In silico design of HDAC6 inhibitors with neuroprotective effects

References

• Abel, T., & Zukin, R. S. (2008). Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Current Opinion in Pharmacology, 8(1), 57–64. https://doi.org/10.1016/j.coph.2007.12.002
   PubMed Web of Science ®Google Scholar
• Aldana-Masangkay, G. I., & Sakamoto, K. M. (2011). The role of HDAC6 in cancer. Journal of Biomedicine & Biotechnology, 2011(2011), 875824. https://doi.org/10.1155/2011/875824
   PubMedGoogle Scholar
• Alonso, H., Bliznyuk, A. A., & Gready, J. E. (2006). Combining docking and molecular dynamic simulations in drug design. Medicinal Research Reviews, 26(5), 531–568. https://doi.org/10.1002/med.20067
   PubMed Web of Science ®Google Scholar
• Brilli, L. L., Swanhart, L. M., de Caestecker, M. P., & Hukriede, N. A. (2013). HDAC inhibitors in kidney development and disease. Pediatric Nephrology (Berlin, Germany), 28(10), 1909–1921.
   PubMed Web of Science ®Google Scholar
• Butler, K. V., Kalin, J., Brochier, C., Vistoli, G., Langley, B., & Kozikowski, A. P. (2010). Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. Journal of the American Chemical Society, 132(31), 10842–10846. https://doi.org/10.1021/ja102758v
   PubMed Web of Science ®Google Scholar
• Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., & Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. https://doi.org/10.1002/jcc.20290
   PubMed Web of Science ®Google Scholar
• Cautain, B., de Pedro, N., Schulz, C., Pascual, J., Sousa, T. d S., Martin, J., Pérez-Victoria, I., Asensio, F., González, I., Bills, G. F., Reyes, F., Genilloud, O., & Vicente, F. (2015). Identification of the lipodepsipeptide MDN-0066, a novel inhibitor of VHL/HIF pathway produced by a new pseudomonas species. PloS One, 10(5), e0125221. https://doi.org/10.1371/journal.pone.0125221
   PubMed Web of Science ®Google Scholar
• Charrier, C., Clarhaut, J., Gesson, J. P., Estiu, G., Wiest, O., Roche, J., & Bertrand, P. (2009). Synthesis and modeling of new benzofuranone histone deacetylase inhibitors that stimulate tumor suppressor gene expression. Journal of Medicinal Chemistry, 52(9), 3112–3115. https://doi.org/10.1021/jm9002439
   PubMed Web of Science ®Google Scholar
• Cheung, Y. T., Lau, W. K., Yu, M. S., Lai, C. S., Yeung, S. C., So, K. F., & Chang, R. C. (2009). Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research. Neurotoxicology, 30(1), 127–135. https://doi.org/10.1016/j.neuro.2008.11.001
   PubMed Web of Science ®Google Scholar
• de Pedro, N., Cantizani, J., Ortiz-Lopez, F. J., Gonzalez-Menendez, V., Cautain, B., Rodriguez, L., Bills, G. F., Reyes, F., Genilloud, O., & Vicente, F. (2016). Protective effects of isolecanoric acid on neurodegenerative in vitro models. Neuropharmacology, 101, 538–548. https://doi.org/10.1016/j.neuropharm.2015.09.029
   PubMed Web of Science ®Google Scholar
• de Ruijter, A. J., van Gennip, A. H., Caron, H. N., Kemp, S., & van Kuilenburg, A. B. (2003). Histone deacetylases (HDACs): Characterization of the classical HDAC family. The Biochemical Journal, 370(Pt 3), 737–749. https://doi.org/10.1042/BJ20021321
   PubMed Web of Science ®Google Scholar
• Dietz, K. C., & Casaccia, P. (2010). HDAC inhibitors and neurodegeneration: At the edge between protection and damage. Pharmacological Research, 62(1), 11–17. https://doi.org/10.1016/j.phrs.2010.01.011
   PubMed Web of Science ®Google Scholar
• D'Mello, S. R. (2009). Histone deacetylases as targets for the treatment of human neurodegenerative diseases. Drug News & Perspectives, 22(9), 513–524. https://doi.org/10.1358/dnp.2009.22.9.1437959
   PubMedGoogle Scholar
• d'Ydewalle, C., Bogaert, E., & Van Den Bosch, L. (2012). HDAC6 at the Intersection of Neuroprotection and Neurodegeneration. Traffic (Copenhagen, Denmark), 13(6), 771–779. https://doi.org/10.1111/j.1600-0854.2012.01347.x
   PubMed Web of Science ®Google Scholar
• Falcon, W. E., Ellingson, S. R., Smith, J. C., & Baudry, J. (2019). Ensemble docking in drug discovery: How many protein configurations from molecular dynamics simulations are needed to reproduce known ligand binding? The Journal of Physical Chemistry. B, 123(25), 5189–5195. https://doi.org/10.1021/acs.jpcb.8b11491
   PubMed Web of Science ®Google Scholar
• Frisch, M. J., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Vreven, T., Kudin, K. N., & Burant, J. C. (2003). Gaussian 03, revision A (9th ed.). Gaussian Inc.
   Google Scholar
• Frisch, M. J., & Schlegel, H. B. (1998). Gaussian 98. Gaussian, Inc.
   Google Scholar
• Gardian, G., Yang, L., Cleren, C., Calingasan, N. Y., Klivenyi, P., & Beal, M. F. (2004). Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity. Neuromolecular Medicine, 5(3), 235–242. https://doi.org/10.1385/NMM:5:3:235
   PubMed Web of Science ®Google Scholar
• Glozak, M. A., Sengupta, N., Zhang, X., & Seto, E. (2005). Acetylation and deacetylation of non-histone proteins. Gene, 363, 15–23. https://doi.org/10.1016/j.gene.2005.09.010
   PubMed Web of Science ®Google Scholar
• Gohlke, H., & Case, D. A. (2004). Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. Journal of Computational Chemistry, 25(2), 238–250. https://doi.org/10.1002/jcc.10379
   PubMed Web of Science ®Google Scholar
• Hai, Y., & Christianson, D. W. (2016). Histone deacetylase 6 structure and molecular basis of catalysis and inhibition. Nature Chemical Biology, 12(9), 741–747. https://doi.org/10.1038/nchembio.2134
   PubMed Web of Science ®Google Scholar
• Hann, M. M., & Oprea, T. I. (2004). Pursuing the leadlikeness concept in pharmaceutical research. Current Opinion in Chemical Biology, 8(3), 255–263. https://doi.org/10.1016/j.cbpa.2004.04.003
   PubMed Web of Science ®Google Scholar
• Hauser, D. N., & Hastings, T. G. (2013). Mitochondrial dysfunction and oxidative stress in Parkinson's disease and monogenic parkinsonism. Neurobiology of Disease, 51, 35–42. https://doi.org/10.1016/j.nbd.2012.10.011
   PubMed Web of Science ®Google Scholar
• Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., & Simmerling, C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65(3), 712–725. https://doi.org/10.1002/prot.21123
   PubMed Web of Science ®Google Scholar
• Jenner, P., & Olanow, C. W. (2006). The pathogenesis of cell death in Parkinson's disease. Neurology, 66(10), S24–S36. https://doi.org/10.1212/wnl.66.10_suppl_4.s24
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kassab, S. E., Mowafy, S., Alserw, A. M., Seliem, J. A., El-Naggar, S. M., Omar, N. N., & Awad, M. M. (2019). Structure-based design generated novel hydroxamic acid based preferential HDAC6 lead inhibitor with on-target cytotoxic activity against primary choroid plexus carcinoma. Journal of Enzyme Inhibition and Medicinal Chemistry, 34(1), 1062–1077. https://doi.org/10.1080/14756366.2019.1613987
   PubMed Web of Science ®Google Scholar
• Kazantsev, A. G., & Thompson, L. M. (2008). Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nature Reviews. Drug Discovery, 7(10), 854–868. https://doi.org/10.1038/nrd2681
   PubMed Web of Science ®Google Scholar
• Khochbin, S., Verdel, A., Lemercier, C., & Seigneurin-Berny, D. (2001). Functional significance of histone deacetylase diversity. Current Opinion in Genetics & Development, 11(2), 162–166. https://doi.org/10.1016/S0959-437X(00)00174-X
   PubMed Web of Science ®Google Scholar
• Knegtel, R. M., Kuntz, I. D., & Oshiro, C. M. (1997). Molecular docking to ensembles of protein structures. Journal of Molecular Biology, 266(2), 424–440. https://doi.org/10.1006/jmbi.1996.0776
   PubMed Web of Science ®Google Scholar
• Kong, Y., Jung, M., Wang, K., Grindrod, S., Velena, A., Lee, S. A., Dakshanamurthy, S., Yang, Y., Miessau, M., Zheng, C., Dritschilo, A., & Brown, M. L. (2011). Histone deacetylase cytoplasmic trapping by a novel fluorescent HDAC inhibitor. Molecular Cancer Therapeutics, 10(9), 1591–1599. https://doi.org/10.1158/1535-7163.MCT-10-0779
   PubMed Web of Science ®Google Scholar
• Kozikowski, A. P., Tapadar, S., Luchini, D. N., Kim, K. H., & Billadeau, D. D. (2008). Use of the nitrile oxide cycloaddition (NOC) reaction for molecular probe generation: A new class of enzyme selective histone deacetylase inhibitors (HDACIs) showing picomolar activity at HDAC6. Journal of Medicinal Chemistry, 51(15), 4370–4373. https://doi.org/10.1021/jm8002894
   PubMed Web of Science ®Google Scholar
• Lee, J. H., Mahendran, A., Yao, Y., Ngo, L., Venta-Perez, G., Choy, M. L., Kim, N., Ham, W. S., Breslow, R., & Marks, P. A. (2013). Development of a histone deacetylase 6 inhibitor and its biological effects. Proceedings of the National Academy of Sciences of the United States of America, 110(39), 15704–15709. https://doi.org/10.1073/pnas.1313893110
   PubMed Web of Science ®Google Scholar
• Lernoux, M., Schnekenburger, M., Dicato, M., & Diederich, M. (2018). Anti-cancer effects of naturally derived compounds targeting histone deacetylase 6-related pathways. Pharmacological Research, 129, 337–356. https://doi.org/10.1016/j.phrs.2017.11.004
   PubMed Web of Science ®Google Scholar
• Liao, K. H., Chen, K. B., Lee, W. Y., Sun, M. F., Lee, C. C., & Chen, C. Y. (2014). Ligand-based and structure-based investigation for Alzheimer's disease from traditional chinese medicine. Evidence-Based Complementary and Alternative Medicine : eCAM, 2014, 364819.
   PubMed Web of Science ®Google Scholar
• Li, G., Jiang, H., Chang, M., Xie, H., & Hu, L. (2011). HDAC6 α-tubulin deacetylase: A potential therapeutic target in neurodegenerative diseases. Journal of the Neurological Sciences, 304(1–2), 1–8. https://doi.org/10.1016/j.jns.2011.02.017
   PubMed Web of Science ®Google Scholar
• Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (1997). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews, 23(1–3), 3–25. https://doi.org/10.1016/S0169-409X(96)00423-1
   Web of Science ®Google Scholar
• Li, Y., Shin, D., & Kwon, S. H. (2013). Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. The FEBS Journal, 280(3), 775–793. https://doi.org/10.1111/febs.12079
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Pang, Y. P., Xu, K., Yazal, J. E., & Prendergas, F. G. (2000). Successful molecular dynamics simulation of the zinc-bound farnesyltransferase using the cationic dummy atom approach. Protein Science : A Publication of the Protein Society, 9(10), 1857–1865.
   PubMed Web of Science ®Google Scholar
• Parmigiani, R. B., Xu, W. S., Venta-Perez, G., Erdjument-Bromage, H., Yaneva, M., Tempst, P., & Marks, P. A. (2008). HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proceedings of the National Academy of Sciences of the United States of America, 105(28), 9633–9638. https://doi.org/10.1073/pnas.0803749105
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Pinho, B. R., Reis, S. D., Guedes-Dias, P., Leitao-Rocha, A., Quintas, C., Valentao, P., Andrade, P. B., Santos, M. M., & Oliveira, J. M. (2016). Pharmacological modulation of HDAC1 and HDAC6 in vivo in a zebrafish model: Therapeutic implications for Parkinson's disease. Pharmacological Research, 103, 328–339. https://doi.org/10.1016/j.phrs.2015.11.024
   PubMed Web of Science ®Google Scholar
• Rivieccio, M. A., Brochier, C., Willis, D. E., Walker, B. A., D'Annibale, M. A., McLaughlin, K., Siddiq, A., Kozikowski, A. P., Jaffrey, S. R., Twiss, J. L., Ratan, R. R., & Langley, B. (2009). HDAC6 is a target for protection and regeneration following injury in the nervous system. Proceedings of the National Academy of Sciences of the United States of America, 106(46), 19599–19604.
   PubMed Web of Science ®Google Scholar
• Roche, J., & Bertrand, P. (2016). Inside HDACs with more selective HDAC inhibitors. European Journal of Medicinal Chemistry, 121, 451–483. https://doi.org/10.1016/j.ejmech.2016.05.047
   PubMed Web of Science ®Google Scholar
• Roy, A., Ghosh, A., Jana, A., Liu, X., Brahmachari, S., Gendelman, H. E., & Pahan, K. (2012). Sodium phenylbutyrate controls neuroinflammatory and antioxidant activities and protects dopaminergic neurons in mouse models of Parkinson's disease. PLoS One, 7(6), e38113. https://doi.org/10.1371/journal.pone.0038113
   PubMed Web of Science ®Google Scholar
• Saha, R. N., & Pahan, K. (2006). HATs and HDACs in neurodegeneration: A tale of disconcerted acetylation homeostasis. Cell Death and Differentiation, 13(4), 539–550. https://doi.org/10.1038/sj.cdd.4401769
   PubMed Web of Science ®Google Scholar
• Santos-Martins, D., Forli, S., Ramos, M. J., & Olson, A. J. (2014). AutoDock4(Zn): An improved AutoDock force field for small-molecule docking to zinc metalloproteins. Journal of Chemical Information and Modeling, 54(8), 2371–2379. https://doi.org/10.1021/ci500209e
   PubMed Web of Science ®Google Scholar
• Seigneurin-Berny, D., Verdel, A., Curtet, S., Lemercier, C., Garin, J., Rousseaux, S., & Khochbin, S. (2001). Identification of components of the murine histone deacetylase 6 complex: Link between acetylation and ubiquitination signaling pathways. Molecular and Cellular Biology, 21(23), 8035–8044. https://doi.org/10.1128/MCB.21.23.8035-8044.2001
   PubMed Web of Science ®Google Scholar
• Simoes-Pires, C., Zwick, V., Nurisso, A., Schenker, E., Carrupt, P. A., & Cuendet, M. (2013). HDAC6 as a target for neurodegenerative diseases: What makes it different from the other HDACs? Molecular Neurodegeneration, 8, 7.
   PubMed Web of Science ®Google Scholar
• Sixto-Lopez, Y., Bello, M., & Correa-Basurto, J. (2019). Structural and energetic basis for the inhibitory selectivity of both catalytic domains of dimeric HDAC6. Journal of Biomolecular Structure & Dynamics, 37(18), 4701–4720. https://doi.org/10.1080/07391102.2018.1557560
   PubMed Web of Science ®Google Scholar
• Sixto-Lopez, Y., Bello, M., Rodriguez-Fonseca, R. A., Rosales-Hernandez, M. C., Martinez-Archundia, M., Gomez-Vidal, J. A., & Correa-Basurto, J. (2017). Searching the conformational complexity and binding properties of HDAC6 through docking and molecular dynamic simulations. Journal of Biomolecular Structure & Dynamics, 35(13), 2794–2814. https://doi.org/10.1080/07391102.2016.1231084
   PubMed Web of Science ®Google Scholar
• Sixto-Lopez, Y., Gomez-Vidal, J. A., de Pedro, N., Bello, M., Rosales-Hernandez, M. C., & Correa-Basurto, J. (2020). Hydroxamic acid derivatives as HDAC1, HDAC6 and HDAC8 inhibitors with antiproliferative activity in cancer cell lines. Scientific Reports, 10(1), 10462. https://doi.org/10.1038/s41598-020-67112-4
   PubMed Web of Science ®Google Scholar
• Stoker, T. B., & Barker, R. A. (2020). Recent developments in the treatment of Parkinson's Disease. F1000Research, 9, 862. https://doi.org/10.12688/f1000research.25634.1
   Google Scholar
• Su, M., Shi, J. J., Yang, Y. P., Li, J., Zhang, Y. L., Chen, J., Hu, L. F., & Liu, C. F. (2011). HDAC6 regulates aggresome-autophagy degradation pathway of α-synuclein in response to MPP+-induced stress . Journal of Neurochemistry, 117(1), 112–120. https://doi.org/10.1111/j.1471-4159.2011.07180.x
   PubMed Web of Science ®Google Scholar
• Tanner, C. M., Kamel, F., Ross, G. W., Hoppin, J. A., Goldman, S. M., Korell, M., Marras, C., Bhudhikanok, G. S., Kasten, M., Chade, A. R., Comyns, K., Richards, M. B., Meng, C., Priestley, B., Fernandez, H. H., Cambi, F., Umbach, D. M., Blair, A., Sandler, D. P., & Langston, J. W. (2011). Rotenone, paraquat, and Parkinson's disease. Environmental Health Perspectives, 119(6), 866–872. https://doi.org/10.1289/ehp.1002839
   PubMed Web of Science ®Google Scholar
• Vigushin, D. M., Ali, S., Pace, P. E., Mirsaidi, N., Ito, K., Adcock, I., & Coombes, R. C. (2001). Trichostatin A Is a Histone Deacetylase Inhibitor with Potent Antitumor Activity against Breast Cancer in Vivo. Clinical Cancer Research : An Official Journal of the American Association for Cancer Research, 7(4), 971–976.
   PubMed Web of Science ®Google Scholar
• Vogerl, K., Ong, N., Senger, J., Herp, D., Schmidtkunz, K., Marek, M., Muller, M., Bartel, K., Shaik, T. B., Porter, N. J., Robaa, D., Christianson, D. W., Romier, C., Sippl, W., Jung, M., & Bracher, F. (2019). Synthesis and biological investigation of phenothiazine-based benzhydroxamic acids as selective histone deacetylase 6 inhibitors. Journal of Medicinal Chemistry, 62(3), 1138–1166. https://doi.org/10.1021/acs.jmedchem.8b01090
   PubMed Web of Science ®Google Scholar
• Wang, D. (2009). Computational studies on the histone deacetylases and the design of selective histone deacetylase inhibitors. Current Topics in Medicinal Chemistry, 9(3), 241–256. https://doi.org/10.2174/156802609788085287
   PubMed Web of Science ®Google Scholar
• Wang, X. X., Wan, R. Z., & Liu, Z. P. (2018). Recent advances in the discovery of potent and selective HDAC6 inhibitors. European Journal of Medicinal Chemistry, 143, 1406–1418. https://doi.org/10.1016/j.ejmech.2017.10.040
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Xie, H. R., Hu, L. S., & Li, G. Y. (2010). SH-SY5Y human neuroblastoma cell line: In vitro cell model of dopaminergic neurons in Parkinson's disease. Chinese Medical Journal, 123(8), 1086–1092.
   PubMed Web of Science ®Google Scholar
• Yan, S., Wei, X., Jian, W., Qin, Y., Liu, J., Zhu, S., Jiang, F., Lou, H., & Zhang, B. (2020). Pharmacological inhibition of HDAC6 attenuates NLRP3 inflammatory response and protects dopaminergic neurons in experimental models of Parkinson's disease. Frontiers in Aging Neuroscience, 12, 78.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Gilquin, B., Khochbin, S., & Matthias, P. (2006). Two catalytic domains are required for protein deacetylation. The Journal of Biological Chemistry, 281(5), 2401–2404. https://doi.org/10.1074/jbc.C500241200
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Li, N., Caron, C., Matthias, G., Hess, D., Khochbin, S., & Matthias, P. (2003). HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. The EMBO Journal, 22(5), 1168–1179. https://doi.org/10.1093/emboj/cdg115
   PubMed Web of Science ®Google Scholar
• Zou, H., Wu, Y., Navre, M., & Sang, B. C. (2006). Characterization of the two catalytic domains in histone deacetylase 6. Biochemical and Biophysical Research Communications, 341(1), 45–50. https://doi.org/10.1016/j.bbrc.2005.12.144
   PubMed Web of Science ®Google Scholar