Combination of tenofovir and emtricitabine plus efavirenz: In vitro modulation of ABC transporter and intracellular drue accumulation

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 3, 2009, Pages 896-902

  Bousquet, Laurence ^a,b   Pruvost, Alain ^a   Guyot, Anne Cécile ^a   Farinotti, Robert ^b,c   Mabondzo, Aloïse ^a  

^a Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; EFAVIRENZ; EMTRICITABINE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; MULTIDRUG RESISTANCE PROTEIN 6; ORGANIC ANION TRANSPORTER; TENOFOVIR;

ARTICLE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TANDEM MASS SPECTROMETRY;

EID: 62949174356     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00733-08     Document Type: Article

References (58)

1. Albermann, N., F. H. Schmitz-Winnenthal, K. Z'graggen, C. Volk, M. M. Hoffmann, W. E. Haefeli, and J. Weiss. 2005. Expression of the drug transporters MDR1/ABCB1, MRP1/ABCC1. MRP2/ABCC2, BCRP/ABCG2, and PXR in peripheral blood mononuclear cells and their relationship with the expression in intestine and liver. Biochem. Pharmacol. 70:949-958.
2. Arribas, J. R., A. L. Pozniak, J. E. Gallant, E. Dejesus, B. Gazzard, R. E. Campo, S. S. Chen, D. McColl, C. B. Holmes, J. Enejosa, J. J. Toole, and A. K. Cheng. 2007. Tenofovir disoproxil fumarate, emtricitabine. and efavirenz compared with zidowdine/lamivudine and efavirenz in treatment- naive patients: 144-week analysis. J. Acquir. Immune. Defic. Syndr. 47:74-78.
3. Bartlett, J. A., S. S. Chen, and J. B. Quinn. 2007. Comparative efficacy of nucleoside/nucleotide reverse transcriptase inhibitors in combination with efavirenz: results of a systematic overview. HIV Clin. Trials 8:221-226.
4. Belinsky, M. G., Z. S. Chen, I. Shchaveleva, H. Zeng, and G. D. Kruh. 2002. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res. 62:6172-6177.
5. Belliard, A. M., S. Tardivel, R Farinotti, B. Lacour, and C. Leroy. 2002. Effect of hr-lL2 treatment on intestinal P-glycoprotein expression and activity in Caco-2 cells. J. Pharm. Pharmacol. 54:1103-1109.
6. Benech, H., F. Theodoro, A. Herbet, N. Page, D. Sehlemmer, A. Pruvost, J. Grassi, and J. R. Deverre. 2004. Peripheral blood mononuclear cell counting using a DNA-detection-based method. Anal. Biochem. 330:172-174.
7. Berruet, N., S. Sentenac, D. Auchere, F. Gimenez, R. Farinotti, and C. Fernandez. 2005. Effect of efavirenz on intestinal P-glycoprotein and hepatic p450 function in rats. J. Pharm. Pharm. Sci. 8:226-234.
8. Borroto-Esoda, K., J. E. Vela, F. Myrick, A. S. Ray, and M. D. Miller. 2006. In vitro evaluation of the anti-HIV activity and metabolic interactions of tenofovir and emtricitabine. Antivir. Ther. 11:377-384.
9. Chandler, B., L. Almond, J. Ford, A. Owen, P. Hoggard, S. Khoo, and D. Back. 2003. 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. 33:551-556.
10. Chearskul, P., C. Rongkavilit, H. Al-Tatari, and B. Asmar. 2006. New antiretroviral drugs in clinical use. Indian J. Pediatr. 73:335-341.
11. Choudhuri, S., and C. D. Klaassen. 2006. Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int. J. Toxicol. 25:231-259.
12. De Moerloose, B., C. Dhooge, and J. Philippe. 1999. Discordance of P- glycoprotein expression and function in acute leukemia. Adv. Exp. Med. Biol. 457:107-118.
13. Dirson, G., C. Fernandez, P. Hindlet, F. Roux, M. German-Fattal, F. Gimenez, and R. Farinotti. 2006. Efavirenz does not interact with the ABCB1 transporter at the blood-brain barrier. Pharm. Res. 23:1525-1532.
14. Faucette, S. R, T. C. Zhang, R. Moore, T. Sueyoshi, C. J. Omiecinski, E. L. LeCluyse, M. Negishi, and H. Wang. 2007. Relative activation of human pregnane X receptor versus constitutive androstane receptor defines distinct classes of CYP2B6 and CYP3A4 inducers. J. Pharmacol. Exp. Ther. 320:72-80.
15. Ford, J., E. R. Meaden, P. G. Hoggard, M. Dalton, P. Newton, I. Williams, S, H. Khoo, and D. J. Back. 2003. Effect of protease inhibitor-containing regimens on lymphocyte multidrug resistance transporter expression. J. Antimicrob. Chemother. 52:354-358.
16. Gekeler, V., W. Ise, K. H. Sanders, W. R Ulrich, and J. Beck. 1995. The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208:345- 352.
17. Gottesman, M. M., C. Cardarelli, S. Goldenberg, T. Licht, and I. Pastan. 1998. Selection and maintenance of multidrug-resistant cells. Methods Enzymol. 292:248-258.
18. Hammer, S. M., M. S. Saag, M. Schechter, J. S. Montaner, R T. Schooley, D. M. Jacobsen, M. A. Thompson, C. C. Carpenter, M. A. Fischl, B. G. Gazzard, J. M. Gatell, M. S. Hirsch, D. A. Katzenstein, D. D. Richman, S. Vella, P. G. Yeni, and P. A. Volberding. 2006. Treatment for adult HIV infection: 2006 recommendations of the International AIDS Society-USA Panel. Top. HIV Med. 14:827-843.
19. Hayashi, A., H. Suzuki, K. Itoh, M. Yamamoto, and Y. Sugiyama. 2003. Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 310:824-829.
20. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
21. Hollo, Z., L, Homolya, T. Hegedus, and B. Sarkadi. 1996. Transport properties of the multidrug resistance-associated protein (MRP) in human tumour cells. FEBS Lett. 383:99-104.
22. Homolya, L., A. Varadi, and B. Sarkadi. 2003. Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 17:103-114.
23. Huisman, M. T., J. W. Smit, H. R. Wiltshire, R M. Hoetelmans, J. H. Beijnen, and A. H. Schinkel. 2001. P-glycoprotein limits oral availability, brain, and fetal penetration of saquinavir even with high doses of ritonavir. Mol. Pharmacol. 59:806-813.
24. Imaoka, T., H. Kusuhara, M. Adachi, J. D. Schuetz, K. Takeuchi, and Y. Sugiyama. 2007. Functional involvement of multidrug resistance-associated protein 4 (MRP4/ABCC4) in the renal elimination of the antiviral drugs adefovir and tenofovir. Mol. Pharmacol. 71:619-627.
25. Jiang, Q., Y. Matsuzaki, K. Li, and J. Uitto. 2006. Transcriptional regulation and characterization of the promoter region of the human ABCC6 gene. J. Investig. Dermatol. 126:325-335.
26. Jorajuria, S., N. Reuddre-Bosquet, F. Becher, S. Martin, F. Poreheray, A. Garrigues, A. Mabondzo, H. Benech, J. Grassi, S. Orlowski, D. Dormont, and P. Clayette. 2004. ATP binding cassette multidrug transporters limit the anti-HlV activity of zidovudine and indinavir in infected human macrophages. Antivir. Ther. 9:519-528.
27. Kast, H. R, B. Goodwin, P. T. Tarr, S. A. Jones, A. M. Anisfeld, C. M. Stoltz, P. Tontonoz, S. Kliewer, T. M. Willson, and P. A. Edwards. 2002. Regulation of multidrug resistance-associated protein 2 (ABCC2) by the nuclear receptors pregnane X receptor, farnesoid X-activated receptor, and constitutive androstane receptor. J. Biol. Chem. 277:2908-2915.
28. Kaufifmann, H. M., S. Pfannschmidt, H. Zoller, A. Benz, B. Vorderstemann, J. I. Webster, and D. Schrenk. 2002. Influence of redox-active compounds and PXR-activators on human MRP1 and MRP2 gene expression. Toxicology 171:137-146.
29. Killingley, B., and A. Pozniak. 2007. The first once-daily single-tablet regimen for the treatment of HIV-infected patients. Drugs Today (Barcelona) 43:427-442.
30. Klein, I., B. Sarkadi, and A. Varadi. 1999. An inventory of the human ABC proteins. Biochim. Biophys. Acta 1461:237-262.
31. Krishna, R, and L. D. Mayer. 2000. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur. J. Pharm. Sci. 11:265-283.
32. Laupeze, B., L. Amiot, L. Payen, B. Drenou, J. M. Grosset, G. Lehne, R. Fauchet, and O, Fardel, 2001. Multidrug resistance protein (MRP) activity in normal mature leukocytes and CD34-positive hematopoietic cells from peripheral blood. Life Sci. 68:1323-1331.
33. Lee, C, G., M, M, Gottesman, C. O. Cardarelli, M, Ramachandra, K, T. Jeang, S. V. Ambudkar, I. Pastan, and S. Dey. 1998. H1V-1 protease inhibitors are substrates for the MDR1 multidrug transporter. Biochemistry 37: 3594-3601.
34. Legrand, O., G. Simonin, J. Y. Perrot, R Zittoun, and J. P. Marie. 1998. Pgp and MRP activities using calcein-AM are prognostic factors in adult acute myeloid leukemia patients. Blood 91:4480-4488.
35. Levi, M., and A. Pruvost. 2006. Sensitive HPLC-ESI-MS/MS method for the simultaneous quantitative determination of abacavir, lamivudine and teno- fovir in human plasma, abstr. 69. Abstr. 7th Int. Workshop Clin. Pharmacol. HIV Ther.
36. Loscher, W., and H. Potschka. 2005. Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2:86-98.
37. Magnarin, M., M. Morelli, A. Rosati, F. Bartoli, L. Candussio, T. Giraldi, and G. Decorti. 2004. Induction of proteins involved in multidrug resistance (P-glycoprotein, MRP1, MRP2, LRP) and of CYP 3A4 by rifampicin in LLC-PK1 cells. Eur. J. Pharmacol. 483:19-28.
38. Masuhr, A., M. Mueller, V. Simon, T. Zwingers, M. Kurowski, H. Jessen, E. Lauenroth-Mai, A. Moll, D. Schranz, C. Moecklinghoff, and K. Arasteh. 2002. Predictors of treatment failure during highly active antiretroviral therapy (racing trial). Eur. J. Med. Res. 7:341-346.
39. Meaden, E. R., P. G. Hoggard, S. H. Khoo, and D. J. Back. 2002. Determination of P-gp and MRP1 expression and function in peripheral blood mononuclear cells in vivo. J Immunol. Methods 262:159-165.
40. Muredda, M., K. Nunoya, R. A. Burtch-Wright, E. U. Kurz, S. P. Cole, and R G. Deeley. 2003. Cloning and characterization of the murine and rat mrpl promoter regions. Mol. Pharmacol. 64:1259-1269.
41. Ozben, T. 2006. Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett. 580:2903-2909.
42. Perloff, M. D., L. L. Von Moltke, J. E. Marchand, and D. J. Greenblatt. 2001. Ritonavir induces P-glycoprotein expression, multidrug resistance-associated protein (MRP1) expression, and drug transporter-mediated activity in a human intestinal cell line. J. Pharm. Sci. 90:1829-1837.
43. Pozniak, A. L., J. E. Gallant, E. Dejesus, J. R Arribas, B. Gazzard, R. E. Campo, S. S. Chen, D. McColl, J. Enejosa, J. J. Toole, and A. K. Cheng. 2006. Tenofovir disoproxil fumarate, emtricitabine, and efavirenz versus fixed-dose zidovudineAamivudine and efavirenz in antiretroviral-naive patients: virologic, immunologic, and morphologic changes-a 96-week analysis. J. Acquir. Immune. Defic. Syndr. 43:535-540.
44. Pruvost, A., F. Theodoro, L. Agrofoglio, E. Negredo, and H. Benech. 2008. Specificity enhancement with LC-positive ESI-MS/MS for the measurement of nucleotides: application to the quantitative determination of carbovir triphosphate, lamivudine triphosphate and tenofovir diphosphate in human peripheral blood mononuclear cells. J. Mass Spectrom. 43:224-233.
45. Rautio, J., J. E. Humphreys, L. O. Webster, A. Balakrishnan, J. P. Keogh, J. R. Kunta, C. J. Serabjit-Singh, and J. W. Polli. 2006. In vitro P-glycoprotein inhibition assays for assessment of clinical drug interaction potential of new drug candidates: a recommendation for probe substrates. Drug Metab. Dispos. 34:786-792.
46. Ray, A. S., T. Cihlar, K. L. Robinson, L. Tong, J. E. Vela, M. D. Fuller, L. M. Wieman, E. J. Eisenberg, and G. R Rhodes. 2006. Mechanism of active renal tubular efflux of tenofovir. Antimicrob. Agents Chemother. 50:3297-3304.
47. Ritter, C. A., G. Jedlitschky, S. H. Meyer Zu, M. Grube, K. Kock, and H. K. Kroemer. 2005. Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5). Drug Metab. Rev. 37:253-278.
48. Seelig, A., X. L. Blatter, and F. Wohnsland. 2000. Substrate recognition by P-glycoprotein and the multidrug resistance-associated protein MRP1: a comparison. Int. J. Clin. Pharmacol. Ther. 38:111-121.
49. Storch, C. H., D. Theile, H. Lindenmaier, W. E. Haefeli, and J. Weiss. 2007. Comparison of the inhibitory activity of anti-HlV drugs on P-glycoprotein. Biochem. Pharmacol. 73:1573-1581.
50. Stormer, E., L. L. Von Moltke, M. D. Perloff, and D. J. Greenblatt. 2002. Differential modulation of P-glycoprotein expression and activity by non- nucleoside HIV-1 reverse transcriptase inhibitors in cell culture. Pharm. Res. 19:1038-1045.
51. Synold, T. W., I. Dussault, and B. M. Forman. 2001. The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nat. Med. 7:584-590.
52. Uwai, Y., H. Ida, Y. Tsuji, T. Katsura, and K. Inui. 2007. Renal transport of adefovir, cidofovir, and tenofovir by SLC22A family members (hOATl, hQAT3, and hOCT2). Pharm. Res. 24:811-815.
53. Veau, C, L. Faivre, S. Tardivel, M. Soursac, H. Banide, B. Lacour, and R. Farinotti. 2002. Effect of interleukin-2 on intestinal P-glycoprotein expression and functionality in mice. J. Pharmacol. Exp. Ther. 302:742-750.
54. Vishnuvardhan, D., L. L, Moltke, C. Richert, and D. J. Greenblatt. 2003. Lopinavir: acute exposure inhibits P-glycoprotein; extended exposure induces P-glycoprotein. AIDS 17:1092-1094.
55. Weiss, J., S. M. Dormann, M. Martin-Facklam, C. J. Kerpen, N. Ketabi- Kiyanvash, and W. E. Haefeli. 2003. Inhibition of P-glycoprotein by newer antidepressants. J. Pharmacol. Exp. Ther. 305:197-204.
56. Weiss, J., D. Theile, N. Ketabi-Kiyanvash, H. Lindenmaier, and W. E. Haefeli. 2007. Inhibition of MRP1/ABCC1, MRP2/ABCC2, and MRP3/ ABCC3 by nucleoside, nucleotide, and non-nucleoside reverse transcriptase inhibitors. Drug Metab. Dispos. 35:340-344.
57. Weiss, J., N. Weis, N. Ketabi-Kiyanvash, C. H. Storch, and W. E. Haefeli. 2008. Comparison of the induction of P-glycoprotein activity by nucleotide, nucleoside, and non-nucleoside reverse transcriptase inhibitors. Eur. J. Pharmacol. 579:104-109.
58. Wijnholds, J., C. A. Mol, L. van Deemter, M. de Haas, G. L. Seheffer, F. Baas, J. H. Beijnen, R J. Seheper, S. Hatse, E. De Clercq, J. Balzarini, and P. Borst. 2000. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. USA 97:7476-7481.