P-glycoprotein,multidrug resistance-associated proteins and human organic anion transporting polypeptide influence the intracellular accumulation of atazanavir

Janneh O. , Owen A. , Chandler B. Modulation of the intracellular accumulation of saquinavir in peripheral blood mononuclear cells by inhibitors of MRP1, MRP2, P-gp and BCRP. AIDS 2005; 19: 2097–2102.

Janneh O. , Jones E. , Chandler B. , Owen A. , Khoo S.H. Inhibition of P-glycoprotein and multidrug resistance-associated proteins modulates the intracellular concentration of lopinavir in cultured CD4 T cells and primary human lymphocytes. J Antimicrob Chemother 2007; 60: 987–993.

Bousquet L. , Roucairol C. , Hembury A. Comparison of ABC transporter modulation by atazanavir in lymphocytes and human brain endothelial cells: ABC transporters are involved in the atazanavir-limited passage across an in vitro human model of the blood–brain barrier. AIDS Res Hum Retroviruses 2008; 24: 1147–1154.

Su Y. , Zhang X. , Sinko P.J. Human organic aniontransporting polypeptide OATP-A (SLC21A3) acts in concert with P-glycoprotein and multidrug resistance protein 2 in the vectorial transport of Saquinavir in Hep G2 cells. Mol Pharm 2004; 1: 49–56.

Zhang L. , Gorset W. , Washington C.B. , Blaschke T.F. , Kroetz D.L. , Giacomini K.M. Interactions of HIV protease inhibitors with a human organic cation transporter in a mammalian expression system. Drug Metab Dispos 2000; 28: 329–334.

Janneh O. , Hartkoorn R.C. , Jones E. Cultured CD4T cells and primary human lymphocytes express hOATPs: intracellular accumulation of saquinavir and lopinavir. Br J Pharmacol 2008; 155: 875–883.

Izzedine H. , Launay-Vacher V. , Deray G. Renal tubular transporters and antiviral drugs: an update. AIDS 2005; 19: 455–462.

Huisman M.T. , Smit J.W. , Wiltshire H.R. , Hoetelmans R.M. , Beijnen J.H. , Schinkel A.H. P-glycoprotein limits oral availability, brain, and fetal penetration of saquinavir even with high doses of ritonavir. Mol Pharmacol 2001; 59: 806–813.

Park S. , Sinko P.J. P-glycoprotein and mutlidrug resistance-associated proteins limit the brain uptake of saquinavir in mice. J Pharmacol Exp Ther 2005; 312: 1249–1256.

Kim A.E. , Dintaman J.M. , Waddell D.S. , Silverman J.A. Saquinavir, an HIV protease inhibitor, is transported by P-glycoprotein. J Pharmacol Exp Ther 1998; 286: 1439–1445.

Lee C.G. , Gottesman M.M. , Cardarelli C.O. HIV-1 protease inhibitors are substrates for the MDR1 multidrug transporter. Biochemistry 1998; 37: 3594–3601.

Washington C.B. , Duran G.E. , Man M.C. , Sikic B.I. , Blaschke T.F. Interaction of anti-HIV protease inhibitors with the multidrug transporter P-glycoprotein (P-gp) in human cultured cells. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 19: 203–209.

Jones K. , Bray P.G. , Khoo S.H. P-Glycoprotein and transporter MRP1 reduce HIV protease inhibitor uptake in CD4 cells: potential for accelerated viral drug resistance? AIDS 2001; 15: 1353–1358.

Huisman M.T. , Smit J.W. , Crommentuyn K.M. Multidrug resistance protein 2 (MRP2) transports HIV protease inhibitors, and transport can be enhanced by other drugs. AIDS 2002; 16: 2295–2301.

Agarwal S. , Pal D. , Mitra A.K. Both P-gp and MRP2 mediate transport of lopinavir, a protease inhibitor. Int J Pharm 2007; 339: 139–147.

Gutmann H. , Fricker G. , Drewe J. , Toeroek M. , Miller D.S. Interactions of HIV protease inhibitors with ATP-dependent drug export proteins. Mol Pharmacol 1999; 56: 383–389.

Ronaldson P.T. , Lee G. , Dallas S. , Bendayan R. Involvement of P-glycoprotein in the transport of saquinavir and indinavir in rat brain microvessel endothelial and microglia cell lines. Pharm Res 2004; 21: 811–818.

Bachmeier C.J. , Spitzenberger T.J. , Elmquist W.F. , Miller D. W. . Quantitative assessment of HIV-1 protease inhibitor interactions with drug efflux transporters in the blood-brain barrier. Pharm Res 2005; 22: 1259–1268.

Williams G.C. , Liu A. , Knipp G. , Sinko P.J. Direct evidence that saquinavir is transported by multidrug resistance-associated protein (MRP1) and canalicular multispecific organic anion transporter (MRP2). Antimicrob Agents Chemother 2002; 46: 3456–3462.

Shiraki N. , Hamada A. , Yasuda K. , Fujii J. , Arimori K. , Nakano M. Inhibitory effect of human immunodeficiency virus protease inhibitors on multidrug resistance transporter P-glycoproteins. Biol Pharm Bull 2000; 23: 1528–1531.

Chandler B. , Almond L. , Ford J. The effects of protease inhibitors and nonnucleoside reverse transcriptase inhibitors on P-glycoprotein expression in peripheral blood mononuclear cells in vitro. J Acquir Immune Defic Syndr 2003; 33: 551–556.

Dupuis M.L. , Flego M. , Molinari A. , Cianfriglia M. Saquinavir induces stable and functional expression of the multidrug transporter P-glycoprotein in human CD4 T-lymphoblastoid CEMrev cells. HIV Med 2003; 4: 338–345.

Storch C.H. , Theile D. , Lindenmaier H. , Haefeli W.E. , Weiss J. Comparison of the inhibitory activity of anti-HIV drugs on P-glycoprotein. Biochem Pharmacol 2007; 73: 1573–1581.

Gupta A. , Zhang Y. , Unadkat J.D. , Mao Q. HIV protease inhibitors are inhibitors but not substrates of the human breast cancer resistance protein (BCRP/ABCG2). J Pharmacol Exp Ther 2004; 310: 334–341.

Weiss J. , Rose J. , Storch C.H. Modulation of human BCRP (ABCG2) activity by anti-HIV drugs. J Antimicrob Chemother 2007; 59: 238–245.

Colombo S. , Soranzo N. , Rotger M. Influence of ABCB1, ABCC1, ABCC2, and ABCG2 haplotypes on the cellular exposure of nelfinavir in vivo. Pharmacogenet Genomics 2005; 15: 599–608.

Wang X. , Furukawa T. , Nitanda T. Breast cancer resistance protein (BCRP/ABCG2) induces cellular resistance to HIV-1 nucleoside reverse transcriptase inhibitors. Mol Pharmacol 2003; 63: 65–72.

Hsu A. , Granneman G.R. , Bertz R.J. Ritonavir. Clinical pharmacokinetics and interactions with other anti-HIV agents. Clin Pharmacokinet 1998; 35: 275–291.

Ford J. , Boffito M. , Maitland D. Influence of atazanavir 200 mg on the intracellular and plasma pharmacokinetics of saquinavir and ritonavir 1600/100 mg administered once daily in HIV-infected patients. J Antimicrob Chemother 2006; 58: 1009–1016.

Perloff E.S. , Duan S.X. , Skolnik P.R. , Greenblatt D.J. , von Moltke L.L. Atazanavir: effects on P-glycoprotein transport and CYP3A metabolism in vitro. Drug Metab Dispos 2005; 33: 764–770.

Chinn L.W. , Gow J.M. , Tse M.M. , Becker S.L. , Kroetz D.L. Interindividual variability in the effect of atazanavir and saquinavir on the expression of lymphocyte P-glycoprotein. J Antimicrob Chemother 2007; 60: 61–67.

Pick A. , Muller H. , Wiese M. Structure-activity relationships of new inhibitors of breast cancer resistance protein (ABCG2). Bioorg Med Chem 2008; 16: 8224–8236.

Kuhnle M. , Egger M. , Muller C. Potent and selective inhibitors of breast cancer resistance protein (ABCG2) derived from the P-glycoprotein (ABCB1) modulator tariquidar. J Med Chem 2009; 52: 1190–1197.

Mistry P. , Stewart A.J. , Dangerfield W. In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Res 2001; 61: 749–758.

Damle B.D. , Sridhar R. , Desai P.B. Dipyridamole modulates multidrug resistance and intracellular as well as nuclear levels of doxorubicin in B16 melanoma cells. Int J Cancer 1994; 56: 113–118.

Verstuyft C. , Strabach S. , El-Morabet H. Dipyridamole enhances digoxin bioavailability via P-glycoprotein inhibition. Clin Pharmacol Ther 2003; 73: 51–60.

Kawamura K. , Yamasaki T. , Yui J. In vivo evaluation of P-glycoprotein and breast cancer resistance protein modulation in the brain using [(11)C]gefitinib. Nucl Med Biol 2009; 36: 239–246.

Chiba P. , Ecker G. , Schmid D. Structural requirements for activity of propafenone-type modulators in P-glycoprotein-mediated multidrug resistance. Mol Pharmacol 1996; 49: 1122–1130.

Tahara H. , Kusuhara H. , Chida M. , Fuse E. , Sugiyama Y. Is the monkey an appropriate animal model to examine drug–drug interactions involving renal clearance? Effect of probenecid on the renal elimination of H2 receptor antagonists. J Pharmacol Exp Ther 2006; 316: 1187–1194.

Sakamoto K. , Mikami H. , Kimura J. Involvement of organic anion transporting polypeptides in the toxicity of hydrophilic pravastatin and lipophilic fluvastatin in rat skeletal myofibres. Br J Pharmacol 2008; 154: 1482–1490.

Jager W. , Winter O. , Halper B. Modulation of liver canalicular transport processes by the tyrosine-kinase inhibitor genistein: implications of genistein metabolism in the rat. Hepatology 1997; 26: 1467–1476.

Bobrowska-Hagerstrand M. , Wrobel A. , Rychlik B. Monitoring of MRP-like activity in human erythrocytes: inhibitory effect of isoflavones. Blood Cells Mol Dis 2001; 27: 894–900.

Evans A.M. Influence of dietary components on the gastrointestinal metabolism and transport of drugs. Ther Drug Monit 2000; 22: 131–136.

Cooray H.C. , Janvilisri T. , van Veen H.W. , Hladky S.B. , Barrand M.A. Interaction of the breast cancer resistance protein with plant polyphenols. Biochem Biophys Res Commun 2004; 317: 269–275.

Wang X. , Wolkoff A.W. , Morris M.E. Flavonoids as a novel class of human organic anion-transporting polypeptide OATP1B1 (OATP-C) modulators. Drug Metab Dispos 2005; 33: 1666–1672.

Nguyen H. , Zhang S. , Morris M.E. Effect of flavonoids on MRP1-mediated transport in Panc-1 cells. J Pharm Sci 2003; 92: 250–257.

Enokizono J. , Kusuhara H. , Sugiyama Y. Effect of breast cancer resistance protein (Bcrp/Abcg2) on the disposition of phytoestrogens. Mol Pharmacol 2007; 72: 967–975.

Hodges M. , Yikilmaz E. , Patterson G. An iron regulatory-like protein expressed in Plasmodium falciparum displays aconitase activity. Mol Biochem Parasitol 2005; 143: 29–38.

Gibbs J.E. , Thomas S.A. The distribution of the anti-HIV drug, 2'3’-dideoxycytidine (ddC), across the blood-brain and blood-cerebrospinal fluid barriers and the influence of organic anion transport inhibitors. J Neurochem 2002; 80: 392–404.

Sanchez Mdel C. , Lopez P. , Velez R. , Yamamura Y. P-glycoprotein expression in HTLV-III cells after treatment with HIV-1 protease inhibitors. Ethn Dis 2008; 18 Suppl 2: S2-60–64.

Profit l , Eagling V.A. , Back D.J. Modulation of P-glycoprotein function in human lymphocytes and Caco-2 cell monolayers by HIV-1 protease inhibitors. AIDS 1999; 13: 1623–1627.

Cremaschi D. , Meyer G. , Rossetti C. , Botta G. , Palestini P. The nature of the neutral Na⁺-Cl(^-)-coupled entry at the apical membrane of rabbit gallbladder epithelium: I. Na⁺/H⁺, Cl^-/ HCO3- double exchange and Na⁺-Cl^- symport. J Membr Biol 1987; 95: 209–218.

Joiner C.H. , Jiang M. , Claussen W.J. , Roszell N.J. , Yasin Z. , Franco R.S. Dipyridamole inhibits sickling-induced cation fluxes in sickle red blood cells. Blood 2001; 97: 3976–3983.

Letschert K. , Faulstich H. , Keller D. , Keppler D. Molecular characterization and inhibition of amanitin uptake into human hepatocytes. Toxicol Sci 2006; 91: 140–149.

Smith N.F. , Acharya M.R. , Desai N. , Figg W.D. , Sparreboom A. Identification of OATP1B3 as a high-affinity hepatocellular transporter of paclitaxel. Cancer Biol Ther 2005; 4: 815–818.

Zhang D. , Chando T.J. , Everett D.W. , Patten C.J. , Dehal S.S. , Humphreys W.G. In vitro inhibition of UDP glucuronosyltransferases by atazanavir and other HIV protease inhibitors and the relationship of this property to in vivo bilirubin glucuronidation. Drug Metab Dispos 2005; 33: 1729–1739.

Lankisch T.O. , Moebius U. , Wehmeier M. Gilbert's disease and atazanavir: from phenotype to UDP-glucuronosyltransferase haplotype. Hepatology 2006; 44: 1324–1332.

Chen J. , Lin H. , Hu M. Absorption and metabolism of genistein and its five isoflavone analogs in the human intestinal Caco-2 model. Cancer Chemother Pharmacol 2005; 55: 159–169.

Versantvoort C.H. , Rhodes T. , Twentyman P.R. Acceleration of MRP-associated efflux of rhodamine 123 by genistein and related compounds. Br J Cancer 1996; 74: 1949–1954.

Maubach J. , Depypere H.T. , Goeman J. Distribution of soy-derived phytoestrogens in human breast tissue and biological fluids. Obstet Gynecol 2004; 103: 892–898.

Bousquet L. , Roucairol C. , Hembury A. Comparison of ABC transporter modulation by atazanavir in lymphocytes and human brain endothelial cells: ABC transporters are involved in the atazanavir-limited passage across an in vitro human model of the blood-brain barrier. AIDS Res Hum Retroviruses 2008; 24: 1147–1154.

Campbell S.D. , de Morais S.M. , Xu J.J. Inhibition of human organic anion transporting polypeptide OATP 1B1 as a mechanism of drug-induced hyperbilirubinemia. Chem Biol Interact 2004; 150: 179–187.

McRae M.P. , Lowe C.M. , Tian X. Ritonavir, saquinavir, and efavirenz, but not nevirapine, inhibit bile acid transport in human and rat hepatocytes. J Pharmacol Exp Ther 2006; 318: 1068–1075.