REFERENCES
1. Gillet JP, Gottesman MM. Mechanisms of multidrug resistance in cancer. Methods Mol Biol 2010;596:47-76.
2. Gottesman MM, Ling V. The molecular basis of multidrug resistance in cancer: the early years of P-glycoprotein research. FEBS Lett 2006;580:998-1009.
3. Gottesman MM, Pastan I. The multidrug transporter, a double-edged sword. J Biol Chem 1988;263:12163-6.
4. Dano K. Cross resistance between vinca alkaloids and anthracyclines in Ehrlich ascites tumor in vivo. Cancer Chemother Rep 1972;56:701-8.
5. Kessel D, Botterill V, Wodinsky I. Uptake and retention of daunomycin by mouse leukemic cells as factors in drug response. Cancer Res 1968;28:938-41.
6. Ling V, Thompson LH. Reduced permeability in CHO cells as a mechanism of resistance to colchicine. J Cell Physiol 1974;83:103-16.
7. Dano K. Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim Biophys Acta 1973;323:466-83.
8. See YP, Carlsen SA, Till JE, Ling V. Increased drug permeability in Chinese hamster ovary cells in the presence of cyanide. Biochim Biophys Acta 1974;373:242-52.
9. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976;455:152-62.
10. Riordan JR, Ling V. Purification of P-glycoprotein from plasma membrane vesicles of Chinese hamster ovary cell mutants with reduced colchicine permeability. J Biol Chem 1979;254:12701-5.
11. Robertson SM, Ling V, Stanners CP. Co-amplification of double minute chromosomes, multiple drug resistance, and cell surface P-glycoprotein in DNA-mediated transformants of mouse cells. Mol Cell Biol 1984;4:500-6.
13. Fojo AT, Ueda K, Slamon DJ, Poplack DG, Gottesman MM, et al. Expression of a multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci U S A 1987;84:265-9.
14. Beck WT, Mueller TJ, Tanzer LR. Altered surface membrane glycoproteins in Vinca alkaloid-resistant human leukemic lymphoblasts. Cancer Res 1979;39:2070-6.
15. Kartner N, Riordan JR, Ling V. Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 1983;221:1285-8.
16. Ueda K, Cornwell MM, Gottesman MM, Pastan I, Roninson IB, et al. The mdr1 gene, responsible for multidrug-resistance, codes for P-glycoprotein. Biochem Biophys Res Commun 1986;141:956-62.
17. Bell DR, Gerlach JH, Kartner N, Buick RN, Ling V. Detection of P-glycoprotein in ovarian cancer: a molecular marker associated with multidrug resistance. J Clin Oncol 1985;3:311-5.
18. Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res 1981;41:1967-72.
19. List AF, Kopecky KJ, Willman CL, Head DR, Persons DL, et al. Benefit of cyclosporine modulation of drug resistance in patients with poor-risk acute myeloid leukemia: a Southwest Oncology Group study. Blood 2001;98:3212-20.
20. Sugawara I, Kataoka I, Morishita Y, Hamada H, Tsuruo T, et al. Tissue distribution of P-glycoprotein encoded by a multidrug-resistant gene as revealed by a monoclonal antibody, MRK 16. Cancer Res 1988;48:1926-9.
21. Tatsuta T, Naito M, Oh-hara T, Sugawara I, Tsuruo T. Functional involvement of P-glycoprotein in blood-brain barrier. J Biol Chem 1992;267:20383-91.
22. Sparreboom A, van Asperen J, Mayer U, Schinkel AH, Smit JW, et al. Limited oral bioavailability and active epithelial excretion of paclitaxel (Taxol) caused by P-glycoprotein in the intestine. Proc Natl Acad Sci U S A 1997;94:2031-5.
23. Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barier and to increased sensitivity to drugs. Cell 1994;77:491-502.
24. Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, et al. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 1986;47:381-9.
25. Gerlach JH, Endicott JA, Juranka PF, Henderson G, Sarangi F, et al. Homology between P-glycoprotein and a bacterial haemolysin transport protein suggests a model for multidrug resistance. Nature 1986;324:485-9.
26. Gros P, Ben Neriah YB, Croop JM, Housman DE. Isolation and expression of a complementary DNA that confers multidrug resistance. Nature 1986;323:728-31.
27. Roninson IB, Chin JE, Choi KG, Gros P, Housman DE, et al. Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells. Proc Natl Acad Sci U S A 1986;83:4538-42.
28. Hamada H, Tsuruo T. Purification of the 170- to 180-kilodalton membrane glycoprotein associated with multidrug resistance. 170- to 180-kilodalton membrane glycoprotein is an ATPase. J Biol Chem 1988;263:1454-8.
29. Germann UA, Willingham MC, Pastan I, Gottesman MM. Expression of the human multidrug transporter in insect cells by a recombinant baculovirus. Biochemistry 1990;29:2295-03.
30. Horio M, Gottesman MM, Pastan I. ATP-dependent transport of vinblastine in vesicles from human multidrug-resistant cells. Proc Natl Acad Sci U S A 1988;85:3580-4.
31. Ambudkar SV, Lelong IH, Zhang J, Cardarelli CO, Gottesman MM, et al. Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drug-stimulatable ATP hydrolysis. Proc Natl Acad Sci U S A 1992;89:8472-6.
32. Sarkadi B, Price EM, Boucher RC, Germann UA, Scarborough GA. Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J Biol Chem 1992;267:4854-8.
33. al-Shawi MK, Senior AE. Characterization of the adenosine triphosphatase activity of Chinese hamster P-glycoprotein. J Biol Chem 1993;268:4197-06.
34. Urbatsch IL, Beaudet L, Carrier I, Gros P. Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry 1998;37:4592-602.
35. Omote H, Figler RA, Polar MK, Al-Shawi MK. Improved energy coupling of human P-glycoprotein by the glycine 185 to valine mutation. Biochemistry 2004;43:3917-28.
36. Urbatsch IL, Sankaran B, Weber J, Senior AE. P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J Biol Chem 1995;270:19383-90.
37. Senior AE, al-Shawi MK, Urbatsch IL. The catalytic cycle of P-glycoprotein. FEBS Lett 1995;377:285-9.
38. Loo TW, Clarke DM. Inhibition of oxidative cross-linking between engineered cysteine residues at positions 332 in predicted transmembrane segments (TM) 6 and 975 in predicted TM12 of human P-glycoprotein by drug substrates. J Biol Chem 1996;271:27482-7.
39. Loo TW, Clarke DM. Identification of residues in the drug-binding site of human P-glycoprotein using a thiol-reactive substrate. J Biol Chem 1997;272:31945-8.
40. Loo TW, Clarke DM. Identification of residues in the drug-binding domain of human P-glycoprotein. Analysis of transmembrane segment 11 by cysteine-scanning mutagenesis and inhibition by dibromobimane. J Biol Chem 1999;274:35388-92.
41. Loo TW, Clarke DM. Identification of residues within the drug-binding domain of the human multidrug resistance P-glycoprotein by cysteine-scanning mutagenesis and reaction with dibromobimane. J Biol Chem 2000;275:39272-8.
42. Loo TW, Clarke DM. Defining the drug-binding site in the human multidrug resistance P-glycoprotein using a methanethiosulfonate analog of verapamil, MTS-verapamil. J Biol Chem 2001;276:14972-9.
43. Bruggemann EP, Currier SJ, Gottesman MM, Pastan I. Characterization of the azidopine and vinblastine binding site of P-glycoprotein. J Biol Chem 1992;267:21020-6.
44. Dey S, Ramachandra M, Pastan I, Gottesman MM, Ambudkar SV. Evidence for two nonidentical drug-interaction sites in the human P-glycoprotein. Proc Natl Acad Sci U S A 1997;94:10594-9.
45. Martin C, Berridge G, Higgins CF, Mistry P, Charlton P, et al. Communication between multiple drug binding sites on P-glycoprotein. Mol Pharmacol 2000;58:624-32.
46. Jin MS, Oldham ML, Zhang Q, Chen J. Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 2012;490:566-9.
47. Higgins CF, Gottesman MM. Is the multidrug transporter a flippase? Trends Biochem Sci 1992;17:18-21.
48. Homolya L, Hollo Z, Germann UA, Pastan I, Gottesman MM, et al. Fluorescent cellular indicators are extruded by the multidrug resistance protein. J Biol Chem 1993;268:21493-6.
49. Raviv Y, Pollard HB, Bruggemann EP, Pastan I, Gottesman MM. Photosensitized labeling of a functional multidrug transporter in living drug-resistant tumor cells. J Biol Chem 1990;265:3975-80.
50. Ramachandra M, Ambudkar SV, Chen D, Hrycyna CA, Dey S, et al. Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry 1998;37:5010-9.
51. Loo TW, Clarke DM. Recent progress in understanding the mechanism of P-glycoprotein-mediated drug efflux. J Membr Biol 2005;206:173-85.
52. Qu Q, Sharom FJ. FRET analysis indicates that the two ATPase active sites of the P-glycoprotein multidrug transporter are closely associated. Biochemistry 2001;40:1413-22.
53. Sauna ZE, Kim IW, Nandigama K, Kopp S, Chiba P, et al. 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;46:13787-99.
54. Zoghbi ME, Mok L, Swartz DJ, Singh A, Fendley GA, et al. Substrate-induced conformational changes in the nucleotide-binding domains of lipid bilayer-associated P-glycoprotein during ATP hydrolysis. J Biol Chem 2017;292:20412-24.
55. Patzlaff JS, van der Heide T, Poolman B. The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J Biol Chem 2003;278:29546-51.
56. Sauna ZE, Muller M, Peng XH, Ambudkar SV. Importance of the conserved Walker B glutamate residues, 556 and 1201, for the completion of the catalytic cycle of ATP hydrolysis by human P-glycoprotein (ABCB1). Biochemistry 2002;41:13989-4000.
57. Krupka RM. Uncoupled active transport mechanisms accounting for low selectivity in multidrug carriers: P-glycoprotein and SMR antiporters. J Membr Biol 1999;172:129-43.
58. van Veen HW, Margolles A, Muller M, Higgins CF, Konings WN. The homodimerric ATP-binding cassette transporter LmrA mediates multidrug transport by an alternating two-site (two-cylinder engine) mechanism. EMBO J 2000;19:2503-14.
59. Higgins CF, Linton KJ. The ATP switch model for ABC transporters. Nat Struct Mol Bio 2004;11:918-26.
61. Hrycyna CA, Ramachandra M, Ambudkar SV, Ko YH, Pedersen PL, et al. Mechanism of action of human P-glycoprotein ATPase activity. Photochemical cleavage during a catalytic transition state using orthovanadate reveals cross-talk between the two ATP sites. J Biol Chem 1998;273:16631-4.
62. Tombline G, Bartholomew LA, Tyndall GA, Gimi K, Urbatsch IL, et al. Properties of P-glycoprotein with mutations in the "catalytic carboxylate" glutamate residues. J Biol Chem 2004;279:46518-26.
63. Urbatsch IL, Sankaran B, Bhagat S, Senior AE. Both P-glycoprotein nucleotide-binding sites are catalytically active. J Biol Chem 1995;270:26956-61.
64. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009;323:1718-22.
65. Li J, Jaimes KF, Aller SG. Refined structures of mouse P-glycoprotein. Protein Sci 2014;23:34-46.
66. Esser L, Zhou F, Pluchino KM, Shiloach J, Ma J, et al. Structures of the Multidrug Transporter P-glycoprotein Reveal Asymmetric ATP Binding and the Mechanism of Polyspecificity. J Biol Chem 2017;292:446-61.
67. Dawson RJ, Locher KP. Structure of a bacterial multidrug ABC transporter. Nature 2006;443:180-5.
68. Reyes CL, Chang G. Lipopolysaccharide stabilizes the crystal packing of the ABC transporter MsbA. Acta Crystallograph Sect F Struct Biol Cryst Commun 2005;61:655-8.
69. Kim Y, Chen J. Molecular structure of human P-glycoprotein in the ATP-bound, outward-facing conformation. Science 2018;359:915-9.
70. Alam A, Kowal J, Broude E, Roninson I, Locher KP. Structural insight into substrate and inhibitor discrimination by human P-glycoprotein. Science 2019;363:753-6.
71. Alam A, Kung R, Kowal J, McLeod RA, Tremp N, et al. Structure of a zosuquidar and UIC2-bound human-mouse chimeric ABCB1. Proc Natl Acad Sci U S A 2018;115:E1973-82.
72. Kodan A, Yamaguchi T, Nakatsu T, Sakiyama K, Hipolito CJ, et al. Structural basis for gating mechanisms of a eukaryotic P-glycoprotein homolog. Proc Natl Acad Sci U S A 2014;111:4049-54.
73. Ward A, Reyes CL, Yu J, Roth CB, Chang G. Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc Natl Acad Sci U S A 2007;104:19005-10.
74. Ward AB, Szewczyk P, Grimard V, Lee CW, Martinez L, et al. Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain. Proc Natl Acad Sci U S A 2013;110:13386-91.
75. Szewczyk P, Tao H, McGrath AP, Villaluz M, Rees SD, et al. Snapshots of ligand entry, malleable binding and induced helical movement in P-glycoprotein. Acta Crystallogr D Biol Crystallogr 2015;71:732-41.
76. Nicklisch SC, Rees SD, McGrath AP, Gokirmak T, Bonito LT, et al. Global marine pollutants inhibit P-glycoprotein: environmental levels, inhibitory effects, and cocrystal structure. Sci Adv 2016;2:e1600001.
77. Khare D, Oldham ML, Orelle C, Davidson AL, Chen J. Alternating access in maltose transporter mediated by rigid-body rotations. Mol Cell 2009;33:528-36.
78. Hrycyna CA, Airan LE, Germann UA, Ambudkar SV, Pastan I, et al. Structural flexibility of the linker region of human P-glycoprotein permits ATP hydrolysis and drug transport. Biochemistry 1998;37:13660-73.
79. Sato T, Kodan A, Kimura Y, Ueda K, Nakatsu T, et al. Functional role of the linker region in purified human P-glycoprotein. FEBS J 2009;276:3504-16.
80. Chen J. Molecular mechanism of the Escherichia coli maltose transporter. Curr Opin Struct Biol 2013;23:492-8.
81. Locher KP. Review. Structure and mechanism of ATP-binding cassette transporters. Philos Trans R Soc Lond B Biol Sci 2009;364:239-45.
82. Verhalen B, Dastvan R, Thangapandian S, Peskova Y, Koteiche HA, et al. Energy transduction and alternating access of the mammalian ABC transporter P-glycoprotein. Nature 2017;543:738-41.
83. Hrycyna CA, Ramachandra M, Germann UA, Cheng PW, Pastan I, et al. Both ATP sites of human P-glycoprotein are essential but not symmetric. Biochemistry 1999;38:13887-99.
84. Loo TW, Clarke DM. Covalent modification of human P-glycoprotein mutants containing a single cysteine in either nucleotide-binding fold abolishes drug-stimulated ATPase activity. J Biol Chem 1995;270:22957-61.
85. Sankaran B, Bhagat S, Senior AE. Inhibition of P-glycoprotein ATPase activity by beryllium fluoride. Biochemistry 1997;36:6847-53.
86. Tombline G, Bartholomew L, Gimi K, Tyndall GA, Senior AE. Synergy between conserved ABC signature Ser residues in P-glycoprotein catalysis. J Biol Chem 2004;279:5363-73.
87. Li MJ, Guttman M, Atkins WM. Conformational dynamics of P-glycoprotein in lipid nanodiscs and detergent micelles reveal complex motions on a wide time scale. J Biol Chem 2018;293:6297-307.
88. Tombline G, Bartholomew LA, Urbatsch IL, Senior AE. Combined mutation of catalytic glutamate residues in the two nucleotide binding domains of P-glycoprotein generates a conformation that binds ATP and ADP tightly. J Biol Chem 2004;279:31212-20.
89. Loo TW, Clarke DM. Identification of the distance between P-glycoprotein's homologous halves that triggers the high/low ATPase activity switch. J Biol Chem 2014;289:8484-92.
90. Wen PC, Verhalen B, Wilkens S, McHaourab HS, Tajkhorshid E. On the Origin of Large Flexibility of P-glycoprotein in the Inward-Facing State. J Biol Chem 2013;288:19211-20.
91. Loo TW, Bartlett MC, Clarke DM. Simultaneous binding of two different drugs in the binding pocket of the human multidrug resistance P-glycoprotein. J Biol Chem 2003;278:39706-10.
92. Frank GA, Shukla S, Rao P, Borgnia MJ, Bartesaghi A, et al. Cryo-EM Analysis of the Conformational Landscape of Human P-glycoprotein (ABCB1) During its Catalytic Cycle. Mol Pharmacol 2016;90:35-41.
93. Moeller A, Lee SC, Tao H, Speir JA, Chang G, et al. Distinct conformational spectrum of homologous multidrug ABC transporters. Structure 2015;23:450-60.
94. Sigdel KP, Wilt LA, Marsh BP, Roberts AG, King GM. The conformation and dynamics of P-glycoprotein in a lipid bilayer investigated by atomic force microscopy. Biochem Pharmacol 2018;156:302-11.
95. Choudhury HG, Tong Z, Mathavan I, Li Y, Iwata S, et al. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state. Proc Natl Acad Sci U S A 2014;111:9145-50.
96. Smith PC, Karpowich N, Millen L, Moody JE, Rosen J, et al. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 2002;10:139-49.
97. Siarheyeva A, Liu R, Sharom FJ. Characterization of an asymmetric occluded state of P-glycoprotein with two bound nucleotides: implications for catalysis. J Biol Chem 2010;285:7575-86.