A comparative quantitative structural assessment of benzothiazine-derived HDAC8 inhibitors by predictive ligand-based drug designing approaches

References

• M.M. Hassan, J. Israelian, N. Nawar, G. Ganda, P. Manaswiyoungkul, Y.S. Raouf, D. Armstrong, A. Sedighi, O.O. Olaoye, F. Erdogan, A.D. Cabral, F. Angeles, R. Altintas, E.D. de Araujo, and P.T. Gunning, Characterization of conformationally constrained benzanilide scaffolds for potent and selective HDAC8 targeting, J. Med. Chem. 63 (2020), pp. 8634–8648. doi:10.1021/acs.jmedchem.0c01025.
   PubMed Web of Science ®Google Scholar
• M. Zhang, J.B. Ying, S.S. Wang, D. He, H. Zhu, C. Zhang, L. Tang, R. Lin, and Y. Zhang, Exploring the binding mechanism of HDAC8 selective inhibitors: Lessons from the modification of Cap group, J. Cell Biochem. 121 (2020), pp. 3162–3172. doi:10.1002/jcb.29583.
   PubMed Web of Science ®Google Scholar
• S. Ropero and M. Esteller, The role of histone deacetylases (HDACs) in human cancer, Mol. Oncol. 1 (2007), pp. 19–25. doi:10.1016/j.molonc.2007.01.001.
   PubMed Web of Science ®Google Scholar
• E. Seto and M. Yoshida, Erasers of histone acetylation: The histone deacetylase enzymes, Cold Spring Harbor Perspect. Biol. 6 (2014), pp. a018713. doi:10.1101/cshperspect.a018713.
   PubMed Web of Science ®Google Scholar
• S. Banerjee, N. Adhikari, S.A. Amin, and T. Jha, Histone deacetylase 8 (HDAC8) and its inhibitors with selectivity to other isoforms: An overview, Eur. J. Med. Chem. 164 (2019), pp. 214–240. doi:10.1016/j.ejmech.2018.12.039.
   PubMed Web of Science ®Google Scholar
• K.J. Falkenberg and R.W. Johnstone, Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders, Nat. Rev. Drug Discov. 13 (2014), pp. 673–691.
   PubMed Web of Science ®Google Scholar
• A. Chakrabarti, I. Oehme, O. Witt, G. Oliveira, W. Sippl, C. Romier, R.J. Pierce, and M. Jung, HDAC8: A multifaceted target for therapeutic interventions, Trends. Pharmacol. Sci. 36 (2015), pp. 481–492. doi:10.1016/j.tips.2015.04.013.
   PubMed Web of Science ®Google Scholar
• T. Eckschlager, J. Plch, M. Stiborova, and J. Hrabeta, Histone deacetylase inhibitors as anticancer drugs, Int. J. Mol. Sci. 18 (2017), pp. 1414. doi:10.3390/ijms18071414.
   PubMed Web of Science ®Google Scholar
• N. Adhikari, S.A. Amin, and T. Jha, Selective and nonselective HDAC8 inhibitors: A therapeutic patent review, Pharm. Pat. Anal. 7 (2018), pp. 259–276. doi:10.4155/ppa-2018-0019.
   PubMed Web of Science ®Google Scholar
• B. Coiffier, B. Pro, H.M. Prince, F. Foss, L. Sokol, M. Greenwood, D. Caballero, P. Borchmann, F. Morschhauser, M. Wilhelm, L. Pinter-Brown, S. Padmanabhan, A. Shustov, J. Nichols, S. Carroll, J. Balser, B. Balser, and S. Horwitz, Results from a pivotal, open-label, phase II study of romidepsin in relapsed or refractory peripheral T-cell lymphoma after prior systemic therapy, J. Clin. Oncol. 30 (2012), pp. 631–636. doi:10.1200/JCO.2011.37.4223.
   PubMed Web of Science ®Google Scholar
• A. Chakrabarti, J. Melesina, F.R. Kolbinger, I. Oehme, J. Senger, O. Witt, W. Sippl, and M. Jung, Targeting histone deacetylase 8 as a therapeutic approach to cancer and neurodegenerative diseases, Future Med. Chem. 8 (2016), pp. 1609–1634. doi:10.4155/fmc-2016-0117.
   PubMed Web of Science ®Google Scholar
• M.J. Bishton, S.J. Harrison, B.P. Martin, N. McLaughlin, C. James, E.C. Josefsson, K.J. Henley, B.T. Kile, H.M. Prince, and R.W. Johnstone, Deciphering the molecular and biologic processes that mediate histone deacetylase inhibitor-induced thrombocytopenia, Blood 117 (2011), pp. 3658–3668. doi:10.1182/blood-2010-11-318055.
   PubMed Web of Science ®Google Scholar
• H.J. Mackay, H. Hirte, T. Colgan, A. Covens, K. MacAlpine, P. Grenci, L. Wang, J. Mason, P.A. Pham, M.S. Tsao, J. Pan, J. Zwiebel, and A.M. Oza, Phase II trial of the histone deacetylase inhibitor belinostat in women with platinum resistant epithelial ovarian cancer and micropapillary (LMP) ovarian tumours, Eur. J. Cancer 46 (2010), pp. 1573–1579. doi:10.1016/j.ejca.2010.02.047.
   PubMed Web of Science ®Google Scholar
• P. Trivedi, N. Adhikari, S.A. Amin, Y. Bobde, R. Ganesh, T. Jha, and B. Ghosh, Design, synthesis, biological evaluation and molecular docking study of arylcarboxamido piperidine and piperazine-based hydroxamates as potential HDAC8 inhibitors with promising anticancer activity, Eur. J. Pharm. Sci. 138 (2019), pp. 105046. doi:10.1016/j.ejps.2019.105046.
   PubMed Web of Science ®Google Scholar
• S. Banerjee, N. Adhikari, S.A. Amin, and T. Jha, Structural exploration of tetrahydroisoquinoline derivatives as HDAC8 inhibitors through multi-QSAR modeling study, J. Biomol. Struct. Dyn. 38 (2020), pp. 1551–1564. doi:10.1080/07391102.2019.1617782.
   PubMed Web of Science ®Google Scholar
• I. Oehme, H.E. Deubzer, D. Wegener, D. Pickert, J.P. Linke, B. Hero, A. Kopp-Schneider, F. Westermann, S.M. Ulrich, A. von Deimling, M. Fischer, and O. Witt, Histone deacetylase 8 in neuroblastoma tumorigenesis, Clin. Cancer Res. 15 (2009), pp. 91–99. doi:10.1158/1078-0432.CCR-08-0684.
   PubMed Web of Science ®Google Scholar
• Y. Li, R. Liang, M. Sun, Z. Li, H. Sheng, J. Wang, P. Xu, S. Liu, W. Yang, B. Lu, S. Zhang, and C. Shan, AMPK-dependent phosphorylation of HDAC8 triggers PGM1 expression to promote lung cancer cell survival under glucose starvation, Cancer Lett. 478 (2020), pp. 82–92. doi:10.1016/j.canlet.2020.03.007.
   PubMed Web of Science ®Google Scholar
• J. Wu, C. Du, Z. Lv, C. Ding, J. Cheng, H. Xie, L. Zhou, and S. Zheng, The up-regulation of histone deacetylase 8 promotes proliferation and inhibits apoptosis in hepatocellular carcinoma, Digest. Dis. Sci. 58 (2013), pp. 3545–3553. doi:10.1007/s10620-013-2867-7.
   PubMed Web of Science ®Google Scholar
• G. Lopez and R.E. Pollock, Evaluating the effect of HDAC8 inhibition in malignant peripheral nerve sheath tumors, Meth. Mol. Biol. 1510 (2017), pp. 365–374.
   PubMedGoogle Scholar
• J.M. Watters, G. Wright, M.A. Smith, B. Shah, and K.L. Wright, Histone deacetylase 8 inhibition suppresses mantle cell lymphoma viability while preserving natural killer cell function, Biochem. Biophys. Res. Commun. 534 (2020), pp. 773–779.
   PubMed Web of Science ®Google Scholar
• M.F. Emmons, F. Faião-Flores, R. Sharma, R. Thapa, J.L. Messina, J.C. Becker, D. Schadendorf, E. Seto, V.K. Sondak, J.M. Koomen, Y.A. Chen, E.K. Lau, L. Wan, J.D. Licht, and K.S.M. Smalley, HDAC8 regulates a stress response pathway in melanoma to mediate escape from braf inhibitor therapy, Cancer Res. 79 (2019), pp. 2947–2961. doi:10.1158/0008-5472.CAN-19-0040.
   PubMed Web of Science ®Google Scholar
• J. Long, M.Y. Jia, W.Y. Fang, X.J. Chen, L.L. Mu, Z.Y. Wang, Y. Shen, R.F. Xiang, L.N. Wang, L. Wang, C.H. Jiang, J.L. Jiang, W.J. Zhang, Y.D. Sun, L. Chang, W.H. Gao, Y. Wang, J.M. Li, D.L. Hong, A.B. Liang, and J. Hu, FLT3 inhibition upregulates HDAC8 via FOXO to inactivate p53 and promote maintenance of FLT3-ITD+ acute myeloid leukemia, Blood 135 (2020), pp. 1472–1483. doi:10.1182/blood.2019003538.
   PubMed Web of Science ®Google Scholar
• M. Spreafico, A.M. Gruszka, D. Valli, M. Mazzola, G. Deflorian, A. Quintè, M.G. Totaro, C. Battaglia, M. Alcalay, A. Marozzi, and A. Pistocchi, HDAC8: A promising therapeutic target for acute myeloid leukemia, Front. Cell Dev. Biol. 8 (2020), pp. 844. doi:10.3389/fcell.2020.00844.
   PubMed Web of Science ®Google Scholar
• T.L. Ramos, L.I. Sánchez-Abarca, A. Redondo, Á. Hernández-Hernández, A.M. Almeida, N. Puig, C. Rodríguez, R. Ortega, S. Preciado, A. Rico, S. Muntión, J.R.G. Porras, C. Del Cañizo, and F. Sánchez-Guijo, HDAC8 overexpression in mesenchymal stromal cells from JAK2+ myeloproliferative neoplasms: A new therapeutic target?, Oncotarget 8 (2017), pp. 28187–28202. doi:10.18632/oncotarget.15969.
   PubMedGoogle Scholar
• A. Umamaheswari, A. Puratchikody, and N. Hari, Synthesis and investigation of therapeutic potential of isoform-specific HDAC8 inhibitors for the treatment of cutaneous t cell lymphoma, Anticancer Agents Med. Chem. 19 (2019), pp. 916–934. doi:10.2174/1871520619666190301150254.
   PubMed Web of Science ®Google Scholar
• P. An, J. Li, L. Lu, Y. Wu, Y. Ling, J. Du, Z. Chen, and H. Wang, Histone deacetylase 8 triggers the migration of triple negative breast cancer cells via regulation of YAP signals, Eur. J. Pharmacol. 845 (2019), pp. 16–23. doi:10.1016/j.ejphar.2018.12.030.
   PubMed Web of Science ®Google Scholar
• G.R. Vanaja, H.G. Ramulu, and A.M. Kalle, Overexpressed HDAC8 in cervical cancer cells shows functional redundancy of tubulin deacetylation with HDAC6, Cell Commun. Signal. 16 (2018), pp. 1–6. doi:10.1186/s12964-018-0231-4.
   PubMed Web of Science ®Google Scholar
• S. Song, Y. Wang, P. Xu, R. Yang, Z. Ma, S. Liang, and G. Zhang, The inhibition of histone deacetylase 8 suppresses proliferation and inhibits apoptosis in gastric adenocarcinoma, Int. J. Oncol. 47 (2015), pp. 1819–1828. doi:10.3892/ijo.2015.3182.
   PubMed Web of Science ®Google Scholar
• M.Y. Ahn and J.H. Yoon, Histone deacetylase 8 as a novel therapeutic target in oral squamous cell carcinoma, Oncol. Rep. 37 (2017), pp. 540–546. doi:10.3892/or.2016.5280.
   PubMed Web of Science ®Google Scholar
• C.H. Lee, Y. Choi, H. Cho, I.H. Bang, L. Hao, S.O. Lee, R. Jeon, E.J. Bae, and B.H. Park, Histone deacetylase 8 inhibition alleviates cholestatic liver injury and fibrosis, Biochem. Pharmacol. 183 (2020), pp. 114312. doi:10.1016/j.bcp.2020.114312.
   PubMed Web of Science ®Google Scholar
• T. Heimburg, A. Chakrabarti, J. Lancelot, M. Marek, J. Melesina, A.T. Hauser, T.B. Shaik, S. Duclaud, D. Robaa, F. Erdmann, M. Schmidt, C. Romier, R.J. Pierce, M. Jung, and W. Sippl, Structure-based design and synthesis of novel inhibitors targeting HDAC8 from Schistosoma mansoni for the treatment of schistosomiasis, J. Med. Chem. 59 (2016), pp. 2423–2435. doi:10.1021/acs.jmedchem.5b01478.
   PubMed Web of Science ®Google Scholar
• S. Saito, Y. Zhuang, T. Suzuki, Y. Ota, M.E. Bateman, A.L. Alkhatib, G.F. Morris, and J.A. Lasky, HDAC8 inhibition ameliorates pulmonary fibrosis, Am. J. Physiol. Lung Cell Mol. Physiol. 316 (2019), pp. L175–L186. doi:10.1152/ajplung.00551.2017.
   PubMed Web of Science ®Google Scholar
• T. Xiao, Y. Fu, W. Zhu, R. Xu, L. Xu, P. Zhang, Y. Du, J. Cheng, and H. Jiang, HDAC8, A Potential therapeutic target, regulates proliferation and differentiation of bone marrow stromal cells in fibrous dysplasia, Stem Cells Transl. Med. 8 (2019), pp. 148–161. doi:10.1002/sctm.18-0057.
   PubMed Web of Science ®Google Scholar
• Y. Zhang, J. Zou, E. Tolbert, T.C. Zhao, G. Bayliss, and S. Zhuang, Identification of histone deacetylase 8 as a novel therapeutic target for renal fibrosis, FASEB J. 34 (2020), pp. 7295–7310.
   PubMed Web of Science ®Google Scholar
• S. Li, G. Fossati, C. Marchetti, D. Modena, P. Pozzi, L.L. Reznikov, M.L. Moras, T. Azam, A. Abbate, P. Mascagni, and C.A. Dinarello, Specific inhibition of histone deacetylase 8 reduces gene expression and production of proinflammatory cytokines in vitro and in vivo, J. Biol. Chem. 290 (2015), pp. 2368–2378.
   PubMed Web of Science ®Google Scholar
• S. Banerjee, S.A. Amin, N. Adhikari, and T. Jha, Essential elements regulating HDAC8 inhibition: A classification based structural analysis and enzyme-inhibitor interaction study of hydroxamate based HDAC8 inhibitors, J. Biomol. Struct. Dyn. 38 (2020), pp. 5513–5525. doi:10.1080/07391102.2019.1704881.
   PubMed Web of Science ®Google Scholar
• S.A. Amin, S. Banerjee, N. Adhikari, and T. Jha, Discriminations of active from inactive HDAC8 inhibitors Part II: Bayesian classification study to find molecular fingerprints, SAR QSAR Environ. Res. 31 (2020), pp. 245–260. doi:10.1080/1062936X.2020.1723136.
   PubMed Web of Science ®Google Scholar
• S.A. Amin, N. Adhikari, and T. Jha, Exploration of histone deacetylase 8 inhibitors through classification QSAR study: Part II, J. Mol. Struct. 1204 (2020), pp. 127529. doi:10.1016/j.molstruc.2019.127529.
   Web of Science ®Google Scholar
• S.A. Amin, N. Adhikari, and T. Jha, Diverse classes of HDAC8 inhibitors: In search of molecular fingerprints that regulate activity, Future Med. Chem. 10 (2018), pp. 1589–1602. doi:10.4155/fmc-2018-0005.
   PubMed Web of Science ®Google Scholar
• A. Kleinschek, C. Meyners, E. Digiorgio, C. Brancolini, and F.-J. Meyer-Almes, Potent and selective non-hydroxamate histone deacetylase 8 inhibitors, ChemMedChem 11 (2016), pp. 2598–2606. doi:10.1002/cmdc.201600528.
   PubMed Web of Science ®Google Scholar
• B. Wolff, N. Jänsch, W.O. Sugiarto, S. Frühschulz, M. Lang, R. Altintas, I. Oehme, and F.-J. Meyer-Almes, Synthesis and structure activity relationship of 1, 3-benzo-thiazine-2-thiones as selective HDAC8 inhibitors, Eur. J. Med. Chem. 184 (2019), pp. 111756. doi:10.1016/j.ejmech.2019.111756.
   PubMed Web of Science ®Google Scholar
• ChemDraw Ultra 5.0, Cambridge Soft Corporation, USA, 2010; software available at http://www.cambridgesoft.com.
   Google Scholar
• Discovery Studio 3.0 (DS 3.0). Accelrys Inc., CA, USA, 2015; software available at http://www.accelrys.com.
   Google Scholar
• S. Sanyal, S.A. Amin, N. Adhikari, and T. Jha, QSAR modelling on a series of arylsulfonamide-based hydroxamates as potent MMP-2 inhibitors, SAR QSAR Env. Res. 30 (2019), pp. 247–263. doi:10.1080/1062936X.2019.1588159.
   PubMed Web of Science ®Google Scholar
• TALETE srl. DRAGON, Milano, Italy, 2007; software available at http://www.talete.mi.it/.
   Google Scholar
• The simple, user-friendly and reliable online standalone tools freely, available at http://dtclab.webs.com/software-tools. (Accessed on 20 Dec 2021).
   Google Scholar
• I.V. Tetko, I. Sushko, A.K. Pandey, H. Zhu, A. Tropsha, E. Papa, T. Oberg, R. Todeschini, D. Fourches, and A. Varnek, Critical assessment of QSAR models of environmental toxicity against Tetrahymena pyriformis: Focusing on applicability domain and overfitting by variable selection, J. Chem. Inf. Model. 48 (2008), pp. 1733–1746. doi:10.1021/ci800151m.
   PubMed Web of Science ®Google Scholar
• S. Katoch, S.S. Chauhan, and V. Kumar, A review on genetic algorithm: Past, present, and future, Multimed. Tools Appl. 31 (2020), pp. 1–36.
   Google Scholar
• K. Roy, S. Kar, and R.N. Das, A Primer on QSAR/QSPR Modeling: Fundamental Concepts, Springer, New York, 2015.
   Google Scholar
• A. Golbraikh and A. Tropsha, Beware of q2!, J. Mol. Graph. Model. 20 (2002), pp. 269–276. doi:10.1016/S1093-3263(01)00123-1.
   PubMed Web of Science ®Google Scholar
• S.K. Baidya, S.A. Amin, S. Banerjee, N. Adhikari, and T. Jha, Structural exploration of arylsulfonamide-based ADAM17 inhibitors through validated comparative multi-QSAR modelling studies, J. Mol. Struct. 1185 (2019), pp. 128–142. doi:10.1016/j.molstruc.2019.02.081.
   Web of Science ®Google Scholar
• A. Nandy, K. Roy, and A. Saha, Structural exploration of PPARγ modulators through pharmacophore mapping, fragment-based design, docking, and molecular dynamics simulation analyses, Med. Chem. Res. 26 (2016), pp. 52–63.
   Web of Science ®Google Scholar
• N. Adhikari, A.K. Halder, C. Mondal, and T. Jha, Exploring structural requirements of aurone derivatives as antimalarials by validated DFT-based QSAR, HQSAR and COMFA–COMSIA approach, Med. Chem. Res. 22 (2013), pp. 6029–6045. doi:10.1007/s00044-013-0590-8.
   Web of Science ®Google Scholar
• SYBYL-X 2.0 Software, Tripos Inc., St. Louis. MO, USA, 2012; software available at http://www.certara.com.
   Google Scholar
• N. Adhikari, S.A. Amin, A. Saha, and T. Jha, Understanding chemico-biological interactions of glutamate MMP-2 inhibitors through rigorous alignment-dependent 3D-QSAR analyses, ChemistrySelect 2 (2017), pp. 7888–7898. doi:10.1002/slct.201701330.
   Web of Science ®Google Scholar
• O. Trott and A.J. Olson, AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading, J. Comp. Chem. 31 (2010), pp. 455–461.
   PubMed Web of Science ®Google Scholar
• J. Eberhardt, D. Santos-Martins, A.F. Tillack, and S. Forli, AutoDock Vina 1.2.0: New docking methods, expanded force field, and python bindings, J. Chem. Inf. Model. 61 (2021), pp. 3891–3898. doi:10.1021/acs.jcim.1c00203.
   PubMed Web of Science ®Google Scholar
• M. Muth, N. Jänsch, A. Kopranovic, A. Krämer, N. Wössner, M. Jung, F. Kirschhöfer, G. Brenner-Weiß, and F.-J. Meyer-Almes, Covalent inhibition of histone deacetylase 8 by 3,4-dihydro-2H-pyrimido[1,2-c][1,3]benzothiazin-6-imine, Biochim. Biophys. Acta Gen. Subj. 1863 (2019), pp. 577–585. doi:10.1016/j.bbagen.2019.01.001.
   PubMed Web of Science ®Google Scholar
• H.J.C. Berendsen, D. van der Spoel, and R. van Drunen, GROMACS: A message-passing parallel molecular dynamics implementation, Comput. Phys. Commun. 1-2 (1995), pp. 43–56. doi:10.1016/0010-4655(95)00042-E.
   Google Scholar
• Groningen machine for chemical simulations; software available at https://www.gromacs.org/.
   Google Scholar
• R.B. Best, X. Zhu, J. Shim, P.E.M. Lopes, J. Mittal, M. Feig, and A.D. Mackerell Jr., Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ(1) and χ(2) dihedral angles, J. Chem. Theory Comput. 8 (2012), pp. 3257–3273. doi:10.1021/ct300400x.
   PubMed Web of Science ®Google Scholar
• CHARMM General Force Field (CGenFF); available at https://cgenff.umaryland.edu/ (Accessed on 5 Nov 2022).
   Google Scholar