn A., Endou H., Burckhardt G., and Sabolic I. Rat renal cortical OAT1 and OAT3 exhibit gender differences determined by both androgen stimulation and estrogen inhibition. Am. J. Physiol. 287 (2004) F124-138
32. Lou I., Wambaugh J.F., Lau C., Hanson R.G., Lindstrom A.B., Strynar M.J., Zehr R.D., Setzer R.W., and Barton H.A. Modeling single and repeated dose pharmacokinetics of PFOA in mice. Toxicol. Sci. 107 (2009) 331-341
33. Lu R., Kanai N., Bao Y., Wolkoff A.W., and Schuster V.L. Regulation of renal oatp mRNA expression by testosterone. Am. J. Physiol. 270 (1996) F332-337
34. Masuda S., Ibaramoto K., Takeuchi A., Saito H., Hashimoto Y., and Inui K.I. Cloning and functional characterization of a new multispecific organic anion transporter, OAT-K2, in rat kidney. Mol. Pharmacol. 55 (1999) 743-752
35. Masuda S., Saito H., Nonoguchi H., Tomita K., and Inui K. mRNA distribution and membrane localization of the OAT-K1 organic anion transporter in rat renal tubules. FEBS Lett. 407 (1997) 127-131
36. Meier P.J., Eckhardt U., Schroeder A., Hagenbuch B., and Stieger B. Substrate specificity of sinusoidal bile acid and organic anion uptake systems in rat and human liver. Hepatology 26 (1997) 1667-1677
37. Nakagawa H., Hirata T., Terada T., Jutabha P., Miura D., Harada J.H., Inoue K., Anzai N., Endou H., Inui K., Kanai Y., and Koizumi A. Roles of organic anion transporters in the renal excretion of perfluorooctanoic acid. Basic Clin. Pharmacol. Toxicol. 103 (2008) 1-8
38. Ohmori K., Kudo N., Katayama K., and Kawashima Y. Comparison of the toxicokinetics between perfluorocarboxylic acids with different carbon chain length. Toxicology 184 (2003) 135-140
39. Olsen G.W., Burris J.M., Ehresman D.J., Froehlich J.W., Seacat A.M., Butenhoff J.L., and Zobel L.R. Half-life of serum elimination of perfluorooctanesulfonate,perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ. Health Perspect. 115 (2007) 1298-1305
40. Poirier A., Lave T., Portmann R., Brun M.E., Senner F., Kansy M., Grimm H.P., and Funk C. Design, data analysis, and simulation of in vitro drug transport kinetic experiments using a mechanistic in vitro model. Drug Metab. Dispos. 36 (2008) 2434-2444
41. Prevedouros K., Cousins I.T., Buck R.C., and Korzeniowski S.H. Sources, fate and transport of perfluorocarboxylates. Environ. Sci. Technol. 40 (2006) 32-44
42. Sabolic I., Asif A.R., Budach W.E., Wanke C., Bahn A., and Burckhardt G. Gender differences in kidney function. Pflugers Arch. 455 (2007) 397-429
43. Satoh H., Yamashita F., Tsujimoto M., Murakami H., Koyabu N., Ohtani H., and Sawada Y. Citrus juices inhibit the function of human organic anion-transporting polypeptide OATP-B. Drug Metab. Dispos. 33 (2005) 518-523
44. Shi X., Bai S., Ford A.C., Burk R.D., Jacquemin E., Hagenbuch B., Meier P.J., and Wolkoff A.W. Stable inducible expression of a functional rat liver organic anion transport protein in HeLa cells. J. Biol. Chem. 270 (1995) 25591-25595
45. Shitara Y., Sugiyama D., Kusuhara H., Kato Y., Abe T., Meier P.J., Itoh T., and Sugiyama Y. Comparative inhibitory effects of different compounds on rat Oatp1 (Slc21a1)-and Oatp2 (Slc21a5)-mediated transport. Pharm. Res. 19 (2002) 147-153
46. Sugiyama D., Kusuhara H., Shitara Y., Abe T., Meier P.J., Sekine T., Endou H., Suzuki H., and Sugiyama Y. Characterization of the efflux transport of 17beta-estradiol-d-17beta-glucuronide from the brain across the blood-brain barrier. J. Pharmacol. Exp. Ther. 298 (2001) 316-322
47. Vanden Heuvel J.P., Kuslikis B.I., Van Rafelghem M.J., and Peterson R.E. Tissue distribution, metabolism, and elimination of perfluorooctanoic acid in male and female rats. J. Biochem. Toxicol. 6 (1991) 83-92
48. Wambaugh J.F., Barton H.A., and Setzer R.W. Comparing models for perfluorooctanoic acid pharmacokinetics using Bayesian analysis. J. Pharmacokinet. Pharmacodyn. 35 (2008) 683-712
49. Wang P., Hata S., Xiao Y., Murray J.W., and Wolkoff A.W. Topological assessment of oatp1a1: a 12-transmembrane domain integral membrane protein with three N-linked carbohydrate chains. Am. J. Physiol. Gastrointest. Liver Physiol. 294 (2008) G1052-1059
50. Youngblood G.L., and Sweet D.H. Identification and functional assessment of the novel murine organic anion transporter Oat5 (Slc22a19) expressed in kidney. Am. J. Physiol. Renal Physiol. 287 (2004) F236-244