Quinolin-4(1 H)-imines are potent antiplasmodial drugs targeting the liver stage of malaria

Journal of Medicinal Chemistry

Volumn 56, Issue 11, 2013, Pages 4811-4815

  Rodrigues, Tiago ^a,b   Da Cruz, Filipa P ^c   Lafuente Monasterio, Maria J ^d   Gonçalves, Daniel ^a   Ressurreição, Ana S ^a   Sitoe, Ana R ^a   Bronze, Maria R ^a   Gut, Jiri ^e   Schneider, Gisbert ^b   Mota, Maria M ^c   Rosenthal, Philip J ^e   Prudeîncio, Miguel ^c   Gamo, Francisco Javier ^d   Lopes, Francisca ^a   Moreira, Rui ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF LISBON   (Portugal)

^d GLAXOSMITHKLINE   (Spain)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; IMINE; QUINOLINE DERIVATIVE;

ARTICLE; IC 50; IN VITRO STUDY; MALARIA; NONHUMAN; PLASMODIUM; CHEMISTRY; DRUG EFFECT; DRUG SENSITIVITY; HUMAN; LIVER; PARASITOLOGY; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; STRUCTURE ACTIVITY RELATION; SYNTHESIS; TUMOR CELL LINE;

ANTIMALARIALS; CELL LINE, TUMOR; HUMANS; IMINES; LIVER; MALARIA; PARASITIC SENSITIVITY TESTS; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; QUINOLINES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84879038195     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm400246e     Document Type: Article

References (40)

1. World Malaria Report 2011; World Health Organization: Geneva, 2011.
2. Gamo, F.-J.; Sanz, L. M.; Vidal, J.; de Cozar, C.; Alvarez, E.; Lavandera, J.-L.; Vanderwall, D. E.; Green, D. V. S.; Kumar, V.; Hasan, S.; Brown, J. R.; Peishoff, C. E.; Cardon, L. R.; Garcia-Bustos, J. F. Thousands of chemical starting points for antimalarial lead identification Nature 2010, 465, 305-310
3. Guiguemde, W. A.; Shelat, A. A.; Bouck, D.; Duffy, S.; Crowther, G. J.; Davis, P. H.; Smithson, D. C.; Connelly, M.; Clark, J.; Zhu, F.; Jiménez-Díaz, M. B.; Martinez, M. S.; Wilson, E. B.; Tripathi, A. K.; Gut, J.; Sharlow, E. R.; Bathurst, I.; Mazouni, F. E.; Fowble, J. W.; Forquer, I.; McGinley, P. L.; Castro, S.; Angulo-Barturen, I.; Ferrer, S.; Rosenthal, P. J.; DeRisi, J. L.; Sullivan, D. J.; Lazo, J. S.; Roos, D. S.; Riscoe, M. K.; Phillips, M. A.; Rathod, P. K.; Voorhis, W. C. V.; Avery, V. M.; Guy, R. K. Chemical genetics of Plasmodium falciparum Nature 2010, 465, 311-315
4. The malERA Consultive Group on Drugs. A research agendafor malaria eradication: drugs. PLoS Med. 2011, 8, e1000402.
5. Prudeîncio, M.; Rodriguez, A.; Mota, M. M. The silent path to thousands of merozoites: the Plasmodium liver stage Nature Rev. Microbiol. 2006, 4, 849-856 (Pubitemid 44593951)
6. Rodrigues, T.; Prudeîncio, M.; Moreira, R.; Mota, M. M.; Lopes, F. Targeting the liver stage of malaria parasites: a yet unmet goal J. Med. Chem. 2012, 55, 995-1012
7. Wells, T. N. C.; Burrows, J. N.; Baird, J. K. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination Trends Parasitol. 2010, 26, 145-151
8. Mazier, D.; Rénia, L.; Snounou, G. A pre-emptive strike against malaria's stealthy hepatic forms Nature Rev. Drug Discovery 2009, 8, 854-864
9. Srivastava, P.; Singh, S.; Jain, G. K.; Puri, S. K.; Pandey, V. C. A simple and rapid evaluation of methemoglobin toxicity of 8-aminoquinolines and related compounds Ecotoxicol. Environ. Saf. 2000, 45, 236-239 (Pubitemid 30154585)
10. Hill, D. R.; Baird, J. K.; Parise, M. E.; Lewis, L. S.; Ryan, E. T.; Magill, A. J. Primaquine: report from CDC expert meeting on malaria chemoprophylaxis I Am. J. Trop. Med. Hyg. 2006, 75, 402-415 (Pubitemid 46941297)
11. da Cruz, F. P.; Martin, C.; Buchholz, K.; Lafuente-Monasterio, M. J.; Rodrigues, T.; Sönnichsen, B.; Moreira, R.; Gamo, F.-J.; Marti, M.; Mota, M. M.; Hannus, M.; Prudeîncio, M. Drug screen targeted at plasmodium liver stages identifies a potent multistage antimalarial drug J. Infect. Dis. 2012, 205, 1278-1286
12. Derbyshire, E. R.; Prudeîncio, M.; Mota, M. M.; Clardy, J. Liver-stage malaria parasites vulnerable to diverse chemical scaffolds Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 8511-8516
13. Pérez, B. C.; Teixeira, C.; Albuquerque, I. S.; Gut, J.; Rosenthal, P. J.; Gomes, J. R. B.; Prudeîncio, M.; Gomes, P. N -Cinnamoylated chloroquine analogues as dual-stage antimalarial leads J. Med. Chem. 2013, 56, 556-567
14. Biagini, G. A.; Fisher, N.; Shone, A. E.; Mubaraki, M. A.; Srivastava, A.; Hill, A.; Antoine, T.; Warman, A. J.; Davies, J.; Pidathala, C.; Amewu, R. K.; Leung, S. C.; Sharma, R.; Gibbons, P.; Hong, D. W.; Pacorel, B.; Lawrenson, A. S.; Charoensutthivarakul, S.; Taylor, L.; Berger, O.; Mbekeani, A.; Stocks, P. A.; Nixon, G. L.; Chadwick, J.; Hemingway, J.; Delves, M. J.; Sinden, R. E.; Zeeman, A.-M.; Kocken, C. H. M.; Berry, N. G.; O'Neill, P. M.; Ward, S. A. Generation of quinolone antimalarials targeting the Plasmodium falciparum mitochondrial respiratory chain for the treatment and prophylaxis of malaria Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 8298-8303
15. Zhang, Y.; Clark, J. A.; Connelly, M. C.; Zhu, F.; Min, J.; Guiguemde, W. A.; Pradhan, A.; Iyer, L.; Furimsky, A.; Gow, J.; Parman, T.; Mazouni, F. E.; Phillips, M. A.; Kyle, D. E.; Mirsalis, J.; Guy, R. K. Lead optimization of 3-carboxyl-4(1 H)-quinolones to deliver orally bioavailable antimalarials J. Med. Chem. 2012, 55, 4205-4219
16. LaCrue, A. N.; Sáenz, F. E.; Cross, R. M.; Udenze, K. O.; Monastyrskyi, A.; Stein, S.; Mutka, T. S.; Manetsch, R.; Kyle, D. E. 4(1 H)-Quinolones with liver stage activity against Plasmodium berghei Antimicrob. Agents Chemother. 2013, 57, 417-424
17. Winter, R. W.; Kelly, J. X.; Smilkstein, M. J.; Dodean, R.; Hinrichs, D.; Riscoe, M. K. Antimalarial quinolones: synthesis, potency, and mechanistic studies Exp. Parasitol. 2008, 118, 487-497
18. Cross, R. M.; Monastyrskyi, A.; Mutka, T. S.; Burrows, J. N.; Kyle, D. E.; Manetsch, R. Endochin optimization: structure-activity and structure-property relationship studies of 3-substituted 2-methyl-4(1 H)-quinolones with antimalarial activity J. Med. Chem. 2010, 53, 7076-7094
19. Nilsen, A.; LaCrue, A. N.; White, K. L.; Forquer, I. P.; Cross, R. M.; Marfurt, J.; Mather, M. W.; Delves, M. J.; Shackleford, D. M.; Saenz, F. E.; Morrisey, J. M.; Steuten, J.; Mutka, T.; Li, Y.; Wirjanata, G.; Ryan, E.; Duffy, S.; Kelly, J. X.; Sebayang, B. F.; Zeeman, A.-M.; Noviyanti, R.; Sinden, R. E.; Kocken, C. H. M.; Price, R. N.; Avery, V. M.; Angulo-Barturen, I.; Jiménez-Díaz, M. B.; Ferrer, S.; Herreros, E.; Sanz, L. M.; Gamo, F.-J.; Bathurst, I.; Burrows, J. N.; Siegl, P.; Guy, R. K.; Winter, R. W.; Vaidya, A. B.; Charman, S. A.; Kyle, D. E.; Manetsch, R.; Riscoe, M. K. Quinolone-3-diarylethers: a new class of antimalarial drug Sci. Transl. Med. 2013, 5, 177ra37
20. Derbyshire, E. R.; Mazitschek, R.; Clardy, J. Characterization of plasmodium liver stage inhibition by halofuginone ChemMedChem 2012, 7, 844-849
21. Rodrigues, T.; Guedes, R. C.; dos Santos, D. J. V. A.; Carrasco, M.; Gut, J.; Rosenthal, P. J.; Moreira, R.; Lopes, F. Design, synthesis and structure-activity relationships of (1 H -pyridin-4-ylidene)amines as potential antimalarials Bioorg. Med. Chem. Lett. 2009, 19, 3476-3480
22. Rodrigues, T.; Moreira, R.; Dacunha-Marinho, B.; Lopes, F. Bis{(E)-3[(diethylmethylammonio)methyl]- N -[3-(N, N -dimethylsulfamoyl)-1- methylpyridin-4-ylidene]-4-methoxyanilinium} tetraiodide pentahydrate Acta Crystallogr., Sect. E: Struct. Rep. Online 2009, 65, O283-U1828
23. Lopes, F.; Capela, R.; Gonçalves, J. O.; Horton, P. N.; Hursthouse, M. B.; Iley, J.; Casimiro, C. M.; Bom, J.; Moreira, R. Amidomethylation of amodiaquine: antimalarial N-Mannich base derivatives Tetrahedron Lett. 2004, 45, 7663-7666 (Pubitemid 39243346)
24. Meister, S.; Plouffe, D. M.; Kuhen, K. L.; Bonamy, G. M. C.; Wu, T.; Barnes, S. W.; Bopp, S. E.; Borboa, R.; Bright, A. T.; Che, J.; Cohen, S.; Dharia, N. V.; Gagaring, K.; Gettayacamin, M.; Gordon, P.; Groessl, T.; Kato, N.; Lee, M. C. S.; McNamara, C. W.; Fidock, D. A.; Nagle, A.; Nam, T.-g.; Richmond, W.; Roland, J.; Rottmann, M.; Zhou, B.; Froissard, P.; Glynne, R. J.; Mazier, D.; Sattabongkot, J.; Schultz, P. G.; Tuntland, T.; Walker, J. R.; Zhou, Y.; Chatterjee, A.; Diagana, T. T.; Winzeler, E. A. Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery Science 2011, 334, 1372-1377
25. Hansch, C.; Leo, A.; Taft, R. W. A survey of Hammett substituent constants and resonance and field parameters Chem. Rev. 1991, 91, 165-195
26. Hansch, C.; Leo, A.; Unger, S. H.; Kim, K. H.; Nikaitani, D.; Lien, E. J. Aromatic substituent constants for structure-activity correlations J. Med. Chem. 1973, 16, 1207-1216
27. Yeates, C. L.; Batchelor, J. F.; Capon, E. C.; Cheesman, N. J.; Fry, M.; Hudson, A. T.; Pudney, M.; Trimming, H.; Woolven, J.; Bueno, J. M.; Chicharro, J.; Fernández, E.; Fiandor, J. M.; Gargallo-Viola, D.; Gómez de las Heras, F.; Herreros, E.; León, M. L. Synthesis and structure-activity relationships of 4-pyridones as potential antimalarials J. Med. Chem. 2008, 51, 2845-2852 (Pubitemid 351620805)
28. Rodrigues, T.; Lopes, F.; Moreira, R. Inhibitors of the mitochondrial electron transport chain and de novo pyrimidine biosynthesis as antimalarials: the present status Curr. Med. Chem. 2010, 17, 929-956
29. Cowley, R.; Leung, S.; Fisher, N.; Al-Helal, M.; Berry, N. G.; Lawrenson, A. S.; Sharma, R.; Shone, A. E.; Ward, S. A.; Biagini, G. A.; O'Neil, P. M. The development of quinolone esters as novel antimalarial agents targeting the Plasmodium falciparum bc1 protein complex Med. Chem. Commun. 2012, 3, 39-44
30. Pidathala, C.; Amewu, R.; Pacorel, B.; Nixon, G. L.; Gibbons, P.; Hong, W. D.; Leung, S. C.; Berry, N. G.; Sharma, R.; Stocks, P. A.; Srivastava, A.; Shone, A. E.; Charoensutthivarakul, S.; Taylor, L.; Berger, O.; Mbekeani, A.; Hill, A.; Fisher, N. E.; Warman, A. J.; Biagini, G. A.; Ward, S. A.; O'Neill, P. M. Identification, design and biological evaluation of bisaryl quinolones targeting Plasmodium falciparum type II NADH:quinone oxidoreductase (PfNDH2) J. Med. Chem. 2012, 55, 1831-1843
31. Painter, H. J.; Morrisey, J. M.; Mather, M. W.; Vaidya, A. B. Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum Nature 2007, 446, 88-91 (Pubitemid 46348043)
32. Vale, N.; Prudeîncio, M.; Marques, C. A.; Collins, M. S.; Gut, J.; Nogueira, F.; Matos, J.; Rosenthal, P. J.; Cushion, M. T.; do Rosario, V. E.; Mota, M. M.; Moreira, R.; Gomes, P. Imidazoquines as antimalarial and antipneumocystis agents J. Med. Chem. 2009, 52, 7800-7807
33. Tarun, A. S.; Peng, X.; Dumpit, R. F.; Ogata, Y.; Silva-Rivera, H.; Camargo, N.; Daly, T. M.; Bergman, L. W.; Kappe, S. H. I. A combined transcriptome and proteome survey of malaria parasite liver stages Proc. Natl. Acad. Sci. U. S. A. 2008, 115, 305-310
34. Andricopuloa, A. D.; Akoachere, M. B.; Krogh, R.; Nickel, C.; McLeish, M. J.; Kenyon, G. L.; Arscott, L. D.; Williams, C. H., Jr.; Davioud-Charvet, E.; Becker, K. Specific inhibitors of Plasmodium falciparum thioredoxin reductase as potential antimalarial agents Bioorg. Med. Chem. Lett. 2006, 16, 2283-2292 (Pubitemid 43351095)
35. Ralph, S. A.; van Dooren, G. G.; Waller, R. F.; Crawford, M. J.; Fraunholz, M. J.; Foth, B. J.; Tonkin, C. J.; Roos, D. S.; McFadden, G. I. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast Nature Rev. Microbiol. 2004, 2, 203-216 (Pubitemid 39490083)
36. Yu, M.; Kumar, T. R. S.; Nkrumah, L. J.; Coppi, A.; Retzlaff, S.; Li, C. D.; Kelly, B. J.; Moura, P. A.; Lakshmanan, V.; Freundlich, J. S.; Valderramos, J.-C.; Vilcheze, C.; Siedner, M.; Tsai, J. H.-C.; Falkard, B.; Sidhu, A. b. S.; Purcell, L. A.; Gratraud, P.; Kremer, L.; Waters, A. P.; Schiehser, G.; Jacobus, D. P.; Janse, C. J.; Ager, A.; William R. Jacobs, J.; Sacchettini, J. C.; Heussler, V.; Sinnis, P.; Fidock, D. A. The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites Cell Host Microbe 2008, 4, 567-578 (Pubitemid 352762958)
37. Egan, T. Interactions of quinoline antimalarials with hematin in solution J. Inorg. Biochem. 2006, 100, 916-926
38. Egan, T. F.; Mavuso, W. W.; Ross, D. C.; Marques, H. M. Thermodynamic factors controlling the interaction of quinoline antimalarial drugs with ferriprotoporphyrin IX J. Inorg. Biochem. 1997, 68, 137-145 (Pubitemid 27441170)
39. Li, A. P. Preclinical in vitro screening assays for drug-like properties Drug Discovery Today: Technol. 2005, 2, 179-185 (Pubitemid 40946326)
40. Hopkins, A. L.; Groom, C. R.; Alex, A. Ligand efficiency: a useful metric for lead selection Drug Discovery Today 2004, 15, 430-431 and Information