Computational insights into β-site amyloid precursor protein enzyme 1 (BACE1) inhibition by tanshinones and salvianolic acids from Salvia miltiorrhiza via molecular docking simulations

Bajda, 2014, Application of computational methods for the design of BACE-1 inhibitors: validation of in silico modelling, Int. J. Mol. Sci., 15, 5128, 10.3390/ijms15035128 Barman, 2011, Computational modeling of substrate specificity and catalysis of the β-secretase (BACE1) enzyme, Biochemistry, 50, 4337, 10.1021/bi200081h Cao, 2013, Salvianolic acid A, a polyphenolic derivative from Salvia miltiorrhiza bunge, as a multifunctional agent for the treatment of Alzheimer's disease, Mol. Divers., 17, 515, 10.1007/s11030-013-9452-z Chen, 2004 Choi, 2014, Effects of C-glycosylation on anti-diabetic, anti-Alzheimer’s disease and anti-inflammatory potential of apigenin, Food Chem. Toxicol., 64, 27, 10.1016/j.fct.2013.11.020 Cole, 2008, BACE1 structure and function in health and Alzheimer's disease, Curr. Alzheimer Res., 5, 100, 10.2174/156720508783954758 Cornish-Bowden, 1974, A simple graphical method for determining the inhibition constants of mixed, uncompetitive and non-competitive inhibitors, Biochem. J., 137, 143, 10.1042/bj1370143 de la Monte, 2008, Alzheimer's disease is type 3 diabetes –evidence reviewed, J. Diabetes Sci. Technol., 2, 1101, 10.1177/193229680800200619 Durairajan, 2008, Salvianolic acid B inhibits Aβ fibril formation and disaggregates preformed fibrils and protects against Aβ-induced cytotoxicty, Neurochem. Int., 52, 741, 10.1016/j.neuint.2007.09.006 Dutta, 2010, Synthesis and ribonuclease a inhibition activity of resorcinol and phloroglucinol derivatives of catechin and epicatechin: importance of hydroxyl groups, Bioorg. Med. Chem., 18, 6538, 10.1016/j.bmc.2010.06.077 Eleftheriou, 2015, Prediction of enzyme inhibition and mode of inhibitory action based on calculation of distances between hydrogen bond donor/acceptor groups of the molecule and docking analysis: an application on the discovery of novel effective PTP1B inhibitors, SAR QSAR Environ. Res., 26, 557, 10.1080/1062936X.2015.1074939 Glenner, 1990, 51 Hernández-Rodríguez, 2016, Asp32 and Asp228 determine the selective inhibition of BACE1 as shown by docking and molecular dynamics simulations, Eur. J. Med. Chem., 124, 1142, 10.1016/j.ejmech.2016.08.028 Hong, 2002, Crystal structure of memapsin 2 (β-secretase) in complex with an inhibitor OM00-3, Biochemistry, 41, 10963, 10.1021/bi026232n Howes, 2017, Effect of Chinese herbal medicine on Alzheimer's disease, Int. Rev. Neurobiol., 135, 29, 10.1016/bs.irn.2017.02.003 Hung, 2015, Kinetics and molecular docking studies of cholinesterase inhibitors derived from water layer of Lycopodiella cernua (L.) Pic. Serm.(II), Chem. Biol. Interact., 240, 74, 10.1016/j.cbi.2015.07.008 Jung, 2017, Structure-related protein tyrosine phosphatase 1B inhibition by naringenin derivatives, Bioorg. Med. Chem. Lett., 27, 2274, 10.1016/j.bmcl.2017.04.054 Karran, 2011, The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics, Nat. Rev. Drug Discov., 10, 698, 10.1038/nrd3505 Kim, 2016, Inhibition of soluble epoxide hydrolase activity by compounds isolated from the aerial parts of Glycosmis stenocarpa, J. Enzyme Inhib. Med. Chem., 31, 640, 10.3109/14756366.2015.1057719 Kim, 2017, Characterization of the inhibitory activity of natural tanshinones from Salvia miltiorrhiza roots on protein tyrosine phosphatase 1B, Chem. Biol. Interact., 278, 65, 10.1016/j.cbi.2017.10.013 Kumar, 2017, Investigation of naphthofuran moiety as potential dual inhibitor against BACE-1 and GSK-3β: molecular dynamics simulations, binding energy, and network analysis to identify first-in-class dual inhibitors against Alzheimer's disease, J. Mol. Model., 23, 239, 10.1007/s00894-017-3396-7 Kumar, 2018, Docking, molecular dynamics, binding energy-MM-PBSA studies of naphthofuran derivatives to identify potential dual inhibitors against BACE-1 and GSK-3β, J. Biomol. Struct. Dyn., 1 Lansbury, 2004, Back to the future: the ‘old-fashioned' way to new medications for neurodegeneration, Nat. Rev. Neurosci., 10, 51, 10.1038/nrn1435 Lee, 2013, Neuroprotective effects of salvianolic acid B on an Aβ 25–35 peptide-induced mouse model of Alzheimer's disease, Eur. J. Pharmacol., 704, 70, 10.1016/j.ejphar.2013.02.015 Li, 2004, Effects of tanshinone on neuropathological changes induced by amyloid β-peptide (1–40) injection in rat hippocampus, Acta Pharmacol. Sin., 25, 861 Li, 2015, Upregulation effects of tanshinone IIA on the expressions of NeuN, Nissl body, and IκB and downregulation effects on the expressions of GFAP and NF-κB in the brain tissues of rat models of Alzheimer’s disease, Neuroreport, 26, 758, 10.1097/WNR.0000000000000419 Lineweaver, 1934, The determination of enzyme dissociation constants, J. Am. Chem. Soc., 56, 658, 10.1021/ja01318a036 Lipinski, 1997, Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings, Adv. Drug Deliv. Rev., 23, 3, 10.1016/S0169-409X(96)00423-1 Ma, 2011, Molecular docking for virtual screening of natural product databases, Chem. Sci., 2, 1656, 10.1039/C1SC00152C Mangialasche, 2010, Alzheimer's disease: clinical trials and drug development, Lancet Neurol., 9, 702, 10.1016/S1474-4422(10)70119-8 Mattson, 2004, Pathways towards and away from Alzheimer's disease, Nature, 430, 631, 10.1038/nature02621 Mei, 2009, Cryptotanshinone, a compound from Salvia miltiorrhiza modulates amyloid precursor protein metabolism and attenuates β-amyloid deposition through upregulating α-secretase in vivo and in vitro, Neurosci. Lett., 452, 90, 10.1016/j.neulet.2009.01.013 Mei, 2012, Cryptotanshinione inhibits β-amyloid aggregation and protects damage from β-amyloid in SH-SY5Y Cells, Neurochem. Res., 37, 622, 10.1007/s11064-011-0652-6 Morris, 2008, 365 Oprea, 2000, Property distribution of drug-related chemical databases, J. Comput. Aided Mol. Des., 14, 251, 10.1023/A:1008130001697 Ozarowski, 2017, Effect of Salvia miltiorrhiza root extract on brain acetylcholinesterase and butyrylcholinesterase activities, their mRNA levels and memory evaluation in rats, Physiol. Behav., 173, 223, 10.1016/j.physbeh.2017.02.019 Patil, 2010, Optimized hydrophobic interactions and hydrogen bonding at the target-ligand interface leads the pathways of drug-designing, PLoS One, 5, e12029, 10.1371/journal.pone.0012029 Schilling, 2016, Unraveling Alzheimer’s: making sense of the relationship between diabetes and Alzheimer’s disease, J. Alzheimer's Dis., 51, 961, 10.3233/JAD-150980 Senol, 2017, Selective in vitro and in silico butyrylcholinesterase inhibitory activity of diterpenes and rosmarinic acid isolated from Perovskia atriplicifolia Benth. and Salvia glutinosa L, Phytochemistry, 133, 33, 10.1016/j.phytochem.2016.10.012 Seong, 2017, BACE1 inhibitory activity and molecular docking analysis of meroterpenoids from Sargassum serratifolium, Bioorg. Med. Chem., 25, 3964, 10.1016/j.bmc.2017.05.033 Steen, 2005, S.M. de la Monte, Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease −is this type 3 diabetes?, J. Alzheimer's Dis., 7, 63, 10.3233/JAD-2005-7107 Stockley, 2007 Takizawa, 2015, Epidemiological and economic burden of Alzheimer's disease: a systematic literature review of data across Europe and the United States of America, J. Alzheimer's Dis., 43, 1271, 10.3233/JAD-141134 Tang, 2016, Salvianolic acid B inhibits Aβ generation by modulating BACE1 activity in SH-SY5Y-APPsw cells, Nutrients, 8, 333, 10.3390/nu8060333 Vistoli, 2008, Assessing drug-likeness −what are we missing?, Drug Discov. Today, 13, 285, 10.1016/j.drudis.2007.11.007 Wang, 2013, Tanshinones inhibit amyloid aggregation by amyloid-β peptide, disaggregate amyloid fibrils, and protect cultured cells, ACS Chem. Neurosci., 4, 1004, 10.1021/cn400051e Wimo, 2013, The worldwide economic impact of dementia 2010, Alzheimer's Dement., 9, 1, 10.1016/j.jalz.2012.11.006 Wong, 2010, Interaction study of two diterpenes, cryptotanshinone and dihydrotanshinone, to human acetylcholinesterase and butyrylcholinesterase by molecular docking and kinetic analysis, Chem. Biol. Interact., 187, 335, 10.1016/j.cbi.2010.03.026 Yin, 2008, Effect of tanshinone on the levels of nitric oxide synthase and acetylcholinesterase in the brain of Alzheimer’s disease rat model, Clin. Invest. Med., 31, 248, 10.25011/cim.v31i5.4871 Youn, 2016, Discovery of polymethoxyflavones from black ginger (Kaempferia parviflora) as potential β-secretase (BACE1) inhibitors, J. Funct. Foods, 20, 567, 10.1016/j.jff.2015.10.036 Yu, 2014, Neuroprotection against Aβ 25–35-induced apoptosis by Salvia miltiorrhiza extract in SH-SY5Y cells, Neurochem. Int., 75, 89, 10.1016/j.neuint.2014.06.001 Zhang, 2012, Effects of salvianolic acid B on survival, self-renewal and neuronal differentiation of bone marrow derived neural stem cells, Eur. J. Pharmacol., 697, 32, 10.1016/j.ejphar.2012.10.008 Zhang, 2016, Salvia miltiorrhiza: a source for anti-Alzheimer's disease drugs, Pharm. Biol., 54, 18, 10.3109/13880209.2015.1027408 Zhang, 2016, Salvia miltiorrhiza: a source for anti-Alzheimer’s disease drugs, Pharm. Biol., 54, 18, 10.3109/13880209.2015.1027408 Zhou, 2011, In Salvia miltiorrhiza, phenolic acids possess protective properties against amyloid β-induced cytotoxicity, and tanshinones act as acetylcholinesterase inhibitors, Environ. Toxicol. Pharmacol., 31, 443, 10.1016/j.etap.2011.02.006 Zhu, 2010, Effect of tanshinone IIA on the change of calcium current induced by β-amyloid protein 25–35 in neurons of nucleus basalis of Meynert, Zhong nan da xue xue bao, 35, 840