[1]
Khamisipour, G.; Jadidi-Niaragh, F.; Jahromi, A.S.; Zandi, K.; Hojjat-Farsangi, M. Mechanisms of tumor cell resistance to the current targeted-therapy agents. Tumour Biol., 2016, 37(8), 10021-10039.
[2]
Rice, A.J.; Park, A.; Pinkett, H.W. Diversity in ABC transporters: type I, II and III importers. Crit. Rev. Biochem. Mol. Biol., 2014, 49(5), 426-437.
[3]
Slot, A.J.; Molinski, S.V.; Cole, S.P. Mammalian multidrug-resistance proteins (MRPs). Essays Biochem., 2011, 50(1), 179-207.
[4]
Cole, S.P. Multidrug resistance protein 1 (MRP1, ABCC1), a “multitasking” ATP-binding cassette (ABC) transporter. J. Biol. Chem., 2014, 289(45), 30880-30888.
[5]
Taylor, N.M.I.; Manolaridis, I.; Jackson, S.M.; Kowal, J.; Stahlberg, H.; Locher, K.P. Structure of the human multidrug transporter ABCG2. Nature, 2017, 546(7659), 504-509.
[6]
Kunjachan, S.; Rychlik, B.; Storm, G.; Kiessling, F.; Lammers, T. Multidrug resistance: Physiological principles and nanomedical solutions. Adv. Drug Deliv. Rev., 2013, 65(13-14), 1852-1865.
[7]
Choi, Y.H.; Yu, A.M. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr. Pharm. Des., 2014, 20(5), 793-807.
[8]
Deeley, R.G.; Westlake, C.; Cole, S.P. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev., 2006, 86(3), 849-899.
[9]
ter Beek, J.; Guskov, A.; Slotboom, D.J. Structural diversity of ABC transporters. J. Gen. Physiol., 2014, 143(4), 419-435.
[10]
Walker, J.E.; Saraste, M.; Runswick, M.J.; Gay, N.J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1982, 1(8), 945-951.
[11]
Juliano, R.L.; Ling, V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta, 1976, 455(1), 152-162.
[12]
Schinkel, A.H.; Borst, P. Multidrug resistance mediated by P-glycoproteins. Semin. Cancer Biol., 1991, 2(4), 213-226.
[13]
Ushigome, F.; Takanaga, H.; Matsuo, H.; Yanai, S.; Tsukimori, K.; Nakano, H.; Uchiumi, T.; Nakamura, T.; Kuwano, M.; Ohtani, H.; Sawada, Y. Human placental transport of vinblastine, vincristine, digoxin and progesterone: contribution of P-glycoprotein. Eur. J. Pharmacol., 2000, 408(1), 1-10.
[14]
Gatmaitan, Z.C.; Arias, I.M. Structure and function of P-glycoprotein in normal liver and small intestine. Adv. Pharmacol., 1993, 24, 77-97.
[15]
Begley, D.J.; Lechardeur, D.; Chen, Z.D.; Rollinson, C.; Bardoul, M.; Roux, F.; Scherman, D.; Abbott, N.J. Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4. J. Neurochem., 1996, 67(3), 988-995.
[16]
Lee, C.H. Induction of P-glycoprotein mRNA transcripts by cycloheximide in animal tissues: evidence that class I Pgp is transcriptionally regulated whereas class II Pgp is post-transcriptionally regulated. Mol. Cell. Biochem., 2001, 216(1-2), 103-110.
[17]
Tsuji, A.; Terasaki, T.; Takabatake, Y.; Tenda, Y.; Tamai, I.; Yamashima, T.; Moritani, S.; Tsuruo, T.; Yamashita, J. P-glycoprotein as the drug efflux pump in primary cultured bovine brain capillary endothelial cells. Life Sci., 1992, 51(18), 1427-1437.
[18]
Rao, V.V.; Dahlheimer, J.L.; Bardgett, M.E.; Snyder, A.Z.; Finch, R.A.; Sartorelli, A.C.; Piwnica-Worms, D. Choroid plexus epithelial expression of MDR1 P glycoprotein and multidrug resistance-associated protein contribute to the blood-cerebrospinal-fluid drug-permeability barrier. Proc. Natl. Acad. Sci. USA, 1999, 96(7), 3900-3905.
[19]
Schinkel, A.H.; Wagenaar, E.; Mol, C.A.; van Deemter, L. P-glycoprotein in the blood-brain barrier of mice influences the brain penetration and pharmacological activity of many drugs. J. Clin. Invest., 1996, 97(11), 2517-2524.
[20]
Smit, J.J.; Schinkel, A.H.; Mol, C.A.; Majoor, D.; Mooi, W.J.; Jongsma, A.P.; Lincke, C.R.; Borst, P. Tissue distribution of the human MDR3 P-glycoprotein. Lab. Invest., 1994, 71(5), 638-649.
[21]
Chan, L.M.; Lowes, S.; Hirst, B.H. The ABCs of drug transport in intestine and liver: efflux proteins limiting drug absorption and bioavailability. Eur. J. Pharm. Sci., 2004, 21(1), 25-51.
[22]
Mahringer, A.; Fricker, G. ABC transporters at the blood-brain barrier. Expert Opin. Drug Metab. Toxicol., 2016, 12(5), 499-508.
[23]
Joshi, A.A.; Vaidya, S.S.; St-Pierre, M.V.; Mikheev, A.M.; Desino, K.E.; Nyandege, A.N.; Audus, K.L.; Unadkat, J.D.; Gerk, P.M. Placental ABC transporters: Biological impact and pharmaceutical significance. Pharm. Res., 2016, 33(12), 2847-2878.
[24]
Raub, T.J. P-glycoprotein recognition of substrates and circumvention through rational drug design. Mol. Pharm., 2006, 3(1), 3-25.
[25]
Wang, R.B.; Kuo, C.L.; Lien, L.L.; Lien, E.J. Structure-activity relationship: analyses of p-glycoprotein substrates and inhibitors. J. Clin. Pharm. Ther., 2003, 28(3), 203-228.
[26]
Sharom, F.J.; Lugo, M.R.; Eckford, P.D. New insights into the drug binding, transport and lipid flippase activities of the p-glycoprotein multidrug transporter. J. Bioenerg. Biomembr., 2005, 37(6), 481-487.
[27]
Ledwitch, K.V.; Roberts, A.G. Cardiovascular ion channel inhibitor drug-drug interactions with P-glycoprotein. AAPS J., 2017, 19(2), 409-420.
[28]
Foy, M.; Sperati, C.J.; Lucas, G.M.; Estrella, M.M. Drug interactions and antiretroviral drug monitoring. Curr. HIV/AIDS Rep., 2014, 11(3), 212-222.
[29]
Yang, X.; Liu, K. P-gp Inhibition-based strategies for modulating pharmacokinetics of anticancer drugs: An update. Curr. Drug Metab., 2016, 17(8), 806-826.
[30]
Nakanishi, T.; Tamai, I. Interaction of drug or food with drug transporters in intestine and liver. Curr. Drug Metab., 2015, 16(9), 753-764.
[31]
Chandra, P.; Brouwer, K.L. The complexities of hepatic drug transport: current knowledge and emerging concepts. Pharm. Res., 2004, 21(5), 719-735.
[32]
Tamaki, A.; Ierano, C.; Szakacs, G.; Robey, R.W.; Bates, S.E. The controversial role of ABC transporters in clinical oncology. Essays Biochem., 2011, 50(1), 209-232.
[33]
Leslie, E.M.; Deeley, R.G.; Cole, S.P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol., 2005, 204(3), 216-237.
[34]
Cole, S.P.; Bhardwaj, G.; Gerlach, J.H.; Mackie, J.E.; Grant, C.E.; Almquist, K.C.; Stewart, A.J.; Kurz, E.U.; Duncan, A.M.; Deeley, R.G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 1992, 258(5088), 1650-1654.
[35]
Valente, R.C.; Capella, L.S.; Nascimento, C.R.; Lopes, A.G.; Capella, M.A. Modulation of multidrug resistance protein (MRP1/ABCC1) expression: a novel physiological role for ouabain. Cell Biol. Toxicol., 2007, 23(6), 421-427.
[36]
Berggren, S.; Gall, C.; Wollnitz, N.; Ekelund, M.; Karlbom, U.; Hoogstraate, J.; Schrenk, D.; Lennernas, H. Gene and protein expression of P-glycoprotein, MRP1, MRP2, and CYP3A4 in the small and large human intestine. Mol. Pharm., 2007, 4(2), 252-257.
[37]
Nies, A.T.; Jedlitschky, G.; Konig, J.; Herold-Mende, C.; Steiner, H.H.; Schmitt, H.P.; Keppler, D. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience, 2004, 129(2), 349-360.
[38]
Albermann, N.; Schmitz-Winnenthal, F.H. Z’Graggen, K.; Volk, C.; Hoffmann, M.M.; Haefeli, W.E.; Weiss, J. 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., 2005, 70(6), 949-958.
[39]
Buchler, M.; Konig, J.; Brom, M.; Kartenbeck, J.; Spring, H.; Horie, T.; Keppler, D. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J. Biol. Chem., 1996, 271(25), 15091-15098.
[40]
Schaub, T.P.; Kartenbeck, J.; Konig, J.; Vogel, O.; Witzgall, R.; Kriz, W.; Keppler, D. Expression of the conjugate export pump encoded by the mrp2 gene in the apical membrane of kidney proximal tubules. J. Am. Soc. Nephrol., 1997, 8(8), 1213-1221.
[41]
Mottino, A.D.; Hoffman, T.; Jennes, L.; Vore, M. Expression and localization of multidrug resistant protein mrp2 in rat small intestine. J. Pharmacol. Exp. Ther., 2000, 293(3), 717-723.
[42]
Potschka, H.; Fedrowitz, M.; Loscher, W. Multidrug resistance protein MRP2 contributes to blood-brain barrier function and restricts antiepileptic drug activity. J. Pharmacol. Exp. Ther., 2003, 306(1), 124-131.
[43]
Korita, P.V.; Wakai, T.; Shirai, Y.; Matsuda, Y.; Sakata, J.; Takamura, M.; Yano, M.; Sanpei, A.; Aoyagi, Y.; Hatakeyama, K.; Ajioka, Y. Multidrug resistance-associated protein 2 determines the efficacy of cisplatin in patients with hepatocellular carcinoma. Oncol. Rep., 2010, 23(4), 965-972.
[44]
Yamasaki, M.; Makino, T.; Masuzawa, T.; Kurokawa, Y.; Miyata, H.; Takiguchi, S.; Nakajima, K.; Fujiwara, Y.; Matsuura, N.; Mori, M.; Doki, Y. Role of multidrug resistance protein 2 (MRP2) in chemoresistance and clinical outcome in oesophageal squamous cell carcinoma. Br. J. Cancer, 2011, 104(4), 707-713.
[45]
Toh, S.; Wada, M.; Uchiumi, T.; Inokuchi, A.; Makino, Y.; Horie, Y.; Adachi, Y.; Sakisaka, S.; Kuwano, M. Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome. Am. J. Hum. Genet., 1999, 64(3), 739-746.
[46]
Konig, J.; Rost, D.; Cui, Y.; Keppler, D. Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology, 1999, 29(4), 1156-1163.
[47]
Borst, P.; Zelcer, N.; van de Wetering, K. MRP2 and 3 in health and disease. Cancer Lett., 2006, 234(1), 51-61.
[48]
Rost, D.; Konig, J.; Weiss, G.; Klar, E.; Stremmel, W.; Keppler, D. Expression and localization of the multidrug resistance proteins MRP2 and MRP3 in human gallbladder epithelia. Gastroenterol., 2001, 121(5), 1203-1208.
[49]
Zollner, G.; Wagner, M.; Fickert, P.; Silbert, D.; Fuchsbichler, A.; Zatloukal, K.; Denk, H.; Trauner, M. Hepatobiliary transporter expression in human hepatocellular carcinoma. Liver Int., 2005, 25(2), 367-379.
[50]
Benderra, Z.; Faussat, A.M.; Sayada, L.; Perrot, J.Y.; Tang, R.; Chaoui, D.; Morjani, H.; Marzac, C.; Marie, J.P.; Legrand, O. MRP3, BCRP, and P-glycoprotein activities are prognostic factors in adult acute myeloid leukemia. Clin. Cancer Res., 2005, 11(21), 7764-7772.
[51]
Takahashi, K.; Tatsunami, R.; Sato, K.; Tampo, Y. Multidrug resistance associated protein 1 together with glutathione plays a protective role against 4-hydroxy-2-nonenal-induced oxidative stress in bovine aortic endothelial cells. Biol. Pharm. Bull., 2012, 35(8), 1269-1274.
[52]
Ji, B.; Ito, K.; Suzuki, H.; Sugiyama, Y.; Horie, T. Multidrug resistance-associated protein2 (MRP2) plays an important role in the biliary excretion of glutathione conjugates of 4-hydroxynonenal. Free Radic. Biol. Med., 2002, 33(3), 370-378.
[53]
Mottino, A.D.; Hoffman, T.; Jennes, L.; Cao, J.; Vore, M. Expression of multidrug resistance-associated protein 2 in small intestine from pregnant and postpartum rats. Am. J. Physiol. Gastrointest. Liver Physiol., 2001, 280(6), G1261-G1273.
[54]
Choudhuri, S.; Cherrington, N.J.; Li, N.; Klaassen, C.D. Constitutive expression of various xenobiotic and endobiotic transporter mRNAs in the choroid plexus of rats. Drug Metab. Dispos., 2003, 31(11), 1337-1345.
[55]
Bauer, B.; Hartz, A.M.; Lucking, J.R.; Yang, X.; Pollack, G.M.; Miller, D.S. Coordinated nuclear receptor regulation of the efflux transporter, Mrp2, and the phase-II metabolizing enzyme, GSTpi, at the blood-brain barrier. J. Cereb. Blood Flow Metab., 2008, 28(6), 1222-1234.
[56]
Chen, Z.; Shi, T.; Zhang, L.; Zhu, P.; Deng, M.; Huang, C.; Hu, T.; Jiang, L.; Li, J. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: A review of the past decade. Cancer Lett., 2016, 370(1), 153-164.
[57]
Doyle, L.A.; Yang, W.; Abruzzo, L.V.; Krogmann, T.; Gao, Y.; Rishi, A.K.; Ross, D.D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA, 1998, 95(26), 15665-15670.
[58]
Mao, Q.; Unadkat, J.D. Role of the breast cancer resistance protein (BCRP/ABCG2) in drug transport--an update. AAPS J., 2015, 17(1), 65-82.
[59]
Ishikawa, T.; Aw, W.; Kaneko, K. Metabolic interactions of purine derivatives with human ABC transporter ABCG2: Genetic testing to assess gout risk. Pharmaceuticals (Basel), 2013, 6(11), 1347-1360.
[60]
Bruhn, O.; Cascorbi, I. Polymorphisms of the drug transporters ABCB1, ABCG2, ABCC2 and ABCC3 and their impact on drug bioavailability and clinical relevance. Expert Opin. Drug Metab. Toxicol., 2014, 10(10), 1337-1354.
[61]
van Herwaarden, A.E.; Wagenaar, E.; Merino, G.; Jonker, J.W.; Rosing, H.; Beijnen, J.H.; Schinkel, A.H. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Mol. Cell. Biol., 2007, 27(4), 1247-1253.
[62]
Jonker, J.W.; Merino, G.; Musters, S.; van Herwaarden, A.E.; Bolscher, E.; Wagenaar, E.; Mesman, E.; Dale, T.C.; Schinkel, A.H. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat. Med., 2005, 11(2), 127-129.
[63]
Keppler, D. Cholestasis and the role of basolateral efflux pumps. Z. Gastroenterol., 2011, 49(12), 1553-1557.
[64]
Ghanem, C.I.; Ruiz, M.L.; Villanueva, S.S.; Luquita, M.G.; Catania, V.A.; Jones, B.; Bengochea, L.A.; Vore, M.; Mottino, A.D. Shift from biliary to urinary elimination of acetaminophen-glucuronide in acetaminophen-pretreated rats. J. Pharmacol. Exp. Ther., 2005, 315(3), 987-995.
[65]
Gottesman, M.M.; Ambudkar, S.V. Overview: ABC transporters and human disease. J. Bioenerg. Biomembr., 2001, 33(6), 453-458.
[66]
Sharom, F.J. The P-glycoprotein multidrug transporter. Essays Biochem., 2011, 50(1), 161-178.
[67]
Roepe, P.D. What is the precise role of human MDR 1 protein in chemotherapeutic drug resistance? Curr. Pharm. Des., 2000, 6(3), 241-260.
[68]
Young, G.; Reuss, L.; Altenberg, G.A. Altered intracellular pH regulation in cells with high levels of P-glycoprotein expression. Int. J. Biochem. Mol. Biol., 2011, 2(3), 219-227.
[69]
Altenberg, G.A.; Young, G.; Horton, J.K.; Glass, D.; Belli, J.A.; Reuss, L. Changes in intra- or extracellular pH do not mediate P-glycoprotein-dependent multidrug resistance. Proc. Natl. Acad. Sci. USA, 1993, 90(20), 9735-9738.
[70]
Hoffman, M.M.; Wei, L.Y.; Roepe, P.D. Are altered pHi and membrane potential in hu MDR 1 transfectants sufficient to cause MDR protein-mediated multidrug resistance? J. Gen. Physiol., 1996, 108(4), 295-313.
[71]
Howard, E.M.; Roepe, P.D. Purified human MDR 1 modulates membrane potential in reconstituted proteoliposomes. Biochemistry, 2003, 42(12), 3544-3555.
[72]
Singh, H.; Velamakanni, S.; Deery, M.J.; Howard, J.; Wei, S.L.; van Veen, H.W. ATP-dependent substrate transport by the ABC transporter MsbA is proton-coupled. Nat. Commun., 2016, 7, 12387.
[73]
Vanoye, C.G.; Castro, A.F.; Pourcher, T.; Reuss, L.; Altenberg, G.A. Phosphorylation of P-glycoprotein by PKA and PKC modulates swelling-activated Cl- currents. Am. J. Physiol., 1999, 276(2 Pt 1), C370-C378.
[74]
Yang, Y.; Wu, N.; Wang, Z.; Zhang, F.; Tian, R.; Ji, W.; Ren, X.; Niu, R. Rack1 mediates the interaction of Pglycoprotein
with Anxa2 and regulates migration and invasion
of multidrug-resistant breast cancer cells. Int. J. Mol.
Sci, 2016, 17(10), pi: E1718.
[75]
Bryan, J.; Munoz, A.; Zhang, X.; Dufer, M.; Drews, G.; Krippeit-Drews, P.; Aguilar-Bryan, L. ABCC8 and ABCC9: ABC transporters that regulate K+ channels. Pflugers Arch., 2007, 453(5), 703-718.
[76]
Li, N.; Wu, J.X.; Ding, D.; Cheng, J.; Gao, N.; Chen, L. Structure of a Pancreatic ATP-Sensitive Potassium Channel. Cell,, 2017, 168(1-2), 101-110 e110.
[77]
Martin, G.M.; Yoshioka, C.; Rex, E.A.; Fay, J.F.; Xie, Q.; Whorton, M.R.; Chen, J.Z.; Shyng, S.L. Cryo-EM structure of the ATP-sensitive potassium channel illuminates mechanisms of assembly and gating. eLife, 2017, 6, e24149.
[78]
Raviv, Y.; Pollard, H.B.; Bruggemann, E.P.; Pastan, I.; Gottesman, M.M. Photosensitized labeling of a functional multidrug transporter in living drug-resistant tumor cells. J. Biol. Chem., 1990, 265(7), 3975-3980.
[79]
Johnson, Z.L.; Chen, J. Structural basis of substrate recognition
by the multidrug resistance protein MRP1. Cell, 2017, 168(6), 1075-1085. e9.
[80]
Ramu, A.; Pollard, H.B.; Rosario, L.M. Doxorubicin resistance in P388 leukemia--evidence for reduced drug influx. Int. J. Cancer, 1989, 44(3), 539-547.
[81]
Shalinsky, D.R.; Jekunen, A.P.; Alcaraz, J.E.; Christen, R.D.; Kim, S.; Khatibi, S.; Howell, S.B. Regulation of initial vinblastine influx by P-glycoprotein. Br. J. Cancer, 1993, 67(1), 30-36.
[82]
Altenberg, G.A.; Vanoye, C.G.; Horton, J.K.; Reuss, L. Unidirectional fluxes of rhodamine 123 in multidrug-resistant cells: evidence against direct drug extrusion from the plasma membrane. Proc. Natl. Acad. Sci. USA, 1994, 91(11), 4654-4657.
[83]
Smith, P.C.; Karpowich, N.; Millen, L.; Moody, J.E.; Rosen, J.; Thomas, P.J.; Hunt, J.F. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell, 2002, 10(1), 139-149.
[84]
Huang, W.; Liao, J.L. Catalytic Mechanism of the Maltose Transporter Hydrolyzing ATP. Biochemistry, 2016, 55(1), 224-231.
[85]
Hwang, T.C.; Sheppard, D.N. Gating of the CFTR Cl- channel by ATP-driven nucleotide-binding domain dimerisation. J. Physiol., 2009, 587(Pt 10), 2151-2161.
[86]
Sauna, Z.E.; Kim, I.W.; Nandigama, K.; Kopp, S.; Chiba, P.; Ambudkar, S.V. Catalytic cycle of ATP hydrolysis by P-glycoprotein: evidence for formation of the E.S reaction intermediate with ATP-gamma-S, a nonhydrolyzable analogue of ATP. Biochemistry, 2007, 46(48), 13787-13799.
[87]
Esser, L.; Zhou, F.; Pluchino, K.M.; Shiloach, J.; Ma, J.; Tang, W.K.; Gutierrez, C.; Zhang, A.; Shukla, S.; Madigan, J.P.; Zhou, T.; Kwong, P.D.; Ambudkar, S.V.; Gottesman, M.M.; Xia, D. Structures of the Multidrug Transporter P-glycoprotein Reveal Asymmetric ATP Binding and the Mechanism of Polyspecificity. J. Biol. Chem., 2017, 292(2), 446-461.
[88]
Gyimesi, G.; Ramachandran, S.; Kota, P.; Dokholyan, N.V.; Sarkadi, B.; Hegedus, T. ATP hydrolysis at one of the two sites in ABC transporters initiates transport related conformational transitions. Biochim. Biophys. Acta, 2011, 1808(12), 2954-2964.
[89]
Wen, P.C.; Tajkhorshid, E. Dimer opening of the nucleotide binding domains of ABC transporters after ATP hydrolysis. Biophys. J., 2008, 95(11), 5100-5110.
[90]
Dawson, R.J.; Locher, K.P. Structure of a bacterial multidrug ABC transporter. Nature, 2006, 443(7108), 180-185.
[91]
Jones, P.M.; George, A.M. Opening of the ADP-bound active site in the ABC transporter ATPase dimer: evidence for a constant contact, alternating sites model for the catalytic cycle. Proteins, 2009, 75(2), 387-396.
[92]
Jones, P.M.; O’Mara, M.L.; George, A.M. ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci., 2009, 34(10), 520-531.
[93]
Moody, J.E.; Millen, L.; Binns, D.; Hunt, J.F.; Thomas, P.J. Cooperative, ATP-dependent association of the nucleotide binding cassettes during the catalytic cycle of ATP-binding cassette transporters. J. Biol. Chem., 2002, 277(24), 21111-21114.
[94]
Janas, E.; Hofacker, M.; Chen, M.; Gompf, S.; van der Does, C.; Tampe, R. The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J. Biol. Chem., 2003, 278(29), 26862-26869.
[95]
Vergani, P.; Lockless, S.W.; Nairn, A.C.; Gadsby, D.C. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature, 2005, 433(7028), 876-880.
[96]
Zoghbi, M.E.; Altenberg, G.A. Hydrolysis at one of the two nucleotide-binding sites drives the dissociation of ATP-binding cassette nucleotide-binding domain dimers. J. Biol. Chem., 2013, 288(47), 34259-34265.
[97]
Zoghbi, M.E.; Krishnan, S.; Altenberg, G.A. Dissociation of ATP-binding cassette nucleotide-binding domain dimers into monomers during the hydrolysis cycle. J. Biol. Chem., 2012, 287(18), 14994-15000.
[98]
Zoghbi, M.E.; Altenberg, G.A. ATP binding to two sites is necessary for dimerization of nucleotide-binding domains of ABC proteins. Biochem. Biophys. Res. Commun., 2014, 443(1), 97-102.
[99]
Urbatsch, I.L.; al-Shawi, M.K.; Senior, A.E. Characterization of the ATPase activity of purified Chinese hamster P-glycoprotein. Biochemistry, 1994, 33(23), 7069-7076.
[100]
Biswas, E.E. Nucleotide binding domain 1 of the human retinal ABC transporter functions as a general ribonucleotidase. Biochemistry, 2001, 40(28), 8181-8187.
[101]
de Wet, H.; Mikhailov, M.V.; Fotinou, C.; Dreger, M.; Craig, T.J.; Venien-Bryan, C.; Ashcroft, F.M. Studies of the ATPase activity of the ABC protein SUR1. FEBS J., 2007, 274(14), 3532-3544.
[102]
Fendley, G.A.; Urbatsch, I.L.; Sutton, R.B.; Zoghbi, M.E.; Altenberg, G.A. Nucleotide dependence of the dimerization of ATP binding cassette nucleotide binding domains. Biochem. Biophys. Res. Commun., 2016, 480(2), 268-272.
[103]
Aller, S.G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P.M.; Trinh, Y.T.; Zhang, Q.; Urbatsch, I.L.; Chang, G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science, 2009, 323(5922), 1718-1722.
[104]
Li, J.; Jaimes, K.F.; Aller, S.G. Refined structures of mouse P-glycoprotein. Protein Sci., 2014, 23(1), 34-46.
[105]
Jin, M.S.; Oldham, M.L.; Zhang, Q.; Chen, J. Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature, 2012, 490(7421), 566-569.
[106]
Szewczyk, P.; Tao, H.; McGrath, A.P.; Villaluz, M.; Rees, S.D.; Lee, S.C.; Doshi, R.; Urbatsch, I.L.; Zhang, Q.; Chang, G. Snapshots of ligand entry, malleable binding and induced helical movement in P-glycoprotein. Acta Crystallogr. D., 2015, 71(Pt 3), 732-741.
[107]
Gutmann, D.A.; Ward, A.; Urbatsch, I.L.; Chang, G.; van Veen, H.W. Understanding polyspecificity of multidrug ABC transporters: closing in on the gaps in ABCB1. Trends Biochem. Sci., 2010, 35(1), 36-42.
[108]
Shapiro, A.B.; Fox, K.; Lam, P.; Ling, V. Stimulation of P-glycoprotein-mediated drug transport by prazosin and progesterone. Evidence for a third drug-binding site. Eur. J. Biochem., 1999, 259(3), 841-850.
[109]
Martin, C.; Berridge, G.; Higgins, C.F.; Mistry, P.; Charlton, P.; Callaghan, R. Communication between multiple drug binding sites on P-glycoprotein. Mol. Pharmacol., 2000, 58(3), 624-632.
[110]
Safa, A.R. Identification and characterization of the binding sites of P-glycoprotein for multidrug resistance-related drugs and modulators. Curr. Med. Chem. Anticancer Agents, 2004, 4(1), 1-17.
[111]
Martinez, L.; Arnaud, O.; Henin, E.; Tao, H.; Chaptal, V.; Doshi, R.; Andrieu, T.; Dussurgey, S.; Tod, M.; Di Pietro, A.; Zhang, Q.; Chang, G.; Falson, P. Understanding polyspecificity within the substrate-binding cavity of the human multidrug resistance P-glycoprotein. The FEBS J., 2014, 281(3), 673-682.
[112]
Shapiro, A.B.; Ling, V. Positively cooperative sites for drug transport by P-glycoprotein with distinct drug specificities. Eur. J. Biochem., 1997, 250(1), 130-137.
[113]
Hulpke, S.; Tomioka, M.; Kremmer, E.; Ueda, K.; Abele, R.; Tampe, R. Direct evidence that the N-terminal extensions of the TAP complex act as autonomous interaction scaffolds for the assembly of the MHC I peptide-loading complex. Cell. Mol. Life Sci., 2012, 69(19), 3317-3327.
[114]
Liu, F.; Zhang, Z.; Csanady, L.; Gadsby, D.C.; Chen, J. Molecular Structure of the Human CFTR Ion Channel Cell, 2012, 169(1), 85-95 e88.
[115]
Bakos, E.; Evers, R.; Szakacs, G.; Tusnady, G.E.; Welker, E.; Szabo, K.; de Haas, M.; van Deemter, L.; Borst, P.; Varadi, A.; Sarkadi, B. Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem., 1998, 273(48), 32167-32175.
[116]
Bakos, E.; Evers, R.; Calenda, G.; Tusnady, G.E.; Szakacs, G.; Varadi, A.; Sarkadi, B. Characterization of the amino-terminal regions in the human multidrug resistance protein (MRP1). J. Cell Sci., 2000, 113(Pt 24), 4451-4461.
[117]
Oldham, M.L.; Chen, J. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science, 2011, 332(6034), 1202-1205.
[118]
Zhang, Z.; Liu, F.; Chen, J. Conformational Changes of
CFTR upon Phosphorylation and ATP Binding. Cell, 2017, 170(3), 483-491 e488.
[119]
Qian, H.; Zhao, X.; Cao, P.; Lei, J.; Yan, N.; Gong, X. Structure of the Human Lipid Exporter ABCA1. Cell, 2017, 169(7), 1228-1239 e1210.
[120]
Lee, J.Y.; Kinch, L.N.; Borek, D.M.; Wang, J.; Wang, J.; Urbatsch, I.L.; Xie, X.S.; Grishin, N.V.; Cohen, J.C.; Otwinowski, Z.; Hobbs, H.H.; Rosenbaum, D.M. Crystal structure of the human sterol transporter ABCG5/ABCG8. Nature, 2016, 533(7604), 561-564.
[121]
Telbisz, A.; Hegedus, C.; Varadi, A.; Sarkadi, B.; Ozvegy-Laczka, C. Regulation of the function of the human ABCG2 multidrug transporter by cholesterol and bile acids: effects of mutations in potential substrate and steroid binding sites. Drug Metab. Dispos., 2014, 42(4), 575-585.
[122]
Ward, A.; Reyes, C.L.; Yu, J.; Roth, C.B.; Chang, G. Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. USA, 2007, 104(48), 19005-19010.
[123]
Brooks-Wilson, A.; Marcil, M.; Clee, S.M.; Zhang, L.H.; Roomp, K.; van Dam, M.; Yu, L.; Brewer, C.; Collins, J.A.; Molhuizen, H.O.; Loubser, O.; Ouelette, B.F.; Fichter, K.; Ashbourne-Excoffon, K.J.; Sensen, C.W.; Scherer, S.; Mott, S.; Denis, M.; Martindale, D.; Frohlich, J.; Morgan, K.; Koop, B.; Pimstone, S.; Kastelein, J.J.; Genest, J., Jr; Hayden, M.R. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet., 1999, 22(4), 336-345.
[124]
Perez, C.; Gerber, S.; Boilevin, J.; Bucher, M.; Darbre, T.; Aebi, M.; Reymond, J.L.; Locher, K.P. Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature, 2015, 524(7566), 433-438.
[125]
Hopfner, K.P.; Karcher, A.; Shin, D.S.; Craig, L.; Arthur, L.M.; Carney, J.P.; Tainer, J.A. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell, 2000, 101(7), 789-800.
[126]
Zoghbi, M.E.; Fuson, K.L.; Sutton, R.B.; Altenberg, G.A. Kinetics of the association/dissociation cycle of an ATP-binding cassette nucleotide-binding domain. J. Biol. Chem., 2012, 287(6), 4157-4164.
[127]
Zoghbi, M.E.; Cooper, R.S.; Altenberg, G.A. The Lipid Bilayer Modulates the Structure and Function of an ATP-binding Cassette Exporter. J. Biol. Chem., 2016, 291(9), 4453-4461.
[128]
Moeller, A.; Lee, S.C.; Tao, H.; Speir, J.A.; Chang, G.; Urbatsch, I.L.; Potter, C.S.; Carragher, B.; Zhang, Q. Distinct Conformational Spectrum of Homologous Multidrug ABC Transporters. Structure, 2015, 23(3), 450-460.
[129]
Marcoux, J.; Wang, S.C.; Politis, A.; Reading, E.; Ma, J.; Biggin, P.C.; Zhou, M.; Tao, H.; Zhang, Q.; Chang, G.; Morgner, N.; Robinson, C.V. Mass spectrometry reveals synergistic effects of nucleotides, lipids, and drugs binding to a multidrug resistance efflux pump. Proc. Natl. Acad. Sci. USA, 2013, 110(24), 9704-9709.
[130]
Pan, L.; Aller, S.G. Equilibrated atomic models of outward-facing P-glycoprotein and effect of ATP binding on structural dynamics. Sci. Rep., 2015, 5, 7880.
[131]
Lee, J.Y.; Urbatsch, I.L.; Senior, A.E.; Wilkens, S. Nucleotide-induced structural changes in P-glycoprotein observed by electron microscopy. J. Biol. Chem., 2008, 283(9), 5769-5779.
[132]
Lee, J.Y.; Urbatsch, I.L.; Senior, A.E.; Wilkens, S. Projection structure of P-glycoprotein by electron microscopy. Evidence for a closed conformation of the nucleotide binding domains. J. Biol. Chem., 2002, 277(42), 40125-40131.
[133]
Cooper, R.S.; Altenberg, G.A. Association/ dissociation of the nucleotide-binding domains of the ATP-binding cassette protein MsbA measured during continuous hydrolysis. J. Biol. Chem., 2013, 288(29), 20785-20796.
[134]
Zou, P.; Bortolus, M.; McHaourab, H.S. Conformational cycle of the ABC transporter MsbA in liposomes: detailed analysis using double electron-electron resonance spectroscopy. J. Mol. Biol., 2009, 393(3), 586-597.
[135]
Verhalen, B.; Dastvan, R.; Thangapandian, S.; Peskova, Y.; Koteiche, H.A.; Nakamoto, R.K.; Tajkhorshid, E.; McHaourab, H.S. Energy transduction and alternating access of the mammalian ABC transporter P-glycoprotein. Nature, 2017, 543(7647), 738-741.