ATP and GSH dependence of MRP1-mediated outward translocation of phospholipid analogs in the human erythrocyte membrane

References

• Bagrij, T., Klokouzas, A., Hladky, S. B. and Barrand, M. A., 2001, Influences of glutathione on anionic substrate efflux in tumour cells expressing the multidrug resistance-associated protein. Biochemical Pharmacology, 62, 199 –206.
   PubMed Web of Science ®Google Scholar
• Beleznay, Z., Zachowski, A., Devaux, P. F. and Ott, P., 1997, Characterization of the correlation between ATP-dependent aminophospholipid translocation and Mg2+-ATPase activity in red blood cell membranes. European Journal of Biochemistry, 243, 58 –65.
   PubMedGoogle Scholar
• Bitbol, M. and Devaux, P. F., 1988, Measurement of outward translocation of phospholipids across human erythrocyte mem- brane. Proceedings of the National Academy of Sciences (USA),85, 6783 -6787.
   Google Scholar
• Borst, P., Evers, R., Kool, M. and Wijnholds, J., 1999, The multidrug resistance protein family. Biochimica et Biophysica Acta, 1461, 347 –357.
   PubMed Web of Science ®Google Scholar
• Bro¨ ring, K., Haest, C. W. M. and Deuticke, B., 1989, Translocation of oleic acid across the erythrocyte membrane. Evidence for a fast process. Biochimica et Biophysica Acta, 986, 321 –331.
   PubMedGoogle Scholar
• Chang, G. and Roth, C. B., 2001, Structure of MsbA from E.coli: a homolog of the multidrug resistance ATP binding casette (ABC) transporters. Science, 293, 1793–1800.
   PubMed Web of Science ®Google Scholar
• Connor, J., Pak, C. H., Zwaal, R. F. and Schroit, A. J., 1992, Bidirectional transbilayer movement of phospholipid analogs in human red cells. Journal of Biological Chemistry, 267, 19412- 19417.
   PubMed Web of Science ®Google Scholar
• Daleke, D. L. and Lyles, J. V., 2000, Identification and purification of aminophospholipid flippases. Biochimica et Biophysica Acta, 1486, 108 –127.
   PubMed Web of Science ®Google Scholar
• Dekkers, D. W. C., Comfurius, P., Schroit, A. J., Bevers, E. M. and Zwaal, R. F. A., 1998, Transbilayer movement of NBD-labeled phospholipids in red blood cell membranes: outward-directed transport by the multidrug resistance protein 1 (MRP1). Biochem- istry, 37, 14833–14837.
   PubMed Web of Science ®Google Scholar
• Dekkers, D. W. C., Comfurius, P., van Gool, R. G. J., Bevers, E. M. and Zwaal, R. F. A., 2000, Multidrug resistance protein 1 regulates lipid asymmetry in erythrocyte membranes. Biochemical Journal, 350, 531 –535.
   PubMed Web of Science ®Google Scholar
• Dolis, D., Moreau, C., Zachowski, A. and Devaux, P. F., 1997, Aminophospholipid translocase and proteins involved in trans- membrane phospholipid traffic. Biophysical Chemistry, 68, 221 – 231.
   PubMed Web of Science ®Google Scholar
• Eidelman, O., Zangvill, M., Razin, M., Ginsburg, H. and Cabantchik,Z. I., 1981, The anion-transfer system of erythrocyte membranes N-(7-Nitrobenzofurazan-4-yl)taurine, a fluorescent substrate-ana- logue of the system. Biochemical Journal, 195, 503 –513.
   PubMed Web of Science ®Google Scholar
• Evers, R., de Haas, M., Sparidans, R., Beijnen, J., Wielinga, P. R., Lankelma, J. and Borst, P., 2000, Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. British Journal of Cancer, 83, 375 –383. Haest, C. W. M., Kamp, D. and Deuticke, B., 1997, Transbilayer reorientation of phospholipid probes in the human erythrocyte membrane. Lessons from studies on electroporated and resealedcells. Biochimica et Biophysica Acta, 1325, 17 –33.
   Google Scholar
• Haimeur, A., Deeley, R. G. and Cole, S. P. C., 2002, Charged amino acids in the sixth transmembrane helix of multidrug resistance protein 1 (MRP1/ABCC1) are critical determinants of transport activity. Journal of Biological Chemistry, 277, 41326–41333.
   PubMed Web of Science ®Google Scholar
• Heijn, M., Hooijberg, J. H., Scheffer, G. L., Szabo´, G., Westerhoff, H.V. and Lankelma, J., 1997, Antracyclines modulate multidrug resistance protein (MRP) mediated organic anion transport. Biochimica et Biophysica Acta, 1326, 12 –22.
   PubMed Web of Science ®Google Scholar
• Higgins, C. F. and Gottesman, M. M., 1992, Is the multidrug transporter a flippase? Trends in Biochemical Sciences, 17, 18 –21.
   PubMed Web of Science ®Google Scholar
• Hipfner, D. R., Deeley, R. G. and Cole, S. P. C., 1999, Structural, mechanistic and clinical aspects of MRP1. Biochimica et Biophy- sica Acta, 1461, 359 –376.
   PubMed Web of Science ®Google Scholar
• Jedlitschky, G., Leier, I., Buchholz, U., Barnouin, K., Kurz, G. and Keppler, D., 1996, Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Research, 56, 988 –994.
   PubMed Web of Science ®Google Scholar
• Juengling, E. and Kammermeier, H., 1980, Rapid assay of adenine nucleotides or creatine compounds in extracts of cardiac tissue by paired-ion reverse-phase high-performance liquid chromatogra- phy. Analytical Biochemistry, 102, 358 –361.
   PubMed Web of Science ®Google Scholar
• Kamp, D. and Haest, C. W. M., 1998, Evidence for a role of the multidrug resistance protein (MRP) in the outward translocation of NBD-phospholipids in the erythrocyte membrane. Biochimica et Biophysica Acta, 1372, 91 –101.
   PubMed Web of Science ®Google Scholar
• Klokouzas, A., Barrand, M. A. and Hladky, S. B., 2001, Effects of clotrimazole on transport mediated by multidrug resistance associated protein 1 (MRP1) in human erythrocytes and tumour cells. European Journal Biochemistry, 268, 6569–6577.
   PubMedGoogle Scholar
• Ko¨ nig, J, Nies, A. T., Cui, Y., Leier, I. and Keppler, D., 1999, Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2- mediated drug resistance. Biochimica et Biophysica Acta, 1461, 377 –394.
   PubMed Web of Science ®Google Scholar
• Loe, D. W., Almquist, K. C., Cole, S. P. C. and Deeley, R. G., 1996, ATP-dependent 17b -estradiol 17-(b -D-glucoronide) transport by multidrug resistance protein (MRP). Inhibition by cholestatic steroids. Journal of Biological Chemistry, 271, 9683–9689.
   PubMed Web of Science ®Google Scholar
• Loe, D. W., Almquist, K. C., Deeley, R. G. and Cole, S. P. C, 1996, Multidrug resistance protein (MRP)-mediated transport of leuko- triene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. Journal of Biological Chemistry, 271, 9675–9682.
   PubMed Web of Science ®Google Scholar
• Loe, D. W., Deeley, R. G. and Cole, S. P. C., 1998, Characterization of vincristine transport by the Mr 190,0000 multidrug resistance protein (MRP): Evidence for cotransport with reduced glutathione. Cancer Research, 58, 5130–5136.
   PubMed Web of Science ®Google Scholar
• Mao, Q., Deeley, R. G. and Cole, S. P. C., 2000, Functional reconstitution of substrate transport by purified multidrug resis- tance protein MRP1 (ABCC1). Journal of Biological Chemistry, 275, 34166–34172.
   PubMed Web of Science ®Google Scholar
• Paulusma, C. C., van Geer, M. A., Evers, R., Heijn, M., Ottenhoff, R., Borst, P. and Oude Elferink, R. P. J., 1999, Canalicular multi- specific organic anion transporter/mutidrug resistance protein 2 mediated low-affinity transport of reduced glutathione. Biochem- ical Journal, 338, 393 –401.
   PubMed Web of Science ®Google Scholar
• Qian, Y. M., Song, W. C., Cui, H., Cole, S. P. and Deeley, R. G., 2001, Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. Journal of Biological Chemistry, 276, 6404 -6411.
   PubMed Web of Science ®Google Scholar
• Raggers, R. J., van Helvoort, A., Evers, R. and van Meer, G., 1999, The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. Journal of Cell Science, 112, 415 –422.
   PubMed Web of Science ®Google Scholar
• Rebbeor, J. F., Connolly, G. C., Dumont, M. E. and Ballatori, N., 1998, ATP-dependent transport of reduced glutathione in yeast secretory vesicles. Biochemical Journal, 334, 723 –729.
   PubMed Web of Science ®Google Scholar
• Rebbeor, J. F., Connolly, G. C., Henson, J. H., Boyer, J. L. and Ballatori, N., 2000, ATP-dependent GSH and glutathione S- conjugate transport in skate liver: role of an Mrp functional homologue. American Journal of Physiology, 279, G417 -G425. Renes, J., de Vries, E. G., Nienhuis, E. F., Jansen, P. L. and Muller, M., 1999, ATP- and glutathione-dependent transport of che- motherapeuticdrugs by the multidrug resistance protein MRP1. British Journal of Pharmacology, 126, 681 -688.
   Google Scholar
• Salerno, M. and Garnier-Suillerot, A., 2001, Kinetics of glutathione and daunomycin efflux from multidrug overexpressing small-cell lung cancer cells. European Journal Pharmacology, 421, 1 –9.
   PubMed Web of Science ®Google Scholar
• Schumacher, M. A., Miller, M. C., Grkovic, S., Brown, M. H., Skurray,R. A. and Brennan, R. G., 2001, Structural mechanisms of QacR induction and multidrug recognition. Science, 294, 2158 -2163.
   PubMed Web of Science ®Google Scholar
• Seigneuret, M. and Devaux, P. F., 1984, ATP-dependent asym-metricdistribution of spin-labeled phospholipids in the erythrocyte membrane: Relation to shape changes. Proceedings of the National Acadamy of Sciences (USA), 81, 3751–3755.
   PubMed Web of Science ®Google Scholar
• Serra, M. V., Kamp, D. and Haest, C. W. M., 1996, Pathways for flip-flop of mono- and di-anionicphospholipids in the erythrocyte membrane. Biochimica et Biophysica Acta, 1282, 263 –273.
   PubMed Web of Science ®Google Scholar
• Sharom, F. J., 1997, The P-glycoprotein efflux pump: how does ittransport drugs Journal of Membrane Biology, 160, 161 –175. Watkins, R. E., Wisely, G. B., Moore, L. B., Collins, J. L., Lambert, M.H., Williams, S. P., Willson, T. M., Kliewer, S. A. and Redinbo, M. R., 2001, The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science, 292, 2329 –2333. Zhang, D. W., Cole, S. P. C. and Deeley, R. G., 2002, Determinants of the substrate specificity of multidrug resistance protein 1. Role of amino acid residues with hydrogen bonding potential in predicted transmembrane helix 17. Journal of Biological Chemistry, 277, 20934–20941.
   Google Scholar