MRP (ABCC) transporters-mediated efflux of anti-HIV drugs, saquinavir and zidovudine, from human endothelial cells

Experimental Biology and Medicine

Volumn 233, Issue 9, 2008, Pages 1149-1160

  Eilers, Mark ^a   Roy, Upal ^a   Mondal, Debasis ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Anti retroviral drugs; Brain reservoirs; HIV 1; Human endothelial cells; MDR 1; MRP

Indexed keywords

ABC TRANSPORTER; CALCEIN; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; SAQUINAVIR; TRITIUM; VERAPAMIL; VERLUKAST; ZIDOVUDINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; FLUORESCEIN DERIVATIVE;

AORTA; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG MONITORING; DRUG RETENTION; DRUG TRANSPORT; ENDOTHELIUM CELL; GENE EXPRESSION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR SPACE; MICROVASCULATURE; PROTEIN EXPRESSION; PROTEIN TRANSPORT; PULMONARY ARTERY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN; BRAIN; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTI-HIV AGENTS; AORTA; BRAIN; CELLS, CULTURED; ENDOTHELIAL CELLS; FLUORESCEINS; GENE EXPRESSION REGULATION; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; SAQUINAVIR; ZIDOVUDINE;

EID: 52649110113     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0802-RM-59     Document Type: Article

References (65)

1. Pomerantz RJ. Reservoirs, sanctuaries and residual disease: the hiding spots of HIV-1. HIV Clin Trials 4(2):137-143, (Review), 2003.
2. Lambotte O, Deiva K, Tardieu M. HIV-1 persistence, viral reservoir and the central nervous system in the HAART era. Brain Pathol 13(1): 95-103, (Review), 2003.
3. Tobin NH, Learn GH, Holte SE, Wang Y, Melvin AJ, McKernan JL, Pawluk DM, Mohan KM, Lewis PF, Mullins JI, Frenkel LM. Evidence that low-level viremias during effective highly active antiretroviral therapy result from two processes: expression of archival virus and replication of virus. J Virol 79(15):9625-9634, 2005.
4. Honda M, Oka S. Current therapy for human immunodeficiency virus infection and acquired immunodeficiency syndrome. Int J Hematol 84(1):18-22, (Review), 2006.
5. Boyd M, Reiss P. The long-term consequences of antiretroviral therapy: a review. J HIV Ther 11(2):26-35, (Review), 2006.
6. Walubo A. The role of cytochrome P450 in antiretroviral drug interactions. Expert Opin Drug Metab Toxicol 3(4):583-598, (Review), 2007.
7. Thomas SA. Anti-HIV drug distribution to the central nervous system. Curr Pharm Des 10(12):1313-1324, 2004.
8. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment and Trojan horses. Clin Cancer Res 13(6):1663-1674, (Review), 2007.
9. Oswald S, Grube M, Siegmund W, Kroemer HK. Transporter-mediated uptake into cellular compartments. Xenobiotica 37(10-11):1171-1195, 2007.
10. Scherrmann JM. Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin Drug Metab Toxicol 1(2):233-246, 2005.
11. Girardin F. Membrane transporter proteins: a challenge for CNS drug development. Dialogues Clin Neurosci 8(3):311-321, (Review), 2006.
12. Hollenstein K, Dawson RJ, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17(4):412-418, 2007.
13. Xu J, Peng H, Zhang JT. Human multidrug transporter ABCG2, a target for sensitizing drug resistance in cancer chemotherapy. Curr Med Chem 14(6):689-701, 2007.
14. Yasuhisa K, Shin-ya M, Michinori M, Kazumitsu U. Mechanism of multidrug recognition by MDR1/ABCB1. Cancer Sci 98(9):1303-1310, 2007.
15. Janneh O, Jones E, Chandler B, Owen A, Khoo SH. 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 60(5):987-993, 2007.
16. Chaillou S, Durant J, Garraffo R, Georgenthum E, Roptin C, Clevenbergh P, Dunais B, Mondain V, Roger PM, Dellamonica P. Intracellular concentration of protease inhibitors in HIV-1-infected patients: correlation with MDR-1 gene expression and low dose of ritonavir. HIV Clin Trials 3(6):493-501, 2002.
17. Agarwal S, Pal D, Mitra AK. Both P-gp and MRP2 mediate transport of Lopinavir, a protease inhibitor. Int J Pharm 339(1-2):139-147, 2007.
18. Leslie EM, Deeley RG, Cole SP. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2 and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204(3):216-237, 2005.
19. Maher JM, Slitt AL, Cherrington NJ, Cheng X, Klaassen CD. Tissue distribution and hepatic and renal ontogeny of the multidrug resistance- associated protein (Mrp) family in mice. Drug Metab Dispos 33(7): 947-955, 2005.
20. Tanaka Y, Slitt AL, Leazer TM, Maher JM, Klaassen CD. Tissue distribution and hormonal regulation of the breast cancer resistance protein (Bcrp/Abcg2) in rats and mice. Biochem Biophys Res Commun 326(1):181-187, 2005.
21. Lee G, Bendayan R. Functional expression and localization of P-glycoprotein in the central nervous system: relevance to the pathogenesis and treatment of neurological disorders. Pharm Res 21(8): 1313-1330, 2004.
22. Ponte-Sucre A. Availability and applications of ATP-binding cassette (ABC) transporter blockers. Appl Microbiol Biotechnol 76(2):279-286, (Review), 2007.
23. Kruh GD, Belinsky MG. The MRP family of drug efflux pumps. Oncogene 22(47):7537-7552, (Review), 2003.
24. Dallas S, Miller DS, Bendayan R. Multidrug resistance-associated proteins: expression and function in the central nervous system. Pharmacol Rev 58(2):140-161, (Review), 2006.
25. Sampath J, Adachi M, Hatse S, Naesens L, Balzarini J, Flatley RM, Matherly LH, Schuetz JD. Role of MRP4 and MRP5 in biology and chemotherapy. AAPS PharmSci 4(3):E14, 2002.
26. Biscardi M, Teodori E, Caporale R, Budriesi R, Balestri F, Scappini B, Gavazzi S, Grossi A. Multidrug reverting activity toward leukemia cells in a group of new verapamil analogues with low cardiovascular activity. Leuk Res 30(1):1-8, 2006.
27. Ronaldson PT, 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 21(5):811- 818, 2004.
28. Bachmeier CJ, Spitzenberger TJ, Elmquist WF, Miller DW. Quantitative assessment of HIV-1 protease inhibitor interactions with drug efflux transporters in the blood-brain barrier. Pharm Res 22(8):1259-1268, 2005.
29. Janneh O, Owen A, Chandler B, Hartkoorn RC, Hart CA, Bray PG, Ward SA, Back DJ, Khoo SH. Modulation of the intracellular accumulation of saquinavir in peripheral blood mononuclear cells by inhibitors of MRP1, MRP2, P-gp and BCRP. AIDS 19(18):2097-2102, 2005.
30. Meaden ER, Hoggard PG, Newton P, Tjia JF, Aldam D, Cornforth D, Lloyd J, Williams I, Back DJ, Khoo SH. P-glycoprotein and MRP1 expression and reduced ritonavir and saquinavir accumulation in HIV-infected individuals. J Antimicrob Chemother 50(4):583-588, 2002.
31. Park S, Sinko PJ. P-glycoprotein and mutlidrug resistance-associated proteins limit the brain uptake of saquinavir in mice. J Pharmacol Exp Ther 312(3):1249-1256, 2005.
32. Owen A, Janneh O, Hartkoorn RC, Chandler B, Bray PG, Martin P, Ward SA, Hart CA, Khoo SH, Back DJ. In vitro synergy and enhanced murine brain penetration of saquinavir coadministered with mefloquine. J Pharmacol Exp Ther 314(3):1202-1209, 2005.
33. Jorajuria S, Dereuddre-Bosquet N, Becher F, Martin S, Porcheray F, Garrigues A, Mabondzo A, Benech H, Grassi J, Orlowski S, Dormont D, Clayette P. ATP binding cassette multidrug transporters limit the anti-HIV activity of zidovudine and indinavir in infected human macrophages. Antivir Ther 9(4):519-528, 2004.
34. Wijnholds J, Mol CA, van Deemter L, de Haas M, Scheffer GL, Baas F, Beijnen JH, Scheper RJ, Hatse S, De Clercq E, Balzarini J, Borst P. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc Natl Acad Sci U S A 97(13):7476-7481, 2000.
35. Gupta A, Zhang Y, Unadkat JD, Mao Q. HIV protease inhibitors are inhibitors but not substrates of the human breast cancer resistance protein (BCRP/ABCG2). J Pharmacol Exp Ther 310(1):334-341, 2004.
36. Boska MD, Mosley RL, Nawab M, Nelson JA, Zelivyanskaya M, Poluektova L, Uberti M, Dou H, Lewis TB, Gendelman HE. Advances in neuroimaging for HIV-1 associated neurological dysfunction: clues to the diagnosis, pathogenesis and therapeutic monitoring. Curr HIV Res 2(1):61-78, 2004.
37. Marcondes MC, Burudi EM, Huitron-Resendiz S, Sanchez-Alavez M, Watry D, Zandonatti M, Henriksen SJ, Fox HS. Highly activated CD8(+) T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection. J Immunol 167(9):5429-5438, 2001.
38. Katoh M, Suzuyama N, Takeuchi T, Yoshitomi S, Asahi S, Yokoi T. Kinetic analyses for species differences in P-glycoprotein-mediated drug transport. J Pharm Sci 95(12):2673-2683, 2006.
39. Suzuyama N, Katoh M, Takeuchi T, Yoshitomi S, Higuchi T, Asashi S, Yokoi T. Species differences of inhibitory effects on P-glycoprotein-mediated drug transport. J Pharm Sci 96(6):1609-1618, 2007.
40. Hauser IA, Koziolek M, Hopfer U, Thevenod F. Therapeutic concentrations of cyclosporine A, but not FK506, increase P-glycoprotein expression in endothelial and renal tubule cells. Kidney Int 54(4):1139-1149, 1998.
41. Iwahana M, Utoguchi N, Mayumi T, Goryo M, Okada K. Drug resistance and P-glycoprotein expression in endothelial cells of newly formed capillaries induced by tumors. Anticancer Res 18(4C):2977-2980, 1998.
42. Liscovitch M, Ravid D. A case study in misidentification of cancer cell lines: MCF-7/AdrR cells (re-designated NCI/ADR-RES) are derived from OVCAR-8 human ovarian carcinoma cells. Cancer Lett 245(1-2): 350-352, 2007.
43. Sarver JG, Klis WA, Byers JP, Erhardt PW. Microplate screening of the differential effects of test agents on Hoechst 33342, rhodamine 123 and rhodamine 6G accumulation in breast cancer cells that overexpress P-glycoprotein. J Biomol Screen 7(1):29-34, 2002.
44. Rosati A, Candussio L, Crivellato E, Klugmann FB, Giraldi T, Damiani D, Michelutti A, Decorti G. Bodipy-FL-verapamil: a fluorescent probe for the study of multidrug resistance proteins. Cell Oncol 26(1-2):3-11, 2004.
45. Sulová Z, Macejová D, Seres M, Sedlák J, Brtko J, Breier A. Combined treatment of P-gp-positive L1210/VCR cells by verapamil and all-trans retinoic acid induces down-regulation of P-glycoprotein expression and transport activity. Toxicol In Vitro 22(1):96-105, 2008.
46. Limtrakul P, Chearwae W, Shukla S, Phisalphong C, Ambudkar SV. Modulation of function of three ABC drug transporters, P-glycoprotein (ABCB1), mitoxantrone resistance protein (ABCG2) and multidrug resistance protein 1 (ABCC1) by tetrahydrocurcumin, a major metabolite of curcumin. Mol Cell Biochem 296(1-2):85-95, 2007.
47. Hua J, Mutch DG, Herzog TJ. Stable suppression of MDR-1 gene using siRNA expression vector to reverse drug resistance in a human uterine sarcoma cell line. Gynecol Oncol 98(1):31-38, 2005.
48. Konig J, Hartel M, Nies AT, Martignoni ME, Guo J, Büchler MW, Friess H, Keppler D. Expression and localization of human multidrug resistance protein (ABCC) family members in pancreatic carcinoma. Int J Cancer 115(3):359-367, 2005.
49. Volk H, Potschka H, Loscher W. Immunohistochemical localization of P-glycoprotein in rat brain and detection of its increased expression by seizures are sensitive to fixation and staining variables. J Histochem Cytochem 53(4):517-531, 2005.
50. Demeule M, Labelle M, Régina A, Bérthelet F, Béliveau R. Isolation of endothelial cells from brain, lung and kidney: expression of the multidrug resistance P-glycoprotein isoforms. Biochem Biophys Res Commun 281(3):827-834, 2001.
51. Salama NN, Kelly EJ, Bui T, Ho RJ. The impact of pharmacologic and genetic knockout of P-glycoprotein on nelfinavir levels in the brain and other tissues in mice. J Pharm Sci 94(6):1216-1225, 2005.
52. Kubota H, Ishihara H, Langmann T, Schmitz G, Stieger B, Wieser HG, Yonekawa Y, Frei K. Distribution and functional activity of P-glycoprotein and multidrug resistance-associated proteins in human brain microvascular endothelial cells in hippocampal sclerosis. Epilepsy Res 68(3):213-228, 2006.
53. Nies AT, Jedlitschky G, König J, Herold-Mende C, Steiner HH, Schmitt HP, Keppler D. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129(2):349-360, 2004.
54. Bronger H, König J, Kopplow K, Steiner HH, Ahmadi R, Herold- Mende C, Keppler D, Nies AT. ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood-tumor barrier. Cancer Res 65(24):11419-11428, 2005.
55. Umeki N, Fukasawa Y, Ohtsuki S, Hori S, Watanabe Y, Kohno Y, Terasaki T. mRNA expression and amino acid transport characteristics of cultured human brain microvascular endothelial cells (hBME). Drug Metab Pharmacokinet 17(4):367-373, 2002.
56. Kuo YC, Su FL. Transport of stavudine, delavirdine and saquinavir across the blood-brain barrier by polybutylcyanoacrylate, methylmeth-acrylate- sulfopropylmethacrylate and solid lipid nanoparticles. Int J Pharm 340(1-2):143-152, 2007.
57. Bachmakov I, Werner U, Endress B, Auge D, Fromm MF. Characterization of beta-adrenoceptor antagonists as substrates and inhibitors of the drug transporter P-glycoprotein. Fundam Clin Pharmacol 20(3): 273-282, 2006.
58. Kurzawski M, Bartnicka L, Florczak M, Górnik W, Droździk M. Impact of ABCB1 (MDR1) gene polymorphism and P-glycoprotein inhibitors on digoxin serum concentration in congestive heart failure patients. Pharmacol Rep 59(1):107-111, 2007.
59. Couture L, Nash JA, Turgeon J. The ATP-binding cassette transporters and their implication in drug disposition: a special look at the heart. Pharmacol Rev 58(2):244-258, (Review), 2006.
60. Yunomae K, Arima H, Hirayama F, Uekama K. Involvement of cholesterol in the inhibitory effect of dimethyl-beta-cyclodextrin on P- glycoprotein and MRP2 function in Caco-2 cells. FEBS Lett 536(1-3): 225-231, 2003.
61. Rothnie A, Theron D, Soceneantu L, Martin C, Traikia M, Berridge G, Higgins CF, Devaux PF, Callaghan R. The importance of cholesterol in maintenance of P-glycoprotein activity and its membrane perturbing influence. Eur Biophys J 30(6):430-442, 2001.
62. Krause MS, Oliveira LP Jr, Silveira EM, Vianna DR, Rossato JS, Almeida BS, Rodrigues MF, Fernandes AJ, Costa JA, Curi R, de Bittencourt PI Jr. MRP1/GS-X pump ATPase expression: is this the explanation for the cytoprotection of the heart against oxidative stress-induced redox imbalance in comparison to skeletal muscle cells? Cell Biochem Funct 25(1):23-32, 2007.
63. Hammond CL, Marchan R, Krance SM, Ballatori N. Glutathione export during apoptosis requires functional multidrug resistance-associated proteins. J Biol Chem 282(19):14337-14347, 2007.
64. Petrovic V, Teng S, Piquette-Miller M. Regulation of drug transporters during infection and inflammation. Mol Interv 7(2):99-111, 2007.
65. Hayashi K, Pu H, Tian J, Andras IE, Lee YW, Hennig B, Toborek M. HIV-Tat protein induces P-glycoprotein expression in brain micro-vascular endothelial cells. J Neurochem 93(5):1231-1241, 2005.