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Research Articles

Structure-based design of selective histone deacetylase 6 zinc binding groups

ORCID Icon, , , &
Pages 3166-3177 | Received 15 Apr 2019, Accepted 29 Jul 2019, Published online: 14 Aug 2019

References

  • Amin, S. A., Adhikari, N., Jha, T., & Ghosh, B. (2019). Designing potential HDAC3 inhibitors to improve memory and learning. Journal of Biomolecular Structure and Dynamics, 37(8), 2133–2142. doi: 10.1080/07391102.2018.1477625
  • Baroni, M., Cruciani, G., Sciabola, S., Perruccio, F., & Mason, J. S. (2007). A common reference framework for analyzing/comparing proteins and ligands. Fingerprints for ligands and proteins (FLAP): Theory and application. Journal of Chemical Information and Modeling, 47(2), 279–294. doi: 10.1021/ci600253e
  • Batchu, S. N., Brijmohan, A. S., & Advani, A. (2016). The therapeutic hope for HDAC6 inhibitors in malignancy and chronic disease. Clinical Science, 130(12), 987–1003. doi: 10.1042/CS20160084
  • Bergman, J. A., Woan, K., Perez-Villarroel, P., Villagra, A., Sotomayor, E. M., & Kozikowski, A. P. (2012). Selective histone deacetylase 6 inhibitors bearing substituted urea linkers inhibit melanoma cell growth. Journal of Medicinal Chemistry, 55(22), 9891–9899. doi: 10.1021/jm301098e
  • Bressi, J. C., Jennings, A. J., Skene, R., Wu, Y., Melkus, R., Jong, R. D., O’Connell, S., Grimshaw, C. E., Navre, M., & Gangloff, A. R. (2010). Exploration of the HDAC2 foot pocket: Synthesis and SAR of substituted N-(2-Aminophenyl)benzamides. Bioorganic & Medicinal Chemistry Letters, 20(10), 3142–3145. doi: 10.1016/j.bmcl.2010.03.091
  • Bürli, R. W., Luckhurst, C. A., Aziz, O., Matthews, K. L., Yates, D., Lyons, K. A., … Dominguez, C. (2013). Design, synthesis, and biological evaluation of potent and selective class IIa histone deacetylase (HDAC) inhibitors as a potential therapy for Huntington’s disease. Journal of Medicinal Chemistry, 56(24), 9934–9954. doi: 10.1021/jm4011884
  • Chem Axon. (2017a). Instant JChem V17.3.27.0. Retrieved from https://chemaxon.com/products/instant-jchem.
  • Chem Axon. (2017b). Marvin Sketch V17.27. Retrieved from https://chemaxon.com/products/marvin.
  • Chen, K., Xu, L., & Wiest, O. (2013). Computational exploration of zinc binding groups for HDAC inhibition. The Journal of Organic Chemistry, 78(10), 5051–5055. doi: 10.1021/jo400406g
  • Cohen, S. M. (2017). A bioinorganic approach to fragment-based drug discovery targeting metalloenzymes. Accounts of Chemical Research, 50(8), 2007–2016. doi: 10.1021/acs.accounts.7b00242
  • Congreve, M., Carr, R., Murray, C., & Jhoti, H. (2003). A ‘rule of three’ for fragment-based lead discovery? Drug Discovery Today, 8(19), 876–877. doi: 10.1016/S1359-6446(03)02831-9
  • Cruciani, G. (2006). Molecular interaction fields: Applications in drug discovery and ADME prediction. Hoboken, NJ: Wiley-VCH. Retrieved from https://www.wiley.com/en-us/Molecular+Interaction+Fields%3A+Applications+in+Drug+Discovery+and+ADME+Prediction-p-9783527607136.
  • Dassault Systèmes BIOVIA. (2016). Discovery Studio v.17.2.0. Retrieved from https://www.3dsbiovia.com/products/collaborative-science/biovia-discovery-studio/visualization-download.php.
  • de Ruijter, A. J. M., van Gennip, A. H., Caron, H. N., Kemp, S., & van Kuilenburg, A. B. P. (2003). Histone Deacetylases (HDACs): Characterization of the Classical HDAC Family. The Biochemical Journal, 370(3), 737–749. doi: 10.1042/bj20021321
  • Eldridge, M. D., Murray, C. W., Auton, T. R., Paolini, G. V., & Mee, R. P. (1997). JCAMD_1997_11_425_Eldridge. 11: 1–21. papers3://publication/uuid/EDB550EA-F218-4741-A298-02AF9CCB2D57.
  • Fass, D. M., Shah, R., Ghosh, B., Hennig, K., Norton, S., Zhao, W.-N., … Haggarty, S. J. (2011). Short-chain HDAC inhibitors differentially affect vertebrate development and neuronal chromatin. ACS Medicinal Chemistry Letters, 2(1), 39–42. doi: 10.1021/ml1001954
  • Gaulton, A., Hersey, A., Nowotka, M., Bento, A. P., Chambers, J., Mendez, D., … Leach, A. R. (2017). The ChEMBL database in 2017. Nucleic Acids Research, 45(D1), D945–D954. doi: 10.1093/nar/gkw1074
  • Giannini, G., Vesci, L., Battistuzzi, G., Vignola, D., Milazzo, F. M., Guglielmi, M. B., … Cabri, W. (2014). ST7612AA1, a thioacetate-ω(γ-lactam carboxamide) derivative selected from a novel generation of oral HDAC inhibitors. Journal of Medicinal Chemistry, 57(20), 8358–8377. doi: 10.1021/jm5008209
  • Goodford, P. J. (1985). A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. Journal of Medicinal Chemistry, 28(7), 849–857. doi: 10.1021/jm00145a002
  • Goracci, L., Deschamps, N., Randazzo, G. M., Petit, C., Dos Santos Passos, C., Carrupt, P.-A., Simões-Pires, C., & Nurisso, A. (2016). A rational approach for the identification of non-hydroxamate HDAC6-selective inhibitors. Scientific Reports, 6(1), 29086. doi: 10.1038/srep29086
  • Hai, Y., & Christianson, D. W. (2016). Histone deacetylase 6 structure and molecular basis of catalysis and inhibition. Nature Chemical Biology, 12(9), 741–747. doi: 10.1038/nchembio.2134
  • Hermant, P., Bosc, D., Piveteau, C., Gealageas, R., Lam, B. V., Ronco, C., … Deprez-Poulain, R. (2017). Controlling plasma stability of hydroxamic acids: A MedChem toolbox. Journal of Medicinal Chemistry, 60(21), 9067–9089. doi: 10.1021/acs.jmedchem.7b01444
  • Homeyer, N., & Gohlke, H. (2012). Free energy calculations by the molecular mechanics Poisson-Boltzmann surface area method. Molecular Informatics, 31(2), 114–122. doi: 10.1002/minf.201100135
  • Ibrahim Uba, A., & Yelekçi, K. (2019). Homology modeling of human histone deacetylase 10 and design of potential selective inhibitors. Journal of Biomolecular Structure and Dynamics, 34(14). doi: 10.1080/07391102.2018.1521747
  • Irwin, J. J., Sterling, T., Mysinger, M. M., Bolstad, E. S., & Coleman, R. G. (2012). ZINC: A free tool to discover chemistry for biology. Journal of Chemical Information and Modeling, 52(7), 1757–1768. doi: 10.1021/ci3001277
  • Jacobsen, J. A., Fullagar, J. L., Miller, M. T., & Cohen, S. M. (2011). Identifying chelators for metalloprotein inhibitors using a fragment-based approach. Journal of Medicinal Chemistry, 54(2), 591–602. doi: 10.1021/jm101266s
  • Jones, G., Willett, P., Glen, R. C., Leach, A. R., & Taylor, R. (1997). Development and validation of a genetic algorithm for flexible docking. Journal of Molecular Biology, 267(3), 727–748. doi: 10.1006/jmbi.1996.0897
  • Jones, P., Bottomley, M. J., Carfí, A., Cecchetti, O., Ferrigno, F., Lo Surdo, P., & Ontoria, J. M. (2008). 2-trifluoroacetylthiophenes, a novel series of potent and selective Class II histone deacetylase inhibitors. Bioorganic & Medicinal Chemistry Letters, 18(11), 3456–3461. doi: 10.1016/j.bmcl.2008.02.026
  • Kalin, J. H., & Bergman, J. A. (2013). Development and therapeutic implications of selective histone deacetylase 6 inhibitors. Journal of Medicinal Chemistry, 56(16), 6297–6313. doi: 10.1021/jm4001659
  • Kashyap, K., & Kakkar, R. (2019). An insight into Selective and potent inhibition of histone deacetylase 8 through induced-fit docking, pharmacophore modeling and QSAR studies. Journal of Biomolecular Structure and Dynamics, 1–18. doi: 10.1080/07391102.2019.1567388
  • Kawai, K., & Nagata, N. (2012). Metal–Ligand interactions: An analysis of zinc binding groups using the protein data bank. European Journal of Medicinal Chemistry, 51, 271–276. doi: 10.1016/j.ejmech.2012.02.028
  • Kemp, M. M., Wang, Q., Fuller, J. H., West, N., Martinez, N. M., Morse, E. M., Weïwer, M., Schreiber, S. L., Bradner, J. E., & Koehler, A. N. (2011). A novel HDAC inhibitor with a hydroxy-pyrimidine scaffold. Bioorganic & Medicinal Chemistry Letters, 21(14), 4164–4169. doi: 10.1016/j.bmcl.2011.05.098
  • KrennHrubec, K., Marshall, B. L., Hedglin, M., Verdin, E., & Ulrich, S. M. (2007). Design and evaluation of ‘Linkerless’ hydroxamic acids as selective HDAC8 inhibitors. Bioorganic & Medicinal Chemistry Letters, 17(10), 2874–2878. doi: 10.1016/j.bmcl.2007.02.064
  • Kutil, Z., Novakova, Z., Meleshin, M., Mikesova, J., Schutkowski, M., & Barinka, C. (2017). HDAC11 is a fatty-acid deacylase. ACS chemical biology, 13(36), 85–693.
  • Lagorce, D., Sperandio, O., Baell, J. B., Miteva, M. A., & Villoutreix, B. O. (2015). FAF-Drugs3: A web server for compound property calculation and chemical library design. Nucleic Acids Research, 43(W1), W200–207. doi: 10.1093/nar/gkv353
  • Liang, T., & Fang, H. (2019). Structure, functions and selective inhibitors of HDAC6. Current Topics in Medicinal Chemistry, 18(28), 2429–2447. doi: 10.2174/1568026619666181129141822
  • Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber Ff99SB protein force field. Proteins: Structure, Function, and Bioinformatics, 78(8), 1950–1958. doi: 10.1002/prot.22711
  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., … Fox, D. J. (2009). Gaussian 09, Revision D.01.
  • Mahalakshmi, R., Husayn Ahmed, P., & Mahadevan, V. (2018). HDAC inhibitors show differential epigenetic regulation and cell survival strategies on P53 mutant colon cancer cells. Journal of Biomolecular Structure and Dynamics, 36(4), 938–955. doi: 10.1080/07391102.2017.1302820
  • Martin, D. P., Blachly, P. G., Marts, A. R., Woodruff, T. M., de Oliveira, C. A. F., McCammon, J. A., Tierney, D. L., & Cohen, S. M. (2014). Unconventional’ coordination chemistry by metal chelating fragments in a metalloprotein active site. Journal of the American Chemical Society, 136(14), 5400–5406. doi: 10.1021/ja500616m
  • Martínez-Rosell, G., Giorgino, T., & De Fabritiis, G. (2017). PlayMolecule ProteinPrepare: A web application for protein preparation for molecular dynamics simulations. Journal of Chemical Information and Modeling, 57(7), 1511–1516. doi: 10.1021/acs.jcim.7b00190
  • Mazitschek, R., Patel, V., Wirth, D. F., & Clardy, J. (2008). Development of a fluorescence polarization based assay for histone deacetylase ligand discovery. Bioorganic & Medicinal Chemistry Letters, 18(9), 2809–2812. doi: 10.1016/j.bmcl.2008.04.007
  • Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., & Olson, A. J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Journal of Computational Chemistry, 19(14), 1639–1662. doi: 10.1002/(SICI)1096-987X(19981115)19:14 < 1639::AID-JCC10 > 3.0.CO;2-B
  • Murray-Thompson, M., Wu, Z., Reid, R. A., Soler, D., Nolan, M. A., Wright, Q. G., & Moyer, M. B. (2013). Selective class IIa histone deacetylase inhibition via a nonchelating zinc-binding group. Nature Chemical Biology, 9(5), 319–325. doi: 10.1038/nchembio.1223
  • Muthyala, R., Shin, W. S., Xie, J., & Sham, Y. Y. (2015). Discovery of 1-hydroxypyridine-2-thiones as selective histone deacetylase inhibitors and their potential application for treating leukemia. Bioorganic & Medicinal Chemistry Letters, 25(19), 4320–4324. doi: 10.1016/j.bmcl.2015.07.065
  • Olson, D. E., Wagner, F. F., Kaya, T., Gale, J. P., Aidoud, N., Davoine, E. L., Lazzaro, F., Weïwer, M., Zhang, Y.-L., & Holson, E. B. (2013). Discovery of the first histone deacetylase 6/8 dual inhibitors. Journal of Medicinal Chemistry, 56(11), 4816–4820. doi: 10.1021/jm400390r
  • Otava Chemicals. (2017). Otava chelator fragment library. Retrieved from http://www.otavachemicals.com/.
  • Paissoni, C., Spiliotopoulos, D., Musco, G., & Spitaleri, A. (2015). GMXPBSA 2.1: A GROMACS tool to perform MM/PBSA and computational alanine scanning. Computer Physics Communications, 186, 105–107. doi: 10.1016/j.cpc.2014.09.010
  • Pande, V. (2016). Understanding the complexity of epigenetic target space. Journal of Medicinal Chemistry, 59(4), 1299–1307. doi: 10.1021/acs.jmedchem.5b01507
  • Patil, V., Sodji, Q. H., Kornacki, J. R., Mrksich, M., & Oyelere, A. K. (2013). 3-hydroxypyridin-2-thione as novel zinc binding group for selective histone deacetylase inhibition. Journal of Medicinal Chemistry, 56(9), 3492–3506. doi: 10.1021/jm301769u
  • PerkinElmer. (2015). ChemDraw—Chemical drawing software, PerkinElmer. Retrieved from http://www.perkinelmer.com/category/chemdraw.
  • Perruccio, F., Mason, J. S., Sciabola, S., & Baroni, M. (2006). FLAP: 4-point pharmacophore fingerprints from GRID. In Molecular interaction fields: Applications in drug discovery and ADME prediction (Vol. 27, pp. 83–102). Hoboken, NJ: Wiley. doi: 10.1073/pnas.1718823114
  • Porter, N. J., Mahendran, A., Breslow, R., & Christianson, D. W. (2017). Unusual zinc-binding mode of HDAC6-selective hydroxamate inhibitors. Proceedings of the National Academy of Sciences, 114(51), 13459–13464. doi: 10.1073/pnas.1718823114
  • Porter, N. J., Osko, J. D., Diedrich, D., Kurz, T., Hooker, J. M., Hansen, F. K., & Christianson, D. W. (2018). Histone deacetylase 6-selective inhibitors and the influence of capping groups on hydroxamate-zinc denticity. Journal of Medicinal Chemistry, 61(17), 8054–8060. doi: 10.1021/acs.jmedchem.8b01013
  • Porter, N. J., Wagner, F. F., & Christianson, D. W. (2018). Entropy as a driver of selectivity for inhibitor binding to histone deacetylase 6. Biochemistry, 57(26), 3916–3924. doi: 10.1021/acs.biochem.8b00367
  • Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29(7), 845–854. doi: 10.1093/bioinformatics/btt055
  • Roche, J., & Bertrand, P. (2016). Inside HDACs with more selective HDAC inhibitors. European Journal of Medicinal Chemistry, 121, 451–483. doi: 10.1016/j.ejmech.2016.05.047
  • Seidel, C., Schnekenburger, M., Dicato, M., & Diederich, M. (2015). Histone deacetylase 6 in health and disease. Epigenomics, 7(1), 103–118. doi: 10.2217/epi.14.69
  • Sharma, M., Jha, P., Verma, P., & Chopra, M. (2019). Combined comparative molecular field analysis, comparative molecular similarity indices analysis, molecular docking and molecular dynamics studies of histone deacetylase 6 inhibitors. Chemical Biology & Drug Design, 93(5), 910–925. doi: 10.1111/cbdd.13488
  • Shen, S., & Kozikowski, A. P. (2016). Why hydroxamates may not be the best histone deacetylase inhibitors—What some may have forgotten or would rather forget? ChemMedChem, 11(1), 15–21. doi: 10.1002/cmdc.201500486
  • Sixto-López, Y., Bello, M., & Correa-Basurto, J. (2019a). Insights into structural features of HDAC1 and its selectivity inhibition elucidated by molecular dynamic simulation and molecular docking. Journal of Biomolecular Structure and Dynamics, 37(3), 584–610. doi: 10.1080/07391102.2018.1441072
  • Sixto-López, Y., Bello, M., & Correa-Basurto, J. (2019b). Structural and energetic basis for the inhibitory selectivity of both catalytic domains of dimeric HDAC6. Journal of Biomolecular Structure and Dynamics, 1–20. doi: 10.1080/07391102.2018.1557560
  • Søndergaard, C. R., Olsson, M. H. M., Rostkowski, M., & Jensen, J. H. (2011). Improved treatment of ligands and coupling effects in empirical calculation and rationalization of p K a values. Journal of Chemical Theory and Computation, 7(7), 2284–2295. doi: 10.1021/ct200133y
  • Sousa da Silva, A. W., & Vranken, W. F. (2012). ACPYPE—AnteChamber PYthon Parser InterfacE. BMC Research Notes, 5(1), 367. doi: 10.1186/1756-0500-5-367
  • Uba, A. I., & Yelekçi, K. (2018). Identification of potential isoform-selective histone deacetylase inhibitors for cancer therapy: A combined approach of structure-based virtual screening, admet prediction and molecular dynamics simulation assay. Journal of Biomolecular Structure and Dynamics, 36(12), 3231–3245. doi: 10.1080/07391102.2017.1384402
  • VanHeyst, M. D., Ononye, S. N., Wright, D. L., Ammar, M., Anderson, A. C., Zhou, W., & Oblak, E. Z. (2013). Tropolones as lead-like natural products: The development of potent and selective histone deacetylase inhibitors. ACS Medicinal Chemistry Letters, 4(8), 757–761. doi: 10.1021/ml400158k
  • Vassetti, D., Pagliai, M., & Procacci, P. (2019). Assessment of GAFF2 and OPLS-AA general force fields in combination with the water models TIP3P, SPCE, and OPC3 for the solvation free energy of druglike organic molecules. Journal of Chemical Theory and Computation, 15(3), 1983–1995. doi: 10.1021/acs.jctc.8b01039
  • Wagner, F. F., Olson, D. E., Jennifer, P. G., Kaya, T., Weïwer, M., Aidoud, N., & Thomas, M. (2013). Potent and selective inhibition of histone deacetylase 6 (HDAC6) does not require a surface-binding motif. Journal of Medicinal Chemistry, 56(4), 1772–1776. doi: 10.1016/j.ejmech.2017.10.040
  • Wagner, F. F., Lundh, M., Kaya, T., McCarren, P., Zhang, Y. L., Chattopadhyay, S., … & Vetere, A. (2016). An isochemogenic set of inhibitors to define the therapeutic potential of histone deacetylases in β-cell protection. ACS Chemical Biology, 11(2), 363–374. doi:10.1021/acschembio.5b00640.
  • 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. doi: 10.1016/j.ejmech.2017.10.040
  • Wang, Y., Yang, L., Hou, J., Zou, Q., Gao, Q., Yao, W., … Zhang, J. (2019). Hierarchical virtual screening of the dual MMP-2/HDAC-6 inhibitors from natural products based on pharmacophore models and molecular docking. Journal of Biomolecular Structure and Dynamics, 37(3), 649–670. doi: 10.1080/07391102.2018.1434833
  • Watson, P. J., Millard, C. J., Riley, A. M., Robertson, N. S., Wright, L. C., Godage, H. Y., … Schwabe, J. W. R. (2016). Insights into the activation mechanism of class I HDAC complexes by inositol phosphates. Nature Communications, 7, 11262. doi: 10.1016/j.bmc.2011.06.030
  • Whitehead, L., Dobler, M. R., Radetich, B., Zhu, Y., Atadja, P. W., Claiborne, T., … Stams, T. (2011). Human HDAC isoform selectivity achieved via exploitation of the acetate release channel with structurally unique small molecule inhibitors. Bioorganic & Medicinal Chemistry, 19(15), 4626–4634. doi: 10.1016/j.bmc.2011.06.030
  • Wu, J., Adejare, A., Wang, J., Wallach, J., Duane, S., Ma, H., Wang, Y., & Wang, Y. (2017). Developing selective histone deacetylases (HDACs) inhibitors through ebselen and analogs. Drug Design, Development and Therapy, 11, 1369–1382. doi: 10.2147/DDDT.S124977
  • Yang, M., Robert Orlowski, P., Hari, S. S., Jones, R. J., Markelewicz, N., Raje, J. G., … Wheeler, C. (2017). Ricolinostat, the first selective histone deacetylase 6 inhibitor, in combination with bortezomib and dexamethasone for relapsed or refractory multiple myeloma. Clinical Cancer Research, 23(13), 3307–3315. doi: 10.1158/1078-0432.CCR-16-2526
  • Yuan, Y., Hu, Z., Bao, M., Sun, R., Long, X., Long, L., … Bao, J. (2018). Screening of novel histone deacetylase 7 inhibitors through molecular docking followed by a combination of molecular dynamics simulations and ligand-based approach. Journal of Biomolecular Structure and Dynamics,37(15), 1–12. doi: 10.1080/07391102.2018.1541141
  • Zhou, H., Wang, C., Deng, T., Tao, R., & Li, W. (2018). Novel urushiol derivatives as HDAC8 inhibitors: Rational design, virtual screening, molecular docking and molecular dynamics studies. Journal of Biomolecular Structure and Dynamics, 36(8), 1966–1978. doi: 10.1080/07391102.2017.1344568

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