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. 2023 Feb 14;72(1):248–262. doi: 10.1007/s11172-023-3730-4

Synthesis of conjugates of (aR,7S)-colchicine with monoterpenoids and investigation of their biological activity

E S Shchegravina 1, S D Usova 1, D S Baev 2, E S Mozhaitsev 2, D N Shcherbakov 3, S V Belenkaya 3,4, E A Volosnikova 3, V Yu Chirkova 5, E A Sharlaeva 5, E V Svirshchevskaya 6, I P Fonareva 1, A R Sitdikova 1, N F Salakhutdinov 2, O I Yarovaya 2, A Yu Fedorov 1,✉
PMCID: PMC9926439  PMID: 36817557

Abstract

Conjugates of the natural alkaloid (aR,7S)-colchicine with bicyclic monoterpenoids and their derivatives were synthesized for the first time. Molecular docking of the synthesized agents in the active site of the main viral protease of the SARS-CoV-2 virus was carried out. The cytotoxic properties of the agents against different cell lines and the ability to inhibit the main viral protease 3CLPro were studied.

Key words: colchicine, monoterpenoids, SARS-Cov-2 3CLPro, molecular docking, antiproliferative activity

Footnotes

Fedorov Aleksey Yuryevich, born in 1971, Head of the Department of Organic Chemistry of the Faculty of Chemistry of the National Research Lobachevsky State University of Nizhny Novgorod (Nizhny Novgorod), Doctor of Chemical Sciences, Professor of the Russian Academy of Sciences (since 2018). He was elected a corresponding member of the Russian Academy of Sciences in 2022 (more information in Russ. Chem. Bull., 2022, 71, 1559; DOI: 10.1007/s11172-022-3565-4).

Published in Russian in Izvestiya Akademii Nauk. Seriya Khimicheskaya, Vol. 72, No. 1, pp. 248–262, January, 2023.

Synthesis of all compounds and biological studies were financially supported by the Russian Science Foundation (Project No. 19-13-00158). Molecular docking was carried out with the financial support from the Ministry of Science and Higher Education of the Russian Federation (Agreement No. 075-15-2021-1355 of October 12, 2021) in the framework of the implementation of selected activities of the Federal Scientific and Technical Program for the Development of Synchrotron and Neutron Research and Research Infrastructure for 2019–2027 years.

No human or animal subjects were used in this research.

The authors declare no competing interests.

References

  • 1.Beigel J H, Tomashek K M, Dodd L E, Mehta A K, Zingman B S, Kalil A C, Hohmann E, Chu H Y, Luetkemeyer A, Kline S, Lopez de Castilla D, Finberg R W, Dierberg K, Tapson V, Hsieh L, Patterson T F, Paredes R, Sweeney D A, Short W R, Touloumi G, Lye D C, Ohmagari N, Oh M, Ruiz-Palacios G M, Benfield T, Fätkenheuer G, Kortepeter M G, Atmar R L, Creech C B, Lundgren J, Babiker A G, Pett S, Neaton J D, Burgess T H, Bonnett T, Green M, Makowski M, Osinusi A, Nayak S, Lane H C. New Engl. J. Med. 2020;383:1813–1826. doi: 10.1056/NEJMoa2007764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Jayk Bernal A, Gomes da Silva M M, Musungaie D B, Kovalchuk E, Gonzalez A, Delos Reyes V, Martín-Quirós A, Caraco Y, Williams-Diaz A, Brown M L, Du J, Pedley A, Assaid C, Strizki J, Grobler J A, Shamsuddin H H, Tipping R, Wan H, Paschke A, Butterton J R, Johnson M G, De Anda C. New Engl. J. Med. 2022;386:509–520. doi: 10.1056/NEJMoa2116044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Abdelnabi R, Foo C S, Jochmans D, Vangeel L, De Jonghe S, Augustijns P, Mols R, Weynand B, Wattanakul T, Hoglund R M, Tarning J, Mowbray C E, Sjö P, Escudié F, Scandale I, Chatelain E, Neyts J. Nat. Commun. 2022;13:719. doi: 10.1038/s41467-022-28354-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Dabbous H M, Abd-Elsalam S, El-Sayed M H, Sherief A F, Ebeid F F S, El Ghafar M S A, Soliman S, Elbahnasawy M, Badawi R, Tageldin M A. Arch. Virol. 2021;166:949–954. doi: 10.1007/s00705-021-04956-9. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
  • 5.K. Srinivasan, M. Rao, Ther. Adv. Infect. Dis., 2021, 8; DOI: 10.1177/20499361211063016. [DOI] [PMC free article] [PubMed]
  • 6.Kim J Y, Jang Y R, Hong J H, Jung J G, Park J-H, Streinu-Cercel A, Streinu-Cercel A, Săndulescu O, Lee S J, Kim S H, Jung N H, Lee S G, Park J E, Kim M K, Jeon D B, Lee Y J, Kim B S, Lee Y M, Kim Y-S. Clin. Ther. 2021;43:1706–1727. doi: 10.1016/j.clinthera.2021.08.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Kim T, Joo D-H, Lee S W, Lee J, Lee S J, Kang J. J. Clin. Med. 2022;11:1412. doi: 10.3390/jcm11051412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Miguez-Rey E, Choi D, Kim S, Yoon S, Săndulescu O. Expert Opin. Invest. Drugs. 2022;31:41–58. doi: 10.1080/13543784.2022.2030310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Syed Y Y. Drugs. 2020;80:91–97. doi: 10.1007/s40265-019-01252-4. [DOI] [PubMed] [Google Scholar]
  • 10.Scarsi M, Piantoni S, Colombo E, Airó P, Richini D, Miclini M, Bertasi V, Bianchi M, Bottone D, Civelli P, Cotelli M-S, Damiolini E, Galbassini G, Gatta D, Ghirardelli M-L, Magri R, Malamani P, Mendeni M, Molinari S, Morotti A, Salada L, Turla M, Vender A, Tincani A, Brucato A, Franceschini F, Furloni R, Andreoli L. Ann. Rheum. Dis. 2020;79:1286–1289. doi: 10.1136/annrheumdis-2020-217712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Deftereos S G, Siasos G, Giannopoulos G, Vrachatis D A, Angelidis C, Giotaki S G, Gargalianos P, Giamarellou H, Gogos C, Daikos G, Lazanas M, Lagiou P, Saroglou G, Sipsas N, Tsiodras S, Chatzigeorgiou D, Moussas N, Kotanidou A, Koulouris N, Oikonomou E, Kaoukis A, Kossyvakis C, Raisakis K, Fountoulaki K, Comis M, Tsiachris D, Sarri E, Theodorakis A, Martinez-Dolz L, Sanz-Sánchez J, Reimers B, Stefanini G G, Cleman M, Filippou D, Olympios C D, Pyrgakis V N, Goudevenos J, Hahalis G, Kolettis T M, Iliodromitis E, Tousoulis D, Stefanadis C. Hell. J. Cardiol. 2020;61:42–45. doi: 10.1016/j.hjc.2020.03.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Schlesinger N, Firestein B L, Brunetti L. Curr. Pharmacol. Rep. 2020;6:137–145. doi: 10.1007/s40495-020-00225-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Lopes M I, Bonjorno L P, Giannini M C, Amaral N B, Menezes P I, Dib S M, Gigante S L, Benatti M N, Rezek U C, Emrich-Filho L L, Sousa B A A, Almeida S C L, Luppino Assad R, Veras F P, Schneider A, Rodrigues T S, Leiria L O S, Cunha L D, Alves-Filho J C, Cunha T M, Arruda E, Miranda C H, Pazin-Filho A, Auxiliadora-Martins M, Borges M C, Fonseca B A L, Bollela V R, Del-Ben C M, Cunha F Q, Zamboni D S, Santana R C, Vilar F C, Louzada-Junior P, Oliveira R D R. RMD Open. 2021;7:e001455. doi: 10.1136/rmdopen-2020-001455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Mareev V Y, Orlova Y A, Plisyuk A G, Pavlikova E P, Akopyan Z A, Matskeplishvili S T, Malakhov P S, Krasnova T N, Seredenina E M, Potapenko A V, Agapov M A, Asratyan D A, Dyachuk L I, Samohodskaya L M, Mershina E A, Sinitsin V E, Pakhomov P V, Zhdanova E A, Mareev Y V, Begrambekova Y L, Kamalov A A. Kardiologiya. 2021;61:15–27. doi: 10.18087/cardio.2021.2.n1560. [DOI] [PubMed] [Google Scholar]
  • 15.Bonaventura A, Vecchié A, Dagna L, Tangianu F, Abbate A, Dentali F. Inflamm. Res. 2022;71:293–307. doi: 10.1007/s00011-022-01540-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Gracheva I A, Shchegravina E S, Schmalz H G, Beletskaya I P, Fedorov A Y. J. Med. Chem. 2020;63:10618–10651. doi: 10.1021/acs.jmedchem.0c00222. [DOI] [PubMed] [Google Scholar]
  • 17.Shchegravina E S, Svirshchevskaya E V, Combes S, Allegro D, Barbier P, Gigant B, Varela P F, Gavryushin A E, Kobanova D A, Shchekotikhin A E, Fedorov A Y. Eur. J. Med. Chem. 2020;207:112724. doi: 10.1016/j.ejmech.2020.112724. [DOI] [PubMed] [Google Scholar]
  • 18.Shchegravina E S, Maleev A A, Ignatov S K, Gracheva I A, Stein A, Schmalz H-G, Gavryushin A E, Zubareva A, Svirshchevskaya E V, Fedorov A Y. Eur. J. Med. Chem. 2017;141:51–60. doi: 10.1016/j.ejmech.2017.09.055. [DOI] [PubMed] [Google Scholar]
  • 19.Gracheva I, Svirshchevskaya E, Zaburdaeva E, Fedorov A. Synthesis. 2017;49:4335–4340. doi: 10.1055/s-0036-1589060. [DOI] [Google Scholar]
  • 20.N. S. Sitnikov, A. S. Kokisheva, G. K. Fukin, J.-M. Neudörfl, H. Sutorius, A. Prokop, V. V. Fokin, H.-G. Schmalz, A. Yu. Fedorov, Eur. J. Org. Chem., 2014, 6481–6492; DOI: 10.1002/ejoc.201402850.
  • 21.Toldo S, Abbate A. Nat. Rev. Cardiol. 2018;15:203–214. doi: 10.1038/nrcardio.2017.161. [DOI] [PubMed] [Google Scholar]
  • 22.Leung Y Y, Yao Hui L L, Kraus V B. Semin. Arthritis Rheum. 2015;45:341–350. doi: 10.1016/j.semarthrit.2015.06.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Tay M Z, Poh C M, Rénia L, MacAry P A, Ng L F P. Nat. Rev. Immunol. 2020;20:363–374. doi: 10.1038/s41577-020-0311-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Richter M, Boldescu V, Graf D, Streicher F, Dimoglo A, Bartenschlager R, Klein C D. ChemMedChem. 2019;14:469–483. doi: 10.1002/cmdc.201800641. [DOI] [PubMed] [Google Scholar]
  • 25.Paduch R, Trytek M, Król S K, Kud J, Frant M, Kandefer-Szerszeń M, Fiedurek J. Pharm. Biol. 2016;54:1096–1107. doi: 10.3109/13880209.2015.1103753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Wang G, Tang W, Bidigare R R. Natural Products. Totowa: Humana Press; 2005. pp. 197–227. [Google Scholar]
  • 27.Wen C-C, Kuo Y-H, Jan J-T, Liang P-H, Wang S-Y, Liu H-G, Lee C-K, Chang S-T, Kuo C-J, Lee S-S, Hou C-C, Hsiao P-W, Chien S-C, Shyur L-F, Yang N-S. J. Med. Chem. 2007;50:4087–4095. doi: 10.1021/jm070295s. [DOI] [PubMed] [Google Scholar]
  • 28.Niedermeyer T H J, Lindequist U, Mentel R, Gördes D, Schmidt E, Thurow K, Lalk M. J. Nat. Prod. 2005;68:1728–1731. doi: 10.1021/np0501886. [DOI] [PubMed] [Google Scholar]
  • 29.Yarovaya O I, Salakhutdinov N F. Russ. Chem. Rev. 2021;90:488–510. doi: 10.1070/RCR4969. [DOI] [Google Scholar]
  • 30.Sokolova A S, Putilova V P, Yarovaya O I, Zybkina A V, Mordvinova E D, Zaykovskaya A V, Shcherbakov D N, Orshanskaya I R, Sinegubova E O, Esaulkova I L, Borisevich S S, Bormotov N I, Shishkina L N, Zarubaev V V, Pyankov O V, Maksyutov R A, Salakhutdinov N F. Molecules. 2021;26:2235. doi: 10.3390/molecules26082235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Kononova A A, Sokolova A S, Cheresiz S V, Yarovaya O I, Nikitina R A, Chepurnov A A, Pokrovsky A G, Salakhutdinov N F. MedChemComm. 2017;8:2233–2237. doi: 10.1039/C7MD00424A. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Sokolova A S, Yarovaya O I, Zybkina A V, Mordvinova E D, Shcherbakova N S, Zaykovskaya A V, Baev D S, Tolstikova T G, Shcherbakov D N, Pyankov O V, Maksyutov R A, Salakhutdinov N F. Eur. J. Med. Chem. 2020;207:112726. doi: 10.1016/j.ejmech.2020.112726. [DOI] [PubMed] [Google Scholar]
  • 33.Sokolova A S, Yarovaya O I, Semenova M D, Shtro A A, Orshanskaya I R, Zarubaev V V, Salakhutdinov N F. MedChemComm. 2017;8:960–963. doi: 10.1039/C6MD00657D. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Zarubaev V V, Garshinina A V, Tretiak T S, Fedorova V A, Shtro A A, Sokolova A S, Yarovaya O I, Salakhutdinov N F. Antiviral Res. 2015;120:126–133. doi: 10.1016/j.antiviral.2015.06.004. [DOI] [PubMed] [Google Scholar]
  • 35.Muhseen Z T, Hameed A R, Al-Hasani H M H, Tahir ul Qamar M, Li G. J. Mol. Liq. 2020;320:114493. doi: 10.1016/j.molliq.2020.114493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Giofrè S V, Napoli E, Iraci N, Speciale A, Cimino F, Muscarà C, Molonia M S, Ruberto G, Saija A. Comput. Biol. Med. 2021;134:104538. doi: 10.1016/j.compbiomed.2021.104538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Hou B, Zhang Y-M, Liao H-Y, Fu L-F, Li D-D, Zhao X, Qi J-X, Yang W, Xiao G-F, Yang L, Zuo Z-Y, Wang L, Zhang X-L, Bai F, Yang L, Gao G F, Song H, Hu J-M, Shang W-J, Zhou J. J. Nat. Prod. 2022;85:327–336. doi: 10.1021/acs.jnatprod.1c00805. [DOI] [PubMed] [Google Scholar]
  • 38.Hassan M Z, Osman H, Ali M A, Ahsan M J. Eur. J. Med. Chem. 2016;123:236–255. doi: 10.1016/j.ejmech.2016.07.056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Artyushin O I, Moiseeva A A, Zarubaev V V, Slita A V, Galochkina A V, Muryleva A A, Borisevich S S, Yarovaya O I, Salakhutdinov N F, Brel V K. Chem. Biodiversity. 2019;16:e1900340. doi: 10.1002/cbdv.201900340. [DOI] [PubMed] [Google Scholar]
  • 40.Yarovaya O I, Kovaleva K S, Zaykovskaya A A, Yashina L N, Scherbakova N S, Scherbakov D N, Borisevich S S, Zubkov F I, Antonova A S, Peshkov R Y, Eltsov I V, Pyankov O V, Maksyutov R A, Salakhutdinov N F. Bioorg. Med. Chem. Lett. 2021;40:127926. doi: 10.1016/j.bmcl.2021.127926. [DOI] [PubMed] [Google Scholar]
  • 41.Sokolova A S, Yarovaya O I, Shernyukov A V, Gatilov Y V, Razumova Y V, Zarubaev V V, Tretiak T S, Pokrovsky A G, Kiselev O I, Salakhutdinov N F. Eur. J. Med. Chem. 2015;105:263–273. doi: 10.1016/j.ejmech.2015.10.010. [DOI] [PubMed] [Google Scholar]
  • 42.Crielaard B J, Van Der Wal S, Le H T, Bode A T L, Lammers T, Hennink W E, Schiffelers R M, Fens M H A M, Storm G. Eur. J. Pharm. Sci. 2012;45:429–435. doi: 10.1016/j.ejps.2011.08.027. [DOI] [PubMed] [Google Scholar]
  • 43.Malysheva Y B, Combes S, Allegro D, Peyrot V, Knochel P, Gavryushin A E, Fedorov A Y. Bioorg. Med. Chem. 2012;20:4271–4278. doi: 10.1016/j.bmc.2012.05.072. [DOI] [PubMed] [Google Scholar]
  • 44.Günther S, Reinke P Y A, Fernández-García Y, Lieske J, Lane T J, Ginn H M, Koua F H M, Ehrt C, Ewert W, Oberthuer D, Yefanov O, Meier S, Lorenzen K, Krichel B, Kopicki J-D, Gelisio L, Brehm W, Dunkel I, Seychell B, Gieseler H, Norton-Baker B, Escudero-Pérez B, Domaracky M, Saouane S, Tolstikova A, White T A, Hänle A, Groessler M, Fleckenstein H, Trost F, Galchenkova M, Gevorkov Y, Li C, Awel S, Peck A, Barthelmess M, Schlünzen F, Lourdu Xavier P, Werner N, Andaleeb H, Ullah N, Falke S, Srinivasan V, França B A, Schwinzer M, Brognaro H, Rogers C, Melo D, Zaitseva-Doyle J J, Knoska J, Peña-Murillo G E, Mashhour A R, Hennicke V, Fischer P, Hakanpää J, Meyer J, Gribbon P, Ellinger B, Kuzikov M, Wolf M, Beccari A R, Bourenkov G, von Stetten D, Pompidor G, Bento I, Panneerselvam S, Karpics I, Schneider T R, Garcia-Alai M M, Niebling S, Günther C, Schmidt C, Schubert R, Han H, Boger J, Monteiro D C F, Zhang L, Sun X, Pletzer-Zelgert J, Wollenhaupt J, Feiler C G, Weiss M S, Schulz E-C, Mehrabi P, Karničar K, Usenik A, Loboda J, Tidow H, Chari A, Hilgenfeld R, Uetrecht C, Cox R, Zaliani A, Beck T, Rarey M, Günther S, Turk D, Hinrichs W, Chapman H N, Pearson A R, Betzel C, Meents A. Science. 2021;372:642–646. doi: 10.1126/science.abf7945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Drayman N, DeMarco J K, Jones K A, Azizi S-A, Froggatt H M, Tan K, Maltseva N I, Chen S, Nicolaescu V, Dvorkin S, Furlong K, Kathayat R S, Firpo M R, Mastrodomenico V, Bruce E A, Schmidt M M, Jedrzejczak R, Muñoz-Alía M Á, Schuster B, Nair V, Han K, O’Brien A, Tomatsidou A, Meyer B, Vignuzzi M, Missiakas D, Botten J W, Brooke C B, Lee H, Baker S C, Mounce B C, Heaton N S, Severson W E, Palmer K E, Dickinson B C, Joachimiak A, Randall G, Tay S. Science. 2021;373:931–936. doi: 10.1126/science.abg5827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Clyde A, Galanie S, Kneller D W, Ma H, Babuji Y, Blaiszik B, Brace A, Brettin T, Chard K, Chard R, Coates L, Foster I, Hauner D, Kertesz V, Kumar N, Lee H, Li Z, Merzky A, Schmidt J G, Tan L, Titov M, Trifan A, Turilli M, Van Dam H, Chennubhotla S C, Jha S, Kovalevsky A, Ramanathan A, Head M S, Stevens R. J. Chem. Inf. Model. 2022;62:116–128. doi: 10.1021/acs.jcim.1c00851. [DOI] [PubMed] [Google Scholar]
  • 47.Lockbaum G J, Reyes A C, Lee J M, Tilvawala R, Nalivaika E A, Ali A, Kurt Yilmaz N, Thompson P R, Schiffer C A. Viruses. 2021;13:174. doi: 10.3390/v13020174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Zhang C-H, Stone E A, Deshmukh M, Ippolito J A, Ghahremanpour M M, Tirado-Rives J, Spasov K A, Zhang S, Takeo Y, Kudalkar S N, Liang Z, Isaacs F, Lindenbach B, Miller S J, Anderson K S, Jorgensen W L. ACS Cent. Sci. 2021;7:467–475. doi: 10.1021/acscentsci.1c00039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Christensen A S, Kubař T, Cui Q, Elstner M. Chem. Rev. 2016;116:5301–5337. doi: 10.1021/acs.chemrev.5b00584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Adeniyi A A, Soliman M E S. Drug Discovery Today. 2017;22:1216–1223. doi: 10.1016/j.drudis.2017.06.012. [DOI] [PubMed] [Google Scholar]
  • 51.Shcherbakov D, Baev D, Kalinin M, Dalinger A, Chirkova V, Belenkaya S, Khvostov A, Krut’ko D, Medved’ko A, Volosnikova E, Sharlaeva E, Shanshin D, Tolstikova T, Yarovaya O, Maksyutov R, Salakhutdinov N, Vatsadze S. ACS Med. Chem. Lett. 2022;13:140–147. doi: 10.1021/acsmedchemlett.1c00299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Ma C, Hu Y, Townsend J A, Lagarias P I, Marty M T, Kolocouris A, Wang J. ACS Pharmacol. Transl. Sci. 2020;3:1265–1277. doi: 10.1021/acsptsci.0c00130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Schrodinger Small Molecule Drug Discovery Suite, Schrodinger, LLC, New York, NY, USA, 2017.
  • 54.Harder E, Damm W, Maple J, Wu C, Reboul M, Xiang J Y, Wang L, Lupyan D, Dahlgren M K, Knight J L, Kaus J W, Cerutti D S, Krilov G, Jorgensen W L, Abel R, Friesner R A. J. Chem. Theory Comput. 2016;12:281–296. doi: 10.1021/acs.jctc.5b00864. [DOI] [PubMed] [Google Scholar]
  • 55.Friesner R A, Murphy R B, Repasky M P, Frye L L, Greenwood J R, Halgren T A, Sanschagrin P C, Mainz D T. J. Med. Chem. 2006;49:6177–6196. doi: 10.1021/jm051256o. [DOI] [PubMed] [Google Scholar]
  • 56.Sherman W, Day T, Jacobson M P, Friesner R A, Farid R. J. Med. Chem. 2006;49:534–553. doi: 10.1021/jm050540c. [DOI] [PubMed] [Google Scholar]
  • 57.Genheden S, Ryde U. Expert Opin. Drug Discovery. 2015;10:449–461. doi: 10.1517/17460441.2015.1032936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Jacobson M P, Pincus D L, Rapp C S, Day T J F, Honig B, Shaw D E, Friesner R A. Proteins: Struct., Funct., Bioinf. 2004;55:351–367. doi: 10.1002/prot.10613. [DOI] [PubMed] [Google Scholar]
  • 59.Hockney R W, Goel S P, Eastwood J W. J. Comput. Phys. 1974;14:148–158. doi: 10.1016/0021-9991(74)90010-2. [DOI] [Google Scholar]
  • 60.J. J. Stewart, MOPAC 2016, 2016.
  • 61.A. Klamt, G. Schüürmann, J. Chem. Soc., Perkin Trans. 2, 1993, 799–805; DOI: 10.1039/P29930000799.
  • 62.Řezáč J, Hobza P. J. Chem. Theory Comput. 2012;8:141–151. doi: 10.1021/ct200751e. [DOI] [PubMed] [Google Scholar]
  • 63.Phillips J C, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel R D, Kalé L, Schulten K. J. Comput. Chem. 2005;26:1781–1802. doi: 10.1002/jcc.20289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Zoete V, Cuendet M A, Grosdidier A, Michielin O. J. Comput. Chem. 2011;32:2359–2368. doi: 10.1002/jcc.21816. [DOI] [PubMed] [Google Scholar]
  • 65.MacKerell A D, Bashford D, Bellott M, Dunbrack R L, Evanseck J D, Field M J, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau F T K, Mattos C, Michnick S, Ngo T, Nguyen D T, Prodhom B, Reiher W E, Roux B, Schlenkrich M, Smith J C, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M. J. Phys. Chem. B. 1998;102:3586–3616. doi: 10.1021/jp973084f. [DOI] [PubMed] [Google Scholar]
  • 66.Humphrey W, Dalke A, Schulten K. J. Mol. Graph. 1996;14:33–38. doi: 10.1016/0263-7855(96)00018-5. [DOI] [PubMed] [Google Scholar]
  • 67.Attouch H, Cominetti R. J. Differ. Equ. 1996;128:519–540. doi: 10.1006/jdeq.1996.0104. [DOI] [Google Scholar]
  • 68.Pedretti A, Mazzolari A, Gervasoni S, Fumagalli L, Vistoli G. Bioinformatics. 2021;37:1174–1175. doi: 10.1093/bioinformatics/btaa774. [DOI] [PubMed] [Google Scholar]

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