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Research Articles

Computational binding affinity and molecular dynamic characterization of annonaceous acetogenins at nucleotide binding domain (NBD) of multi-drug resistance ATP-binding cassette sub-family B member 1 (ABCB1)

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Pages 821-832 | Received 23 Feb 2021, Accepted 28 Nov 2021, Published online: 15 Dec 2021

References

  • Abe, M., Kubo, A., Yamamoto, S., Hatoh, Y., Murai, M., Hattori, Y., Makabe, H., Nishioka, T., & Miyoshi, H. (2008). Dynamic function of the spacer region of acetogenins in the inhibition of bovine mitochondrial NADH-ubiquinone oxidoreductase (complex I). Biochemistry, 47(23), 6260–6266. https://doi.org/10.1021/bi800506s
  • Alali, F. Q., Liu, X. X., & McLaughlin, J. L. (2010). Annonaceous acetogenins: Recent progress. ChemInform, 30(28), no–no. https://doi.org/10.1002/chin.199928305
  • Aller, S. G. (2010). Structure of p-glycoprotein reveals a molecular basis for poly-specific drug binding. Biophysical Journal, 98(3), 755a. https://doi.org/10.1016/j.bpj.2009.12.4143
  • Ayati, A., Falahati, M., Irannejad, H., & Emami, S. (2012). Synthesis, in vitro antifungal evaluation and in silico study of 3-azolyl-4-chromanone phenylhydrazones. Daru: Journal of Faculty of Pharmacy, Tehran University of Medical Sciences, 20(1), 46 https://doi.org/10.1186/2008-2231-20-46
  • Brewer, F. K., Follit, C. A., Vogel, P. D., & Wise, J. G. (2014). In silico screening for inhibitors of P-glycoprotein that target the nucleotide binding domains. Molecular Pharmacology, 86(6), 716–726. https://doi.org/10.1124/mol.114.095414
  • Bunting, K. D. (2002). ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells, 20(1), 11–20. https://doi.org/10.1002/stem.200011
  • Caparros-Lefebvre, D., & Elbaz, A. (1999). Possible relation of atypical parkinsonism in the French West Indies with consumption of tropical plants: A case-control study. The Lancet, 354(9175), 281–286. https://doi.org/10.1016/S0140-6736(98)10166-6
  • Carmen Zafra-Polo, M., Figadère, B., Gallardo, T., Tormo, J. R., & Cortes, D. (1998). Natural acetogenins from Annonaceae, synthesis and mechanisms of action. Phytochemistry, 48(7), 1087–1117. https://doi.org/10.1016/S0031-9422(97)00917-5
  • Carugo, O., & Pongor, S. (2001). A normalized root-mean-square distance for comparing protein three-dimensional structures. Protein Science: A Publication of the Protein Society, 10(7), 1470–1473. https://doi.org/10.1110/ps.690101
  • Conseil, G., Baubichon-Cortay, H., Dayan, G., Jault, J.-M., Barron, D., & Di Pietro, A. (1998). Flavonoids: A class of modulators with bifunctional interactions at vicinal ATP- and Steroid-binding sites on Mouse P-glycoprotein. Proceedings of the National Academy of Sciences of the United States of America, 95(17), 9831–9836. https://doi.org/10.1073/pnas.95.17.9831
  • Dantzig, A. H., de Alwis, D. P., & Burgess, M. (2003). Considerations in the design and development of transport inhibitors as adjuncts to drug therapy. Advanced Drug Delivery Reviews, 55(1), 133–150. https://doi.org/10.1016/S0169-409X(02)00175-8
  • Degli Esposti, M., Ghelli, A., Ratta, M., Cortes, D., & Estornell, E. (1994). Natural substances (acetogenins) from the family Annonaceae are powerful inhibitors of Mitochondrial NADH dehydrogenase (Complex I). Biochemical Journal, 301(1), 161–167. https://doi.org/10.1042/bj3010161
  • Dilipkumar, J., & Agliandeshwari, D. (2017). Preparation & evaluation of Annona Muricata extract against cancer cells with modified release. PharmaTutor, 5(10), 63–106.
  • Ferreira, R. J., Ferreira, M. J. U., & dos Santos, D. J. (2012). Insights on P-glycoprotein’s efflux mechanism obtained by molecular dynamics simulations. Journal of Chemical Theory and Computation, 8(6), 1853–1864. https://doi.org/10.1021/ct300083m
  • Fu, L. W., He, L. R., Liang, Y. J., Chen, L. M., Xiong, H. Y., Yang, X. P., & Pan, Q. C. (2003). Experimental chemotherapy against xenografts derived from multidrug resistant KBv200 cells and parental drug-sensitive KB cells in nude mice by annonaceous acetogenin 89-2. Yao Xuexue Bao = Acta pharmaceuticaSinica, 38(8), 565–570.
  • Fu, L. W., Pan, Q. C., Liang, Y. J., & Huang, H. B. (1999). Circumvention of tumor multidrug resistance by a new annonaceousacetogenin: Atemoyacin-B. Zhongguoyao li Xue Bao = Acta pharmacologicaSinica, 20(5), 435–439.
  • Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
  • Giacomini, K. M., Huang, S. M., Tweedie, D. J., Benet, L. Z., Brouwer, K. L. R., Chu, X., Dahlin, A., Evers, R., Fischer, V., Hillgren, K. M., Hoffmaster, K. A., Ishikawa, T., Keppler, D., Kim, R. B., Lee, C. A., Niemi, M., Polli, J. W., Sugiyama, Y., Swaan, P. W., … Zhang, L., International Transporter Consortium (2010). Membrane transporters in drug development. Nature Reviews Drug Discovery, 9(3), 215–236. https://doi.org/10.1038/nrd3028
  • Gottesman, M. M., Ambudkar, S. V., & Xia, D. (2009). Structure of a multidrug transporter. Nature Biotechnology, 27(6), 546–547. https://doi.org/10.1038/nbt0609-546
  • Gutmann, D. A. P., 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/10.1016/j.tibs.2009.07.009
  • Hrycyna, C. A., Ramachandra, M., Ambudkar, S. V., Ko, Y. H., Pedersen, P. L., Pastan, I., & Gottesman, M. M. (1998). 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. The Journal of Biological Chemistry, 273(27), 16631–16634. https://doi.org/10.1074/jbc.273.27.16631
  • Jeevitha Priya, M., Vidyalakshmi, S., & Rajeswari, M. (2020). Study on reversal of ABCB1 Mediated multidrug resistance in colon cancer by acetogenins: An in-silico approach. Journal of Biomolecular Structure and Dynamics, 38, 1–12. https://doi.org/10.1080/07391102.2020.1855249
  • Jones, P. M., & George, A. M. (2014). A reciprocating twin-channel model for ABC transporters. Quarterly Reviews of Biophysics, 47(3), 189–220. https://doi.org/10.1017/S0033583514000031
  • Katayama, K., Noguchi, K., & Sugimoto, Y. (2014). Regulations of p-glycoprotein/abcb1/mdr1 in human cancer cells. New Journal of Science, 2014, 1–10. https://doi.org/10.1155/2014/476974
  • Kim, I.-W., Peng, X. H., Sauna, Z. E., FitzGerald, P. C., Xia, D., Müller, M., Nandigama, K., & Ambudkar, S. V. (2006). The conserved tyrosine residues 401 and 1044 in ATP sites of human P-glycoprotein are critical for ATP binding and hydrolysis: Evidence for a conserved subdomain, the A-loop in the ATP-binding cassette. Biochemistry, 45(24), 7605–7616. https://doi.org/10.1021/bi060308o
  • Kim, Y. J., & Chen, J. (2018). Molecular structure of human P-glycoprotein in the ATP-bound, outward-facing conformation. Science 359, 915–919. https://doi.org/10.2210/pdb6c0v/pdb
  • Lannuzel, A., Michel, P. P., Caparros-Lefebvre, D., Abaul, J., Hocquemiller, R., & Ruberg, M. (2002). Toxicity of Annonaceae for dopaminergic neurons: Potential role in atypical parkinsonism in Guadeloupe. Movement Disorders: Official Journal of the Movement Disorder Society, 17(1), 84–90. https://doi.org/10.1002/mds.1246
  • Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51(10), 2778–2786. https://doi.org/10.1021/ci200227u
  • Linn, S. C., & Giaccone, G. (1995). Mdr1/p-glycoprotein expression in colorectal cancer. European Journal of Cancer, 31(7–8), 1291–1294. https://doi.org/10.1016/0959-8049(95)00278-Q
  • Lipinski, C. A. (2004). Lead- and drug-like compounds: THE rule-of-five revolution. Drug Discovery Today Technologies, 1(4), 337–341. https://doi.org/10.1016/j.ddtec.2004.11.007
  • Lippert, T., Ruoff, H. J., & Volm, M. (2008). Intrinsic and acquired drug resistance in malignant tumors. The main reason for therapeutic failure. Arzneimittel-Forschung, 58(6), 261–264. https://doi.org/10.1055/s-0031-1296504
  • Liu, M., Hou, T., Feng, Z., & Li, Y. (2013). The flexibility of P-glycoprotein for its poly-specific drug binding from molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 31(6), 612–629. https://doi.org/10.1080/07391102.2012.706079
  • Liu, T., Liu, X., Xiong, H., Xu, C., Yao, J., Zhu, X., Zhou, J., & Yao, J. (2018). Mechanisms of TPGS and its derivatives inhibiting P-glycoprotein efflux pump and application for reversing multidrug resistance in hepatocellular carcinoma. Polymer Chemistry, 9(14), 1827–1839. https://doi.org/10.1039/C8PY00344K
  • Martin, C., Berridge, G., Higgins, C. F., Mistry, P., Charlton, P., & Callaghan, R. (2000). Communication between multiple drug binding sites on P-glycoprotein. Molecular Pharmacology, 58(3), 624–632. https://doi.org/10.1124/mol.58.3.624
  • Mishra, J., Drummond, J., Quazi, S. H., Karanki, S. S., Shaw, J. J., Chen, B., & Kumar, N. (2013). Prospective of colon cancer treatments and scope for combinatorial approach to enhanced cancer cell apoptosis. Critical Reviews in Oncology/Hematology, 86(3), 232–250. https://doi.org/10.1016/j.critrevonc.2012.09.014
  • O’Mara, M. L., & Mark, A. E. (2012). The effect of environment on the structure of a Membrane Protein: P-glycoprotein under physiological conditions. Journal of Chemical Theory and Computation, 8(10), 3964–3976. https://doi.org/10.1021/ct300254y
  • Ozben, T. (2006). Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Letters, 580(12), 2903–2909. https://doi.org/10.1016/j.febslet.2006.02.020
  • Palmeira, A., Sousa, E., H., Vasconcelos, MM., & Pinto, M. (2012). Three decades of P-gp Inhibitors: Skimming through several generations and scaffolds. Current Medicinal Chemistry, 19(13), 1946–2025. https://doi.org/10.2174/092986712800167392
  • Qian, J. Q., Sun, P., Pan, Z. Y., & Fang, Z. Z. (2015). Annonaceous acetogenins reverses drug resistance of human hepatocellular carcinoma BEL-7402/5-FU and HepG2/ADM cell lines. International Journal of Clinical and Experimental Pathology, 8(9), 11934–11944.
  • Sachs, J., Döhl, K., Weber, A., Bonus, M., Ehlers, F., Fleischer, E., Klinger, A., Gohlke, H., Pietruszka, J., Schmitt, L., & Teusch, N. (2019). Novel 3,4-dihydroisocoumarins inhibit human P-gp and BCRP in multidrug resistant tumors and Demonstrate substrate inhibition of Yeast pdr5. Frontiers in Pharmacology, 10, 400. https://doi.org/10.3389/fphar.2019.00400
  • Saeed, M., Kadioglu, O., Khalid, H., Sugimoto, Y., & Efferth, T. (2015). Activity of the dietary flavonoid, apigenin, against multidrug-resistant tumor cells as determined by pharmacogenomics and molecular docking. The Journal of Nutritional Biochemistry, 26(1), 44–56. https://doi.org/10.1016/j.jnutbio.2014.09.008
  • Salentin, S., Schreiber, S., Haupt, V. J., Adasme, M. F., & Schroeder, M. (2015). PLIP: Fully automated protein–ligand interaction profiler. Nucleic Acids Research, 43(W1), W443–W447. https://doi.org/10.1093/nar/gkv315
  • Sauna, Z. E., & Ambudkar, S. V. (2007). About a switch: How P-glycoprotein (ABCB1) harnesses the energy of ATP binding and hydrolysis to do mechanical work. Molecular Cancer Therapeutics, 6(1), 13–23. https://doi.org/10.1158/1535-7163.MCT-06-0155
  • Schrödinger Release 2019-1a.(2019). Glide. Schrödinger, LLC.
  • Schrödinger Release 2019-1b.(2019). Prime. Schrödinger, LLC.
  • Schrödinger Release 2019-1c. (2019). Protein preparation wizard. Epik. Schrödinger, LLC.
  • Schrodinger release 2019-1d. (2019). QikProp. Schrödinger, LLC.
  • Schrödinger Release 2019-1e. (2019). LigPrep. Schrödinger, LLC.
  • Schrödinger Release 2019-1f. (2019). Desmond molecular dynamics system. D. E. Shaw Research.; Maestro-Desmond interoperability tools. Schrödinger.
  • Shapiro, A. B., & Ling, V. (1997). Positively cooperative sites for drug transport by P-glycoprotein with distinct drug specificities. European Journal of Biochemistry, 250(1), 130–137. https://doi.org/10.1111/j.1432-1033.1997.00130.x
  • Shapiro, A. B., Fox, K., Lam, P., & Ling, V. (1999). Stimulation of P-glycoprotein-mediated drug transport by prazosin and progesterone. Evidence for a third drug-binding site. European Journal of Biochemistry, 259(3), 841–850. https://doi.org/10.1046/j.1432-1327.1999.00098.x
  • Sharom, F. J. (2006). Shedding light on drug transport: Structure and function of the P-glycoprotein multidrug transporter (ABCB1). Biochemistry and Cell Biology = Biochimie et Biologie Cellulaire, 84(6), 979–992. https://doi.org/10.1139/o06-199
  • Srivalli, K. M., & Lakshmi, P. K. (2012). Overview of P-glycoprotein inhibitors: A rational outlook. Brazilian Journal of Pharmaceutical Sciences, 48(3), 353–367. https://doi.org/10.1590/S1984-82502012000300002
  • Thomas, H., & Coley, H. M. (2003). Overcoming multidrug resistance in cancer: An update on the clinical strategy of Inhibiting P-glycoprotein. Cancer Control: Journal of the Moffitt Cancer Center, 10(2), 159–165. https://doi.org/10.1177/107327480301000207
  • Urbatsch, I. L., Beaudet, L., Carrier, I., & Gros, P. (1998). Mutations in either nucleotide-binding site of P-glycoprotein (Mdr3) prevent vanadate trapping of nucleotide at both sites. Biochemistry, 37(13), 4592–4602. https://doi.org/10.1021/bi9728001
  • Volm, M., & Efferth, T. (2015). Prediction of cancer drug resistance and implications for personalized medicine. Frontiers in Oncology, 5, 282. https://doi.org/10.3389/fonc.2015.00282
  • Wan, C. K., Zhu, G. Y., Shen, X. L., Chattopadhyay, A., Dey, S., & Fong, W. F. (2006). Gomisin a alters substrate interaction and reverses P-glycoprotein-mediated multidrug resistance In HepG2-DR cells. Biochemical Pharmacology, 72(7), 824–837. https://doi.org/10.1016/j.bcp.2006.06.036
  • 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/10.1074/jbc.M113.450114
  • Wolvetang, E. J., Johnson, K. L., Krauer, K., Ralph, S. J., & Linnane, A. W. (1994). Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Letters, 339(1–2), 40–44. https://doi.org/10.1016/0014-5793(94)80380-3
  • Yang, R., Cui, L., Hou, Y. X., Riordan, J. R., & Chang, X. B. (2003). ATP binding to the first nucleotide binding domain of multidrug resistance-associated protein plays a regulatory role at low nucleotide concentration, whereas ATP Hydrolysis at the second plays a dominant role in ATP-dependent leukotriene C4 transport. The Journal of Biological Chemistry, 278(33), 30764–30771. https://doi.org/10.1074/jbc.M304118200
  • Yuan, S., Chan, H. C. S., & Hu, Z. (2017). Using pymol as a platform for computational drug design. WIREs Computational Molecular Science, 7(2), e1298. https://doi.org/10.1002/wcms.1298
  • Zafra-Polo, M. C., González, M. C., Estornell, E., Sahpaz, S., & Cortes, D. (1996). Acetogenins from Annonaceae, inhibitors of mitochondrial complex I. Phytochemistry, 42(2), 253–271. https://doi.org/10.1016/0031-9422(95)00836-5
  • Zhang, S., & Morris, M. E. (2003). Effects of the flavonoids Biochanin a, morin, Phloretin, and silymarin on P-glycoprotein-mediated transport. The Journal of Pharmacology and Experimental Therapeutics, 304(3), 1258–1267. https://doi.org/10.1124/jpet.102.044412
  • Zhang, Z., Ma, C., Li, P., Wu, M., Ye, S., Fu, L., & Xu, J. (2019). Reversal effect OF Fw-04-806, a macrolide dilactone compound, on multidrug resistance mediated by abcb1 and ABCG2 in vitro and in vivo. Cell Communication and Signaling, 17(1), 110. https://doi.org/10.1186/s12964-019-0408-5
  • Zorofchian Moghadamtousi, S., Rouhollahi, E., Karimian, H., Fadaeinasab, M., Firoozinia, M., Ameen Abdulla, M., & Abdul Kadir, H. (2015). The chemopotential effect of annona muricata leaves against Azoxymethane-induced colonic aberrant crypt foci in rats and the apoptotic effect of acetogenin annomuricin E in HT-29 cells: A bioassay-guided approach. PLoS One, 10(4), e0122288. https://doi.org/10.1371/journal.pone.0122288

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