References
- Agarwal, S., Sane, R., Oberoi, R., Ohlfest, J. R., & Elmquist, W. F. (2011). Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert Reviews in Molecular Medicine, 13, e17. https://doi.org/https://doi.org/10.1017/S1462399411001888
- Alam, A., Kowal, J., Broude, E. V., Roninson, I. B., & Locher, K. P. (2019). Structural insight into substrate and inhibitor discrimination by human P-glycoprotein. Science (New York, N.Y.), 363(6428), 753–756. https://doi.org/https://doi.org/10.1126/science.aav7102
- 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. (2009). Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science (New York, N.Y.), 323(5922), 1718–1722. https://doi.org/https://doi.org/10.1126/science.1168750
- Ambudkar, S. V., Dey, S., Hrycyna, C. A., Ramachandra, M., Pastan, I., & Gottesman, M. M. (1999). Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annual Review of Pharmacology and Toxicology, 39(1), 361–398. Retrieved from https://doi.org/https://doi.org/10.1146/annurev.pharmtox.39.1.361
- Baker, N. A., Sept, D., Joseph, S., Holst, M. J., & McCammon, J. A. (2001). Electrostatics of nanosystems: Application to microtubules and the ribosome. Proceedings of the National Academy of Sciences of the United States of America, 98(18), 10037–10041. https://doi.org/https://doi.org/10.1073/pnas.181342398
- Chan, P. F., Srikannathasan, V., Huang, J., Cui, H., Fosberry, A. P., Gu, M., Hann, M. M., Hibbs, M., Homes, P., Ingraham, K., Pizzollo, J., Shen, C., Shillings, A. J., Spitzfaden, C. E., Tanner, R., Theobald, A. J., Stavenger, R. A., Bax, B. D., & Gwynn, M. N. (2015). Structural basis of DNA gyrase inhibition by antibacterial QPT-1, anticancer drug etoposide and moxifloxacin. Nature Communications, 6, 10048. https://doi.org/https://doi.org/10.1038/ncomms10048
- Chandra, P., & Brouwer, K. L. (2004). The complexities of hepatic drug transport: Current knowledge and emerging concepts. Pharmaceutical Research, 21(5), 719–735. https://doi.org/https://doi.org/10.1023/B:PHAM.0000026420.79421.8f
- Chen, C. Y., Liu, N. Y., Lin, H. C., Lee, C. Y., Hung, C. C., & Chang, C. S. (2016). Synthesis and bioevaluation of novel benzodipyranone derivatives as P-glycoprotein inhibitors for multidrug resistance reversal agents. European Journal of Medicinal Chemistry, 118, 219–229. https://doi.org/https://doi.org/10.1016/j.ejmech.2016.03.070
- Chrencik, J. E., Staker, B. L., Burgin, A. B., Pourquier, P., Pommier, Y., Stewart, L., & Redinbo, M. R. (2004). Mechanisms of camptothecin resistance by human topoisomerase I mutations. Journal of Molecular Biology, 339(4), 773–784. https://doi.org/https://doi.org/10.1016/j.jmb.2004.03.077
- Clark, G. R., Pytel, P. D., & Squire, C. J. (2012). The high-resolution crystal structure of a parallel intermolecular DNA G-4 quadruplex/drug complex employing syn glycosyl linkages. Nucleic Acids Research, 40(12), 5731–5738. https://doi.org/https://doi.org/10.1093/nar/gks193
- Daniel, C., Bell, C., Burton, C., Harguindey, S., Reshkin, S. J., & Rauch, C. (2013). The role of proton dynamics in the development and maintenance of multidrug resistance in cancer. Biochimica et Biophysica Acta, 1832(5), 606–617. https://doi.org/https://doi.org/10.1016/j.bbadis.2013.01.020
- Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅ log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/https://doi.org/10.1063/1.464397
- Dean, M. (2009). ABC transporters, drug resistance, and cancer stem cells. Journal of Mammary Gland Biology and Neoplasia, 14(1), 3–9. https://doi.org/https://doi.org/10.1007/s10911-009-9109-9
- Dean, M., Fojo, T., & Bates, S. (2005). Tumour stem cells and drug resistance. Nature Reviews. Cancer, 5(4), 275–284. https://doi.org/https://doi.org/10.1038/nrc1590
- Domicevica, L., Koldsø, H., & Biggin, P. C. (2018). Multiscale molecular dynamics simulations of lipid interactions with P-glycoprotein in a complex membrane. Journal of Molecular Graphics & Modelling, 80, 147–156. https://doi.org/https://doi.org/10.1016/j.jmgm.2017.12.022
- Foster, S. A., Whalen, D. M., Özen, A., Wongchenko, M. J., Yin, J., Yen, I., Schaefer, G., Mayfield, J. D., Chmielecki, J., Stephens, P. J., Albacker, L. A., Yan, Y., Song, K., Hatzivassiliou, G., Eigenbrot, C., Yu, C., Shaw, A. S., Manning, G., Skelton, N. J., … Malek, S. (2016). Activation mechanism of oncogenic deletion mutations in BRAF, EGFR, and HER2. Cancer Cell, 29(4), 477–493. https://doi.org/https://doi.org/10.1016/j.ccell.2016.02.010
- Frisch, M. J. E. A., Trucks, G. W., Schlegel, H., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J., Vreven, T., Kudin, K.-N., Burant, J., Millam, J., Iyengar, S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, A., … Johnson, B. A. (2004). Gaussian 03, revision c.02. Gaussian Inc.
- Gajiwala, K. S., Feng, J., Ferre, R., Ryan, K., Brodsky, O., Weinrich, S., Kath, J. C., & Stewart, A. (2013). Insights into the aberrant activity of mutant EGFR kinase domain and drug recognition. Structure (London, England: 1993), 21(2), 209–219. https://doi.org/https://doi.org/10.1016/j.str.2012.11.014
- Gottesman, M. M., Fojo, T., & Bates, S. E. (2002). Multidrug resistance in cancer: Role of ATP-dependent transporters. Nature Reviews. Cancer, 2(1), 48–58. https://doi.org/https://doi.org/10.1038/nrc706
- Gutmann, D. A., Ward, A., Urbatsch, I. L., Chang, G., & van Veen, H. W. (2010). Understanding polyspecificity of multidrug ABC transporters: Closing in on the gaps in ABCB1. Trends in Biochemical Sciences, 35(1), 36–42. https://doi.org/https://doi.org/10.1016/j.tibs.2009.07.009
- Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
- Hirschfelder, J. O., Curtiss, C. F., Bird, R. B., & Mayer, M. G. (1954). Molecular theory of gases and liquids. Wiley.
- Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review. A, General Physics, 31(3), 1695–1697. https://doi.org/https://doi.org/10.1103/physreva.31.1695
- Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/https://doi.org/10.1016/0263-7855(96)00018-5
- Jones, P. M., & George, A. M. (2013). Mechanism of the ABC transporter ATPase domains: Catalytic models and the biochemical and biophysical record. Critical Reviews in Biochemistry and Molecular Biology, 48(1), 39–50. https://doi.org/https://doi.org/10.3109/10409238.2012.735644
- Kandt, C., Ash, W. L., & Tieleman, D. P. (2007). Setting up and running molecular dynamics simulations of membrane proteins. Methods (San Diego, Calif.), 41(4), 475–488. https://doi.org/https://doi.org/10.1016/j.ymeth.2006.08.006
- Kodaira, H., Kusuhara, H., Ushiki, J., Fuse, E., & Sugiyama, Y. (2010). Kinetic analysis of the cooperation of P-glycoprotein (P-gp/Abcb1) and breast cancer resistance protein (Bcrp/Abcg2) in limiting the brain and testis penetration of erlotinib, flavopiridol, and mitoxantrone. The Journal of Pharmacology and Experimental Therapeutics, 333(3), 788–796. https://doi.org/https://doi.org/10.1124/jpet.109.162321
- Komdeur, R., Plaat, B. E. C., van der Graaf, W. T. A., Hoekstra, H. J., Hollema, H., van den Berg, E., Zwart, N., Scheper, R. J., & Molenaar, W. M. (2003). Expression of multidrug resistance proteins, P-gp, MRP1 and LRP, in soft tissue sarcomas analysed according to their histological type and grade. European Journal of Cancer, 39(7), 909–916. https://doi.org/https://doi.org/10.1016/S0959-8049(03)00029-7
- Kumari, R., Kumar, R., & Lynn, A. M. (2014). g_mmpbsa – A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/https://doi.org/10.1021/ci500020m
- Li, J., Jaimes, K. F., & Aller, S. G. (2014). Refined structures of mouse P-glycoprotein. Protein Science, 23(1), 34–46. https://doi.org/https://doi.org/10.1002/pro.2387
- Li, J., Liu, S., Lakshminarayanan, R., Bai, Y., Pervushin, K., Verma, C., & Beuerman, R. W. (2013). Molecular simulations suggest how a branched antimicrobial peptide perturbs a bacterial membrane and enhances permeability. Biochimica et Biophysica Acta, 1828(3), 1112–1121. https://doi.org/https://doi.org/10.1016/j.bbamem.2012.12.015
- Loo, T. W., & Clarke, D. M. (2000). The packing of the transmembrane segments of human multidrug resistance P-glycoprotein is revealed by disulfide cross-linking analysis. The Journal of Biological Chemistry, 275(8), 5253–5256. https://doi.org/https://doi.org/10.1074/jbc.275.8.5253
- Loo, T. W., & Clarke, D. M. (2001). Defining the drug-binding site in the human multidrug resistance P-glycoprotein using a methanethiosulfonate analog of verapamil, MTS-verapamil. The Journal of Biological Chemistry, 276(18), 14972–14979. https://doi.org/https://doi.org/10.1074/jbc.M100407200
- Loo, T. W., & Clarke, D. M. (2002). Location of the rhodamine-binding site in the human multidrug resistance P-glycoprotein. The Journal of Biological Chemistry, 277(46), 44332–44338. https://doi.org/https://doi.org/10.1074/jbc.M208433200
- Lumen, A. A., Acharya, P., Polli, J. W., Ayrton, A., Ellens, H., & Bentz, J. (2010). If the KI is defined by the free energy of binding to P-glycoprotein, which kinetic parameters define the IC50 for the Madin-Darby canine kidney II cell line overexpressing human multidrug resistance 1 confluent cell monolayer? Drug Metabolism and Disposition: The Biological Fate of Chemicals, 38(2), 260–269. https://doi.org/https://doi.org/10.1124/dmd.109.029843
- Maki, N., Moitra, K., Silver, C., Ghosh, P., Chattopadhyay, A., & Dey, S. (2006). Modulator-induced interference in functional cross talk between the substrate and the ATP sites of human P-glycoprotein. Biochemistry, 45(8), 2739–2751. https://doi.org/https://doi.org/10.1021/bi0521745
- Mitscher, L. A., Pillai, S. P., Gentry, E. J., & Shankel, D. M. (1999). Multiple drug resistance. Medicinal Research Reviews, 19(6), 477–496. https://doi.org/10.1002/(sici)1098-1128(199911)19:6<477::aid-med2>3.3.co;2-n
- Mittra, R., Pavy, M., Subramanian, N., George, A. M., O’Mara, M. L., Kerr, I. D., & Callaghan, R. (2017). Location of contact residues in pharmacologically distinct drug binding sites on P-glycoprotein. Biochemical Pharmacology, 123, 19–28. https://doi.org/https://doi.org/10.1016/j.bcp.2016.10.002
- Nosé, S. (1984). A unified formulation of the constant temperature molecular dynamics methods. The Journal of Chemical Physics, 81(1), 511–519. https://doi.org/https://doi.org/10.1063/1.447334
- Paissoni, C., Spiliotopoulos, D., Musco, G., & Spitaleri, A. (2014). GMXPBSA 2.0: A GROMACS tool to perform MM/PBSA and computational alanine scanning. Computer Physics Communications, 185(11), 2920–2929. https://doi.org/https://doi.org/10.1016/j.cpc.2014.06.019
- Panagiotopoulou, V., Richardson, G., Jensen, O. E., & Rauch, C. (2010). On a biophysical and mathematical model of Pgp-mediated multidrug resistance: Understanding the “space–time” dimension of MDR. European Biophysics Journal: EBJ, 39(2), 201–211. https://doi.org/https://doi.org/10.1007/s00249-009-0555-5
- Park, J. H., Liu, Y., Lemmon, M. A., & Radhakrishnan, R. (2012). Erlotinib binds both inactive and active conformations of the EGFR tyrosine kinase domain. The Biochemical Journal, 448(3), 417–423. https://doi.org/https://doi.org/10.1042/BJ20121513
- Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/https://doi.org/10.1063/1.328693
- Pastan, I., & Gottesman, M. (1987). Multiple-drug resistance in human cancer. The New England Journal of Medicine, 316(22), 1388–1393. https://doi.org/https://doi.org/10.1056/NEJM198705283162207
- Pegan, S. D., Sturdy, M., Ferry, G., Delagrange, P., Boutin, J. A., & Mesecar, A. D. (2011). X-ray structural studies of quinone reductase 2 nanomolar range inhibitors. Protein Science, 20(7), 1182–1195. https://doi.org/https://doi.org/10.1002/pro.647
- Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/https://doi.org/10.1093/bioinformatics/btt055
- Qu, Q., & Sharom, F. J. (2002). Proximity of bound Hoechst 33342 to the ATPase catalytic sites places the drug binding site of P-glycoprotein within the cytoplasmic membrane leaflet. Biochemistry, 41(14), 4744–4752. https://doi.org/https://doi.org/10.1021/bi0120897
- Rees, D. C., Johnson, E., & Lewinson, O. (2009). ABC transporters: The power to change. Nature Reviews. Molecular Cell Biology, 10(3), 218–227. https://doi.org/https://doi.org/10.1038/nrm2646
- Ren, P., Chun, J., Thomas, D. G., Schnieders, M. J., Marucho, M., Zhang, J., & Baker, N. A. (2012). Biomolecular electrostatics and solvation: A computational perspective. Quarterly Reviews of Biophysics, 45(4), 427–491. https://doi.org/https://doi.org/10.1017/S003358351200011X
- Schinkel, A. H., & Jonker, J. W. (2012). Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: An overview. Advanced Drug Delivery Reviews, 64, 138–153. https://doi.org/https://doi.org/10.1016/j.addr.2012.09.027
- Sharom, F. J. (2008). ABC multidrug transporters: Structure, function and role in chemoresistance. Pharmacogenomics, 9(1), 105–127. https://doi.org/https://doi.org/10.2217/14622416.9.1.105
- Subramanian, N., Condic-Jurkic, K., Mark, A. E., & O’Mara, M. L. (2015). Identification of possible binding sites for morphine and nicardipine on the multidrug transporter P-glycoprotein using umbrella sampling techniques. Journal of Chemical Information and Modeling, 55(6), 1202–1217. https://doi.org/https://doi.org/10.1021/ci5007382
- Szewczyk, P., Tao, H., McGrath, A. P., Villaluz, M., Rees, S. D., Lee, S. C., Doshi, R., Urbatsch, I. L., Zhang, Q., & Chang, G. (2015). Snapshots of ligand entry, malleable binding and induced helical movement in P-glycoprotein. Acta Crystallographica. Section D, Biological Crystallography, 71(Pt 3), 732–741. https://doi.org/https://doi.org/10.1107/S1399004715000978
- Ter Beek, J., Guskov, A., & Slotboom, D. J. (2014). Structural diversity of ABC transporters. The Journal of General Physiology, 143(4), 419–435. https://doi.org/https://doi.org/10.1085/jgp.201411164
- Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/https://doi.org/10.1002/jcc.21334
- Verhalen, B., Dastvan, R., Thangapandian, S., Peskova, Y., Koteiche, H. A., Nakamoto, R. K., Tajkhorshid, E., & Mchaourab, H. S. (2017). Energy transduction and alternating access of the mammalian ABC transporter P-glycoprotein. Nature, 543(7647), 738–741. https://doi.org/https://doi.org/10.1038/nature21414
- Wallace, A. C., Laskowski, R. A., & Thornton, J. M. (1995). LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Engineering, 8(2), 127–134. https://doi.org/https://doi.org/10.1093/protein/8.2.127
- Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2001). Antechamber: An accessory software package for molecular mechanical calculations. Journal of the American Chemical Society, 222, U403.
- Wang, Y., Benz, F. W., Wu, Y., Wang, Q., Chen, Y., Chen, X., Li, H., Zhang, Y., Zhang, R., & Yang, J. (2016). Structural insights into the pharmacophore of vinca domain inhibitors of microtubules. Molecular Pharmacology, 89(2), 233–242. https://doi.org/https://doi.org/10.1124/mol.115.100149
- Wang, Z.-M., Ho, J. X., Ruble, J. R., Rose, J., Rüker, F., Ellenburg, M., Murphy, R., Click, J., Soistman, E., Wilkerson, L., & Carter, D. C. (2013). Structural studies of several clinically important oncology drugs in complex with human serum albumin. Biochimica et Biophysica Acta, 1830(12), 5356–5374. https://doi.org/https://doi.org/10.1016/j.bbagen.2013.06.032
- Wen, P. C., Verhalen, B., Wilkens, S., Mchaourab, H. S., & Tajkhorshid, E. (2013). On the origin of large flexibility of P-glycoprotein in the inward-facing state. The Journal of Biological Chemistry, 288(26), 19211–19220. https://doi.org/https://doi.org/10.1074/jbc.M113.450114
- Wu, C. C., Li, Y. C., Wang, Y. R., Li, T. K., & Chan, N. L. (2013). On the structural basis and design guidelines for type II topoisomerase-targeting anticancer drugs. Nucleic Acids Research, 41(22), 10630–10640. https://doi.org/https://doi.org/10.1093/nar/gkt828