Abstract
Background: The replication of monkeypox in the skin is critical to understanding its pathogenesis and spread. p37, a highly conserved 37 kDa peripheral membrane protein encoded by the F13L gene in Orthopoxvitidae is a validated target for anti-poxviral medication like tecovirimat, the first FDA-approved anti-poxviral drug that was approved in 2018. The detailed recognition mechanism of tecovirimat on p37 of monkeypox has not been fully clarified. As p37, HSV-1 gD and HSV-2 gD proteins of HSV are viral envelope glycoproteins identified as ligands for the human nectin-1 as a functional receptor of permissive cells. The use of non-damaging light for microbial inactivation (MI) has been documented for different virus like HSV, where photosensitizers (PSs) are used as lightresponsive agents which could generate antiviral responses primarily by oxidation. In addition, some PSs could elicit antiviral responses in a light-independent way by interacting within the viral-cell recognition sites.
Objective: This paper aims to evaluate the formation of complexes between the latest structural data available on the range of monkeypox and HSV-1/2 envelope proteins with the approved PSs protoporphyrin IX, chlorin e6, and methylene blue.
Methods: Ligands and receptors preparation, and molecular docking analyses were performed with Chimera and the Autodock Vina Software. Molecular docking and molecular dynamics simulation (MD) analyses for a 100 ns trajectory were also performed for the p37 – Methylene blue complex.
Results: PSs studies were found to form complexes into the patch regions of recognition between HSV-1/2 gD and human receptors, while MB was found to form a complex with the p37 protein into de pocket region where tecovirimat acts. MD simulation showed stability in the interaction of MB with the pocket region of the p37 protein.
Conclusion: The molecular mechanisms of potential dual antiviral activity for these complexes were clarified showing that MI with the use of these PSs could be further evaluated for viral skin lesions produced by monkeypox and HSV.
[1]
Tommasi, C.; Breuer, J. The biology of varicella-zoster virus replication in the skin. Viruses, 2022, 14(5), 982.
[http://dx.doi.org/10.3390/v14050982]
[http://dx.doi.org/10.3390/v14050982]
[2]
Adler, H.; Gould, S.; Hine, P.; Snell, L.B.; Wong, W.; Houlihan, C.F.; Osborne, J.C.; Rampling, T.; Beadsworth, M.B.J.; Duncan, C.J.A.; Dunning, J.; Fletcher, T.E.; Hunter, E.R.; Jacobs, M.; Khoo, S.H.; Newsholme, W.; Porter, D.; Porter, R.J.; Ratcliffe, L.; Schmid, M.L.; Semple, M.G.; Tunbridge, A.J.; Wingfield, T.; Price, N.M.; Abouyannis, M.; Al-Balushi, A.; Aston, S.; Ball, R.; Beeching, N.J.; Blanchard, T.J.; Carlin, F.; Davies, G.; Gillespie, A.; Hicks, S.R.; Hoyle, M-C.; Ilozue, C.; Mair, L.; Marshall, S.; Neary, A.; Nsutebu, E.; Parker, S.; Ryan, H.; Turtle, L.; Smith, C.; van Aartsen, J.; Walker, N.F.; Woolley, S.; Chawla, A.; Hart, I.; Smielewska, A.; Joekes, E.; Benson, C.; Brindley, C.; Das, U.; Eyton-Chong, C.K.; Gnanalingham, C.; Halfhide, C.; Larru, B.; Mayell, S.; McBride, J.; Oliver, C.; Paul, P.; Riordan, A.; Sridhar, L.; Storey, M.; Abdul, A.; Abrahamsen, J.; Athan, B.; Bhagani, S.; Brown, C.S.; Carpenter, O.; Cropley, I.; Frost, K.; Hopkins, S.; Joyce, J.; Lamb, L.; Lyons, A.; Mahungu, T.; Mepham, S.; Mukwaira, E.; Rodger, A.; Taylor, C.; Warren, S.; Williams, A.; Levitt, D.; Allen, D.; Dixon, J.; Evans, A.; McNicholas, P.; Payne, B.; Price, D.A.; Schwab, U.; Sykes, A.; Taha, Y.; Ward, M.; Emonts, M.; Owens, S.; Botgros, A.; Douthwaite, S.T.; Goodman, A.; Luintel, A.; MacMahon, E.; Nebbia, G.; O’Hara, G.; Parsons, J.; Sen, A.; Stevenson, D.; Sullivan, T.; Taj, U. van Nipsen tot Pannerden, C.; Winslow, H.; Zatyka, E.; Alozie-Otuka, E.; Beviz, C.; Ceesay, Y.; Gargee, L.; Kabia, M.; Mitchell, H.; Perkins, S.; Sasson, M.; Sehmbey, K.; Tabios, F.; Wigglesworth, N.; Aarons, E.J.; Brooks, T.; Dryden, M.; Furneaux, J.; Gibney, B.; Small, J.; Truelove, E.; Warrell, C.E.; Firth, R.; Hobson, G.; Johnson, C.; Dewynter, A.; Nixon, S.; Spence, O.; Bugert, J.J.; Hruby, D.E. Clinical features and management of human monkeypox: A retrospective observational study in the UK. Lancet Infect. Dis., 2022, 22(8), 1153-1162.
[http://dx.doi.org/10.1016/S1473-3099(22)00228-6]
[http://dx.doi.org/10.1016/S1473-3099(22)00228-6]
[3]
Hraib, M.; Jouni, S.; Albitar, M.M.; Alaidi, S.; Alshehabi, Z. The outbreak of monkeypox 2022: An overview. Ann. Med. Surg., 2022, 79, 104069.
[http://dx.doi.org/10.1016/j.amsu.2022.104069]
[http://dx.doi.org/10.1016/j.amsu.2022.104069]
[4]
Ogoina, D.; Iroezindu, M.; James, H.I.; Oladokun, R.; Yinka-Ogunleye, A.; Wakama, P.; Otike-odibi, B.; Usman, L.M.; Obazee, E.; Aruna, O.; Ihekweazu, C. Clinical course and outcome of human monkeypox in Nigeria. Clin. Infect. Dis., 2020, 71(8), e210-e214.
[http://dx.doi.org/10.1093/cid/ciaa143]
[http://dx.doi.org/10.1093/cid/ciaa143]
[5]
Fine, P.E.M.; Jezek, Z.; Grab, B.; Dixon, H. The transmission potential of monkeypox virus in human populations. Int. J. Epidemiol., 1988, 17(3), 643-650.
[http://dx.doi.org/10.1093/ije/17.3.643]
[http://dx.doi.org/10.1093/ije/17.3.643]
[6]
Smee, D.F. Progress in the discovery of compounds inhibiting orthopoxviruses in animal models. Antivir. Chem. Chemother., 2008, 19(3), 115-124.
[http://dx.doi.org/10.1177/095632020801900302]
[http://dx.doi.org/10.1177/095632020801900302]
[7]
Wu, C.; Liu, Y.; Yang, Y.; Zhang, P.; Zhong, W.; Wang, Y.; Wang, Q.; Xu, Y.; Li, M.; Li, X.; Zheng, M.; Chen, L.; Li, H. Analysis of therapeutic targets for SARS-CoV-2 and discovery of potential drugs by computational methods. Acta Pharm. Sin. B, 2020, 10(5), 766-788.
[http://dx.doi.org/10.1016/j.apsb.2020.02.008]
[http://dx.doi.org/10.1016/j.apsb.2020.02.008]
[8]
Luo, D.; Carter, K.A.; Miranda, D.; Lovell, J.F. Chemophototherapy: An emerging treatment option for solid tumors. Adv. Sci., 2017, 4(1), 1600106.
[http://dx.doi.org/10.1002/advs.201600106]
[http://dx.doi.org/10.1002/advs.201600106]
[9]
Kwiatkowski, S.; Knap, B.; Przystupski, D.; Saczko, J.; Kędzierska, E.; Knap-Czop, K.; Kotlińska, J.; Michel, O.; Kotowski, K.; Kulbacka, J. Photodynamic therapy – mechanisms, photosensitizers and combinations. Biomed. Pharmacother., 2018, 106, 1098-1107.
[http://dx.doi.org/10.1016/j.biopha.2018.07.049]
[http://dx.doi.org/10.1016/j.biopha.2018.07.049]
[10]
Nowak-Stepniowska, A.; Pergoł, P.; Padzik-Graczyk, A. Photodynamic method of cancer diagnosis and therapy--mechanisms and applications. Postepy Biochem., 2013, 59, 53-63.
[11]
Luksiene, Z. Photodynamic therapy: Mechanism of action and ways to improve the efficiency of treatment. Medicina, 2003, 39, 1137-1150.
[12]
Juzeniene, A.; Moan, J. The history of PDT in Norway. Photodiagn. Photodyn. Ther., 2007, 4(1), 3-11.
[http://dx.doi.org/10.1016/j.pdpdt.2006.11.002]
[http://dx.doi.org/10.1016/j.pdpdt.2006.11.002]
[13]
Wiehe, A.; O’Brien, J.M.; Senge, M.O. Trends and targets in antiviral phototherapy. Photochem. Photobiol. Sci., 2019, 18(11), 2565-2612.
[http://dx.doi.org/10.1039/c9pp00211a]
[http://dx.doi.org/10.1039/c9pp00211a]
[14]
Tomé, J.P.C.; Silva, E.M.P.; Pereira, A.M.V.M.; Alonso, C.M.A.; Faustino, M.A.F.; Neves, M.G.P.M.S.; Tomé, A.C.; Cavaleiro, J.A.S.; Tavares, S.A.P.; Duarte, R.R.; Caeiro, M.F.; Valdeira, M.L. Synthesis of neutral and cationic tripyridylporphyrin-d-galactose conjugates and the photoinactivation of HSV-1. Bioorg. Med. Chem., 2007, 15(14), 4705-4713.
[http://dx.doi.org/10.1016/j.bmc.2007.05.005]
[http://dx.doi.org/10.1016/j.bmc.2007.05.005]
[15]
Jendželovská, Z.; Jendželovský, R.; Kuchárová, B.; Fedoročko, P. Hypericin in the light and in the dark: Two sides of the same coin. Front. Plant Sci., 2016, 7, 560.
[http://dx.doi.org/10.3389/fpls.2016.00560]
[http://dx.doi.org/10.3389/fpls.2016.00560]
[16]
Adimoolam, M.G. A, V.; Nalam, M.R.; Sunkara, M.V. Chlorin e6 loaded lactoferrin nanoparticles for enhanced photodynamic therapy. J. Mater. Chem. B Mater. Biol. Med., 2017, 5(46), 9189-9196.
[http://dx.doi.org/10.1039/C7TB02599H]
[http://dx.doi.org/10.1039/C7TB02599H]
[17]
Gu, C.; Wu, Y.; Guo, H.; Zhu, Y.; Xu, W.; Wang, Y.; Zhou, Y.; Sun, Z.; Cai, X.; Li, Y.; Liu, J.; Huang, Z.; Yuan, Z.; Zhang, R.; Deng, Q.; Qu, D.; Xie, Y. Protoporphyrin IX and verteporfin potently inhibit SARS-CoV-2 infection in vitro and in a mouse model expressing human ACE2. Sci. Bull., 2021, 66(9), 925-936.
[http://dx.doi.org/10.1016/j.scib.2020.12.005]
[http://dx.doi.org/10.1016/j.scib.2020.12.005]
[18]
Dias, L.D.; Blanco, K.C.; Bagnato, V.S. COVID-19: Beyond the virus. The use of photodynamic therapy for the treatment of infections in the respiratory tract. Photodiagn. Photodyn. Ther., 2020, 31, 101804.
[http://dx.doi.org/10.1016/j.pdpdt.2020.101804]
[http://dx.doi.org/10.1016/j.pdpdt.2020.101804]
[19]
Floyd, R.A.; Schneider, J.E., Jr; Dittmer, D.P. Methylene blue photoinactivation of RNA viruses. Antiviral Res., 2004, 61(3), 141-151.
[http://dx.doi.org/10.1016/j.antiviral.2003.11.004]
[http://dx.doi.org/10.1016/j.antiviral.2003.11.004]
[20]
Guidelines on viral inacti- vation and removal procedures intended to assure the viral safety of human blood plasma products, WHO Tech; World Health Organization, 2004, pp. 150-224.
[21]
Pinzi, L.; Rastelli, G. Molecular docking: Shifting paradigms in drug discovery. Int. J. Mol. Sci., 2019, 20(18), 4331.
[http://dx.doi.org/10.3390/ijms20184331]
[http://dx.doi.org/10.3390/ijms20184331]
[22]
Smith, G.L.; Vanderplasschen, A.; Law, M. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol., 2002, 83(12), 2915-2931.
[http://dx.doi.org/10.1099/0022-1317-83-12-2915]
[http://dx.doi.org/10.1099/0022-1317-83-12-2915]
[24]
Blasco, R.; Moss, B. Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein. J. Virol., 1991, 65(11), 5910-5920.
[http://dx.doi.org/10.1128/jvi.65.11.5910-5920.1991]
[http://dx.doi.org/10.1128/jvi.65.11.5910-5920.1991]
[25]
Grosenbach, D.W.; Honeychurch, K.; Rose, E.A.; Chinsangaram, J.; Frimm, A.; Maiti, B.; Lovejoy, C.; Meara, I.; Long, P.; Hruby, D.E. Oral tecovirimat for the treatment of smallpox. N. Engl. J. Med., 2018, 379(1), 44-53.
[http://dx.doi.org/10.1056/NEJMoa1705688]
[http://dx.doi.org/10.1056/NEJMoa1705688]
[26]
Zheng, L.; Meng, J.; Lin, M.; Lv, R.; Cheng, H.; Zou, L.; Sun, J.; Li, L.; Ren, R.; Wang, S. Structure prediction of the entire proteome of monkeypox variants. Acta Materia Medica, 2022, 1(2)
[http://dx.doi.org/10.15212/AMM-2022-0017]
[http://dx.doi.org/10.15212/AMM-2022-0017]
[27]
Minasov, G.; Inniss, N.L.; Shuvalova, L.; Anderson, W.F.; Satchell, K.J.F. Structure of the Monkeypox profilin-like protein A42R reveals potential function differences from cellular profilins. BioRxiv, 2022.
[http://dx.doi.org/10.1101/2022.08.07.503103]
[http://dx.doi.org/10.1101/2022.08.07.503103]
[28]
Roper, R.L. Characterization of the vaccinia virus A35R protein and its role in virulence. J. Virol., 2006, 80(1), 306-313.
[http://dx.doi.org/10.1128/JVI.80.1.306-313.2006]
[http://dx.doi.org/10.1128/JVI.80.1.306-313.2006]
[29]
van Eijl, H.; Hollinshead, M.; Smith, G.L. The vaccinia virus A36R protein is a type ib membrane protein present on intracellular but not extracellular enveloped virus particles. Virology, 2000, 271(1), 26-36.
[http://dx.doi.org/10.1006/viro.2000.0260]
[http://dx.doi.org/10.1006/viro.2000.0260]
[30]
Liu, X.; Zhu, Z.; Miao, Q.; Lim, J.W.; Lu, H. Monkeypox – A danger approaching Asia. Biosci. Trends, 2022, 16(4), 245-248.
[http://dx.doi.org/10.5582/bst.2022.01343]
[http://dx.doi.org/10.5582/bst.2022.01343]
[31]
Lu, G.; Zhang, N.; Qi, J.; Li, Y.; Chen, Z.; Zheng, C.; Gao, G.F.; Yan, J. Crystal structure of herpes simplex virus 2 gD bound to nectin-1 reveals a conserved mode of receptor recognition. J. Virol., 2014, 88(23), 13678-13688.
[http://dx.doi.org/10.1128/JVI.01906-14]
[http://dx.doi.org/10.1128/JVI.01906-14]
[32]
Levin, M.J.; Weinberg, A.; Schmid, D.S. Herpes simplex virus and varicella-zoster virus. Microbiol. Spectr., 2016, 4(3), 4.3.49..
[http://dx.doi.org/10.1128/microbiolspec.DMIH2-0017-2015]
[http://dx.doi.org/10.1128/microbiolspec.DMIH2-0017-2015]
[33]
Zhang, N.; Yan, J.; Lu, G.; Guo, Z.; Fan, Z.; Wang, J.; Shi, Y.; Qi, J.; Gao, G.F. Binding of herpes simplex virus glycoprotein D to nectin-1 exploits host cell adhesion. Nat. Commun., 2011, 2(1), 577.
[http://dx.doi.org/10.1038/ncomms1571]
[http://dx.doi.org/10.1038/ncomms1571]
[34]
Ion, R-M.; Calin, M. Comparative study of some nano- And micro - sensitizers in photodynamic inactivation of microorganisms. J. Optoelectron. Adv. Mater., 2007, 9, 1933-1938.
[35]
Zverev, V.V.; Makarov, O.V.; Khashukoeva, A.Z.; Svitich, O.A.; Dobrokhotova, Y.E.; Markova, E.A. In vitro studies of the antiherpetic effect of photodynamic therapy. Lasers Med. Sci., 2016, 31, 849-855.
[http://dx.doi.org/10.1007/s10103-016-1912-0]
[http://dx.doi.org/10.1007/s10103-016-1912-0]
[36]
Latief, M.A.; Chikama, T.; Shibasaki, M.; Sasaki, T.; Ko, J.A.; Kiuchi, Y.; Sakaguchi, T.; Obana, A. Antimicrobial action from a novel porphyrin derivative in photodynamic antimicrobial chemotherapy in vitro. Lasers Med. Sci., 2015, 30(1), 383-387.
[http://dx.doi.org/10.1007/s10103-014-1681-6]
[http://dx.doi.org/10.1007/s10103-014-1681-6]
[37]
Jumper, J.; Evans, R.; Pritzel, A.; Green, T.; Figurnov, M.; Ronneberger, O.; Tunyasuvunakool, K.; Bates, R.; Žídek, A.; Potapenko, A.; Bridgland, A.; Meyer, C.; Kohl, S.A.A.; Ballard, A.J.; Cowie, A.; Romera-Paredes, B.; Nikolov, S.; Jain, R.; Adler, J.; Back, T.; Petersen, S.; Reiman, D.; Clancy, E.; Zielinski, M.; Steinegger, M.; Pacholska, M.; Berghammer, T.; Bodenstein, S.; Silver, D.; Vinyals, O.; Senior, A.W.; Kavukcuoglu, K.; Kohli, P.; Hassabis, D. Highly accurate protein structure prediction with AlphaFold. Nature, 2021, 596(7873), 583-589.
[http://dx.doi.org/10.1038/s41586-021-03819-2]
[http://dx.doi.org/10.1038/s41586-021-03819-2]
[38]
Hanwell, M.D.; Curtis, D.E.; Lonie, D.C.; Vandermeersch, T.; Zurek, E.; Hutchison, G.R. Avogadro: An advanced semantic chemical editor, visualization, and analysis platform. J. Cheminform., 2012, 4(1), 17.
[http://dx.doi.org/10.1186/1758-2946-4-17]
[http://dx.doi.org/10.1186/1758-2946-4-17]
[39]
Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera?A visualization system for exploratory research and analysis. J. Comput. Chem., 2004, 25(13), 1605-1612.
[http://dx.doi.org/10.1002/jcc.20084]
[http://dx.doi.org/10.1002/jcc.20084]
[40]
Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem., 2009, 31(2), 455-461.
[http://dx.doi.org/10.1002/jcc.21334]
[http://dx.doi.org/10.1002/jcc.21334]
[42]
Adasme, M.F.; Linnemann, K.L.; Bolz, S.N.; Kaiser, F.; Salentin, S.; Haupt, V.J.; Schroeder, M. PLIP 2021: Expanding the scope of the protein–ligand interaction profiler to DNA and RNA. Nucleic Acids Res., 2021, 49(W1), W530-W534.
[http://dx.doi.org/10.1093/nar/gkab294]
[http://dx.doi.org/10.1093/nar/gkab294]
[43]
Morris, G.M.; Huey, R.; Lindstrom, W.; Sanner, M.F.; Belew, R.K.; Goodsell, D.S.; Olson, A.J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J. Comput. Chem., 2009, 30(16), 2785-2791.
[http://dx.doi.org/10.1002/jcc.21256]
[http://dx.doi.org/10.1002/jcc.21256]
[45]
Prichard, M.N.; Kern, E.R. Orthopoxvirus targets for the development of new antiviral agents. Antiviral Res., 2012, 94(2), 111-125.
[http://dx.doi.org/10.1016/j.antiviral.2012.02.012]
[http://dx.doi.org/10.1016/j.antiviral.2012.02.012]
[46]
Moss, B. Membrane fusion during poxvirus entry. Semin. Cell Dev. Biol., 2016, 60, 89-96.
[http://dx.doi.org/10.1016/j.semcdb.2016.07.015]
[http://dx.doi.org/10.1016/j.semcdb.2016.07.015]
[47]
Abraham, M.J.; Murtola, T.; Schulz, R.; Páll, S.; Smith, J.C.; Hess, B.; Lindahl, E. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 2015, 1-2, 19-25.
[http://dx.doi.org/10.1016/j.softx.2015.06.001]
[http://dx.doi.org/10.1016/j.softx.2015.06.001]
[48]
Jo, S.; Kim, T.; Iyer, V.G. Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM. J. Comput. Chem., 2008, 29(11), 1859-1865.
[http://dx.doi.org/10.1002/jcc.20945]
[http://dx.doi.org/10.1002/jcc.20945]
[49]
Vanommeslaeghe, K.; Raman, E.P.; MacKerell, A.D., Jr Automation of the CHARMM general force field (CGenFF) II: Assignment of bonded parameters and partial atomic charges. J. Chem. Inf. Model., 2012, 52(12), 3155-3168.
[http://dx.doi.org/10.1021/ci3003649]
[http://dx.doi.org/10.1021/ci3003649]
[50]
O’Boyle, N.M.; Banck, M.; James, C.A.; Morley, C.; Vandermeersch, T.; Hutchison, G.R. Open Babel: An open chemical toolbox. J. Cheminform., 2011, 3(1), 33.
[http://dx.doi.org/10.1186/1758-2946-3-33]
[http://dx.doi.org/10.1186/1758-2946-3-33]
[51]
Kim, S.; Lee, J.; Jo, S.; Brooks, C.L., III; Lee, H.S. Im, W. CHARMM-GUI ligand reader and modeler for CHARMM force field generation of small molecules. J. Comput. Chem., 2017, 38(21), 1879-1886.
[http://dx.doi.org/10.1002/jcc.24829]
[http://dx.doi.org/10.1002/jcc.24829]
[52]
Earl, D.J.; Deem, M.W. Monte carlo simulations. In: Molecular Modeling of Proteins; Springer, 2008; pp. 25-36.
[http://dx.doi.org/10.1007/978-1-59745-177-2_2]
[http://dx.doi.org/10.1007/978-1-59745-177-2_2]
[53]
Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys., 2007, 126(1), 014101.
[http://dx.doi.org/10.1063/1.2408420]
[http://dx.doi.org/10.1063/1.2408420]
[54]
Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys., 1981, 52(12), 7182-7190.
[http://dx.doi.org/10.1063/1.328693]
[http://dx.doi.org/10.1063/1.328693]
[55]
Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J. Comput. Chem., 2009, 31(4), 671-690.
[http://dx.doi.org/10.1002/jcc.21367]
[http://dx.doi.org/10.1002/jcc.21367]
[56]
Turner, P.J. XMGRACE, version 5.1; Center for Coastal Land-Margin Research; Oregon Graduate Institute of Science Technology: Beaverton, OR 2, 2005.
[57]
Krummenacher, C.; Supekar, V.M.; Whitbeck, J.C.; Lazear, E.; Connolly, S.A.; Eisenberg, R.J.; Cohen, G.H.; Wiley, D.C.; Carfí, A. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J., 2005, 24(23), 4144-4153.
[http://dx.doi.org/10.1038/sj.emboj.7600875]
[http://dx.doi.org/10.1038/sj.emboj.7600875]
[58]
Liu, X.; Shi, D.; Zhou, S.; Liu, H.; Liu, H.; Yao, X. Molecular dynamics simulations and novel drug discovery. Expert Opin. Drug Discov., 2018, 13(1), 23-37.
[http://dx.doi.org/10.1080/17460441.2018.1403419]
[http://dx.doi.org/10.1080/17460441.2018.1403419]
[59]
Sinyani, A.; Idowu, K.; Shunmugam, L.; Kumalo, H.M.; Khan, R. A molecular dynamics perspective into estrogen receptor inhibition by selective flavonoids as alternative therapeutic options. J. Biomol. Struct. Dyn., 2022, 41(9), 1-13.
[http://dx.doi.org/10.1080/07391102.2022.2062786]
[http://dx.doi.org/10.1080/07391102.2022.2062786]
[60]
Dixit, S.B.; Ponomarev, S.Y.; Beveridge, D.L. Root mean square deviation probability analysis of molecular dynamics trajectories on DNA. J. Chem. Inf. Model., 2006, 46(3), 1084-1093.
[http://dx.doi.org/10.1021/ci0504925]
[http://dx.doi.org/10.1021/ci0504925]
[61]
Martínez, L. Automatic identification of mobile and rigid substructures in molecular dynamics simulations and fractional structural fluctuation analysis. PLoS One, 2015, 10(3), e0119264.
[http://dx.doi.org/10.1371/journal.pone.0119264]
[http://dx.doi.org/10.1371/journal.pone.0119264]
[62]
Baig, M.H.; Sudhakar, D.R.; Kalaiarasan, P.; Subbarao, N.; Wadhawa, G.; Lohani, M.; Khan, M.K.A.; Khan, A.U. Insight into the effect of inhibitor resistant s130g mutant on physico-chemical properties of SHV type beta-lactamase: A molecular dynamics study. PLoS One, 2014, 9(12), e112456.
[http://dx.doi.org/10.1371/journal.pone.0112456]
[http://dx.doi.org/10.1371/journal.pone.0112456]
[63]
Ahamad, S.; Gupta, D.; Kumar, V. Targeting SARS-CoV-2 nucleocapsid oligomerization: Insights from molecular docking and molecular dynamics simulations. J. Biomol. Struct. Dyn., 2022, 40(6), 2430-2443.
[http://dx.doi.org/10.1080/07391102.2020.1839563]
[http://dx.doi.org/10.1080/07391102.2020.1839563]
[64]
Gao, Y.; Mei, Y.; Zhang, J.Z.H. Treatment of Hydrogen Bonds in Protein Simulations; Advanced Materials for Renewable Hydrogen Production, Storage and Utilization, InTech, 2015.
[http://dx.doi.org/10.5772/61049]
[http://dx.doi.org/10.5772/61049]
[65]
Felgenträger, A.; Maisch, T.; Dobler, D.; Späth, A. Hydrogen bond acceptors and additional cationic charges in methylene blue derivatives: Photophysics and antimicrobial efficiency. BioMed Res. Int., 2013, 2013, 1-12.
[http://dx.doi.org/10.1155/2013/482167]
[http://dx.doi.org/10.1155/2013/482167]
