Quinolone-3-diarylethers: A new class of antimalarial drug

Science Translational Medicine

Volumn 5, Issue 177, 2013, Pages

  Nilsen, Aaron ^a   LaCrue, Alexis N ^b   White, Karen L ^c   Forquer, Isaac P ^a   Cross, R Matthew ^d   Marfurt, Jutta ^e   Mather, Michael W ^f   Delves, Michael J ^g   Shackleford, David M ^c   Saenz, Fabian E ^b,q   Morrisey, Joanne M ^f   Steuten, Jessica ^c   Mutka, Tina ^b   Li, Yuexin ^a   Wirjanata, Grennady ^e   Ryan, Eileen ^c   Duffy, Sandra ^h   Kelly, Jane Xu ^a   Sebayang, Boni F ⁱ   Zeeman, Anne Marie ^j   Noviyanti, Rintis ⁱ   Sinden, Robert E ^g   Kocken, Clemens H M ^j   Price, Ric N ^e,k   Avery, Vicky M ^h   Angulo Barturen, Iñigo ^l   Jiménez Díaz, María Belén ^l   Ferrer, Santiago ^l   Herreros, Esperanza ^l   Sanz, Laura M ^l   Gamo, Francisco Javier ^l   Bathurst, Ian ^m   Burrows, Jeremy N ^m   Siegl, Peter ⁿ   Guy, R Kiplin ^o   Winter, Rolf W ^a   Vaidya, Akhil B ^f   Charman, Susan A ^c   Kyle, Dennis E ^b   Manetsch, Roman ^d   Riscoe, Michael K ^a,p   more..

^a PORTLAND VA MEDICAL CENTER   (United States)

^b NATIONAL SCHOOL OF PUBLIC HEALTH   (United States)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^f DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h GRIFFITH UNIVERSITY   (Australia)

ⁱ EIJKMAN INSTITUTE FOR MOLECULAR BIOLOGY   (Indonesia)

^j BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l GLAXOSMITHKLINE   (Spain)

^m Medicines for Malaria Venture   (Switzerland)

ⁿ Siegl Pharma Consulting LLC   (United States)

^o ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^p Department of Molecular Microbiology and Immunology ^*  (United States)

^q PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR   (Ecuador)

more..

Author keywords

[No Author keywords available]

Indexed keywords

4(1H) QUINOLONE 3 DIARYLETHER DERIVATIVE; AMODIAQUINE; ANTIMALARIAL AGENT; ARTESUNATE; ATOVAQUONE; CHLOROQUINE; ELQ 271; ELQ 300; GSK 932121A; MEFLOQUINE; P 4Q 391; PIPERAQUINE; PROGUANIL; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; APICOMPLEXAN LIFE CYCLE STAGE; AREA UNDER THE CURVE; ARTICLE; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG CLEARANCE; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; DRUG SELECTIVITY; DRUG SENSITIVITY; DRUG STRUCTURE; ENZYME INHIBITION; EX VIVO STUDY; FEMALE; GAMETOCYTE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; MALARIA; MALARIA CONTROL; MALARIA FALCIPARUM; MOUSE; NONHUMAN; PARASITE TRANSMISSION; PARASITE VECTOR; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PLASMODIUM YOELII; PRIORITY JOURNAL; SINGLE DRUG DOSE;

ANIMALS; ANTIMALARIALS; ATOVAQUONE; DRUG RESISTANCE; DRUG SYNERGISM; LIFE CYCLE STAGES; MALARIA; MALARIA, FALCIPARUM; MICE; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROGUANIL; PYRIDONES; QUINOLONES;

EID: 84876002292     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005029     Document Type: Article

References (58)

1. C. J. Murray, L. C. Rosenfeld, S. S. Lim, K. G. Andrews, K. J. Foreman, D. Haring, N. Fullman, M. Naghavi, R. Lozano, A. D. Lopez, Global malaria mortality between 1980 and 2010: A systematic analysis. Lancet 379, 413-431 (2012).
2. A. M. Dondorp, R. M. Fairhurst, L. Slutsker, J. R. Macarthur, J. G. Breman, P. J. Guerin, T. E. Wellems, P. Ringwald, R. D. Newman, C. V. Plowe, The threat of artemisinin-resistant malaria. N. Engl. J. Med. 365, 1073-1075 (2011).
3. A. P. Phyo, S. Nkhoma, K. Stepniewska, E. A. Ashley, S. Nair, R. McGready, C. ler Moo, S. Al-Saai, A. M. Dondorp, K. M. Lwin, P. Singhasivanon, N. P. Day, N. J. White, T. J. Anderson, F. Nosten, Emergence of artemisinin-resistant malaria on the western border of Thailand: A longitudinal study. Lancet 379, 1960-1966 (2012).
4. L. Lucantoni, V. Avery, Whole-cell in vitro screening for gametocytocidal compounds. Future Med. Chem. 4, 2337-2360 (2012).
5. malERA Consultative Group on Drugs, A research agenda for malaria eradication: Drugs. PLoS Med. 8, e1000402 (2011).
6. W. Salzer, H. Timmler, H. Andersag, Über einen neuen, gegen Vogelmalaria wirksamen Verbindungstypus. Chem. Ber. 81, 12-19 (1948).
7. W. Kikuth, L. Mudrow-Reichenow, Über kausalprophylaktisch bei Vogelmalaria wirksame Substanzen. Z. Hyg. Infektionskr. 127, 151-165 (1947).
8. R. M. Cross, A. Monastyrskyi, T. S. Mutka, J. N. Burrows, D. E. Kyle, R. Manetsch, Endochin optimization: Structure-activity and structure-property relationship studies of 3- substituted 2-methyl-4(1H)-quinolones with antimalarial activity. J. Med. Chem. 53, 7076-7094 (2010).
9. R. Winter, J. X. Kelly, M. J. Smilkstein, D. Hinrichs, D. R. Koop, M. K. Riscoe, Optimization of endochin-like quinolones for antimalarial activity. Exp. Parasitol. 127, 545-551 (2011).
10. M. Fry, M. Pudney, Site of action of the antimalarial hydroxynaphthoquinone, 2-[trans-4- (4'-chlorophenyl) cyclohexyl]-3-hydroxy-1,4- naphthoquinone (566C80). Biochem. Pharmacol. 43, 1545-1553 (1992).
11. C. L. Yeates, J. F. Batchelor, E. C. Capon, N. J. Cheesman, M. Fry, A. T. Hudson, M. Pudney, H. Trimming, J. Woolven, J. M. Bueno, J. Chicharro, E. Fernández, J. M. Fiandor, D. Gargallo-Viola, F. Gómez de las Heras, E. Herreros, M. L. León, Synthesis and structure-activity relationships of 4-pyridones as potential antimalarials. J. Med. Chem. 51, 2845-2852 (2008).
12. J. M. Bueno, E. Herreros, I. Angulo-Barturen, S. Ferrer, J. M. Fiandor, F. J. Gamo, D. Gargallo-Viola, G. Derimanov, Exploration of 4(1H)-pyridones as a novel family of potent antimalarial inhibitors of the plasmodial cytochrome bc1. Future Med. Chem. 4, 2311-2323 (2012).
13. R. W. Winter, J. X. Kelly, M. J. Smilkstein, R. Dodean, D. Hinrichs, M. K. Riscoe, Antimalarial quinolones: Synthesis, potency, and mechanistic studies. Exp. Parasitol. 118, 487-497 (2008).
14. M. K. Riscoe, J. X. Kelly, R. W. Winter, D. J. Hinrichs, M. J. Smilkstein, A. Nilsen, J. Burrows, D. E. Kyle, M. Manetsch, R. M. Cross, A. Monastyrskyi, D. L. Flanigan, WIPO #WO/2010/065905 (2010).
15. M. Smilkstein, N. Sriwilaijaroen, J. X. Kelly, P. Wilairat, M. Riscoe, Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob. Agents Chemother. 48, 1803-1806 (2004).
16. R. E. Desjardins, C. J. Canfield, J. D. Haynes, J. D. Chulay, Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemother. 16, 710-718 (1979).
17. M. J. Smilkstein, I. Forquer, A. Kanazawa, J. X. Kelly, R. W. Winter, D. J. Hinrichs, D. M. Kramer, M. K. Riscoe, A drug-selected Plasmodium falciparum lacking the need for conventional electron transport. Mol. Biochem. Parasitol. 159, 64-68 (2008).
18. H. Ke, J. M. Morrisey, S. M. Ganesan, H. J. Painter, M. W. Mather, A. B. Vaidya, Variation among Plasmodium falciparum strains in their reliance on mitochondrial electron transport chain function. Eukaryot. Cell 10, 1053-1061 (2011).
19. H. J. Painter, J. M. Morrisey, M. W. Mather, A. B. Vaidya, Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446, 88-91 (2007).
20. J. Marfurt, F. Chalfein, P. Prayoga, F. Wabiser, E. Kenangalem, K. A. Piera, D. P. Fairlie, E. Tjitra, N. M. Anstey, K. T. Andrews, R. N. Price, Ex vivo activity of histone deacetylase inhibitors against multidrug-resistant clinical isolates of Plasmodium falciparum and P. vivax. Antimicrob. Agents Chemother. 55, 961-966 (2011).
21. B. Russell, F. Chalfein, B. Prasetyorini, E. Kenangalem, K. Piera, R. Suwanarusk, A. Brockman, P. Prayoga, P. Sugiarto, Q. Cheng, E. Tjitra, N. M. Anstey, R. N. Price, Determinants of in vitro drug susceptibility testing of Plasmodium vivax. Antimicrob. Agents Chemother. 52, 1040-1045 (2008).
22. M. W. Mather, J. M. Morrisey, A. B. Vaidya, Hemozoin-free Plasmodium falciparum mitochondria for physiological and drug susceptibility studies. Mol. Biochem. Parasitol. 174, 150-153 (2010).
23. L. M. Sanz, B. Crespo, C. De-Cózar, X. C. Ding, J. L. Llergo, J. N. Burrows, J. F. García-Bustos, F. J. Gamo, P. falciparum in vitro killing rates allow to discriminate between different antimalarial mode-of-action. PLoS One 7, e30949 (2012).
24. Q. L. Fivelman, I. S. Adagu, D. C. Warhurst, Modified fixed-ratio isobologram method for studying in vitro interactions between atovaquone and proguanil or dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Antimicrob. Agents Chemother. 48, 4097-4102 (2004).
25. A. J. Ager, Rodent Malaria Models (Springer-Verlag, New York, 1984), vol. 68, pp. 225-264.
26. M. B. Jiménez-Díaz, T. Mulet, S. Viera, V. Gómez, H. Garuti, J. Ibáñez, A. Alvarez-Doval, L. D. Shultz, A. Martínez, D. Gargallo-Viola, I. Angulo-Barturen, Improved murine model of malaria using Plasmodium falciparum competent strains and non-myelodepleted NOD-scid IL2Rgnull mice engrafted with human erythrocytes. Antimicrob. Agents Chemother. 53, 4533-4536 (2009).
27. M. B. Jiménez-Díaz, J. Rullas, T. Mulet, L. Fernández, C. Bravo, D. Gargallo-Viola, I. Angulo-Barturen, Improvement of detection specificity of Plasmodium-infected murine erythrocytes by flow cytometry using autofluorescence and YOYO-1. Cytometry A 67, 27-36 (2005).
28. L. Dembele, A. Gego, A. M. Zeeman, J. F. Franetich, O. Silvie, A. Rametti, R. Le Grand, N. Dereuddre-Bosquet, R. Sauerwein, G. J. van Gemert, J. C. Vaillant, A. W. Thomas, G. Snounou, C. H. Kocken, D. Mazier, Towards an in vitro model of Plasmodium hypnozoites suitable for drug discovery. PLoS One 6, e18162 (2011).
29. G. A. Biagini, N. Fisher, A. E. Shone, M. A. Mubaraki, A. Srivastava, A. Hill, T. Antoine, A. J. Warman, J. Davies, C. Pidathala, R. K. Amewu, S. C. Leung, R. Sharma, P. Gibbons, D. W. Hong, B. Pacorel, A. S. Lawrenson, S. Charoensutthivarakul, L. Taylor, O. Berger, A. Mbekeani, P. A. Stocks, G. L. Nixon, J. Chadwick, J. Hemingway, M. J. Delves, R. E. Sinden, A. M. Zeeman, C. H. Kocken, N. G. Berry, P. M. O'Neill, S. A. Ward, 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. 109, 8298-8303 (2012).
30. L. H. Schmidt, Relationships between chemical structures of 8-aminoquinolines and their capacities for radical cure of infections with Plasmodium cynomolgi in rhesus monkeys. Antimicrob. Agents Chemother. 24, 615-652 (1983).
31. W. Peters, in Epidemiology, Chemotherapy, Morphology, and Metabolism, J. P. Kreier, Ed. (Academic Press, New York, 1980), pp. 214-283.
32. S. Duffy, V. M. Avery, Development and optimization of a novel 384-well anti-malarial imaging assay validated for high-throughput screening. Am. J. Trop. Med. Hyg. 86, 84-92 (2012).
33. M. Delves, D. Plouffe, C. Scheurer, S. Meister, S. Wittlin, E. A. Winzeler, R. E. Sinden, D. Leroy, The activities of current antimalarial drugs on the life cycle stages of Plasmodium: A comparative study with human and rodent parasites. PLoS Med. 9, e1001169 (2012).
34. M. J. Delves, C. Ramakrishnan, A. M. Blagborough, D. Leroy, T. N. Wells, R. E. Sinden, A highthroughput assay for the identification of malarial transmission-blocking drugs and vaccines. Int. J. Parasitol. 42, 999-1006 (2012).
35. C. J. Janse, J. Ramesar, A. P. Waters, High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat. Protoc. 1, 346-356 (2006).
36. M. J. Delves, R. E. Sinden, A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar. J. 9, 35 (2010).
37. J. C. van Pelt-Koops, H. E. Pett, W. Graumans, M. van der Vegte-Bolmer, G. J. van Gemert, M. Rottmann, B. K. Yeung, T. T. Diagana, R. W. Sauerwein, The spiroindolone drug candidate NITD609 potently inhibits gametocytogenesis and blocks Plasmodium falciparum transmission to Anopheles mosquito vector. Antimicrob. Agents Chemother. 56, 3544-3548 (2012).
38. J. S. Doggett, A. Nilsen, I. Forquer, K. W. Wegmann, L. Jones-Brando, R. H. Yolken, C. Bordón, S. A. Charman, K. Katneni, T. Schultz, J. N. Burrows, D. J. Hinrichs, B. Meunier, V. B. Carruthers, M. K. Riscoe, Endochin-like quinolones are highly efficacious against acute and latent experimental toxoplasmosis. Proc. Natl. Acad. Sci. U.S.A. 109, 15936-15941 (2012).
39. W. Trager, J. B. Jensen, Human malaria parasites in continuous culture. Science 193, 673-675 (1976).
40. J. Marfurt, F. Chalfein, P. Prayoga, F. Wabiser, E. Kenangalem, K. A. Piera, B. Machunter, E. Tjitra, N. M. Anstey, R. N. Price, Ex vivo drug susceptibility of ferroquine against chloroquine-resistant isolates of Plasmodium falciparum and P. vivax. Antimicrob. Agents Chemother. 55, 4461-4464 (2011).
41. G. W. Gervais, K. Trujillo, B. L. Robinson, W. Peters, A. E. Serrano, Plasmodium berghei: Identification of an mdr-like gene associated with drug resistance. Exp. Parasitol. 91, 86-92 (1999).
42. A. N. Lacrue, F. E. Sáenz, R. M. Cross, K. O. Udenze, A. Monastyrskyi, S. Stein, T. S. Mutka, R. Manetsch, D. E. Kyle, 4(1H)-Quinolones with liver stage activity against Plasmodium berghei. Antimicrob. Agents Chemother. 57, 417-424 (2013).
43. I. H. Ploemen,M. Prudêncio, B. G. Douradinha, J. Ramesar, J. Fonager, G. J. van Gemert, A. J. Luty, C. C. Hermsen, R. W. Sauerwein, F. G. Baptista, M. M. Mota, A. P. Waters, I. Que, C. W. Lowik, S. M. Khan, C. J. Janse, B. M. Franke-Fayard, Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS One 4, e7881 (2009).
44. R. M. Cross, N. K. Namelikonda, T. S. Mutka, L. Luong, D. E. Kyle, R. Manetsch, Synthesis, antimalarial activity, and structure-activity relationship of 7-(2-phenoxyethoxy)-4(1H)-quinolones. J. Med. Chem. 54, 8321-8327 (2011).
45. M. E. Hart, K. L. Suchland, M. Miyakawa, J. R. Bunzow, D. K. Grandy, T. S. Scanlan, Trace amine-associated receptor agonists: Synthesis and evaluation of thyronamines and related analogues. J. Med. Chem. 49, 1101-1112 (2006).
46. W. M. Eling, Separation of parasitized erythrocytes from Plasmodium berghei infected mouse blood. Trans. R. Soc. Trop. Med. Hyg. 71, 267-268 (1977).
47. J. Krungkrai, S. R. Krungkrai, N. Suraveratum, P. Prapunwattana, Mitochondrial ubiquinolcytochrome c reductase and cytochrome c oxidase: Chemotherapeutic targets in malarial parasites. Biochem. Mol. Biol. Int. 42, 1007-1014 (1997).
48. J. Krungkrai, The multiple roles of the mitochondrion of the malarial parasite. Parasitology 129, 511-524 (2004).
49. R. D. Guarino, L. E. Dike, T. A. Haq, J. A. Rowley, J. B. Pitner, M. R. Timmins, Method for determining oxygen consumption rates of static cultures from microplate measurements of pericellular dissolved oxygen concentration. Biotechnol. Bioeng. 86, 775-787 (2004).
50. B. L. Trumpower, C. A. Edwards, Purification of a reconstitutively active iron-sulfur protein (oxidation factor) from succinate•cytochrome c reductase complex of bovine heart mitochondria. J. Biol. Chem. 254, 8697-8706 (1979).
51. I. Angulo-Barturen, M. B. Jiménez-Díaz, T. Mulet, J. Rullas, E. Herreros, S. Ferrer, E. Jiménez, A. Mendoza, J. Regadera, P. J. Rosenthal, I. Bathurst, D. L. Pompliano, F. Gómez de las Heras, D. Gargallo-Viola, A murine model of falciparum-malaria by in vivo selection of competent strains in non-myelodepleted mice engrafted with human erythrocytes. PLoS One 3, e2252 (2008).
52. M. B. Jiménez-Díaz, T. Mulet, V. Gómez, S. Viera, A. Alvarez, H. Garuti, Y. Vázquez, A. Fernandez, J. Ibáñez, M. Jiménez, D. Gargallo-Viola, I. Angulo-Barturen, Quantitative measurement of Plasmodium-infected erythrocytes in murine models of malaria by flow cytometry using bidimensional assessment of SYTO-16 fluorescence. Cytometry A 75, 225-235 (2009).
53. R. S. Obach, Prediction of human clearance of twenty-nine drugs from hepatic microsomal intrinsic clearance data: An examination of in vitro half-life approach and nonspecific binding to microsomes. Drug Metab. Dispos. 27, 1350-1359 (1999).
54. V. C. Broudy, K. S. Zuckerman, S. Jetmalani, J. H. Fitchen, G. C. Bagby Jr., Monocytes stimulate fibroblastoid bone marrow stromal cells to produce multilineage hematopoietic growth factors. Blood 68, 530-534 (1986).
55. R. K. Rathbun, T. A. Christianson, G. R. Faulkner, G. Jones, W. Keeble, M. O'Dwyer, G. C. Bagby, Interferon-g-induced apoptotic responses of Fanconi anemia group C hematopoietic progenitor cells involve caspase 8-dependent activation of caspase 3 family members. Blood 96, 4204-4211 (2000).
56. Y. Li, X. M. Qi, X. Xue, X. F. Wu, Y. F. Wu, M. Chen, G. Z. Xing, Y. Luan, J. Ren, The relationship between diphenylamine structure and NSAIDs-induced hepatocytes injury. Toxicol. Lett. 186, 111-114 (2009).
57. J. A. Dykens, L. D. Marroquin, Y. Will, Strategies to reduce late-stage drug attrition due to mitochondrial toxicity. Expert Rev. Mol. Diagn. 7, 161-175 (2007).
58. L. D. Marroquin, J. Hynes, J. A. Dykens, J. D. Jamieson, Y. Will, Circumventing the Crabtree effect: Replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol. Sci. 97, 539-547 (2007).