Insights into interaction mechanism of inhibitors E3T, E3H and E3B with CREB binding protein by using molecular dynamics simulations and MM-GBSA calculations

References

• R. Eckner, M.E. Ewen, D. Newsome, M. Gerdes, J.A. DeCaprio, J.B. Lawrence, and D.M. Livingston, Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor, Genes Dev. 8 (1994), pp. 869–884. doi:10.1101/gad.8.8.869.
   PubMed Web of Science ®Google Scholar
• X.N. Chen and J.R. Korenberg, Localization of human CREBBP (CREB binding protein) to 16p13.3 by fluorescence in situ hybridization, Cytogenet. Cell Genet. 71 (1995), pp. 56–57. doi:10.1159/000134062.
   PubMedGoogle Scholar
• Z. Arany, W.R. Sellers, D.M. Livingston, and R. Eckner, E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators, Cell 77 (1994), pp. 799–800. doi:10.1016/0092-8674(94)90127-9.
   PubMed Web of Science ®Google Scholar
• H.M. Chan and N.B. La Thangue, p300/CBP proteins: HATs for transcriptional bridges and scaffolds, J. Cell Sci. 114 (2001), pp. 2363–2373.
   PubMed Web of Science ®Google Scholar
• C.H. Arrowsmith, C. Bountra, P.V. Fish, K. Lee, and M. Schapira, Epigenetic protein families: A new frontier for drug discovery, Nat. Rev. Drug Discov. 11 (2012), pp. 384–400. doi:10.1038/nrd3674.
   PubMed Web of Science ®Google Scholar
• P. Filippakopoulos, S. Picaud, M. Mangos, T. Keates, J.P. Lambert, D. Barsyte-Lovejoy, I. Felletar, R. Volkmer, S. Müller, T. Pawson, A.C. Gingras, C.H. Arrowsmith, and S. Knapp, Histone recognition and large-scale structural analysis of the human bromodomain family, Cell 149 (2012), pp. 214–231. doi:10.1016/j.cell.2012.02.013.
   PubMed Web of Science ®Google Scholar
• C. Dhalluin, J.E. Carlson, L. Zeng, C. He, A.K. Aggarwal, and M.M. Zhou, Structure and ligand of a histone acetyltransferase bromodomain, Nature 399 (1999), pp. 491–496. doi:10.1038/20974.
   PubMed Web of Science ®Google Scholar
• E.L. Chekler, J.A. Pellegrino, T.A. Lanz, R.A. Denny, A.C. Flick, J. Coe, J. Langille, A. Basak, S. Liu, I.A. Stock, P. Sahasrabudhe, P.D. Bonin, K. Lee, M.T. Pletcher, and L.H. Jones, Transcriptional profiling of a selective CREB binding protein bromodomain inhibitor highlights therapeutic opportunities, Chem. Biol. 22 (2015), pp. 1588–1596. doi:10.1016/j.chembiol.2015.10.013.
   PubMed Web of Science ®Google Scholar
• S. Ghosh, A. Taylor, M. Chin, H.R. Huang, A.R. Conery, J.A. Mertz, A. Salmeron, P.J. Dakle, D. Mele, A. Cote, H. Jayaram, J.W. Setser, F. Poy, G. Hatzivassiliou, D. DeAlmeida-Nagata, P. Sandy, C. Hatton, F.A. Romero, E. Chiang, T. Reimer, T. Crawford, E. Pardo, V.G. Watson, V. Tsui, A.G. Cochran, L. Zawadzke, J.C. Harmange, J.E. Audia, B.M. Bryant, R.T. Cummings, S.R. Magnuson, J.L. Grogan, S.F. Bellon, B.K. Albrecht, R.J. Sims 3rd, and J.M. Lora, Regulatory T cell modulation by CBP/EP300 bromodomain inhibition, J. Biol. Chem. 291 (2016), pp. 13014–13027. doi:10.1074/jbc.M115.708560.
   PubMed Web of Science ®Google Scholar
• D.A. Hay, O. Fedorov, S. Martin, D.C. Singleton, C. Tallant, C. Wells, S. Picaud, M. Philpott, O.P. Monteiro, C.M. Rogers, S.J. Conway, T.P. Rooney, A. Tumber, C. Yapp, P. Filippakopoulos, M.E. Bunnage, S. Müller, S. Knapp, C.J. Schofield, and P.E. Brennan, Discovery and optimization of small-molecule ligands for the CBP/p300 bromodomains, J. Am. Chem. Soc. 136 (2014), pp. 9308–9319. doi:10.1021/ja412434f.
   PubMed Web of Science ®Google Scholar
• I. Ianculescu, D.Y. Wu, K.D. Siegmund, and M.R. Stallcup, Selective roles for cAMP response element-binding protein binding protein and p300 protein as coregulators for androgen-regulated gene expression in advanced prostate cancer cells, J. Biol. Chem. 287 (2012), pp. 4000–4013. doi:10.1074/jbc.M111.300194.
   PubMed Web of Science ®Google Scholar
• F. Wang, C.B. Marshall, and M. Ikura, Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: Structural and functional versatility in target recognition, Cell. Mol. Life Sci. 70 (2013), pp. 3989–4008.
   PubMed Web of Science ®Google Scholar
• R.E. Kiernan, C. Vanhulle, L. Schiltz, E. Adam, H. Xiao, F. Maudoux, C. Calomme, A. Burny, Y. Nakatani, K.T. Jeang, M. Benkirane, and C. Van Lint, HIV-1 tat transcriptional activity is regulated by acetylation, Embo J. 18 (1999), pp. 6106–6118. doi:10.1093/emboj/18.21.6106.
   PubMed Web of Science ®Google Scholar
• R.H. Giles, D.J. Peters, and M.H. Breuning, Conjunction dysfunction: CBP/p300 in human disease, Trends Genet. 14 (1998), pp. 178–183. doi:10.1016/S0168-9525(98)01438-3.
   PubMed Web of Science ®Google Scholar
• H. Ohnishi, T. Taki, H. Yoshino, J. Takita, K. Ida, M. Ishii, K. Nishida, Y. Hayashi, M. Taniwaki, F. Bessho, and T. Watanabe, A complex t(1;22;11)(q44;q13;q23) translocation causing MLL-p300 fusion gene in therapy-related acute myeloid leukemia, Eur. J. Haematol. 81 (2008), pp. 475–480. doi:10.1111/j.1600-0609.2008.01154.x.
   PubMed Web of Science ®Google Scholar
• K. Frønsdal, N. Engedal, T. Slagsvold, and F. Saatcioglu, CREB binding protein is a coactivator for the androgen receptor and mediates cross-talk with AP-1, J. Biol. Chem. 273 (1998), pp. 31853–31859. doi:10.1074/jbc.273.48.31853.
   PubMed Web of Science ®Google Scholar
• J. Bouchal, F.R. Santer, P.P. Höschele, E. Tomastikova, H. Neuwirt, and Z. Culig, Transcriptional coactivators p300 and CBP stimulate estrogen receptor-beta signaling and regulate cellular events in prostate cancer, Prostate 71 (2011), pp. 431–437. doi:10.1002/pros.21257.
   PubMed Web of Science ®Google Scholar
• Q. Xiang, C. Wang, Y. Zhang, X. Xue, M. Song, C. Zhang, C. Li, C. Wu, K. Li, X. Hui, Y. Zhou, J.B. Smaill, A.V. Patterson, D. Wu, K. Ding, and Y. Xu, Discovery and optimization of 1-(1H-indol-1-yl)ethanone derivatives as CBP/EP300 bromodomain inhibitors for the treatment of castration-resistant prostate cancer, Eur. J. Med. Chem. 147 (2018), pp. 238–252. doi:10.1016/j.ejmech.2018.01.087.
   PubMed Web of Science ®Google Scholar
• T.D. Crawford, F.A. Romero, K.W. Lai, V. Tsui, A.M. Taylor, G. De Leon Boenig, C.L. Noland, J. Murray, J. Ly, E.F. Choo, T.L. Hunsaker, E.W. Chan, M. Merchant, S. Kharbanda, K.E. Gascoigne, S. Kaufman, M.H. Beresini, J. Liao, W. Liu, K.X. Chen, Z. Chen, A.R. Conery, A. Côté, H. Jayaram, Y. Jiang, J.R. Kiefer, T. Kleinheinz, Y. Li, J. Maher, E. Pardo, F. Poy, K.L. Spillane, F. Wang, J. Wang, X. Wei, Z. Xu, Z. Xu, I. Yen, L. Zawadzke, X. Zhu, S. Bellon, R. Cummings, A.G. Cochran, B.K. Albrecht, and S. Magnuson, Discovery of a potent and selective in vivo probe (GNE-272) for the bromodomains of CBP/EP300, J. Med. Chem. 59 (2016), pp. 10549–10563. doi:10.1021/acs.jmedchem.6b01022.
   PubMedGoogle Scholar
• S. Picaud, O. Fedorov, A. Thanasopoulou, K. Leonards, K. Jones, J. Meier, H. Olzscha, O. Monteiro, S. Martin, M. Philpott, A. Tumber, P. Filippakopoulos, C. Yapp, C. Wells, K.H. Che, A. Bannister, S. Robson, U. Kumar, N. Parr, K. Lee, D. Lugo, P. Jeffrey, S. Taylor, M.L. Vecellio, C. Bountra, P.E. Brennan, A. O’Mahony, S. Velichko, S. Müller, D. Hay, D.L. Daniels, M. Urh, N.B. La Thangue, T. Kouzarides, R. Prinjha, J. Schwaller, and S. Knapp, Generation of a selective small molecule inhibitor of the CBP/p300 bromodomain for leukemia therapy, Cancer Res. 75 (2015), pp. 5106–5119. doi:10.1158/0008-5472.CAN-15-0236.
   PubMed Web of Science ®Google Scholar
• T.A. Popp, C. Tallant, C. Rogers, O. Fedorov, P.E. Brennan, S. Müller, S. Knapp, and F. Bracher, Development of selective CBP/P300 benzoxazepine bromodomain inhibitors, J. Med. Chem. 59 (2016), pp. 8889–8912. doi:10.1021/acs.jmedchem.6b00774.
   PubMed Web of Science ®Google Scholar
• A.M. Taylor, A. Côté, M.C. Hewitt, R. Pastor, Y. Leblanc, C.G. Nasveschuk, F.A. Romero, T.D. Crawford, N. Cantone, H. Jayaram, J. Setser, J. Murray, M.H. Beresini, G. De Leon Boenig, Z. Chen, A.R. Conery, R.T. Cummings, L.A. Dakin, E.M. Flynn, O.W. Huang, S. Kaufman, P.J. Keller, J.R. Kiefer, T. Lai, Y. Li, J. Liao, W. Liu, H. Lu, E. Pardo, V. Tsui, J. Wang, Y. Wang, Z. Xu, F. Yan, D. Yu, L. Zawadzke, X. Zhu, X. Zhu, R.J. Sims 3rd, A.G. Cochran, S. Bellon, J.E. Audia, S. Magnuson, and B.K. Albrecht, Fragment-based discovery of a selective and cell-active benzodiazepinone CBP/EP300 bromodomain inhibitor (CPI-637), ACS Med. Chem. Lett. 7 (2016), pp. 531–536. doi:10.1021/acsmedchemlett.6b00075.
   PubMed Web of Science ®Google Scholar
• M. Xu, A. Unzue, J. Dong, D. Spiliotopoulos, C. Nevado, and A. Caflisch, Discovery of CREBBP bromodomain inhibitors by high-throughput docking and hit optimization guided by molecular dynamics, J. Med. Chem. 59 (2016), pp. 1340–1349. doi:10.1021/acs.jmedchem.5b00171.
   PubMed Web of Science ®Google Scholar
• M. Pervaiz, P. Mishra, and S. Günther, Bromodomain drug discovery – The past, the present, and the future, Chem. Rec. 18 (2018), pp. 1808–1817. doi:10.1002/tcr.201800074.
   PubMed Web of Science ®Google Scholar
• Y. Xiong, M. Zhang, and Y. Li, Recent advances in the development of CBP/p300 bromodomain inhibitors, Curr. Med. Chem. 27 (2020), pp. 5583–5598. doi:10.2174/0929867326666190731141055.
   Web of Science ®Google Scholar
• A. Hammitzsch, C. Tallant, O. Fedorov, A. O’Mahony, P.E. Brennan, D.A. Hay, F.O. Martinez, M.H. Al-Mossawi, J. De Wit, M. Vecellio, C. Wells, P. Wordsworth, S. Müller, S. Knapp, and P. Bowness, CBP30, a selective CBP/p300 bromodomain inhibitor, suppresses human Th17 responses, Proc. Natl. Acad. Sci. U. S. A. 112 (2015), pp. 10768–10773. doi:10.1073/pnas.1501956112.
   PubMed Web of Science ®Google Scholar
• F. Romero, J. Murray, K. Lai, V. Tsui, B. Albrecht, L. An, M. Beresini, G. Boenig, S. Bronner, E. Chan, K. Chen, Z. Chen, E. Choo, K. Clagg, K. Clark, T. Crawford, P. Cyr, D. Nagata, K. Gascoigne, and S. Magnuson, GNE-781, A highly advanced potent and selective bromodomain inhibitor of cyclic adenosine monophosphate response element binding protein, binding protein (CBP), J. Med. Chem. 60 (2017), pp. 9162–9183. doi:10.1021/acs.jmedchem.7b00796.
   PubMed Web of Science ®Google Scholar
• M. Hügle, X. Lucas, D. Ostrovskyi, P. Regenass, S. Gerhardt, O. Einsle, M. Hau, M. Jung, B. Breit, S. Günther, and D. Wohlwend, Beyond the BET family: Targeting CBP/p300 with 4-Acyl pyrroles, Angew. Chem. Int. Edit. 56 (2017), pp. 12476–12480. doi:10.1002/anie.201705516.
   PubMed Web of Science ®Google Scholar
• K.W. Lai, F.A. Romero, V. Tsui, M.H. Beresini, G. De Leon Boenig, S.M. Bronner, K. Chen, Z. Chen, E.F. Choo, T.D. Crawford, P. Cyr, S. Kaufman, Y. Li, J. Liao, W. Liu, J. Ly, J. Murray, W. Shen, J. Wai, F. Wang, C. Zhu, X. Zhu, and S. Magnuson, Design and synthesis of a biaryl series as inhibitors for the bromodomains of CBP/P300, Bioorg. Med. Chem. Lett. 28 (2018), pp. 15–23. doi:10.1016/j.bmcl.2017.11.025.
   PubMedGoogle Scholar
• M.A. Azam, S. Jupudi, N. Saha, and R.K. Paul, Combining molecular docking and molecular dynamics studies for modelling Staphylococcus aureus MurD inhibitory activity, SAR QSAR Environ. Res. 30 (2019), pp. 1–20. doi:10.1080/1062936X.2018.1539034.
   PubMed Web of Science ®Google Scholar
• P. Kamsri, A. Punkvang, S. Hannongbua, K. Suttisintong, P. Kittakoop, J. Spencer, A.J. Mulholland, and P. Pungpo, In silico study directed towards identification of the key structural features of GyrB inhibitors targeting MTB DNA gyrase: HQSAR, CoMSIA and molecular dynamics simulations, SAR QSAR Environ. Res. 30 (2019), pp. 775–800. doi:10.1080/1062936X.2019.1658218.
   PubMed Web of Science ®Google Scholar
• J. Chen, J. Wang, B. Yin, L. Pang, W. Wang, and W. Zhu, Molecular mechanism of binding selectivity of inhibitors toward BACE1 and BACE2 revealed by multiple short molecular dynamics simulations and free-energy predictions, ACS Chem. Neurosci. 10 (2019), pp. 4303–4318. doi:10.1021/acschemneuro.9b00348.
   PubMed Web of Science ®Google Scholar
• J. Devillers, Computational Design of Chemicals for the Control of Mosquitoes and Their Diseases, CRC Press, Boca Raton, FL, 2018.
   Google Scholar
• J. Wang and Y. Miao, Mechanistic insights into specific G protein interactions with adenosine receptors, J. Phys. Chem. B 123 (2019), pp. 6462–6473. doi:10.1021/acs.jpcb.9b04867.
   PubMed Web of Science ®Google Scholar
• J. Wang and Y. Miao, Peptide Gaussian accelerated molecular dynamics (Pep-GaMD): Enhanced sampling and free energy and kinetics calculations of peptide binding, J. Chem. Phys. 153 (2020), pp. 154109. doi:10.1063/5.0021399.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• J. Wang, Q. Shao, B.P. Cossins, J. Shi, K. Chen, and W. Zhu, Thermodynamics calculation of protein-ligand interactions by QM/MM polarizable charge parameters, J. Biomol. Struct. Dyn. 34 (2016), pp. 163–176. doi:10.1080/07391102.2015.1019928.
   PubMed Web of Science ®Google Scholar
• X. Jia, M. Wang, Y. Shao, G. König, B.R. Brooks, J.Z. Zhang, and Y. Mei, Calculations of solvation free energy through energy reweighting from molecular mechanics to quantum mechanics, J. Chem. Theory Comput. 12 (2016), pp. 499–511. doi:10.1021/acs.jctc.5b00920.
   PubMed Web of Science ®Google Scholar
• T. Hou, J. Wang, Y. Li, and W. Wang, Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations, J. Chem. Inf. Model. 51 (2011), pp. 69–82. doi:10.1021/ci100275a.
   Google Scholar
• J. Chen, X. Wang, T. Zhu, Q. Zhang, and J.Z. Zhang, A comparative insight into amprenavir resistance of mutations V32I, G48V, I50V, I54V, and I84V in HIV-1 protease based on thermodynamic integration and MM-PBSA methods, J. Chem. Inf. Model. 55 (2015), pp. 1903–1913. doi:10.1021/acs.jcim.5b00173.
   PubMed Web of Science ®Google Scholar
• U. Raj, H. Kumar, and P.K. Varadwaj, Molecular docking and dynamics simulation study of flavonoids as BET bromodomain inhibitors, J. Biomol. Struct. Dyn. 35 (2017), pp. 2351–2362. doi:10.1080/07391102.2016.1217276.
   PubMed Web of Science ®Google Scholar
• J. Chen, X. Wang, L. Pang, J.Z.H. Zhang, and T. Zhu, Effect of mutations on binding of ligands to guanine riboswitch probed by free energy perturbation and molecular dynamics simulations, Nucleic Acids Res. 47 (2019), pp. 6618–6631. doi:10.1093/nar/gkz499.
   PubMed Web of Science ®Google Scholar
• F. Yan, X. Liu, S. Zhang, J. Su, Q. Zhang, and J. Chen, Computational revelation of binding mechanisms of inhibitors to endocellular protein tyrosine phosphatase 1B using molecular dynamics simulations, J. Biomol. Struct. Dyn. 36 (2018), pp. 3636–3650.
   PubMed Web of Science ®Google Scholar
• S. Majumdar, S.C. Basak, C.N. Lungu, M.V. Diudea, and G.D. Grunwald, Mathematical structural descriptors and mutagenicity assessment: A study with congeneric and diverse datasets, SAR QSAR Environ. Res. 29 (2018), pp. 579–590. doi:10.1080/1062936X.2018.1496475.
   PubMed Web of Science ®Google Scholar
• J. Chen, B. Yin, W. Wang, and H. Sun, Effects of disulfide bonds on binding of inhibitors to β-amyloid cleaving enzyme 1 decoded by multiple replica accelerated molecular dynamics simulations, ACS Chem. Neurosci. 11 (2020), pp. 1811–1826. doi:10.1021/acschemneuro.0c00234.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Q. Wang, X. An, J. Xu, Y. Wang, L. Liu, E.L. Leung, and X. Yao, Classical molecular dynamics and metadynamics simulations decipher the mechanism of CBP30 selectively inhibiting CBP/p300 bromodomains, Org. Biomol. Chem. 16 (2018), pp. 6521–6530. doi:10.1039/C8OB01526K.
   PubMed Web of Science ®Google Scholar
• J. Zhu, J. Dong, L. Batiste, A. Unzue, A. Dolbois, V. Pascanu, P. Śledź, C. Nevado, and A. Caflisch, Binding Motifs in the CBP bromodomain: An analysis of 20 crystal structures of complexes with small molecules, ACS Med. Chem. Lett. 9 (2018), pp. 929–934. doi:10.1021/acsmedchemlett.8b00286.
   PubMed Web of Science ®Google Scholar
• J. Chen, W. Wang, H. Sun, L. Pang, and B. Yin, Mutation-mediated influences on binding of anaplastic lymphoma kinase to crizotinib decoded by multiple replica gaussian accelerated molecular dynamics, J. Comput. Aid. Mol. Des. 34 (2020), pp. 1289–1305. doi:10.1007/s10822-020-00355-5.
   PubMed Web of Science ®Google Scholar
• D.A. Case, T.E. Cheatham 3rd, T. Darden, H. Gohlke, R. Luo, K.M. Merz Jr., A. Onufriev, C. Simmerling, B. Wang, and R.J. Woods, The Amber biomolecular simulation programs, J. Comput. Chem. 26 (2005), pp. 1668–1688. doi:10.1002/jcc.20290.
   PubMed Web of Science ®Google Scholar
• D.C. Bas, D.M. Rogers, and J.H. Jensen, Very fast prediction and rationalization of pKa values for protein-ligand complexes, Proteins 73 (2008), pp. 765–783. doi:10.1002/prot.22102.
   PubMed Web of Science ®Google Scholar
• H. Li, A.D. Robertson, and J.H. Jensen, Very fast empirical prediction and rationalization of protein pKa values, Proteins 61 (2005), pp. 704–721. doi:10.1002/prot.20660.
   PubMed Web of Science ®Google Scholar
• A. Jakalian, D.B. Jack, and C.I. Bayly, Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation, J. Comput. Chem. 23 (2002), pp. 1623–1641. doi:10.1002/jcc.10128.
   PubMed Web of Science ®Google Scholar
• A. Jakalian, B.L. Bush, D.B. Jack, and C.I. Bayly, Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method, J. Comput. Chem. 21 (2000), pp. 132–146. doi:10.1002/(SICI)1096-987X(20000130)21:2<132::AID-JCC5>3.0.CO;2-P.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• J.A. Maier, C. Martinez, K. Kasavajhala, L. Wickstrom, K.E. Hauser, and C. Simmerling, ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB, J. Chem. Theory Comput. 11 (2015), pp. 3696–3713. doi:10.1021/acs.jctc.5b00255.
   PubMed Web of Science ®Google Scholar
• W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein, Comparison of simple potential functions for simulating liquid water, J. Chem. Phys. 79 (1983), pp. 926–935. doi:10.1063/1.445869.
   Web of Science ®Google Scholar
• R. Salomon-Ferrer, A.W. Götz, D. Poole, S. Le Grand, and R.C. Walker, Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle Mesh Ewald, J. Chem. Theory Comput 9 (2013), pp. 3878–3888. doi:10.1021/ct400314y.
   PubMed Web of Science ®Google Scholar
• T.G. Coleman, H.C. Mesick, and R.L. Darby, Numerical integration: A method for improving solution stability in models of the circulation, Ann. Biomed. Eng. 5 (1977), pp. 322–328. doi:10.1007/BF02367312.
   PubMed Web of Science ®Google Scholar
• J.A. Izaguirre, D.P. Catarello, J.M. Wozniak, and R.D. Skeel, Langevin stabilization of molecular dynamics, J. Chem. Phys. 114 (2001), pp. 2090–2098. doi:10.1063/1.1332996.
   Web of Science ®Google Scholar
• U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen, A smooth particle mesh Ewald method, J. Chem. Phys. 103 (1995), pp. 8577–8593. doi:10.1063/1.470117.
   Web of Science ®Google Scholar
• H. Sun, Y. Li, S. Tian, L. Xu, and T. Hou, Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set, Phys. Chem. Chem. Phys. 16 (2014), pp. 16719–11629. doi:10.1039/C4CP01388C.
   Web of Science ®Google Scholar
• H. Sun, Y. Li, M. Shen, S. Tian, L. Xu, P. Pan, Y. Guan, and T. Hou, Assessing the performance of MM/PBSA and MM/GBSA methods. 5. Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring, Phys. Chem. Chem. Phys. 16 (2014), pp. 22035–22045. doi:10.1039/C4CP03179B.
   PubMed Web of Science ®Google Scholar
• C. Suri and P.K. Naik, Combined molecular dynamics and continuum solvent approaches (MM-PBSA/GBSA) to predict noscapinoid binding to γ-tubulin dimer, SAR QSAR Environ. Res. 26 (2015), pp. 507–519. doi:10.1080/1062936X.2015.1070200.
   PubMed Web of Science ®Google Scholar
• S. Tian, J. Zeng, X. Liu, J. Chen, J.Z.H. Zhang, and T. Zhu, Understanding the selectivity of inhibitors toward PI4KIIIα and PI4KIIIβ based molecular modeling, Phys. Chem. Chem. Phys. 21 (2019), pp. 22103–22112. doi:10.1039/C9CP03598B.
   PubMed Web of Science ®Google Scholar
• W. Wang and P.A. Kollman, Free energy calculations on dimer stability of the HIV protease using molecular dynamics and a continuum solvent model, J. Mol. Biol. 303 (2000), pp. 567–582. doi:10.1006/jmbi.2000.4057.
   PubMed Web of Science ®Google Scholar
• J. Chen, X. Liu, S. Zhang, J. Chen, H. Sun, L. Zhang, and Q. Zhang, Molecular mechanism with regard to the binding selectivity of inhibitors toward FABP5 and FABP7 explored by multiple short molecular dynamics simulations and free energy analyses, Phys. Chem. Chem. Phys. 22 (2020), pp. 2262–2275. doi:10.1039/C9CP05704H.
   PubMed Web of Science ®Google Scholar
• Q. Wang, X. An, J. Xu, Y. Wang, L. Liu, E.L.-H. Leung, and X. Yao, Classical molecular dynamics and metadynamics simulations decipher the mechanism of CBP30 selectively inhibiting CBP/p300 bromodomains, Org. Biomol. Chem. 16 (2018), pp. 6521–6530.
   PubMed Web of Science ®Google Scholar
• Y. Wang, S. Wu, L. Wang, Z. Yang, J. Zhao, and L. Zhang, Binding selectivity of inhibitors toward the first over the second bromodomain of BRD4: Theoretical insights from free energy calculations and multiple short molecular dynamics simulations, RSC Adv. 11 (2021), pp. 745–759. doi:10.1039/D0RA09469B.
   Web of Science ®Google Scholar
• I. Massova and P.A. Kollman, Computational alanine scanning to probe protein−protein interactions:  A novel approach to evaluate binding free energies, J. Am. Chem. Soc. 121 (1999), pp. 8133–8143. doi:10.1021/ja990935j.
   Web of Science ®Google Scholar
• Y. Gao, T. Zhu, and J. Chen, Exploring drug-resistant mechanisms of I84V mutation in HIV-1 protease toward different inhibitors by thermodynamics integration and solvated interaction energy method, Chem. Phys. Lett. 706 (2018), pp. 400–408. doi:10.1016/j.cplett.2018.06.040.
   Web of Science ®Google Scholar
• T. Ichiye and M. Karplus, Collective motions in proteins: A covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations, Proteins 11 (1991), pp. 205–217. doi:10.1002/prot.340110305.
   PubMed Web of Science ®Google Scholar
• J. Chen, W. Wang, L. Pang, and W. Zhu, Unveiling conformational dynamics changes of H-Ras induced by mutations based on accelerated molecular dynamics, Phys. Chem. Chem. Phys. 22 (2020), pp. 21238–21250. doi:10.1039/D0CP03766D.
   PubMed Web of Science ®Google Scholar
• J. Zhao, H. Sun, W. Wang, L. Zhang, and J. Chen, Theoretical insights into mutation-mediated conformational changes of the GNP-bound H-RAS, Chem. Phys. Lett. 759 (2020), pp. 138042. doi:10.1016/j.cplett.2020.138042.
   Web of Science ®Google Scholar
• M. Laberge and T. Yonetani, Molecular dynamics simulations of hemoglobin A in different states and bound to DPG: Effector-linked perturbation of tertiary conformations and HbA concerted dynamics, Biophys. J. 94 (2008), pp. 2737–2751. doi:10.1529/biophysj.107.114942.
   PubMed Web of Science ®Google Scholar
• J. Su, X. Liu, S. Zhang, F. Yan, Q. Zhang, and J. Chen, A theoretical insight into selectivity of inhibitors toward two domains of bromodomain-containing protein 4 using molecular dynamics simulations, Chem. Biol. Drug Des. 91 (2018), pp. 828–840. doi:10.1111/cbdd.13148.
   PubMed Web of Science ®Google Scholar
• J. Chen, J. Wang, F. Lai, W. Wang, L. Pang, and W. Zhu, Dynamics revelation of conformational changes and binding modes of heat shock protein 90 induced by inhibitor associations, RSC Adv. 8 (2018), pp. 25456–25467. doi:10.1039/C8RA05042B.
   Web of Science ®Google Scholar
• J. Zhao, B. Yin, H. Sun, L. Pang, and J. Chen, Identifying hot spots of inhibitor-CDK2 bindings by computational alanine scanning, Chem. Phys. Lett. 747 (2020), pp. 137329.
   Web of Science ®Google Scholar
• W. Humphrey, A. Dalke, and K. Schulten, VMD: Visual molecular dynamics, J. Mol. Graph. 14 (1996), pp. 33–38. doi:10.1016/0263-7855(96)00018-5.
   PubMed Web of Science ®Google Scholar
• J. Chen, J. Wang, Q. Zhang, K. Chen, and W. Zhu, A comparative study of trypsin specificity based on QM/MM molecular dynamics simulation and QM/MM GBSA calculation, J. Biomol. Struct. Dyn. 33 (2015), pp. 2606–2618. doi:10.1080/07391102.2014.1003146.
   PubMed Web of Science ®Google Scholar
• D.S. Goodsell, G.M. Morris, and A.J. Olson, Automated docking of flexible ligands: Applications of AutoDock, J. Mol. Recognit. 9 (1996), pp. 1–5. doi:10.1002/(SICI)1099-1352(199601)9:1<1::AID-JMR241>3.0.CO;2-6.
   PubMed Web of Science ®Google Scholar