High-Throughput Luciferase-Based Assay for the Discovery of Therapeutics That Prevent Malaria

ACS Infectious Diseases

Volumn 2, Issue 4, 2016, Pages 281-293

  Swann, Justine ^a   Corey, Victoria ^a   Scherer, Christina A ^b   Kato, Nobutaka ^b   Comer, Eamon ^b   Maetani, Micah ^b   Antonova Koch, Yevgeniya ^a   Reimer, Christin ^a   Gagaring, Kerstin ^c,f   Ibanez, Maureen ^c,g   Plouffe, David ^c   Zeeman, Anne Marie ^d   Kocken, Clemens H M ^d   McNamara, Case W ^b,f   Schreiber, Stuart L ^b   Campo, Brice ^e   Winzeler, Elizabeth A ^a   Meister, Stephan ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^d BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^e Medicines for Malaria Venture (MMV)   (Switzerland)

^f California Institute for Biomedical Research   (United States)

^g Samumed LLC   (United States)

Author keywords

drug discovery; exoerythrocytic stage malaria; high throughput screening; liver stage malaria; malaria

Indexed keywords

ARTICLE; CONTROLLED STUDY; DIVERSITY ORIENTED SYNTHESIS; HEPATOCELLULAR CARCINOMA CELL LINE; HIGH THROUGHPUT SCREENING; HOST CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LUCIFERASE ASSAY; MALARIA; MOLECULAR LIBRARY; NONHUMAN; PHENOTYPE; PLASMODIUM BERGHEI; PRIORITY JOURNAL; RODENT MALARIA; SYNTHESIS;

EID: 85019538549     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.5b00143     Document Type: Article

References (43)

1. Carter, R. and Mendis, K. N. (2002) Evolutionary and historical aspects of the burden of malaria Clin. Microbiol. Rev. 15, 564-594 10.1128/CMR.15.4.564-594.2002
2. Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y., and Hay, S. I. (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria Nature 434, 214-217 10.1038/nature03342
3. Sachs, J. and Malaney, P. (2002) The economic and social burden of malaria Nature 415, 680-685 10.1038/415680a
4. Sinka, M. E., Bangs, M. J., Manguin, S., Rubio-Palis, Y., Chareonviriyaphap, T., Coetzee, M., Mbogo, C. M., Hemingway, J., Patil, A. P., Temperley, W. H., Gething, P. W., Kabaria, C. W., Burkot, T. R., Harbach, R. E., and Hay, S. I. (2012) A global map of dominant malaria vectors Parasites Vectors 5, 69 10.1186/1756-3305-5-69
5. Flannery, E. L., Chatterjee, A. K., and Winzeler, E. A. (2013) Antimalarial drug discovery-approaches and progress towards new medicines Nat. Rev. Microbiol. 11, 849-862 10.1038/nrmicro3138
6. Prudencio, M., Rodriguez, A., and Mota, M. M. (2006) The silent path to thousands of merozoites: the Plasmodium liver stage Nat. Rev. Microbiol. 4, 849-856 10.1038/nrmicro1529
7. Wells, T. N., Burrows, J. N., and Baird, J. K. (2010) Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination Trends Parasitol. 26, 145-151 10.1016/j.pt.2009.12.005
8. Clark, I. A., al Yaman, F. M., and Jacobson, L. S. (1997) Int. J. Parasitol. 27, 1237-1249 10.1016/S0020-7519(97)00121-5
9. Baker, D. A. (2010) Malaria gametocytogenesis Mol. Biochem. Parasitol. 172, 57-65 10.1016/j.molbiopara.2010.03.019
10. Delves, M., Plouffe, D., Scheurer, C., Meister, S., Wittlin, S., Winzeler, E. A., Sinden, R. E., and Leroy, D. (2012) The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites PLoS medicine 9, e1001169 10.1371/journal.pmed.1001169
11. Tan, K. R., Magill, A. J., Parise, M. E., and Arguin, P. M. (2011) Doxycycline for malaria chemoprophylaxis and treatment: report from the CDC expert meeting on malaria chemoprophylaxis Am. J. Trop. Med. Hyg. 84, 517-531 10.4269/ajtmh.2011.10-0285
12. Hyde, J. E. (2002) Mechanisms of resistance of Plasmodium falciparum to antimalarial drugs Microbes Infect. 4, 165-174 10.1016/S1286-4579(01)01524-6
13. Ganesan, S., Chaurasiya, N. D., Sahu, R., Walker, L. A., and Tekwani, B. L. (2012) Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway Toxicology 294, 54-60 10.1016/j.tox.2012.01.015
14. Meister, S., Plouffe, D. M., Kuhen, K. L., Bonamy, G. M., 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., 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., and Winzeler, E. A. (2011) Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery Science 334, 1372-1377 10.1126/science.1211936
15. Derbyshire, E. R., Mota, M. M., and Clardy, J. (2011) The next opportunity in anti-malaria drug discovery: the liver stage PLoS Pathog. 7, e1002178 10.1371/journal.ppat.1002178
16. Reader, J., Botha, M., Theron, A., Lauterbach, S. B., Rossouw, C., Engelbrecht, D., Wepener, M., Smit, A., Leroy, D., Mancama, D., Coetzer, T. L., and Birkholtz, L. M. (2015) Nowhere to hide: interrogating different metabolic parameters of Plasmodium falciparum gametocytes in a transmission blocking drug discovery pipeline towards malaria elimination Malar. J. 14, 213 10.1186/s12936-015-0718-z
17. Derbyshire, E. R., Prudencio, M., Mota, M. M., and Clardy, J. (2012) Liver-stage malaria parasites vulnerable to diverse chemical scaffolds Proc. Natl. Acad. Sci. U. S. A. 109, 8511-8516 10.1073/pnas.1118370109
18. Spangenberg, T., Burrows, J. N., Kowalczyk, P., McDonald, S., Wells, T. N., and Willis, P. (2013) The open access malaria box: a drug discovery catalyst for neglected diseases PLoS One 8, e62906 10.1371/journal.pone.0062906
19. Janse, C. J., Franke-Fayard, B., Mair, G. R., Ramesar, J., Thiel, C., Engelmann, S., Matuschewski, K., van Gemert, G. J., Sauerwein, R. W., and Waters, A. P. (2006) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures Mol. Biochem. Parasitol. 145, 60-70 10.1016/j.molbiopara.2005.09.007
20. Silvie, O., Greco, C., Franetich, J. F., Dubart-Kupperschmitt, A., Hannoun, L., van Gemert, G. J., Sauerwein, R. W., Levy, S., Boucheix, C., Rubinstein, E., and Mazier, D. (2006) Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species Cell. Microbiol. 8, 1134-1146 10.1111/j.1462-5822.2006.00697.x
21. Ignowski, J. M. and Schaffer, D. V. (2004) Kinetic analysis and modeling of firefly luciferase as a quantitative reporter gene in live mammalian cells Biotechnol. Bioeng. 86, 827-834 10.1002/bit.20059
22. Dandapani, S. and Marcaurelle, L. A. (2010) Grand challenge commentary: Accessing new chemical space for 'undruggable' targets Nat. Chem. Biol. 6, 861-863 10.1038/nchembio.479
23. Nielsen, T. E. and Schreiber, S. L. (2008) Towards the optimal screening collection: a synthesis strategy Angew. Chem., Int. Ed. 47, 48-56 10.1002/anie.200703073
24. Plouffe, D., Brinker, A., McNamara, C., Henson, K., Kato, N., Kuhen, K., Nagle, A., Adrian, F., Matzen, J. T., Anderson, P., Nam, T. G., Gray, N. S., Chatterjee, A., Janes, J., Yan, S. F., Trager, R., Caldwell, J. S., Schultz, P. G., Zhou, Y., and Winzeler, E. A. (2008) In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen Proc. Natl. Acad. Sci. U. S. A. 105, 9059-9064 10.1073/pnas.0802982105
25. Dong, C. K., Urgaonkar, S., Cortese, J. F., Gamo, F. J., Garcia-Bustos, J. F., Lafuente, M. J., Patel, V., Ross, L., Coleman, B. I., Derbyshire, E. R., Clish, C. B., Serrano, A. E., Cromwell, M., Barker, R. H., Jr., Dvorin, J. D., Duraisingh, M. T., Wirth, D. F., Clardy, J., and Mazitschek, R. (2011) Identification and validation of tetracyclic benzothiazepines as Plasmodium falciparum cytochrome bc1 inhibitors Chem. Biol. 18, 1602-1610 10.1016/j.chembiol.2011.09.016
26. Capper, M. J., O'Neill, P. M., Fisher, N., Strange, R. W., Moss, D., Ward, S. A., Berry, N. G., Lawrenson, A. S., Hasnain, S. S., Biagini, G. A., and Antonyuk, S. V. (2015) Antimalarial 4(1H)-pyridones bind to the Qi site of cytochrome bc1 Proc. Natl. Acad. Sci. U. S. A. 112, 755-760 10.1073/pnas.1416611112
27. 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., Price, R. N., Avery, V. M., Angulo-Barturen, I., Jimenez-Diaz, 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., and Riscoe, M. K. (2013) Quinolone-3-diarylethers: a new class of antimalarial drug Sci. Transl. Med. 5, 177ra37 10.1126/scitranslmed.3005029
28. Kuhen, K. L., Chatterjee, A. K., Rottmann, M., Gagaring, K., Borboa, R., Buenviaje, J., Chen, Z., Francek, C., Wu, T., Nagle, A., Barnes, S. W., Plouffe, D., Lee, M. C., Fidock, D. A., Graumans, W., van de Vegte-Bolmer, M., van Gemert, G. J., Wirjanata, G., Sebayang, B., Marfurt, J., Russell, B., Suwanarusk, R., Price, R. N., Nosten, F., Tungtaeng, A., Gettayacamin, M., Sattabongkot, J., Taylor, J., Walker, J. R., Tully, D., Patra, K. P., Flannery, E. L., Vinetz, J. M., Renia, L., Sauerwein, R. W., Winzeler, E. A., Glynne, R. J., and Diagana, T. T. (2014) KAF156 is an antimalarial clinical candidate with potential for use in prophylaxis, treatment, and prevention of disease transmission Antimicrob. Agents Chemother. 58, 5060-5067 10.1128/AAC.02727-13
29. Malmquist, N. A., Moss, T. A., Mecheri, S., Scherf, A., and Fuchter, M. J. (2012) Small-molecule histone methyltransferase inhibitors display rapid antimalarial activity against all blood stage forms in Plasmodium falciparum Proc. Natl. Acad. Sci. U. S. A. 109, 16708-16713 10.1073/pnas.1205414109
30. Kato, N., Sakata-Kato, T., Maetani, M., Bastien, J., Corey, V., Derbyshire, E. R., Dornan, G., Duffy, S., Eckley, S., Karin, M. J., Koolen, T. A. L., Lukens, A. K., Lund, E., Riera, S., Bennett, C., Meier, J. M., Branko, M., Moss, E. L., Sayes, M., VanGessel, Y., Wawer, M. J., Yoshinaga, T., Zeeman, A.-M., Avery, V. M., Bhatia, S. N., Burke, J. E., Catteruccia, F., Clardy, J. C., Clemons, P. A., Dechering, K. J., Duvall, J. R., Foley, M. A., Gusovsky, F., Kocken, C. H. M., Morningstar, M. L., Munoz, B., Neafsey, D. E., Winzeler, E. A., Wirth, D. F., Scherer, C. A., and Schreiber, S. L. Diversity synthesis yields multistage antimalarial inhibitors including of a novel target that results in low single-dose cures in mice. Manuscript in review.
31. Ross, L. S., Gamo, F. J., Lafuente-Monasterio, M. J., Singh, O. M., Rowland, P., Wiegand, R. C., and Wirth, D. F. (2014) In vitro resistance selections for Plasmodium falciparum dihydroorotate dehydrogenase inhibitors give mutants with multiple point mutations in the drug-binding site and altered growth J. Biol. Chem. 289, 17980-17995 10.1074/jbc.M114.558353
32. Prudencio, M., Rodrigues, C. D., Ataide, R., and Mota, M. M. (2008) Dissecting in vitro host cell infection by Plasmodium sporozoites using flow cytometry Cell. Microbiol. 10, 218-224 10.1111/j.1462-5822.2007.01032.x
33. Sinnis, P., De La Vega, P., Coppi, A., Krzych, U., and Mota, M. M. (2012) Quantification of sporozoite invasion, migration, and development by microscopy and flow cytometry Methods Mol. Biol. 923, 385-400 10.1007/978-1-62703-026-7-27
34. Mota, M. M., Pradel, G., Vanderberg, J. P., Hafalla, J. C., Frevert, U., Nussenzweig, R. S., Nussenzweig, V., and Rodriguez, A. (2001) Migration of Plasmodium sporozoites through cells before infection Science 291, 141-144 10.1126/science.291.5501.141
35. McNamara, C. W., Lee, M. C., Lim, C. S., Lim, S. H., Roland, J., Nagle, A., Simon, O., Yeung, B. K., Chatterjee, A. K., McCormack, S. L., Manary, M. J., Zeeman, A. M., Dechering, K. J., Kumar, T. R., Henrich, P. P., Gagaring, K., Ibanez, M., Kato, N., Kuhen, K. L., Fischli, C., Rottmann, M., Plouffe, D. M., Bursulaya, B., Meister, S., Rameh, L., Trappe, J., Haasen, D., Timmerman, M., Sauerwein, R. W., Suwanarusk, R., Russell, B., Renia, L., Nosten, F., Tully, D. C., Kocken, C. H., Glynne, R. J., Bodenreider, C., Fidock, D. A., Diagana, T. T., and Winzeler, E. A. (2013) Targeting Plasmodium PI(4)K to eliminate malaria Nature 504, 248-253 10.1038/nature12782
36. Corish, P. and Tyler-Smith, C. (1999) Attenuation of green fluorescent protein half-life in mammalian cells Protein Eng., Des. Sel. 12, 1035-1040 10.1093/protein/12.12.1035
37. Peterson, D. S., Walliker, D., and Wellems, T. E. (1988) Evidence that a point mutation in dihydrofolate reductase-thymidylate synthase confers resistance to pyrimethamine in falciparum malaria Proc. Natl. Acad. Sci. U. S. A. 85, 9114-9118 10.1073/pnas.85.23.9114
38. Baragana, B., Hallyburton, I., Lee, M. C., Norcross, N. R., Grimaldi, R., Otto, T. D., Proto, W. R., Blagborough, A. M., Meister, S., Wirjanata, G., Ruecker, A., Upton, L. M., Abraham, T. S., Almeida, M. J., Pradhan, A., Porzelle, A., Martinez, M. S., Bolscher, J. M., Woodland, A., Norval, S., Zuccotto, F., Thomas, J., Simeons, F., Stojanovski, L., Osuna-Cabello, M., Brock, P. M., Churcher, T. S., Sala, K. A., Zakutansky, S. E., Jimenez-Diaz, M. B., Sanz, L. M., Riley, J., Basak, R., Campbell, M., Avery, V. M., Sauerwein, R. W., Dechering, K. J., Noviyanti, R., Campo, B., Frearson, J. A., Angulo-Barturen, I., Ferrer-Bazaga, S., Gamo, F. J., Wyatt, P. G., Leroy, D., Siegl, P., Delves, M. J., Kyle, D. E., Wittlin, S., Marfurt, J., Price, R. N., Sinden, R. E., Winzeler, E. A., Charman, S. A., Bebrevska, L., Gray, D. W., Campbell, S., Fairlamb, A. H., Willis, P. A., Rayner, J. C., Fidock, D. A., Read, K. D., and Gilbert, I. H. (2015) A novel multiple-stage antimalarial agent that inhibits protein synthesis Nature 522, 315-320 10.1038/nature14451
39. Dembele, L., Gego, A., Zeeman, A. M., Franetich, J. F., Silvie, O., Rametti, A., Le Grand, R., Dereuddre-Bosquet, N., Sauerwein, R., van Gemert, G. J., Vaillant, J. C., Thomas, A. W., Snounou, G., Kocken, C. H., and Mazier, D. (2011) Towards an in vitro model of Plasmodium hypnozoites suitable for drug discovery PLoS One 6, e18162 10.1371/journal.pone.0018162
40. Zeeman, A. M., van Amsterdam, S. M., McNamara, C. W., Voorberg-van der Wel, A., Klooster, E. J., van den Berg, A., Remarque, E. J., Plouffe, D. M., van Gemert, G. J., Luty, A., Sauerwein, R., Gagaring, K., Borboa, R., Chen, Z., Kuhen, K., Glynne, R. J., Chatterjee, A. K., Nagle, A., Roland, J., Winzeler, E. A., Leroy, D., Campo, B., Diagana, T. T., Yeung, B. K., Thomas, A. W., and Kocken, C. H. (2014) KAI407, a potent non-8-aminoquinoline compound that kills Plasmodium cynomolgi early dormant liver stage parasites in vitro Antimicrob. Agents Chemother. 58, 1586-1595 10.1128/AAC.01927-13
41. Van Voorhis, W. C., Roberto Adelfio, J. H. A., Ahyong, V., Akabas, M. H., Alano, P., Alday, A., Resto, Y. A., Alsibaee, A., Alzualde, A., Andrews, K. T., Avery, S. V., Avery, V. M., Ayong, L., Baker, M., Baker, S., Mamoum, C. B., Bhatia, S., Bickle, Q., Bounaadja, L., Bowling, T., Bosch, J., Boucher, L. E., Boyom, F. F., Brea, J., Brennan, M., Burton, A., Caffrey, C. R., Camarda, G., Carrasquilla, M., Carter, D., Cassera, M. B., Cheng, K. C.-C., Chindaudomsate, W., Chubb, A., Colon, B. L., Colón-López, D. C., Corbett, Y., Crowther, G. J., Cowan, N., D'Alessandro, S., Dang, N. L., Delves, M., DeRisi, J. L., Du, A. Y., Duffy, S., Abd El-Salam El-Sayed, S., Ferdig, M. T., Fernández Robledo, J. A., Fidock, D. A., Florent, I., Patrick, V. T., Galstian, A., Javier Gamo, F., Gokool, S., Gold, B., Golub, T., Goldgof, G. M., Guha, R., Guiguemde, W. A., Gural, N., Kiplin, G. R., Hansen, M., Hanson, K. K., Hemphill, A., van Huijsduijnen, R. H., Horii, T., Horrocks, P., Hughes, T. B., Huston, C., Igarashi, I., Ingram-Sieber, K., Itoe, M. A., Jadhav, A., Jensen, A. N., Jensen, L. T., Jiang, R. H. Y., Kaiser, A., Keiser, J., Ketas, T., Kicka, S., Kim, S., Kirk, K., Kumar, V., Kyle, D. E., Lafuente, M. J., Landfear, S., Lee, N., Lee, S., Lehane, A., Li, F., Little, D., Liu, L., Llinás, M., Loza, M. I., Lubar, A., Lucantoni, L., Lucet, I., Maes, L., Mansour, N. R., March, S., McGowan, S., Vera, I. M., Meister, S., Mercer, L., Mestres, J., Mfopa, A. N., Misra, R. N., Moon, A. B., Moore, J. P., Müller, J., Muriana, A., Nakazawa, S., Hewitt, M. S., Nare, B., Nathan, C., Narraidoo, N., Nawaratna, S., Ojo, K. K., Ortiz, D., Panic, G., Papadatos, G., Parapini, S., Patra, K., Pham, N., Prats, S., Plouffe, D. M., Poulsen, S.-A., Pradhan, A., Quevedo, C., Quinn, R. J., Rice, C. A., Rizk, M. A., Ruecker, A., St.Onge, R., Samra, J., Natalie, G., Schlecht, U., Schmitt, M., Sinden, R., Silvestrini, F., Smith, D. A., Soldati, T., Spitzmüller, A., Stamm, S. M., Sullivan, D. J., Sullivan, W., Suresh, S., Suzuki, B. M., Suzuki, Y., Swamidass, S. J., Taramelli, D., Tchokouaha, L. R. Y., Thomas, D., Tonissen, K. F., Townson, S., Tripathi, A. K., Trofimov, V., Udenze, K. O., Ullah, I., Vallieres, C., Vigil, E., Vinetz, J. M., Vinh, P. V., Vu, H., Watanabe, N.-a., Weatherby, K., White, P. M., Winzeler, E. A., Wojcik, E., Wree, M., Wu, W., Yokoyama, N., Zollo, P. H. A., Abla, N., Blasco, B., Burrows, J., Laleu, B., Leroy, D., Spangenberg, T., Wells, T., and Willis, P. Open-source drug discovery with the Malaria Box compound collection for neglected diseases and beyond. Manuscript in revew.
42. da Cruz, F. P., Martin, C., Buchholz, K., Lafuente-Monasterio, M. J., Rodrigues, T., Sonnichsen, B., Moreira, R., Gamo, F. J., Marti, M., Mota, M. M., Hannus, M., and Prudencio, M. (2012) Drug screen targeted at Plasmodium liver stages identifies a potent multistage antimalarial drug J. Infect. Dis. 205, 1278-1286 10.1093/infdis/jis184
43. Srivastava, I. K., Morrisey, J. M., Darrouzet, E., Daldal, F., and Vaidya, A. B. (1999) Resistance mutations reveal the atovaquone-binding domain of cytochrome b in malaria parasites Mol. Microbiol. 33, 704-711 10.1046/j.1365-2958.1999.01515.x