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Meng Li, Xinguo Liu, Shaolong Zhang, Jiahao Sun, Qinggang Zhang, Jianzhong Chen. Selective Mechanism of Inhibitors to Two Bromodomains of BRD4 Revealed by Multiple Replica Molecular Dynamics Simulations and Free Energy Analyses[J]. Chinese Journal of Chemical Physics . doi: 10.1063/1674-0068/cjcp2208126
Citation: Meng Li, Xinguo Liu, Shaolong Zhang, Jiahao Sun, Qinggang Zhang, Jianzhong Chen. Selective Mechanism of Inhibitors to Two Bromodomains of BRD4 Revealed by Multiple Replica Molecular Dynamics Simulations and Free Energy Analyses[J]. Chinese Journal of Chemical Physics . doi: 10.1063/1674-0068/cjcp2208126

Selective Mechanism of Inhibitors to Two Bromodomains of BRD4 Revealed by Multiple Replica Molecular Dynamics Simulations and Free Energy Analyses

doi: 10.1063/1674-0068/cjcp2208126
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  • Bromodomain-containing protein 4 (BRD4) is critical in cell cycle regulation and has emerged as a potential target for treatment of various cancers. BRD4 contains two bromodomains, namely BD1 and BD2. Research suggests that selectively inhibiting BD1 or BD2 may provide more effective treatment options. Therefore, understanding the selective mechanism of inhibitor binding to BD1 and BD2 is essential for development of high selective inhibitors to BD1 and BD2. Multiple replica molecular dynamics (MRMD) simulations are utilized to investigate the binding selectivity of inhibitors SG3-179, GSK778, and GSK620 for BD1 and BD2. The results show that BD1 has stronger structural flexibility than BD2, moreover BD1 and BD2 exhibit different internal dynamics. The analyses of free energy landscapes reveal significant differences in the conformational distribution of BD1 and BD2. Binding free energy predictions suggest that entropy changes, electrostatic interactions, and van der Waals interactions are key factors in the selective binding of BD1 and BD2 by SG3-179, GSK778, and GSK620. The calculations of the energy contributions of individual residues demonstrate that residues (W81, W374), (P82, P375), (Q85, K378), (V87, V380), (L92, L385), (N93, G386), (L94, L387), (C136, C429), (N140, N433), (K141, P434), (D144, H437) and (I146, V439) corresponding to (BD1, BD2) generate significant energy difference in binding of SG3-179, GSK778, and GSK620 to BD1 and BD2, and they can serve as effective targets for development of high selective inhibitors against BD1 or BD2. The related information may provide significant theoretical guidance for improving the selectivity of inhibitors for BD1 and BD2.

     

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  • [1]
    A. C. Belkina and G. V. Denis, Nat. Rev. Cancer 12, 465 (2012). doi: 10.1038/nrc3256
    [2]
    P. Filippakopoulos and S. Knapp, FEBS Lett. 586, 2692 (2012). doi: 10.1016/j.febslet.2012.04.045
    [3]
    Z. Yang, J. H. N. Yik, R. Chen, N. He, M. K. Jang, K. Ozato, and Q. Zhou, Mol. Cell 19, 535 (2005). doi: 10.1016/j.molcel.2005.06.029
    [4]
    T. Fujisawa and P. Filippakopoulos, Nat. Rev. Mol. Cell Bio. 18, 246 (2017). doi: 10.1038/nrm.2016.143
    [5]
    E. Ferri, C. Petosa, and C. E. McKenna, Biochem. Pharmacol. 106, 1 (2016). doi: 10.1016/j.bcp.2015.12.005
    [6]
    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, Cell 149, 214 (2012). doi: 10.1016/j.cell.2012.02.013
    [7]
    S. Y. Wu and C. M. Chiang, J. Biol. Chem. 282, 13141 (2007). doi: 10.1074/jbc.R700001200
    [8]
    X. Tang, R. Peng, J. E. Phillips, J. Deguzman, Y. Ren, S. Apparsundaram, Q. Luo, C. M. Bauer, M. E. Fuentes, J. A. DeMartino, G. Tyagi, R. Garrido, C. M. Hogaboam, C. P. Denton, A. M. Holmes, C. Kitson, C. S. Stevenson, and D. C. Budd, Am. J. Pathol. 183, 470 (2013). doi: 10.1016/j.ajpath.2013.04.020
    [9]
    O. Goundiam, P. Gestraud, T. Popova, T. De la Motte Rouge, V. Fourchotte, D. Gentien, P. Hupé, V. Becette, C. Houdayer, S. Roman-Roman, M. H. Stern, and X. Sastre-Garau, Int. J. Cancer 137, 1890 (2015). doi: 10.1002/ijc.29568
    [10]
    X. Mu, L. Bai, Y. Xu, J. Wang, and H. Lu, Biochem. Bioph. Res. Co. 521, 833 (2020). doi: 10.1016/j.bbrc.2019.11.007
    [11]
    C. A. French, C. L. Ramirez, J. Kolmakova, T. T. Hickman, M. J. Cameron, M. E. Thyne, J. L. Kutok, J. A. Toretsky, A. K. Tadavarthy, U. R. Kees, J. A. Fletcher, and J. C. Aster, Oncogene 27, 2237 (2008). doi: 10.1038/sj.onc.1210852
    [12]
    S. Mujtaba, L. Zeng, and M. M. Zhou, Oncogene 26, 5521 (2007). doi: 10.1038/sj.onc.1210618
    [13]
    S. G. Smith and M. M. Zhou, ACS Chem. Biol. 11, 598 (2016). doi: 10.1021/acschembio.5b00831
    [14]
    Y. Duan, Y. Guan, W. Qin, X. Zhai, B. Yu, and H. Liu, MedChemComm 9, 1779 (2018). doi: 10.1039/C8MD00198G
    [15]
    P. Filippakopoulos, J. Qi, S. Picaud, Y. Shen, W. B. Smith, O. Fedorov, E. M. Morse, T. Keates, T. T. Hickman, I. Felletar, M. Philpott, S. Munro, M. R. McKeown, Y. Wang, A. L. Christie, N. West, M. J. Cameron, B. Schwartz, T. D. Heightman, N. La Thangue, C. A. French, O. Wiest, A. L. Kung, S. Knapp, and J. E. Bradner, Nature 468, 1067 (2010). doi: 10.1038/nature09504
    [16]
    C. Berthon, E. Raffoux, X. Thomas, N. Vey, C. Gomez Roca, K. Yee, D. C. Taussig, K. Rezai, C. Roumier, P. Herait, C. Kahatt, B. Quesnel, M. Michallet, C. Recher, F. Lokiec, C. Preudhomme, and H. Dombret, Lancet Haematol. 3, e186 (2016). doi: 10.1016/S2352-3026(15)00247-1
    [17]
    O. Mirguet, R. Gosmini, J. Toum, C. A. Clément, M. Barnathan, J. M. Brusq, J. E. Mordaunt, R. M. Grimes, M. Crowe, O. Pineau, M. Ajakane, A. Daugan, P. Jeffrey, L. Cutler, A. C. Haynes, N. N. Smithers, C. w. Chung, P. Bamborough, I. J. Uings, A. Lewis, J. Witherington, N. Parr, R. K. Prinjha, and E. Nicodème, J. Med. Chem. 56, 7501 (2013). doi: 10.1021/jm401088k
    [18]
    T. Lu, W. Lu, and C. Luo, Expert Opin. Ther. Pat. 30, 57 (2020). doi: 10.1080/13543776.2020.1702645
    [19]
    G. Andrieu, A. C. Belkina, and G. V. Denis, Drug Discov. Today Technol. 19, 45 (2016). doi: 10.1016/j.ddtec.2016.06.004
    [20]
    D. B. Doroshow, J. P. Eder, and P. M. LoRusso, Ann. Oncol. 28, 1776 (2017). doi: 10.1093/annonc/mdx157
    [21]
    S. Picaud, C. Wells, I. Felletar, D. Brotherton, S. Martin, P. Savitsky, B. Diez Dacal, M. Philpott, C. Bountra, H. Lingard, O. Fedorov, S. Müller, E. Brennan Paul, S. Knapp, and P. Filippakopoulos, Proc. Natl. Acad. Sci. USA 110, 19754 (2013). doi: 10.1073/pnas.1310658110
    [22]
    J. Liu, Z. Duan, W. Guo, L. Zeng, Y. Wu, Y. Chen, F. Tai, Y. Wang, Y. Lin, Q. Zhang, Y. He, J. Deng, R. L. Stewart, C. Wang, P. C. Lin, S. Ghaffari, B. M. Evers, S. Liu, M. M. Zhou, B. P. Zhou, and J. Shi, Nat. Commun. 9, 5200 (2018). doi: 10.1038/s41467-018-07258-y
    [23]
    L. T. Wang, S. N. Wang, S. S. Chiou, K. Y. Liu, C. Y. Chai, C. M. Chiang, S. K. Huang, K. K. Yokoyama, and S. H. Hsu, Oncogene 38, 518 (2019). doi: 10.1038/s41388-018-0457-z
    [24]
    C. M. Chiang, Chem. Biol. 21, 804 (2014). doi: 10.1016/j.chembiol.2014.07.003
    [25]
    M. Gacias, G. Gerona Navarro, Alexander N. Plotnikov, G. Zhang, L. Zeng, J. Kaur, G. Moy, E. Rusinova, Y. Rodriguez, B. Matikainen, A. Vincek, J. Joshua, P. Casaccia, and M. M. Zhou, Chem. Biol. 21, 841 (2014). doi: 10.1016/j.chembiol.2014.05.009
    [26]
    C. Galdeano and A. Ciulli, Future Med. Chem. 8, 1655 (2016). doi: 10.4155/fmc-2016-0059
    [27]
    Y. Liu, X. Wang, J. Zhang, H. Huang, B. Ding, J. Wu, and Y. Shi, Biochemistry 47, 6403 (2008). doi: 10.1021/bi8001659
    [28]
    O. Gilan, I. Rioja, K. Knezevic, J. Bell Matthew, M. Yeung Miriam, R. Harker Nicola, Y. N. Lam Enid, C. Chung, P. Bamborough, M. Petretich, M. Urh, J. Atkinson Stephen, K. Bassil Anna, J. Roberts Emma, D. Vassiliadis, L. Burr Marian, G. S. Preston Alex, C. Wellaway, T. Werner, R. Gray James, A. M. Michon, T. Gobbetti, V. Kumar, E. Soden Peter, A. Haynes, J. Vappiani, F. Tough David, S. Taylor, S. J. Dawson, M. Bantscheff, M. Lindon, G. Drewes, H. Demont Emmanuel, L. Daniels Danette, P. Grandi, K. Prinjha Rab, and A. Dawson Mark, Science 368, 387 (2020). doi: 10.1126/science.aaz8455
    [29]
    E. J. Faivre, K. F. McDaniel, D. H. Albert, S. R. Mantena, J. P. Plotnik, D. Wilcox, L. Zhang, M. H. Bui, G. S. Sheppard, L. Wang, V. Sehgal, X. Lin, X. Huang, X. Lu, T. Uziel, P. Hessler, L. T. Lam, R. J. Bellin, G. Mehta, S. Fidanze, J. K. Pratt, D. Liu, L. A. Hasvold, C. Sun, S. C. Panchal, J. J. Nicolette, S. L. Fossey, C. H. Park, K. Longenecker, L. Bigelow, M. Torrent, S. H. Rosenberg, W. M. Kati, and Y. Shen, Nature 578, 306 (2020). doi: 10.1038/s41586-020-1930-8
    [30]
    G. S. Sheppard, L. Wang, S. D. Fidanze, L. A. Hasvold, D. Liu, J. K. Pratt, C. H. Park, K. Longenecker, W. Qiu, M. Torrent, P. J. Kovar, M. Bui, E. Faivre, X. Huang, X. Lin, D. Wilcox, L. Zhang, Y. Shen, D. H. Albert, T. J. Magoc, G. Rajaraman, W. M. Kati, and K. F. McDaniel, J. Med. Chem. 63, 5585 (2020). doi: 10.1021/acs.jmedchem.0c00628
    [31]
    M. Yang, X. Zhang, and K. Han, Proteins 78, 2222 (2010). doi: 10.1002/prot.22734
    [32]
    S. Lu, W. Huang, Q. Wang, Q. Shen, S. Li, R. Nussinov, and J. Zhang, Biophys. J. 108, 528a (2015). doi: 10.1016/j.bpj.2014.11.2894
    [33]
    M. J. Yang, X. Q. Pang, X. Zhang, and K. L. Han, J. Struct. Biol. 173, 57 (2011). doi: 10.1016/j.jsb.2010.07.013
    [34]
    G. Li, H. Shen, D. Zhang, Y. Li, and H. Wang, J. Chem. Theory Comput. 12, 676 (2016). doi: 10.1021/acs.jctc.5b00903
    [35]
    G. Hu, A. Ma, X. Dou, L. Zhao, and J. Wang, Int. J. Mol. Sci. 17, 819 (2016). doi: 10.3390/ijms17060819
    [36]
    J. Su, X. Liu, S. Zhang, F. Yan, Q. Zhang, and J. Chen, J. Biomol. Struct. Dyn. 36, 1212 (2018). doi: 10.1080/07391102.2017.1317666
    [37]
    J. Chen, X. Wang, L. Pang, J. Z. H. Zhang, and T. Zhu, Nucleic Acids Res. 47, 6618 (2019). doi: 10.1093/nar/gkz499
    [38]
    Q. Wang, Y. Li, J. Xu, Y. Wang, D. Shi, L. Liu, E. L. H. Leung, and X. Yao, Proteins 87, 3 (2019). doi: 10.1002/prot.25611
    [39]
    R. Tumdam, A. Kumar, N. Subbarao, and B. S. Balaji, SAR QSAR Environ. Res. 29, 975 (2018). doi: 10.1080/1062936X.2018.1537301
    [40]
    S. Chen, Y. He, Y. Geng, Z. Wang, L. Han, and W. Han, Molecules 27, 118 (2022).
    [41]
    T. Fu, G. Zheng, G. Tu, F. Yang, Y. Chen, X. Yao, X. Li, W. Xue, and F. Zhu, ACS Chem. Neurosci. 9, 1492 (2018). doi: 10.1021/acschemneuro.8b00059
    [42]
    J. Wang and Y. Miao, J. Phys. Chem. B 123, 6462 (2019). doi: 10.1021/acs.jpcb.9b04867
    [43]
    J. Wang, P. R. Arantes, A. Bhattarai, R. V. Hsu, S. Pawnikar, Y.-m. M. Huang, G. Palermo, and Y. Miao, Wires Comput. Mol. Scimol. Sci 11, e1521 (2021). doi: 10.1002/wcms.1521
    [44]
    Z. Sun, Z. Gong, F. Xia, and X. He, Chem. Phys. 548, 111245 (2021). doi: 10.1016/j.chemphys.2021.111245
    [45]
    W. Xue, P. Wang, G. Tu, F. Yang, G. Zheng, X. Li, X. Li, Y. Chen, X. Yao, and F. Zhu, Phys. Chem. Chem. Phys. 20, 6606 (2018). doi: 10.1039/C7CP07869B
    [46]
    L. Wang, Y. Wang, H. Sun, J. Zhao, and Q. Wang, Chem. Phys. Lett. 736, 136785 (2019). doi: 10.1016/j.cplett.2019.136785
    [47]
    G. Hu, A. Ma, and J. Wang, J. Chem. Inf. Model. 57, 918 (2017). doi: 10.1021/acs.jcim.7b00139
    [48]
    L. Duan, X. Liu, and J. Z. H. Zhang, J. Am. Chem. Soc. 138, 5722 (2016). doi: 10.1021/jacs.6b02682
    [49]
    X. Jia, M. Wang, Y. Shao, G. König, B. R. Brooks, J. Z. H. Zhang, and Y. Mei, J. Chem. Theory Comput. 12, 499 (2016). doi: 10.1021/acs.jctc.5b00920
    [50]
    M. Aldeghi, A. Heifetz, M. J. Bodkin, S. Knapp, and P. C. Biggin, Chem. Sci. 7, 207 (2016). doi: 10.1039/C5SC02678D
    [51]
    Y. Gao, T. Zhu, and J. Chen, Chem. Phys. Lett. 706, 400 (2018). doi: 10.1016/j.cplett.2018.06.040
    [52]
    L. F. Wang, Y. Wang, Z. Y. Yang, J. Zhao, H. B. Sun, and S. L. Wu, SAR QSAR Environ. Res. 31, 373 (2020). doi: 10.1080/1062936X.2020.1748107
    [53]
    W. Wang and A. Kollman Peter, Proc. Natl. Acad. Sci. USA 98, 14937 (2001). doi: 10.1073/pnas.251265598
    [54]
    T. Hou, J. Wang, Y. Li, and W. Wang, J. Comput. Chem. 32, 866 (2011). doi: 10.1002/jcc.21666
    [55]
    Z. Sun, Z. Huai, Q. He, and Z. Liu, J. Chem. Inf. Model. 61, 6107 (2021). doi: 10.1021/acs.jcim.1c01208
    [56]
    W. Xue, F. Yang, P. Wang, G. Zheng, Y. Chen, X. Yao, and F. Zhu, ACS Chem. Neurosci. 9, 1128 (2018). doi: 10.1021/acschemneuro.7b00490
    [57]
    T. Hou and R. Yu, J. Med. Chem. 50, 1177 (2007). doi: 10.1021/jm0609162
    [58]
    J. Su, X. Liu, S. Zhang, F. Yan, Q. Zhang, and J. Chen, Chem. Biol. Drug Des. 93, 163 (2019). doi: 10.1111/cbdd.13398
    [59]
    D. Shi, Q. Bai, S. Zhou, X. Liu, H. Liu, and X. Yao, Proteins 86, 43 (2018). doi: 10.1002/prot.25401
    [60]
    M. Aldeghi, A. Heifetz, M. J. Bodkin, S. Knapp, and P. C. Biggin, J. Am. Chem. Soc. 139, 946 (2017). doi: 10.1021/jacs.6b11467
    [61]
    M. Shi, J. He, T. Weng, N. Shi, W. Qi, Y. Guo, T. Chen, L. Chen, and D. Xu, Phys. Chem. Chem. Phys. 24, 5125 (2022). doi: 10.1039/D1CP05490B
    [62]
    Q. Wang, Y. Li, J. Xu, Y. Wang, E. L. H. Leung, L. Liu, and X. Yao, Sci. Rep. 7, 8857 (2017). doi: 10.1038/s41598-017-08909-8
    [63]
    J. Chen, X. Liu, S. Zhang, J. Chen, H. Sun, L. Zhang, and Q. Zhang, Phys. Chem. Chem. Phys. 22, 2262 (2020). doi: 10.1039/C9CP05704H
    [64]
    P. Auffinger and E. Westhof, J. Mol. Biol. 269, 326 (1997). doi: 10.1006/jmbi.1997.1022
    [65]
    L. S. D. Caves, J. D. Evanseck, and M. Karplus, Protein Sci. 7, 649 (1998). doi: 10.1002/pro.5560070314
    [66]
    B. Knapp, L. Ospina, and C. M. Deane, J. Chem. Theory Comput. 14, 6127 (2018). doi: 10.1021/acs.jctc.8b00391
    [67]
    J. Chen, J. Wang, B. Yin, L. Pang, W. Wang, and W. Zhu, ACS Chem. Neurosci. 10, 4303 (2019). doi: 10.1021/acschemneuro.9b00348
    [68]
    Y. Wang, S. Wu, L. Wang, Z. Yang, J. Zhao, and L. Zhang, RSC Adv. 11, 745 (2021). doi: 10.1039/D0RA09469B
    [69]
    J. chen, B. Yin, L. Pang, W. Wang, J. Z. H. Zhang, and T. Zhu, J. Biomol. Struct. Dyn. 38, 2141 (2020). doi: 10.1080/07391102.2019.1624616
    [70]
    S. Liang, X. Liu, S. Zhang, M. Li, Q. Zhang, and J. Chen, Phys. Chem. Chem. Phys. 24, 1743 (2022). doi: 10.1039/D1CP04361G
    [71]
    J. Chen, S. Zhang, Q. Zeng, W. Wang, Q. Zhang, and X. Liu, Fron. Mol. Biosci. 9, 912518 (2022). doi: 10.3389/fmolb.2022.912518
    [72]
    F. Yan, X. Liu, S. Zhang, J. Su, Q. Zhang, and J. Chen, Int. J. Mol. Sci. 19, 2496 (2018). doi: 10.3390/ijms19092496
    [73]
    J. T. Seal, S. J. Atkinson, H. Aylott, P. Bamborough, C. W. Chung, R. C. B. Copley, L. Gordon, P. Grandi, J. R. J. Gray, L. A. Harrison, T. G. Hayhow, M. Lindon, C. Messenger, A. M. Michon, D. Mitchell, A. Preston, R. K. Prinjha, I. Rioja, S. Taylor, I. D. Wall, R. J. Watson, J. M. Woolven, and E. H. Demont, J. Med. Chem. 63, 9093 (2020). doi: 10.1021/acs.jmedchem.0c00796
    [74]
    S. W. Ember, Q. T. Lambert, N. Berndt, S. Gunawan, M. Ayaz, M. Tauro, J. Y. Zhu, P. J. Cranfill, P. Greninger, C. C. Lynch, C. H. Benes, H. R. Lawrence, G. W. Reuther, N. J. Lawrence, and E. Schönbrunn, Mol. Cancer Ther. 16, 1054 (2017). doi: 10.1158/1535-7163.MCT-16-0568-T
    [75]
    T. Ichiye and M. Karplus, Proteins 11, 205 (1991). doi: 10.1002/prot.340110305
    [76]
    J. Chen, L. Wang, W. Wang, H. Sun, L. Pang, and H. Bao, Comput. Biol. Med. 135, 104639 (2021). doi: 10.1016/j.compbiomed.2021.104639
    [77]
    R. M. Levy, A. R. Srinivasan, W. K. Olson, and J. A. McCammon, Biopolymers 23, 1099 (1984). doi: 10.1002/bip.360230610
    [78]
    A. E. García, Phys. Rev. Lett. 68, 2696 (1992). doi: 10.1103/PhysRevLett.68.2696
    [79]
    R. M. Karim, M. J. Bikowitz, A. Chan, J. Y. Zhu, D. Grassie, A. Becker, N. Berndt, S. Gunawan, N. J. Lawrence, and E. Schönbrunn, J. Med. Chem. 64, 15772 (2021). doi: 10.1021/acs.jmedchem.1c01096
    [80]
    R. Anandakrishnan, B. Aguilar, and A. V. Onufriev, Nucleic Acids Res. 40, W537 (2012). doi: 10.1093/nar/gks375
    [81]
    A. Jakalian, B. L. Bush, D. B. Jack, and C. I. Bayly, J. Comput. Chem. 21, 132 (2000). doi: 10.1002/(SICI)1096-987X(20000130)21:2<132::AID-JCC5>3.0.CO;2-P
    [82]
    A. Jakalian, D. B. Jack, and C. I. Bayly, J. Comput. Chem. 23, 1623 (2002). doi: 10.1002/jcc.10128
    [83]
    J. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman, and D. A. Case, J. Comput. Chem. 25, 1157 (2004). doi: 10.1002/jcc.20035
    [84]
    J. P. Ryckaert, G. Ciccotti, and H. J. C. Berendsen, J. Comput. Phys. 23, 327 (1977). doi: 10.1016/0021-9991(77)90098-5
    [85]
    W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein, J. Chem. Phys. 79, 926 (1983). doi: 10.1063/1.445869
    [86]
    T. Darden, D. York, and L. Pedersen, J. Chem. Phys. 98, 10089 (1993). doi: 10.1063/1.464397
    [87]
    U. Essmann, L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen, J. Chem. Phys. 103, 8577 (1995). doi: 10.1063/1.470117
    [88]
    S. Le Grand, A. W. Götz, and R. C. Walker, Comput. Phys. Commun. 184, 374 (2013). doi: 10.1016/j.cpc.2012.09.022
    [89]
    A. W. Götz, M. J. Williamson, D. Xu, D. Poole, S. Le Grand, and R. C. Walker, J. Chem. Theory Comput. 8, 1542 (2012). doi: 10.1021/ct200909j
    [90]
    R. Salomon Ferrer, A. W. Götz, D. Poole, S. Le Grand, and R. C. Walker, J. Chem. Theory Comput. 9, 3878 (2013). doi: 10.1021/ct400314y
    [91]
    J. Wang, P. Morin, W. Wang, and P. A. Kollman, J. Am. Chem. Soc. 123, 5221 (2001). doi: 10.1021/ja003834q
    [92]
    J. Su, X. Liu, S. Zhang, F. Yan, Q. Zhang, and J. Chen, Chem. Biol. Drug Des. 91, 828 (2018). doi: 10.1111/cbdd.13148
    [93]
    J. Chen, S. Zhang, W. Wang, H. Sun, Q. Zhang, and X. Liu, ACS Chem. Neurosci. 12, 2591 (2021). doi: 10.1021/acschemneuro.0c00813
    [94]
    E. L. Wu, K. Han, and J. Z. H. Zhang, Chem. Eur. J. 14, 8704 (2008). doi: 10.1002/chem.200800277
    [95]
    H. Sun, Y. Li, S. Tian, L. Xu, and T. Hou, Phys. Chem. Chem. Phys. 16, 16719 (2014). doi: 10.1039/C4CP01388C
    [96]
    H. Sun, Y. Li, M. Shen, S. Tian, L. Xu, P. Pan, Y. Guan, and T. Hou, Phys. Chem. Chem. Phys. 16, 22035 (2014). doi: 10.1039/C4CP03179B
    [97]
    D. Sitkoff, K. A. Sharp, and B. Honig, J. Phys. Chem. 98, 1978 (1994). doi: 10.1021/j100058a043
    [98]
    H. Gohlke, C. Kiel, and D. A. Case, J. Mol. Biol. 330, 891 (2003). doi: 10.1016/S0022-2836(03)00610-7
    [99]
    B. R. Miller, T. D. McGee, J. M. Swails, N. Homeyer, H. Gohlke, and A. E. Roitberg, J. Chem. Theory Comput. 8, 3314 (2012). doi: 10.1021/ct300418h
    [100]
    B. Xu, H. Shen, X. Zhu, and G. Li, J. Comput. Chem. 32, 3188 (2011). doi: 10.1002/jcc.21900
    [101]
    J. Chen, S. Zhang, W. Wang, L. Pang, Q. Zhang, and X. Liu, J. Chem. Inf. Model. 61, 1954 (2021). doi: 10.1021/acs.jcim.0c01470
    [102]
    M. Laberge and T. Yonetani, Biophys. J. 94, 2737 (2008). doi: 10.1529/biophysj.107.114942
    [103]
    A. D. McLachlan, J. Mol. Biol. 128, 49 (1979). doi: 10.1016/0022-2836(79)90308-5
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