Review
Use of Integrated Computational Approaches in the Search for New Therapeutic Agents
Marco Persico,
Antonio Di Dato,
Nausicaa Orteca,
Paola Cimino,
Ettore Novellino,
Caterina Fattorusso,
Marco Persico
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorAntonio Di Dato
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorNausicaa Orteca
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorPaola Cimino
Department of Pharmacy, University of Salerno, Via Giovanni Paolo II 132, 84084 Fisciano, Salerno, Italy
Search for more papers by this authorEttore Novellino
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Search for more papers by this authorCorresponding Author
Caterina Fattorusso
- [email protected]
- /fax:+39081678544/+39081678552
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorMarco Persico,
Antonio Di Dato,
Nausicaa Orteca,
Paola Cimino,
Ettore Novellino,
Caterina Fattorusso,
Marco Persico
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorAntonio Di Dato
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorNausicaa Orteca
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorPaola Cimino
Department of Pharmacy, University of Salerno, Via Giovanni Paolo II 132, 84084 Fisciano, Salerno, Italy
Search for more papers by this authorEttore Novellino
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Search for more papers by this authorCorresponding Author
Caterina Fattorusso
- [email protected]
- /fax:+39081678544/+39081678552
Department of Pharmacy, University of Naples “Federico II”, Via D. Montesano 49, 80131 Napoli, Italy
Italian Malaria Network – Centro Interuniversitario di Ricerche Sulla Malaria (CIRM), Department of Experimental Medicine and Biochemical Sciences, Via Del Giochetto, 06126 Perugia, Italy
Search for more papers by this authorGraphical Abstract
Abstract
Computer-aided drug discovery plays a strategic role in the development of new potential therapeutic agents. Nevertheless, the modeling of biological systems still represents a challenge for computational chemists and at present a single computational method able to face such challenge is not available. This prompted us, as computational medicinal chemists, to develop in-house methodologies by mixing various bioinformatics and computational tools. Importantly, thanks to multi-disciplinary collaborations, our computational studies were integrated and validated by experimental data in an iterative process. In this review, we describe some recent applications of such integrated approaches and how they were successfully applied in i) the search of new allosteric inhibitors of protein-protein interactions and ii) the development of new redox-active antimalarials from natural leads.
References
- 1G. Sliwoski, S. Kothiwale, J. Meiler, E. W. Lowe Jr., Pharmacol. Rev. 2014, 66, 334–395.
- 2C. Liao, M. Sitzmann, A. Pugliese, M. C. Nicklaus, Future Med. Chem. 2011, 3, 1057–1085.
- 3V. I. Pérez-Nueno, D. W. Ritchie, O. Rabal, R. Pascual, J. I. Borrell, J. Teixidó, J. Chem. Inf. Model. 2008, 48, 509–533.
- 4E. Callaway, Nature 2015, 525, 172–174.
- 5A. R. Leach, H. Jhoti, in Structure-based Drug Discovery, Springer, Berlin 2007.
10.1007/1-4020-4407-0_3 Google Scholar
- 6C. H. Lee, H. C. Huang, H. F. Juan, Int. J. Mol. Sci. 2011, 12, 5304–5318.
- 7B. O. Villoutreix, D. Lagorce, C. M. Labbé, O. Sperandio, M. A. Miteva, Drug Discov. Today 2013, 18, 1081–1089.
- 8G. L. Wilson, M. A. Lill, Future Med. Chem. 2011, 3, 735–750.
- 9B. Kuhn, W. Guba, J. Hert, D. Banner, C. Bissantz, S. Ceccarelli, W. Haap, M. Körner, A. Kuglstatter, C. Lerner, P. Mattei, W. Neidhart, E. Pinard, M. G. Rudolph, T. Schulz-Gasch, T. Woltering, M. Stahl, J. Med. Chem. 2016, 59, 4087–4102.
- 10B. K. Allen, S. Mehta, S. W. Ember, E. Schonbrunn, N. Ayad, S. C. Schürer, Sci. Rep. 2015, 5, 16924.
- 11C. H. Reynolds, Curr. Pharm. Des. 2014, 20, 3380–3386.
- 12T. T. Talele, S. A. Khedkar, A. C. Rigby, Curr. Top. Med. Chem. 2010, 10, 127–141.
- 13J. Michel, Phys. Chem. Chem. Phys. 2014, 16, 4465–4477.
- 14L. Wang, Y. Wu, Y. Deng, B. Kim, L. Pierce, G. Krilov, D. Lupyan, S. Robinson, M. K. Dahlgren, J. Greenwood, D. L. Romero, C. Masse, J. L. Knight, T. Steinbrecher, T. Beuming, W. Damm, E. Harder, W. Sherman, M. Brewer, R. Wester, M. Murcko, L. Frye, R. Farid, T. Lin, D. L. Mobley, W. L. Jorgensen, B. J. Berne, R. A. Friesner, R. Abel, J. Am. Chem. Soc. 2015, 137, 2695–2703.
- 15C. Ferlini, L. Cicchillitti, G. Raspaglio, S. Bartollino, S. Cimitan, C. Bertucci, S. Mozzetti, D. Gallo, M. Persico, C. Fattorusso, G. Campiani, G. Scambia, Cancer. Res. 2009, 69, 6906–6914.
- 16A. Camperchioli, M. Mariani, S. Bartollino, L. Petrella, M. Persico, N. Orteca, G. Scambia, S. Shahabi, C. Ferlini, C. Fattorusso, Biochim. Biophys. Acta 2011, 1813, 850–857.
- 17M. Andreoli, M. Persico, A. Kumar, N. Orteca, V. Kumar, A. Pepe, S. Mahalingam, A. E. Alegria, L. Petrella, L. Sevciunaite, A. Camperchioli, M. Mariani, A. Di Dato, E. Novellino, G. Scambia, S. V. Malhotra, C. Ferlini, C. Fattorusso, J. Med. Chem. 2014, 57, 7916–7932.
- 18M. Persico, L. Petrella, N. Orteca, A. Di Dato, M. Mariani, M. Andreoli, M. De Donato, G. Scambia, E. Novellino, C. Ferlini, C. Fattorusso, Eur. J. Med. Chem. 2015, 91, 132–144.
- 19C. Fattorusso, G. Campiani, B. Catalanotti, M. Persico, N. Basilico, S. Parapini, D. Taramelli, C. Campagnuolo, E. Fattorusso, A. Romano, O. Taglialatela-Scafati, J. Med. Chem. 2006, 49, 7088–7094.
- 20O. Taglialatela-Scafati, E. Fattorusso, A. Romano, F. Scala, V. Barone, P. Cimino, E. Stendardo, B. Catalanotti, M. Persico, C. Fattorusso, Org. Biomol. Chem. 2010, 8, 846–856.
- 21C. Fattorusso, M. Persico, B. Calcinai, C. Cerrano, S. Parapini, D. Taramelli, E. Novellino, A. Romano, F. Scala, E. Fattorusso, O. Taglialatela-Scafati, J. Nat. Prod. 2010, 73, 1138–1145.
- 22M. Persico, A. Quintavalla, F. Rondinelli, C. Trombini, M. Lombardo, C. Fattorusso, V. Azzarito, D. Taramelli, S. Parapini, Y. Corbett, G. Chianese, E. Fattorusso, O. Taglialatela-Scafati, J. Med. Chem. 2011, 54, 8526–8540.
- 23C. Fattorusso, M. Persico, N. Basilico, D. Taramelli, E. Fattorusso, F. Scala, O. Taglialatela-Scafati, Bioorg. Med. Chem. 2011, 19, 312–320.
- 24M. Persico, S. Parapini, G. Chianese, C. Fattorusso, M. Lombardo, L. Petrizza, A. Quintavalla, F. Rondinelli, N. Basilico, D. Taramelli, C. Trombini, E. Fattorusso, O. Taglialatela-Scafati, Eur. J. Med. Chem. 2013, 70, 875–886.
- 25G. Chianese, M. Persico, F. Yang, H. W. Lin, Y. W. Guo, N. Basilico, S. Parapini, D. Taramelli, O. Taglialatela-Scafati, C. Fattorusso, Bioorg. Med. Chem. 2014, 22, 4572–4580.
- 26M. Lombardo, D. P. Sonawane, A. Quintavalla, C. Trombini, D. D. Dhavale, D. Taramelli, Y. Corbett, F. Rondinelli, C. Fattorusso, M. Persico, O. Taglialatela-Scafati, Eur. J. Org. Chem. 2014, 2014, 1607–1614.
- 27O. A. Skorokhod, D. Davalos-Schafler, V. Gallo, E. Valente, D. Ulliers, A. Notarpietro, G. Mandili, F. Novelli, M. Persico, O. Taglialatela-Scafati, P. Arese, E. Schwarzer Free Radic Biol Med. 2015, 89, 624–637.
- 28D. P. Sonawane, M. Persico, Y. Corbett, G. Chianese, A. Di Dato, C. Fattorusso, O. Taglialatela-Scafati, D. Taramelli, C. Trombini, D. D. Dhavale, A. Quintavalla, M. Lombardo, RSC Adv. 2015, 5, 72995–73010.
- 29C. Imperatore, M. Persico, A. Aiello, P. Luciano, M. Guiso, M. F. Sanasi, D. Taramelli, S. Parapini, G. Cebrián-Torrejón, A. Doménech-Carbó, C. Fattorusso, M. Menna, RSC Adv., 2015, 5, 70689–70702.
- 30H. M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, P. E. Bourne, Nucleic Acids Res. 2000, 28, 235–242.
- 31J. A. Marsh, S. A. Teichmann, J. D. Forman-Kay, Curr. Opin. Struct. Biol. 2012, 22, 643–650.
- 32A. Mittermaier, L. E. Kay, Science 2006, 312, 224–228.
- 33J. L. Klepeis, K. Lindorff-Larsen, R. O. Dror, D. E. Shaw, Curr Opin. Struct. Biol. 2009, 19, 120–127.
- 34M. A. Rohrdanz, W. Zheng, C. Clementi, Ann. Rev. Phys. Chem. 2013, 64, 295–316.
- 35D. Li, M. S. Liu, B. Ji, K. Hwang, Y. Huang, J. Chem. Phys. 2009, 130, 215102.
- 36Y. Matsunaga, H. Fujisaki, T. Terada, T. Furuta, K. Moritsugu, PLoS Comput. Biol. 2012, 8, e 1002555.
- 37P. L. Freddolino, C. B. Harrison, Y. Liu, K. Schulten, Nat. Phys. 2010, 6, 751–758.
- 38N. P. Schafer, B. L. Kim, W. Zheng, P. G. Wolynes, Israel J. Chem. 2014, 54, 1311–1337.
- 39A. J. Campbell, M. L. Lamb, D. Joseph-McCarthy, J. Chem. Inf. Model. 2014, 54, 2127–2138.
- 40I. A. Hubner, E. J. Deeds, E. I. Shakhnovich, Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 17747–17752.
- 41P. I. Zhuravlev, G. A. Papoian, Q. Rev. Biophys. 2010, 43, 295–332.
- 42F. Zeller, M. Zacharias, Biophys J. 2015, 109, 1978–1985.
- 43Y. Sugita, Y. Okamoto, Chem. Phys. Lett. 1999, 314, 141–151.
- 44A. Laio, M. Parrinello, Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12562–12566.
- 45A. Cavalli, A. Spitaleri, G. Saladino, F. L. Gervasio, Acc. Chem. Res. 2015, 48, 277–285.
- 46C. Tsallis, D. A. Stariolob, Physica A 1996, 233, 395–406.
- 47H. Fujisaki, K. Moritsugu, Y. Matsunaga, T. Morishita, L. Maragliano, Front. Bioeng. Biotechnol. 2015, 3, 125.
- 48M. R. Shirts, J. D. Chodera, J. Chem. Phys. 2008, 129, 124105.
- 49R. C. Bernardi, M. C. Melo, K. Schulten, Biochim. Biophys. Acta. 2015, 1850, 872–877..
- 50A. C. Pan, T. M. Weinreich, S. Piana, D. E. Shaw, J. Chem. Theory Comput. 2016, 12, 1360–1367.
- 51P. Liu, B. Kim, R. A. Friesner, B. J. Berne, Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 13749–13754.
- 52D. R. Roe, C. Bergonzo, T. E. Cheatham 3rd, J. Phys. Chem. B. 2014, 118, 3543–3552.
- 53Z. Huang, C. F. Wong, R. A. Wheeler, Proteins 2008, 71, 440–454.
- 54M. C. Melo, R. C. Bernardi, T. V. Fernandes, P. G. Pascutti, Proteins 2012, 80, 2305–2310.
- 55S. Kannan, M. Zacharias, J. Struct. Biol. 2009, 166, 288–294.
- 56D. A. Antunes, D. Devaurs, L. E. Kavraki, Expert Opin. Drug Discov. 2015, 28, 1–13.
- 57N. Deschamps, C. A. Simões-Pires, P. A. Carrupt, A. Nurisso, Drug Discov. Today 2015, 20, 736–742.
- 58O. F. Lange, N. A. Lakomek, C. Farès, G. F. Schröder, K. F. Walter, S. Becker, J. Meiler, H. Grubmüller, C. Griesinger, B. L. de Groot, Science 2008, 320, 1471–1475.
- 59D. E. Koshland, Angew. Chem. Int. Ed. 1994, 33, 2375–2378.
- 60D. D. Boehr, P. E. Wright, Science 2008, 320, 1429–1430.
- 61
- 61aH. Dinkel, K. Van Roey, S. Michael, N. E. Davey, R. J. Weatheritt, D. Born, T. Speck, D. Krüger, G. Grebnev, M. Kuban, M. Strumillo, B. Uyar, A. Budd, B. Altenberg, M. Seiler, L. B. Chemes, J. Glavina, I. E. Sánchez, F. Diella, T. J. Gibson, Acids Res. 2014, 42, D 259–D266;
- 61bK. Van Roey, H. Dinkel, R. J. Gibson, T. J. Weatheritt, N. E. Davey, Sci. Signal. 2013, 6, rs 7.
10.1126/scisignal.6301er7 Google Scholar
- 62V. Neduva, R. B. Russell, FEBS Lett., 2005, 579, 3342–3345.
- 63G. B. Cohen, R. Ren, D. Baltimore, Cell 1995, 80, 237–248.
- 64M. Persico, A. Di Dato, N. Orteca, C. Fattorusso, E. Novellino, M. Andreoli, C. Ferlini, Curr. Top. Med. Chem. 2015, 15, 2019–2031.
- 65S. Butini, G. Campiani, M. Borriello, S. Gemma, A. Panico, M. Persico, B. Catalanotti, S. Ros, M. Brindisi, M. Agnusdei, I. Fiorini, V. Nacci, E. Novellino, T. Belinskaya, A. Saxena, C. Fattorusso, J. Med. Chem. 2008, 51, 3154–3170.
- 66C. B. Botta, W. Cabri, E. Cini, L. De Cesare, C. Fattorusso, G. Giannini, M. Persico, A. Petrella, F. Rondinelli, M. Rodriquez, A. Russo, M. Taddei, J. Med. Chem. 2011, 54, 2165–2182.
- 67A. M. Santoro, A. Cunsolo, A. D’ Urso, D. Sbardella, G. R. Tundo, C. Ciaccio, M. Coletta, D. Diana, R. Fattorusso, M. Persico, A. Di Dato, C. Fattorusso, D. Milardi, R. Purrello, Chem. Sci. 2016, 7, 1286–1297.
- 68J. Pei, B. H. Kim, N. V. Grishin, Nucleic Acids Res. 2008, 36, 2295–2300.
- 69H. Senderowitz, F. Guarnieri, W. C. Still, J. Am. Chem. Soc. 1995, 117, 8211–8219..
- 70M. E. Tuckerman, G. J. Martyna, J. Phys. Chem. B. 2000, 104, 159–178.
- 71H. Q. Ding, N. Karasawa, W. A. Goddard, J. Chem. Phys. 1992, 97, 4309–4315.
- 72R. A. Laskowski, M. W. MacArthur, D. S. Moss, J. M Thornton, J. Appl. Crystallogr. 1993, 26, 283–291..
- 73I. W. Davis, A. Leaver-Fay, V. B. Chen, J. N. Block, G. J. Kapral, X. Wang, L.W. Murray, W. B. Arendall, J. Snoeyink, J.S. Richardson, D. C. Richardson, Nucl. Acids Res., 2007, 35, W 375–W383.
- 74G. Raspaglio, F. Filippetti, S. Prislei, R. Penci, I. De Maria, L. Cicchillitti, S. Mozzetti, G. Scambia, C. Ferlini, Gene 2008, 409, 100–108.
- 75C. Ferlini, G. Raspaglio, L. Cicchillitti, S. Mozzetti, S. Prislei, S. Bartollino, G. Scambia, Curr. Cancer Drug Targets 2007, 7, 704–712.
- 76P. Seve, C. Dumontet, Lancet Oncol. 2008, 9, 168–175.
- 77M. Mariani, S. Shahabi, S. Sieber, G. Scambia, C. Ferlini, Curr. Mol. Med. 2011, 11, 726–731.
- 78M. De Donato, M. Mariani, L. Petrella, E. Martinelli, G. F. Zannoni, V. Vellone, G. Ferrandina, S. Shahabi, G. Scambia, C. Ferlini, J. Cell. Physiol. 2012, 227, 1034–1041.
- 79C. D. Katsetos, P. Draber, Curr. Pharm. Des. 2012, 18, 2778–2792.
- 80A. Ghosh, G. J. K. Praefcke, L. Renault, A. Wittinghofer, C. Herrmann, Nature 2006, 440, 101–104.
- 81B. Prakash, L. Renault, G. J. K. Praefcke, C. Herrmann, A. Wittinghofer, Embo J. 2000, 19, 4555–4564.
- 82B. Prakash, G. J. K. Praefcke, L. Renault, A. Wittinghofer, C. Herrmann, Nature 2000, 403, 567–571.
- 83G. J. Praefcke, H. T. McMahon, Nat. Rev. Mol. Cell Biol. 2004, 5, 133–147.
- 84T. Vöpel, A. Syguda, N. Britzen-Laurent, S. Kunzelmann, M. B. Lüdemann, C. Dovengerds, M. Stürzl, C. Herrmann, J. Mol. Biol. 2010, 400, 63–70.
- 85A. Syguda, M. Bauer, U. Benscheid, N. Ostler, E. Naschberger, S. Ince, M. Sturzl, C. Herrmann, FEBS J. 2012, 279, 2544–2554.
- 86T. Vöpel, S. Kunzelmann, C. Herrmann, FEBS Lett. 2009, 583, 1923–1927.
- 87B. Prakash, N. Abdullah, B. Srinivasan, N. Modiano, P. Cresswell, A. K. Sau, Mol. Biol. 2009, 386, 690–703.
- 88G. T. Wondrak, Antioxid. Redox Signal. 2009, 11, 3013–3069.
- 89M. Goyal, A. Alam, U. Bandyopadhyay, Curr. Med. Chem. 2012, 19, 1475–1503.
- 90
- 90aM. H. Baik, R. A. Friesner, J. Phys. Chem. A 2002, 106, 7407–7412;
- 90bR. L. Donkers, M. S. Workentin, J. Phys. Chem. B 1998, 102, 4061–4063;
- 90cL. Johann, D. A. Lanfranchi, E. Davioud-Charvet, M. Elhabiri, Curr. Pharm. Des. 2012, 18, 3539–3566.
- 91W. Czechtizky, P. Hamley, in Small Molecule Medicinal Chemistry: Strategies and Technologies, Wiley, Hoboken 2015.
- 92K. A. Brameld, B. Kuhn, D. C. Reuter, M. Stahl, J. Chem. Inf. Model. 2008, 48, 1–24.
- 93J. D. Dunitz, H.B. Burgi, in Structure Correlation, VCH, Weinheim, 1994.
- 94A. R. Leach, in Reviews in Computational Chemistry, Vol. 2, (Eds: ), VCH, New York 1991, pp. 1–55.
10.1002/9780470125793.ch1 Google Scholar
- 95D. K. Agrafiotis, A. C. Gibbs, F. Zhu, S. Izrailev, E. Martin, J. Chem. Inf. Model. 2007, 47, 1067–1086..
- 96
- 96aJ. J. Stewart, J. Mol. Model. 2013, 19, 1–32;
- 96bJ. P. Stewart, MOPAC2012; Computational Chemistry: Colorado Springs, CO, 2012; http://OpenMOPAC.net.
- 97J. Baker, J. Comput. Chem. 1986, 7, 385–395.
- 98M. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G. A. Petersson, H. Nakatsuji, M. Caricato, X. Li, H. P. Hratchian, A. F. Izmaylov, J. Bloino, G. Zheng, J. L. Sonnenberg, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, J. A. Montgomery Jr., J. E. Peralta, F. Ogliaro, M. Bearpark, J. J. Heyd, E. Brothers, K. N. Kudin, V. N. Staroverov, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J. C. Burant, S. S. Iyengar, J. Tomasi, M. Cossi, N. Rega, N. J. Millam, M. Klene, J. E. Knox, J. B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, R. L. Martin, K. Morokuma, V. G. Zakrzewski, G. A. Voth, P. Salvador, J. J. Dannenberg, S. Dapprich, A. D. Daniels, Ö. Farkas, J. B. Foresman, J. V. Ortiz, J. Cioslowski, D. J. Fox, Gaussian 09, Gaussian, Inc., Wallingford, 2009.
- 99A. D. Becke, J. Chem. Phys. 1993, 98, 5648–5652.
- 100C. Lee, W. Yang, R. G. Parr, Phys. Rev. 1988, B37, 785–789.
- 101
- 101aF. Lipparini, B. Mennucci, J. Chem. Phys. 2016, 144, 160901;
- 101bM. Cossi, G. Scalmani, N. Rega, V. Barone, J. Chem. Phys. 2002, 117, 43–54;
- 101cG. Scalmani, V. Barone, K. N. Kudin, C. S. Pomelli, G. E. Scuseria, M. Frisch, J. Theor. Chem. Acc. 2004, 111, 90–100.
- 102S. Chiodo, N. Russo, E. Sicilia, J. Comput. Chem. 2005, 26, 175–183.
- 103G. R. Marshall, C. D. Barry, H. E. Bosshard, R. A. Dammkoehler, D. A. Dunn In The Conformational Parameter in Drug Design: the Active Analog Approach. In Computer-Assisted Drug Desig, vol. 112, (Eds: ), American Chemical Society, 1979, pp. 205–225.
10.1021/bk-1979-0112.ch009 Google Scholar
- 104M. Persico, A. Ramunno, V. Maglio, S. Franceschelli, C. Esposito, A. Carotenuto, D. Brancaccio, V. De Pasquale, L. M. Pavone, M. Varra, N. Orteca, E. Novellino, C. Fattorusso, J. Med. Chem. 2013, 56, 6666–6680..
- 105E. Pavadai, F. El Mazouni, S. Wittlin, C. de Kock, M. A. Phillips, K. Chibale, J. Chem. Inf. Model. 2016, 56, 548–562..
- 106E. Bolton, Y. Wang, P. A. Thiessen, S. H. Bryant, in Annual Reports in Computational Chemistry, Vol. 4 (Eds: ), American Chemical Society, Washington, DC 2008, pp. 217–241.
- 107Y. Wang, J. Xiao, T. O. Suzek, J. Zhang, J. Wang, Z. Zhou, L. Han, K. Karapetyan, S. Dracheva, B. A. Shoemaker, E. Bolton, A. Gindulyte, S. H. Bryant, Nucleic Acids Res. 2012, 40, D 400–D412.
- 108WHO, World Malaria Report 2015, ISBN: 978 92 4 156515 8
- 109R. Arav-Boger, T. A. Shapiro, Annu. Rev. Pharmacol. Toxicol. 2005, 45, 565–585.
- 110M. Goyal, A. Alam, U. Bandyopadhyay, Curr. Med. Chem. 2012, 19, 1475–1503.
- 111F. Nepveu, F. Turrini, Future Med. Chem. 2013, 5, 1993–2006.
- 112J. Wang, C. J. Zhang, W. N. Chia, C. C. Loh, Z. Li, Y. M. Lee, Y. He, L. X. Yuan, T. K. Lim, M. Liu, C. X. Liew, Y. Q. Lee, J. Zhang, N. Lu, C. T. Lim, Z. C. Hua, B. Liu, H. M. Shen, K. S. Tan, Q. Lin, Nat. Commun. 2015, 6, 10111.
- 113D. K. Ro, E. M. Paradise, M. Ouellet, K. J. Fisher, K. L. Newman, J. M. Ndungu, K. A. Ho, R. A. Eachus, T. S. Ham, J. Kirby, M. C. Chang, S. T. Withers, Y. Shiba, R. Sarpong, J. D. Keasling, Nature 2006, 440, 940–943.
- 114Q. Li, M. Hickman, Toxicology 2011, 279, 1–9.
- 115A. M. Dondorp, S. Yeung, L. White, C. Nguon, N. P. J. Day, D. Socheat, L. von Seidlein, Nat. Rev. Microbiol. 2010, 8, 272–280.
- 116Y. Tang, Y. Dong, J. L. Vennerstrom, Med. Res. Rev. 2004, 24, 425–448.
- 117F. Cafieri, E. Fattorusso, O. Taglialatela-Scafati A. Ianaro, Tetrahedron 1999, 55, 7045–7056.
- 118E. Fattorusso, S. Parapini, C. Campagnuolo, N. Basilico, O. Taglialatela-Scafati, D. Taramelli, J. Antimicrob. Chemother. 2002, 50, 883–888.
- 119C. Campagnuolo, E. Fattorusso, A. Romano, O. Taglialatela-Scafati, N. Basilico, S. Parapini, D. Taramelli, Eur. J. Org. Chem. 2005, 23, 5077–5083.
- 120ANTIMAL project – EU contract LSHP-CT-2005-018834, 2005.
- 121C. W. Jefford, Curr. Med. Chem. 2001, 15, 1803–1826.
10.2174/0929867013371608 Google Scholar
- 122C. W. Jefford, Drug Discov. Today 2007, 12, 487–495.
- 123A. Robert, F. Benoit-Vical, O. Dechy-Cabaret, B. Meunier, Pure Appl. Chem. 2001, 73, 1173–1188..
- 124M. A. Clark, M. M. Goheen, C. Cerami, Front. Pharmacol. 2014, 5, 84.
- 125R. K. Haynes, S. C. Vonwiller, Tetrahedron Lett. 1996, 37, 257–260.
- 126C. Magri, R. L. Donkers, M. S. Workentin, J. Photochem. Photobiol. A. Chem. 2001, 138, 29–34.
- 127E. L. Dodd, D. S. Bohle, Chem. Commun. 2014, 50, 13765–13768.
- 128H. C. Ha, N. S. Sirisoma, P. Kuppusamy, J. L. Zweier, P. M. Woster, R. A. Casero Jr., Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 11140–11145.
- 129
- 129aK. C. Das, H. P. Misra, Mol. Cell. Biochem. 2004, 262, 127–133;
- 129bY. Maeda, K. U. Ingold, J. Am. Chem. Soc. 1980, 102, 328–331;
- 129cD. Griller, J. A. Howard, P. R. Marriott, J. C. Scaiano, J. Am. Chem. Soc. 1981, 103, 619–623;
- 129dJ. M. Tanko, R. Friedline, N. K. Suleman, N. Castagnoli Jr., J. Am. Chem. Soc. 2001, 123, 5808–5809;
- 129eU. Pischel, W. M. Nau, J. Am. Chem. Soc. 2001, 123, 9727–9737.
Citing Literature
