299
Views
13
CrossRef citations to date
0
Altmetric
Research Articles

Structural basis of fullerene derivatives as novel potent inhibitors of protein acetylcholinesterase without catalytic active site interaction: insight into the inhibitory mechanism through molecular modeling studies

, , , , , & show all
Pages 410-425 | Received 20 Nov 2018, Accepted 26 Jan 2019, Published online: 27 Feb 2019

References

  • Abellan Flos, M., Garcia Moreno, M. I., Ortiz Mellet, C., Garcia Fernandez, J. M., Nierengarten, J. F., & Vincent, S. P. (2016). Potent glycosidase inhibition with heterovalent fullerenes: Unveiling the binding modes triggering multivalent inhibition. Chemistry, 22(32), 11450–11460. doi: 10.1002/chem.201601673
  • Abreu, H. D. F., Melo Filho, A. A. D., Ribeiro, P. R. E., Linhares, B. D. M., Campêlo, M. D. C. F., Takahashi, J. A., & Costa, H. N. R. D. (2018). Fatty acid composition, acetylcholinesterase and bacterial inhibition by Inga cinnamomea pulp. Journal of Agricultural Science, 10(2), 281. doi: 10.5539/jas.v10n2p281
  • Ahmed, L., Rasulev, B., Kar, S., Krupa, P., Mozolewska, M. A., & Leszczynski, J. (2017). Inhibitors or toxins? Large library target-specific screening of fullerene-based nanoparticles for drug design purpose. Nanoscale, 9(29), 10263–10276. doi: 10.1039/C7NR00770A
  • Almeida, J. S. F. D. D., Cavalcante, S. F. D. A., Dolezal, R., Kuca, K., Musilek, K., Jun, D., & França, T. C. C. (2018). Molecular modeling studies on the interactions of aflatoxin B1 and its metabolites with the peripheral anionic site (PAS) of human acetylcholinesterase. Journal of Biomolecular Structure & Dynamics, 1–23. doi: 10.1080/07391102.2018.1475259
  • Ariel, N., Ordentlich, A., Barak, D., Bino, T., Velan, B., & Shafferman, A. (1998). The 'aromatic patch' of three proximal residues in the human acetylcholinesterase active centre allows for versatile interaction modes with inhibitors. Biochemical Journal, 335(1), 95–102. doi: 10.1042/bj3350095
  • Axelsen, P. H., Harel, M., Silman, I., & Sussman, J. L. (1994). Structure and dynamics of the active site gorge of acetylcholinesterase: Synergistic use of molecular dynamics simulation and X-ray crystallography. Protein Science: A Publication of the Protein Society, 3(2), 188–197. doi: 10.1002/pro.5560030204
  • Baruah, P., Basumatary, G., Yesylevskyy, S. O., Aguan, K., Bez, G., & Mitra, S. (2018). Novel coumarin derivatives as potent acetylcholinesterase inhibitors: Insight into efficacy, mode and site of inhibition. Journal of Biomolecular Structure & Dynamics, 1–52. doi: 10.1080/07391102.2018.1465853
  • Batista, P. R., Costa, M. G., Pascutti, P. G., Bisch, P. M., & de Souza, W. (2011). High temperatures enhance cooperative motions between CBM and catalytic domains of a thermostable cellulase: Mechanism insights from essential dynamics. Physical Chemistry Chemical Physics, 13(30), 13709–13720. doi: 10.1039/c0cp02697b
  • Belgorodsky, B., Fadeev, L., Kolsenik, J., & Gozin, M. (2006). Formation of a soluble stable complex between pristine C60-fullerene and a native blood protein. Chembiochem, 7(11), 1783–1789. doi: 10.1002/cbic.200600237
  • Benzi, G., & Moretti, A. (1998). Is there a rationale for the use of acetylcholinesterase inhibitors in the therapy of Alzheimer's disease? European Journal of Pharmacology, 346(1), 1–13. doi: 10.1016/S0014-2999(98)00093-4
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. doi: 10.1063/1.448118
  • Bourne, Y., Radic, Z., Taylor, P., & Marchot, P. (2010). Conformational remodeling of femtomolar inhibitor-acetylcholinesterase complexes in the crystalline state. Journal of the American Chemical Society, 132(51), 18292–18300. doi: 10.1021/ja106820e
  • Bourne, Y., Sharpless, K. B., Taylor, P., & Marchot, P. (2016). Steric and dynamic parameters influencing in situ cycloadditions to form triazole inhibitors with crystalline acetylcholinesterase. Journal of the American Chemical Society, 138(5), 1611–1621. doi: 10.1021/jacs.5b11384
  • Bourne, Y., Grassi, J., Bougis, P. E., & Marchot, P. (1999). Conformational flexibility of the acetylcholinesterase tetramer suggested by X-ray crystallography. Journal of Biological Chemistry, 274(43), 30370–30376. doi: 10.1074/jbc.274.43.30370
  • Branduardi, D., Gervasio, F. L., Cavalli, A., Recanatini, M., & Parrinello, M. (2005). The role of the peripheral anionic site and cation–pi interactions in the ligand penetration of the human AChE gorge. Journal of the American Chemical Society, 127(25), 9147–9155. doi: 10.1021/ja0512080
  • Bui, J. M., Tai, K., & McCammon, J. A. (2004). Acetylcholinesterase: Enhanced fluctuations and alternative routes to the active site in the complex with fasciculin-2. Journal of the American Chemical Society, 126(23), 7198–7205. doi: 10.1021/ja0485715
  • Calvaresi, M., & Zerbetto, F. (2010). Baiting proteins with C60. ACS Nano, 4(4), 2283–2299.
  • Canzar, S., El-Kebir, M., Pool, R., Elbassioni, K., Malde, A. K., Mark, A. E., … Klau, G. W. (2013). Charge group partitioning in biomolecular simulation. Journal of Computational Biology, 20(3), 188–198. doi: 10.1089/cmb.2012.0239
  • Cheng, S., Song, W., Yuan, X., & Xu, Y. (2017). Gorge motions of acetylcholinesterase revealed by microsecond molecular dynamics simulations. Scientific Reports, 7(1), 3219. doi: 10.1038/s41598-017-03088-y
  • Cormack, R. M. (1971). A review of classification. Journal of the Royal Statistical Society, 134(3), 321–367. doi: 10.2307/2344237
  • 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. doi: 10.1063/1.464397
  • Dvir, H., Silman, I., Harel, M., Rosenberry, T. L., & Sussman, J. L. (2010). Acetylcholinesterase: From 3D structure to function. Chemico-Biological Interactions, 187(1-3), 10–22. doi: 10.1016/j.cbi.2010.01.042
  • Gao, Y., Wang, Z., Ou, Z., Li, Y., Wang, X., & Yang, G. (2012). Regulation of glucose oxidase activity through interaction with fullerene derivatives. Chinese Journal of Chemistry, 30(2), 418–426. doi: 10.1002/cjoc.201180479
  • Giosia, M. D., Valle, F., Cantelli, A., Bottoni, A., & Calvaresi, M. (2018). C60 bioconjugation with proteins: Towards a palette of carriers for all pH ranges. Materials, 11(5), 691. doi: 10.3390/ma11050691
  • Gonçalves, A. D. S., França, A.,T. C. C., & Oliveira, O. V. D. (2015). Computational studies of acetylcholinesterase complexed with fullerene derivatives: A new insight for Alzheimer disease treatment. Journal of Biomolecular Structure & Dynamics, 34(6), 1307–1316. doi: 10.1080/07391102.2015.1077345
  • Gouet, P., & Courcelle, E. (2002). ENDscript: A workflow to display sequence and structure information. Bioinformatics, 18(5), 767–768. doi: 10.1093/bioinformatics/18.5.767
  • Zuo, G., Huang, Q., Wei, G., Zhou, R., & Fang, H. (2010). Plugging into proteins: Poisoning protein function by a hydrophobic nanoparticle. ACS Nano, 4(12), 7508–7514. doi: 10.1021/nn101762b
  • Gurung, A. B., Aguan, K., Mitra, S., & Bhattacharjee, A. (2016). Identification of molecular descriptors for design of novel Isoalloxazine derivatives as potential acetylcholinesterase inhibitors against Alzheimer's disease. Journal of Biomolecular Structure & Dynamics, 35(8), 1–40. doi: 10.1080/07391102.2016.1192485
  • Harel, M., Schalk, I., Ehret-Sabatier, L., Bouet, F., Goeldner, M., Hirth, C., … Sussman, J. L. (1993). Quaternary ligand binding to aromatic residues in the active-site gorge of acetylcholinesterase. Proceedings of the National Academy of Sciences of the United States of America, 90(19), 9031–9035. doi: 10.1073/pnas.90.19.9031
  • Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. doi: 10.1021/ct700301q
  • Huang, L., Shi, A., He, F., & Li, X. (2010). Synthesis, biological evaluation, and molecular modeling of berberine derivatives as potent acetylcholinesterase inhibitors. Bioorganic & Medicinal Chemistry, 18(3), 1244–1251. doi: 10.1016/j.bmc.2009.12.035
  • Isakovic, A., Markovic, Z., Todorovic-Markovic, B., Nikolic, N., Vranjes-Djuric, S., Mirkovic, M., … Trajkovic, V. (2006). Distinct cytotoxic mechanisms of pristine versus hydroxylated fullerene. Toxicological Sciences, 91(1), 173–183. doi: 10.1093/toxsci/kfj127
  • Jain, A. K. (2010). Data clustering: 50 years beyond K-means. Pattern Recognition Letters, 31(8), 651–666. doi: 10.1016/j.patrec.2009.09.011
  • Jin, H., Zhou, Z., Wang, D., Guan, S., & Han, W. (2015). Molecular dynamics simulations of acylpeptide hydrolase bound to chlorpyrifosmethyl oxon and dichlorvos. International Journal of Molecular Sciences, 16(12), 6217–6234. doi: 10.3390/ijms16036217
  • Junaid, M., Almuqri, E. A., Liu, J., & Zhang, H. (2016). Analyses of the binding between water soluble C60 derivatives and potential drug targets through a molecular docking approach. PLoS One, 11(2), e0147761. doi: 10.1371/journal.pone.0147761
  • Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., … Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. doi: 10.1002/chin.200110299
  • Kumari, R., Kumar, R., Open Source Drug Discovery, C., & Lynn, A. (2014). g_mmpbsa – A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. doi: 10.1021/ci500020m
  • Laatikainen, R., Saarela, J., Tuppurainen, K., & Hassinen, T. (1998). Internal motions of native lysozyme are more organized than those of mutants: A principal component analysis of molecular dynamics data. Biophysical Chemistry, 73(1-2), 1–5. doi: 10.1016/S0301-4622(98)00141-0
  • Leonis, G., Avramopoulos, A., Papavasileiou, K. D., Reis, H., Steinbrecher, T., & Papadopoulos, M. G. (2015). A comprehensive computational study of the interaction between human serum albumin and fullerenes. The Journal of Physical Chemistry B, 119(48), 14971–14985. doi: 10.1021/acs.jpcb.5b05998
  • Liu, S., Sui, Y., Guo, K., Yin, Z., & Gao, X. (2012). Spectroscopic study on the interaction of pristine C-60 and serum albumins in solution. Nanoscale Research Letters, 7(1), 433. doi: 10.1186/1556-276x-7-433
  • Liu, Y., Yan, B., Winkler, D. A., Fu, J., & Zhang, A. (2017). Competitive inhibition mechanism of acetylcholinesterase without catalytic active site interaction: Study on functionalized C60 nanoparticles via in vitro and in silico assays. ACS Applied Materials & Interfaces, 9(22), 18626–18638. doi: 10.1021/acsami.7b05459
  • López-Camacho, M. J., García-Godoy, J., García-Nieto Nebro, A. J., & J. F. Aldana-Montes, (2016). A new multi-objective approach for molecular docking based on RMSD and binding energy. Algorithms for Computational Biology. New York, NY: Springer International Publishing.
  • Lushington, G. H., Guo, J. X., & Hurley, M. M. (2006). Acetylcholinesterase: Molecular modeling with the whole toolkit. Current Topics in Medicinal Chemistry, 6(1), 57–73. doi: 10.2174/156802606775193293
  • Malde, A. K., Zuo, L., Breeze, M., Stroet, M., Poger, D., Nair, P. C., … Mark, A. E. (2011). An Automated force field topology builder (ATB) and repository: Version 1.0. Journal of Chemical Theory and Computation, 7(12), 4026–4037. doi: 10.1021/ct200196m
  • Mehta, M., Adem, A., & Sabbagh, M. (2012). New acetylcholinesterase inhibitors for Alzheimer's disease. International Journal of Alzheimer’s Disease, 2012, 728983. doi: 10.1155/2012/728983
  • Mesaric, T., Baweja, L., Drasler, B. & Darko, (2013). Effects of surface curvature and surface characteristics of carbon-based nanomaterials on the adsorption and activity of acetylcholinesterase. Carbon, 62(5), 222–232. doi: 10.1016/j.carbon.2013.05.060
  • Millard, C. B., Kryger, G., Ordentlich, A., Greenblatt, H. M., Harel, M., Raves, M. L., … Sussman, J. L. (1999). Crystal structures of aged phosphonylated acetylcholinesterase: Nerve agent reaction products at the atomic level. Biochemistry, 38(22), 7032–7039. doi: 10.1021/bi982678l
  • Nemukhin, A. V., Grigorenko, B. L., Morozov, D. I., Kochetov, M. S., Lushchekina, S. V., & Varfolomeev, S. D. (2013). On quantum mechanical–molecular mechanical (QM/MM) approaches to model hydrolysis of acetylcholine by acetylcholinesterase. Chemico-Biological Interactions, 203(1), 51–56. doi: 10.1016/j.cbi.2012.08.027
  • Niu, B., Zhao, M., Su, Q., Zhang, M., Lv, W., Chen, Q., … Zhang, Y. (2017). 2D-SAR and 3D-QSAR analyses for acetylcholinesterase inhibitors. Molecular Diversity, 21(2), 413–426. doi: 10.1007/s11030-017-9732-0
  • Ousaka, N., Mamiya, F., Iwata, Y., Nishimura, K., & Yashima, E. (2017). "Helix-in-helix" superstructure formation through encapsulation of fullerene-bound helical peptides within a helical poly(methyl methacrylate) cavity. Angewandte Chemie International Edition, 56(3), 791–795. doi: 10.1002/anie.201611349
  • Pastorin, G., Marchesan, S., Hoebeke, J., Da Ros, T., Ehret-Sabatier, L., Briand, J.-P., … Bianco, A. (2006). Design and activity of cationic fullerene derivatives as inhibitors of acetylcholinesterase. Organic & Biomolecular Chemistry, 4(13), 2556–2562. doi: 10.1039/b604361e
  • Qian, M., Shan, Y., Guan, S., Zhang, H., Wang, S., & Han, W. (2016). Structural basis of fullerene derivatives as novel potent inhibitors of protein tyrosine phosphatase 1B: Insight into the inhibitory mechanism through molecular modeling studies. Journal of Chemical Information and Modeling, 56(10), 2024–2034. doi: 10.1021/acs.jcim.6b00482
  • Rokach, L., & Maimon, O. (2005). Clustering methods. Data Mining & Knowledge Discovery Handbook, 3(3), 321–352. doi: 10.1007/0-387-25465-X_15
  • Sant'Anna, C. M., Viana Ados, S., & do Nascimento Junior, N. M. (2006). A semiempirical study of acetylcholine hydrolysis catalyzed by Drosophila melanogaster acetylcholinesterase. Bioorganic Chemistry, 34(2), 77–89. doi: 10.1016/j.bioorg.2006.01.002
  • Shigeru Yamago, H. T. (1995). In vivo biological behavior of a water-miscible fullerene: 14C labeling, absorption, distribution, excretion and acute toxicity. Chemistry & Biology, 2(6), 385–389. doi: 10.1016/1074-5521(95)90219-8
  • Shiri, F., Pirhadi, S., & Ghasemi, J. B. (2018). Dynamic structure based pharmacophore modeling of the acetylcholinesterase reveals several potential inhibitors. Journal of Biomolecular Structure & Dynamics, 1–13. doi: 10.1080/07391102.2018.1468281
  • Silman, I., & Sussman, J. L. (2008). Acetylcholinesterase: How is structure related to function?. Chem Biol Interact, 175(1-3), 3–10. doi: 10.1016/j.cbi.2008.05.035
  • Skariyachan, S., Parveen, A., & Garka, S. (2017). Nanoparticle fullerene (C60) demonstrated stable binding with antibacterial potential towards probable targets of drug resistant Salmonella typhi – A computational perspective and in vitro investigation. Journal of Biomolecular Structure & Dynamics, 35(16), 3449–3468. doi: 10.1080/07391102.2016.1257441
  • Spiliotopoulos, D., Spitaleri, A., & Musco, G. (2012). Exploring PHD fingers and H3K4me0 interactions with molecular dynamics simulations and binding free energy calculations: AIRE-PHD1, a comparative study. PLoS One, 7(10), e46902. doi: 10.1371/journal.pone.0046902
  • Swetha, R. G., Ramaiah, S., & Anbarasu, A. (2016). Molecular dynamics studies on D835N mutation in FLT3 – Its impact on FLT3 protein structure. Journal of Cellular Biochemistry, 117(6), 1439–1445. doi: 10.1002/jcb.25434
  • Tai, K., Shen, T. Y., Borjesson, U., Philippopoulos, M., & McCammon, J. A. (2001). Analysis of a 10-ns molecular dynamics simulation of mouse acetylcholinesterase. Biophysical Journal, 81(2), 715–724. doi: 10.1016/S0006-3495(01)75736-0
  • 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. doi: 10.1002/jcc.21334
  • Vagedes, P., Rabenstein, B., Aqvist, J., Marelius, J., & Knapp, E. W. (2000). The deacylation step of acetylcholinesterase: Computer simulation studies. Journal of the American Chemical Society, 122(49), 12254–12262. doi: 10.1021/ja0004581
  • Wang, Z., Zhao, J., Li, F., Gao, D., & Xing, B. (2009). Adsorption and inhibition of acetylcholinesterase by different nanoparticles. Chemosphere, 77(1), 67–73. doi: 10.1016/j.chemosphere.2009.05.015
  • Wlodek, S. T., Clark, T. W., Scott, L. R., and., & McCammon, J. A. (1997). Molecular dynamics of acetylcholinesterase dimer complexed with tacrine. Journal of the American Chemical Society, 119(40), 9513–9522. doi: 10.1021/ar010025i
  • Wong, D. M., Greenblatt, H. M., Dvir, H., Carlier, P. R., Han, Y.-F., Pang, Y.-P., … Sussman, J. L. (2003). Acetylcholinesterase complexed with bivalent ligands related to huperzine A: Experimental evidence for species-dependent protein–ligand complementarity. Journal of the American Chemical Society, 125(2), 363–373. doi: 10.1021/ja021111w
  • Xu, Y., Colletier, J. P., Weik, M., Jiang, H., Moult, J., Silman, I., & Sussman, J. L. (2008). Flexibility of aromatic residues in the active-site gorge of acetylcholinesterase: X-ray versus molecular dynamics. Biophysical Journal, 95(5), 2500–2511. doi: 10.1529/biophysj.108.129601
  • Yu, Y., Sun, H., Hou, T., Wang, S., & Li, Y. (2018). Fullerene derivatives act as inhibitors of leukocyte common antigen based on molecular dynamics simulations. RSC Advances, 8(25), 13997–14008. doi: 10.1039/C7RA13543B
  • Zhang, Y., Zou, T., Guan, M., Zhen, M., Chen, D., Guan, X., … Shu, C. (2016). Synergistic effect of human serum albumin and fullerene on Gd-DO3A for tumor-targeting imaging. ACS Applied Materials & Interfaces, 8(18), 11246–11254. doi: 10.1021/acsami.5b12848
  • Zhang, Y. K., Kua, J., & McCammon, J. A. (2002). Role of the catalytic triad and oxyanion hole in acetylcholinesterase catalysis: An ab initio QM/MM study. Journal of the American Chemical Society, 124(35), 10572–10577. doi: 10.1021/ja020243m
  • Zhou, X., Xi, W., Luo, Y., Cao, S., & Wei, G. (2014). Interactions of a water-soluble fullerene derivative with amyloid-beta protofibrils: Dynamics, binding mechanism, and the resulting salt-bridge disruption. The Journal of Physical Chemistry B, 118(24), 6733–6741. doi: 10.1021/jp503458w
  • Zhou, Y., Wang, S., & Zhang, Y. (2010). Catalytic reaction mechanism of acetylcholinesterase determined by Born–Oppenheimer ab initio QM/MM molecular dynamics simulations. The Journal of Physical Chemistry B, 114(26), 8817–8825. doi: 10.1021/jp104258d

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.