A significant mechanism of molecular recognition between bioflavonoids and P-glycoprotein leading to herb-drug interactions

References

• Badhan R, Penny J. 2006. In silico modelling of the interaction of flavonoids with human P-glycoprotein nucleotide-binding domain. Eur J Med Chem. 41:285–295.
   PubMed Web of Science ®Google Scholar
• Chung S, Sung M, Kim N, Jang J, Go E, Lee H. 2005. Inhibition of P-glycoprotein by natural products in human breast cancer cells. Arch Pharm Res. 28:823–828.
   PubMed Web of Science ®Google Scholar
• Dewitte RS, Shakhnovich EI. 1996. SMoG: de novo design method based on simple, fast, and accurate free energy estimates. 1. Methodology and supporting evidence. J Am Chem Soc. 118:11733–11744.
   Web of Science ®Google Scholar
• Di Pietro A, Conseil G, Pérez-Victoria JM, Dayan G, Baubichon-Cortay H, Trompier D, Steinfels E, Jault JM, De Wet H, Maitrejean M, et al. 2002. Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. CMLS. 59:307–322.
   PubMed Web of Science ®Google Scholar
• Dickson CJ, Madej BD, Skjevik ÅA, Betz RM, Teigen K, Gould IR, Walker RC. 2014. Lipid14: the amber lipid force field. J Chem Theory Comput. 10:865–879.
   PubMed Web of Science ®Google Scholar
• Eaton BE, Gold L, Zichi DA. 1995. Let’s get specific: the relationship between specificity and affinity. Chem Biol. 2:633–638.
   PubMed Web of Science ®Google Scholar
• El-Readi MZ, Hamdan D, Farrag N, El-Shazly A, Wink M. 2010. Inhibition of P-glycoprotein activity by limonin and other secondary metabolites from Citrus species in human colon and leukaemia cell lines. Eur J Pharmacol. 626:139–145.
   PubMed Web of Science ®Google Scholar
• Fenner KS, Troutman MD, Kempshall S, Cook JA, Ware JA, Smith DA, Lee CA. 2009. Drug–drug interactions mediated through P-glycoprotein: clinical relevance and in vitro-in vivo correlation using digoxin as a probe drug. Clin Pharmacol Ther. 85:173–181.
   PubMed Web of Science ®Google Scholar
• Gadhe CG, Kothandan G, Cho SJ. 2013. In silico study of desmosdumotin as an anticancer agent: homology modeling, docking and molecular dynamics simulation approach. ACAMC. 13:1636–1644.
   Google Scholar
• Götz AW, Williamson MJ, Xu D, Poole D, Le Grand S, Walker RC. 2012. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J Chem Theory Comput. 8:1542–1555.
   PubMed Web of Science ®Google Scholar
• Gyémant N, Tanaka M, Antus S, Hohmann J, Csuka O, Mandoky L, Molnar J. 2005. In vitro search for synergy between flavonoids and epirubicin on multidrug-resistant cancer cells. In Vivo. 19:367–374.
   PubMed Web of Science ®Google Scholar
• Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J Mol Graph.14:33–38, 27–28.
   PubMed Web of Science ®Google Scholar
• Joycharat N, Boonma C, Thammavong S, Yingyongnarongkul BE, Limsuwan S, Voravuthikunchai SP. 2016. Chemical constituents and biological activities of Albizia myriophylla wood. Pharm Biol. 54:62–73.
   PubMed Web of Science ®Google Scholar
• Kitagawa S, Nabekura T, Kamiyama S. 2004. Inhibition of P-glycoprotein function by tea catechins in KB-C2 cells. J Pharm Pharmacol. 56:1001–1005.
   PubMed Web of Science ®Google Scholar
• Kitchen DB, Decornez H, Furr JR, Bajorath J. 2004. Docking and scoring in virtual screening for drug discovery: methods and applications. Nat Rev Drug Discov. 3:935–949.
   PubMed Web of Science ®Google Scholar
• Lazaridis T, Karplus M. 1999. Discrimination of the native from misfolded protein models with an energy function including implicit solvation 1. J Mol Biol. 288:477–487.
   PubMed Web of Science ®Google Scholar
• Le Grand S, Götz AW, Walker RC. 2013. SPFP: speed without compromise—A mixed precision model for GPU accelerated molecular dynamics simulations. Comput Phys Commun. 184:374–380.
   Web of Science ®Google Scholar
• Li X, Hu J, Wang B, Sheng L, Liu Z, Yang S, Li Y. 2014. Inhibitory effects of herbal constituents on P-glycoprotein in vitro and in vivo: herb–drug interactions mediated via P-gp. Toxicol Appl Pharmacol. 275:163–175.
   PubMed Web of Science ®Google Scholar
• Lopez D, Martinez-Luis S. 2014. Marine natural products with P-glycoprotein inhibitor properties. Mar Drugs. 12:525–546.
   PubMed Web of Science ®Google Scholar
• Martins A, Vasas A, Schelz Z, Viveiros M, Molnár J, Hohmann J, Amaral L. 2010. Constituents of Carpobrotus edulis inhibit P-glycoprotein of MDR1-transfected mouse lymphoma cells. Anticancer Res. 30:829–835.
   PubMed Web of Science ®Google Scholar
• Mohana S, Ganesan M, Agilan B, Karthikeyan R, Srithar G, Beaulah Mary R, Ananthakrishnan D, Velmurugan D, Rajendra Prasad N, Ambudkar SV. 2016. Screening dietary flavonoids for the reversal of P-glycoprotein-mediated multidrug resistance in cancer. Mol Biosyst. 12:2458–2470.
   PubMed Web of Science ®Google Scholar
• Palestro PH, Gavernet L, Estiu GL, Bruno Blanch LE. 2014. Docking applied to the prediction of the affinity of compounds to P-glycoprotein. Biomed Res Int. 2014:10.
   Web of Science ®Google Scholar
• Palmeira A, Vasconcelos MH, Paiva A, Fernandes MX, Pinto M, Sousa E. 2012. Dual inhibitors of P-glycoprotein and tumor cell growth: (Re)discovering thioxanthones. Biochem Pharmacol. 83:57–68.
   PubMed Web of Science ®Google Scholar
• Prajapati R, Singh U, Patil A, Khomane KS, Bagul P, Bansal AK, Sangamwar AT. 2013. In silico model for P-glycoprotein substrate prediction: insights from molecular dynamics and in vitro studies. J Comput Aided Mol Des. 27:347–363.
   PubMed Web of Science ®Google Scholar
• Qiu JX, Zhou ZW, He ZX, Zhang X, Zhou SF, Zhu S. 2015. Estimation of the binding modes with important human cytochrome P450 enzymes, drug interaction potential, pharmacokinetics, and hepatotoxicity of ginger components using molecular docking, computational, and pharmacokinetic modeling studies. Drug Des Devel Ther. 9:841–866.
   PubMed Web of Science ®Google Scholar
• 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. J Nutr Biochem. 26:44–56.
   PubMed Web of Science ®Google Scholar
• Salomon-Ferrer R, Götz AW, Poole D, Le Grand S, Walker RC. 2013. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald. J Chem Theory Comput. 9:3878–3888.
   PubMed Web of Science ®Google Scholar
• Sangmalee S, Laorpaksa A, Sritularak B, Sukrong S. 2016. Bioassay-guided isolation of two flavonoids from Derris scandens with topoisomerase II poison activity. Biol Pharm Bulletin. 39:631–635.
   Google Scholar
• Sharma R, Panigrahi P, Suresh CG. 2014. In-silico analysis of binding site features and substrate selectivity in plant flavonoid-3-O glycosyltransferases (F3GT) through molecular modeling, Docking and dynamics simulation studies. PLoS One. 9:e92636.
   PubMed Web of Science ®Google Scholar
• Szewczyk P, Tao H, Mcgrath AP, Villaluz M, Rees SD, Lee SC, Doshi R, Urbatsch IL, Zhang Q, Chang G. 2015. Snapshots of ligand entry, malleable binding and induced helical movement in P-glycoprotein. Acta Crystallogr D Biol Crystallogr. 71:732–741.
   PubMedGoogle Scholar
• Václavíková R, Boumendjel A, Ehrlichová M, Kovář J, Gut I. 2006. Modulation of paclitaxel transport by flavonoid derivatives in human breast cancer cells. Is there a correlation between binding affinity to NBD of P-gp and modulation of transport? Bioorg Med Chem. 14:4519–4525.
   PubMed Web of Science ®Google Scholar
• Wang YH, Li Y, Yang SL, Yang L. 2005. An in silico approach for screening flavonoids as P-glycoprotein inhibitors based on a Bayesian-regularized neural network. J Comput Aided Mol Des. 19:137–147.
   PubMed Web of Science ®Google Scholar
• Wolber G, Langer T. 2004. LigandScout: 3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. J Chem Inf Model. 45:160–169.
   Web of Science ®Google Scholar
• Wongrattanakamon P, Lee VS, Nimmanpipug P, Chansakaow S, Jiranusornkul S. 2016a. Insight into the molecular mechanism of P-glycoprotein mediated drug toxicity induced by bioflavonoids: an integrated computational approach. Toxicol Mech Methods. 27:253–271.
   Web of Science ®Google Scholar
• Wongrattanakamon P, Lee VS, Nimmanpipug P, Jiranusornkul S. 2016b. Nucleotide-binding domain 1 modelling: a novel molecular docking approach for screening of P-glycoprotein inhibitory activity of bioflavonoids. Chemical Data Collections. 2:10–16.
   Google Scholar
• Wongrattanakamon P, Lee VS, Nimmanpipug P, Jiranusornkul S. 2016c. Nucleotide binding domain 1 pharmacophore modeling for visualization and analysis of P-glycoprotein–flavonoid molecular interactions. Front Biol. 11:391–395.
   Google Scholar
• Zeino M, Saeed MEM, Kadioglu O, Efferth T. 2014. The ability of molecular docking to unravel the controversy and challenges related to P-glycoprotein—a well-known, yet poorly understood drug transporter. Invest New Drugs. 32:618–625.
   PubMed Web of Science ®Google Scholar
• Zhang S, Morris ME. 2003. Effects of the flavonoids biochanin A, Morin, phloretin, and silymarin on P-glycoprotein-mediated transport. J Pharmacol Exp Ther. 304:1258–1267.
   PubMed Web of Science ®Google Scholar