1,768
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Computational studies with flavonoids and terpenoids as BRPF1 inhibitors: in silico biological activity prediction, molecular docking, molecular dynamics simulations, MM/PBSA calculations

Pages 533-550 | Received 02 Jun 2022, Accepted 26 Jun 2022, Published online: 13 Jul 2022

References

  • R.L. Siegel, K.D. Miller, H.E. Fuchs, and A. Jemal, Cancer statistics, 2021, CA, Cancer J. Clin. 71 (2021), pp. 7–33. doi:10.3322/caac.21654.
  • J. Zhu, C. Zhou, and A. Caflisch, Structure-based discovery of selective BRPF1 bromodomain inhibitors, Eur. J. Med. Chem. 155 (2018), pp. 337–352. doi:10.1016/j.ejmech.2018.05.037.
  • S.P. Boyson, C. Gao, K. Quinn, J. Boyd, H. Paculova, S. Frietze, and K.C. Glass, Functional roles of bromodomain proteins in cancer, Cancers (Basel) 13 (2021), pp. 3606. doi:10.3390/cancers13143606.
  • S. Gokani and L.K. Bhatt, Bromodomains: A novel target for the anticancer therapy, Eur. J. Pharmacol. 911 (2021), pp. 174523. doi:10.1016/j.ejphar.2021.174523.
  • E.H. Demont, P. Bamborough, C. Chung, P.D. Craggs, D. Fallon, L.J. Gordon, P. Grandi, C.I. Hobbs, J. Hussain, E.J. Jones, A. Le Gall, A.-M. Michon, D.J. Mitchell, R.K. Prinjha, A.D. Roberts, R.J. Sheppard, and R.J. Watson, 1,3-Dimethyl benzimidazolones are potent, selective inhibitors of the BRPF1 bromodomain, ACS Med. Chem. Lett. 5 (2014), pp. 1190–1195. doi:10.1021/ml5002932.
  • C.L.H. Cheng, F.H.C. Tsang, L. Wei, M. Chen, D.W.C. Chin, J. Shen, C.T. Law, D. Lee, C.C.L. Wong, I.O.L. Ng, and C.M. Wong, Bromodomain-containing protein BRPF1 is a therapeutic target for liver cancer, Commun. Biol. 4 (2021), pp. 1–14. doi:10.1038/s42003-021-02405-6.
  • J. Cheung, E.N. Gary, K. Shiomi, and T.L. Rosenberry, Structures of human acetylcholinesterase bound to dihydrotanshinone I and territrem B show peripheral site flexibility, ACS Med. Chem. Lett. 4 (2013), pp. 1091–1096. doi:10.1021/ml400304w.
  • S.R. Lin, C.H. Chang, C.F. Hsu, M.J. Tsai, H. Cheng, M.K. Leong, P.J. Sung, J.C. Chen, and C.F. Weng, Natural compounds as potential adjuvants to cancer therapy: Preclinical evidence, Br. J. Pharmacol. 177 (2020), pp. 1409–1423. doi:10.1111/bph.14816.
  • X. Montané, O. Kowalczyk, B. Reig-Vano, A. Bajek, K. Roszkowski, R. Tomczyk, W. Pawliszak, M. Giamberini, A. Mocek-Płóciniak, and B. Tylkowski, Current perspectives of the applications of polyphenols and flavonoids in cancer therapy, Molecules. 25 (2020), pp. 3342. doi:10.3390/molecules25153342.
  • B.M.F. Gonçalves, D.S.P. Cardoso, and M.J.U. Ferreira, Overcoming multidrug resistance: Flavonoid and terpenoid nitrogen-containing derivatives as ABC transporter modulators, Molecules. 25 (2020), pp. 3364. doi:10.3390/molecules25153364.
  • F. Fontana, M. Raimondi, M. Marzagalli, A. Di Domizio, and P. Limonta, Natural compounds in prostate cancer prevention and treatment: Mechanisms of action and molecular targets, Cells. 9 (2020), pp. 460. doi:10.3390/cells9020460.
  • E.R. Sauter, Cancer prevention and treatment using combination therapy with natural compounds, Expert Rev. Clin. Pharmacol. 13 (2020), pp. 265–285. doi:10.1080/17512433.2020.1738218.
  • W.K. Yu, Z.Y. Xu, L. Yuan, S. Mo, B. Xu, X.D. Cheng, and J.J. Qin, Targeting β-catenin signaling by natural products for cancer prevention and therapy, Front. Pharmacol. 11 (2020), pp. 1–12. doi:10.3389/fphar.2020.00984.
  • D. Jones, G.O. Ormondroyd, S.F. Curling, C.-M. Popescu, and M.-C. Popescu. 2 - Chemical Compositions of Natural Fibres, M. Fan and F. Fu, eds., Woodhead Publishing, Sawston, United Kingdom, 2017, pp. 23–58.
  • R. Li, S.L. Morris-Natschke, and K.-H. Lee, Clerodane diterpenes: Sources, structures, and biological activities, Nat. Prod. Rep. 33 (2016), pp. 1166–1226. doi:10.1039/c5np00137d.
  • A.N. Panche, A.D. Diwan, and S.R. Chandra, Flavonoids: An overview, J. Nutr. Sci. 5 (2016), pp. e47. doi:10.1017/jns.2016.41.
  • D. Luo, J.B. Tong, X.C. Xiao, S. Bian, X. Zhang, J. Wang, and H.Y. Xu, Theoretically exploring selective-binding mechanisms of BRD4 through integrative computational approaches, SAR QSAR Environ. Res. 32 (2021), pp. 985–1011. doi:10.1080/1062936X.2021.1999317.
  • S.L. Wu, J. Zhao, H.B. Sun, H.Y. Li, Y.Y. Yin, and L.L. Zhang, Insights into interaction mechanism of inhibitors E3T, E3H and E3B with CREB binding protein by using molecular dynamics simulations and MM-GBSA calculations, SAR QSAR Environ. Res. 32 (2021), pp. 221–246. doi:10.1080/1062936X.2021.1887351.
  • S.L. Wu, L.F. Wang, H.B. Sun, W. Wang, and Y.X. Yu, Probing molecular mechanism of inhibitor bindings to bromodomain-containing protein 4 based on molecular dynamics simulations and principal component analysis, SAR QSAR Environ. Res. 31 (2020), pp. 547–570. doi:10.1080/1062936X.2020.1777584.
  • L.F. Wang, Y. Wang, Z.Y. Yang, J. Zhao, H.B. Sun, and S.L. Wu, Revealing binding selectivity of inhibitors toward bromodomain-containing proteins 2 and 4 using multiple short molecular dynamics simulations and free energy analyses, SAR QSAR Environ. Res. 31 (2020), pp. 373–398. doi:10.1080/1062936X.2020.1748107.
  • Y. Wang, L.F. Wang, L.L. Zhang, H.B. Sun, and J. Zhao, Molecular mechanism of inhibitor bindings to bromodomain-containing protein 9 explored based on molecular dynamics simulations and calculations of binding free energies, SAR QSAR Environ. Res. 31 (2020), pp. 149–170. doi:10.1080/1062936X.2019.1701075.
  • Y.H. Kim, M. Kim, M. Yoo, J.E. Kim, H.K. Lee, J.N. Heo, C.O. Lee, M. Yoo, K.Y. Jung, C.S. Yun, S.W. Moon, H.K. Chang, C.W. Chung, S. Pyo, S.U. Choi, and C.H. Park, A natural compound, aristoyagonine, is identified as a potent bromodomain inhibitor by mid-throughput screening, Biochem. Biophys. Res. Commun. 503 (2018), pp. 882–887. doi:10.1016/j.bbrc.2018.06.091.
  • F.D. Prieto-Martinez and J.L. Medina-Franco, Charting the bromodomain BRD4: Towards the identification of novel inhibitors with molecular similarity and receptor mapping, Lett. Drug Des. Discov. 15 (2018), pp. 1002–1011. doi:10.2174/1570180814666171121145731.
  • J. Li, W. Zou, K. Yu, B. Liu, W. Liang, L. Wang, Y. Lu, Z. Jiang, A. Wang, and J. Zhu, Discovery of the natural product 3’,4’,7,8-tetrahydroxyflavone as a novel and potent selective BRD4 bromodomain 2 inhibitor, J. Enzyme Inhib. Med. Chem. 36 (2021), pp. 903–913. doi:10.1080/14756366.2021.1906663.
  • I.A. Ramallo, V.L. Alonso, F. Rua, E. Serra, and R.L.E. Furlan, A bioactive Trypanosoma cruzi bromodomain inhibitor from chemically engineered extracts, ACS Comb. Sci. 20 (2018), pp. 220–228. doi:10.1021/acscombsci.7b00172.
  • D.A. Filimonov, A.A. Lagunin, T.A. Gloriozova, A.V. Rudik, D.S. Druzhilovskii, P.V. Pogodin, and V.V. Poroikov, Prediction of the biological activity spectra of organic compounds using the pass online web resource, Chem. Heterocycl. Compd. 50 (2014), pp. 444–457. doi:10.1007/s10593-014-1496-1.
  • S. Kim, P.A. Thiessen, E.E. Bolton, J. Chen, G. Fu, A. Gindulyte, L. Han, J. He, S. He, B.A. Shoemaker, J. Wang, B. Yu, J. Zhang, and S.H. Bryant, PubChem substance and compound databases, Nucl. Acids Res. 44 (2016), pp. D1202–D1213. doi:10.1093/nar/gkv951.
  • Discovery studio visualizer. Dassault Systèmes, San Diego, USA, 2019; software available at https://www.3dsbiovia.com/products/collaborative-science/biovia-discovery-studio/visualization-download.php.
  • O. Trott and A. Olson, AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading, J. Comput. Chem. 31 (2010), pp. 455–461. doi:10.1002/jcc.21334.
  • T. Gaillard, Evaluation of AutoDock and AutoDock Vina on the CASF-2013 benchmark, J. Chem. Inf. Model. 58 (2018), pp. 1697–1706. doi:10.1021/acs.jcim.8b00312.
  • S.K. Burley, C. Bhikadiya, C. Bi, S. Bittrich, L. Chen, G.V. Crichlow, C.H. Christie, K. Dalenberg, L. Di Costanzo, J.M. Duarte, S. Dutta, Z. Feng, S. Ganesan, D.S. Goodsell, S. Ghosh, R.K. Green, V. Guranović, D. Guzenko, B.P. Hudson, C.L. Lawson, Y. Liang, R. Lowe, H. Namkoong, E. Peisach, I. Persikova, C. Randle, A. Rose, Y. Rose, A. Sali, J. Segura, M. Sekharan, C. Shao, Y.-P. Tao, M. Voigt, J.D. Westbrook, J.Y. Young, C. Zardecki, and M. Zhuravleva, RCSB protein data bank: Powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences, Nucl. Acids Res. 49 (2021), pp. D437–D451. doi:10.1093/nar/gkaa1038.
  • M.Y. Lubula, B.E. Eckenroth, S. Carlson, A. Poplawski, M. Chruszcz, and K.C. Glass, Structural insights into recognition of acetylated histone ligands by the BRPF1 bromodomain, FEBS Lett. 588 (2014), pp. 3844–3854. doi:10.1016/j.febslet.2014.09.028.
  • G.M. Morris, H. Ruth, W. Lindstrom, M.F. Sanner, R.K. Belew, D.S. Goodsell, and A.J. Olson, AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility, J. Comput. Chem. 30 (2009), pp. 2785–2791. doi:10.1002/jcc.21256.
  • E. Bautista, R.A. Toscano, and A. Ortega, 5,10- seco - neo -clerodanes and neo -clerodanes from Salvia microphylla, J. Nat. Prod. 77 (2014), pp. 1088–1092. doi:10.1021/np4009893.
  • S.Y. Ng, T. Kamada, M. Suleiman, and C.S. Vairappan, A new seco-clerodane-type diterpenoid from Bornean liverwort Schistochila acuminata, Nat. Prod. Commun. 11 (2016), pp. 1071–1072.
  • A. Moulishankar and K. Lakshmanan, Data on molecular docking of naturally occurring flavonoids with biologically important targets, Data Br. 29 (2020), pp. 105243. doi:10.1016/j.dib.2020.105243.
  • J. Rivera-Chávez, C. Bustos-Brito, E. Aguilar-Ramírez, D. Martínez-Otero, L.D. Rosales-Vázquez, A. Dorazco-González, and P. Cano-Sánchez, Hydroxy- neo-clerodanes and 5,10-seco-neo-clerodanes from Salvia decora, J. Nat. Prod. 83 (2020), pp. 2212–2220. doi:10.1021/acs.jnatprod.0c00313.
  • S. Shaker, J. Sang, X.L. Yan, R.Z. Fan, G.H. Tang, Y.K. Xu, and S. Yin, Diterpenoids from Euphorbia royleana reverse P-glycoprotein-mediated multidrug resistance in cancer cells, Phytochemistry. 176 (2020), pp. 112395. doi:10.1016/j.phytochem.2020.112395.
  • F. Aydoğan, E.H. Anouar, M. Aygün, H. Yusufoglu, C. Karaalp, and E. Bedir, An unprecedented diterpene with three new neoclerodanes from Teucrium sandrasicum O. Schwarz, J. Mol. Struct. 1231 (2021), pp. 1–12.
  • C. Bustos-Brito, D. Pérez-Juanchi, J. Rivera-Chávez, A.D. Hernández-Herrera, B.Y. Bedolla-García, S. Zamudio, T. Ramírez-Apan, L. Quijano, and B. Esquivel, Clerodane and 5 10-seco-clerodane-type diterpenoids from Salvia involucrata, J. Mol. Struct. 1237 (2021), pp. 130367. doi:10.1016/j.molstruc.2021.130367.
  • ACD/ChemSketch, Advanced Chemistry Development Inc., Toronto, Canada, 2001; software available at www.acdlabs.com
  • D.A. Case, H.M. Aktulga, K. Belfon, I.Y. Ben-Shalom, S.R. Brozell, D.S. Cerutti, T.E. Cheatham, V.W.D. Cruzeiro, T.A. Darden, R.E. Duke, G. Giambasu, M.K. Gilson, H. Gohlke, A.W. Goetz, R. Harris, S. Izadi, S.A. Izmailov, C. Jin, K. Kasavajhala, and P.A. Kollman, Amber 2021, 2021; software available at https://ambermd.org/AmberMD.php
  • J. Wang, R.M. Wolf, J.W. Caldwell, P.A. Kollman, and D.A. Case, Development and testing of a general amber force field, J. Comput. Chem. 25 (2004), pp. 1157–1174. doi:10.1002/jcc.20035.
  • D.R. Roe and T.E. Cheatham, PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data, J. Chem. Theory Comput. 9 (2013), pp. 3084–3095. doi:10.1021/ct400341p.
  • S. Genheden and U. Ryde, The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities, Expert Opin. Drug Discov. 10 (2015), pp. 449–461. doi:10.1517/17460441.2015.1032936.
  • S.S. Timur, G. Yalçın, Ö. Çevik, C. Andaç, and R.N. Gürsoy, Molecular dynamics, thermodynamic, and mutational binding studies for tumor-specific LyP-1 in complex with p32, J. Biomol. Struct. Dyn. 1102 (2017), pp. 1–11.
  • S. Burmaoglu, E.A. Kazancioglu, M.Z. Kazancioglu, R. Sağlamtaş, G. Yalcin, I. Gulcin, and O. Algul, Synthesis, molecular docking and some metabolic enzyme inhibition properties of biphenyl-substituted chalcone derivatives, J. Mol. Struct. 1254 (2022), pp. 132358. doi:10.1016/j.molstruc.2022.132358.
  • A.S.A. Manap, A.C.W. Tan, W.H. Leong, A.Y.Y. Chia, S. Vijayabalan, A. Arya, E.H. Wong, F. Rizwan, U. Bindal, S. Koshy, and P. Madhavan, Synergistic effects of curcumin and piperine as potent acetylcholine and amyloidogenic inhibitors with significant neuroprotective activity in sh-sy5y cells via computational molecular modeling and in vitro assay, Front. Aging Neurosci. 10 (2019), pp. 1–17.
  • M.C. Lee, R. Yang, and Y. Duan, Comparison between generalized-Born and Poisson-Boltzmann methods in physics-based scoring functions for protein structure prediction, J. Mol. Model. 12 (2005), pp. 101–110. doi:10.1007/s00894-005-0013-y.
  • G. Poli, G. Carlotta, F. Rizzolio, and T. Tuccinardi, Application of MM-PBSA methods in virtual screening, Molecules. 25 (2020), pp. 459–494. doi:10.3390/molecules25081971.
  • Y.C. Huang, P.C. Lee, J.J. Wang, and Y.C. Hsu, Anticancer effect and mechanism of hydroxygenkwanin in oral squamous cell carcinoma, Front. Oncol. 9 (2019), pp. 1–10.
  • V. Singamaneni, B. Lone, J. Singh, P. Kumar, S. Gairola, S. Singh, and P. Gupta, Coronarin K and L: Two novel labdane diterpenes from Roscoea purpurea: An ayurvedic crude drug, Front. Chem. 9 (2021), pp. 1–7.
  • Y. Xia, R. Chen, G. Lu, C. Li, S. Lian, T.W. Kang, and Y. Do Jung, Natural phytochemicals in bladder cancer prevention and therapy, Front. Oncol. 11 (2021), pp. 1–22. doi:10.3389/fonc.2021.652033.
  • S.S. Çınaroǧlu and E. Timuçin, Comprehensive evaluation of the MM-GBSA method on bromodomain-inhibitor sets, Brief. Bioinform. 21 (2020), pp. 2112–2125. doi:10.1093/bib/bbz143.
  • W.S. Palmer, Development of small molecule inhibitors of BRPF1 and TRIM24 bromodomains, Drug Discov. Today Technol. 19 (2016), pp. 65–71. doi:10.1016/j.ddtec.2016.06.005.