Biochemical screening of five protein kinases from plasmodium falciparum against 14,000 Cell-Active compounds

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Crowther, Gregory J ^a   Hillesland, Heidi K ^a   Keyloun, Katelyn R ^a   Reid, Molly C ^a   Lafuente Monasterio, Maria Jose ^b   Ghidelli Disse, Sonja ^c   Leonard, Stephen E ^a   He, Panqing ^a   Jones, Jackson C ^a   Krahn, Mallory M ^a   Mo, Jack S ^a   Dasari, Kartheek S ^a   Fox, Anna M W ^a   Boesche, Markus ^c   Bakkouri, Majida El ^d   Rivas, Kasey L ^a   Leroy, Didier ^e   Hui, Raymond ^d   Drewes, Gerard ^c   Maly, Dustin J ^a   Van Voorhis, Wesley C ^a   Ojo, Kayode K ^a   more..

^a UNIVERSITY OF WASHINGTON   (United States)

^b GLAXOSMITHKLINE   (Spain)

^c GLAXOSMITHKLINE   (United Kingdom)

^d UNIVERSITY OF TORONTO   (Canada)

^e Medicines for Malaria Venture   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM DEPENDENT PROTEIN KINASE 1; CALCIUM DEPENDENT PROTEIN KINASE 4; DORAMAPIMOD; ENZYME INHIBITOR; GW 8510; HYMENIALDISINE; MITOGEN ACTIVATED PROTEIN KINASE 1; OLOMOUCINE; PROTEIN KINASE; PROTEIN KINASE 6; PROTEIN KINASE 6 INHIBITOR; PROTEIN KINASE 7; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT; CALCIUM; CALCIUM-DEPENDENT PROTEIN KINASE-1, PLASMODIUM FALCIPARUM; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PK7 PROTEIN, PLASMODIUM FALCIPARUM; PROTEIN KINASE INHIBITOR; PROTEIN KINASE PK60; PROTEIN SERINE THREONINE KINASE; PROTOZOAL PROTEIN;

ARTICLE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG POTENCY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; HEPG2 CELL LINE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC50; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN TARGETING; PROTEOMICS; DRUG EFFECTS; HEP-G2 CELL LINE; MALARIA, FALCIPARUM; METABOLISM; TUMOR CELL LINE;

ANTIMALARIALS; CALCIUM; CELL LINE, TUMOR; HEP G2 CELLS; HUMANS; MALARIA, FALCIPARUM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PLASMODIUM FALCIPARUM; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTOZOAN PROTEINS;

EID: 84962239755     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149996     Document Type: Article

References (44)

1. Kinnamon KE, Rothe WE. Biological screening in the U.S. Army antimalarial drug development program. Am J Trop Med Hyg 1975; 24: 174-178. PMID: 804264.
2. Plouffe D, Brinker A, McNamara C, Henson K, Kato N, Kuhen K, et al. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc Natl Acad Sci U S A 2008; 105: 9059-9064. doi:10.1073/pnas.0802982105 PMID: 18579783.
3. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, Lavandera JL, et al. Thousands of chemical starting points for antimalarial lead identification. Nature 2010; 465: 305-310. doi:10.1038/nature09107 PMID: 20485427.
4. Guiguemde WA, Shelat AA, Bouck D, Duffy S, Crowther GJ, Davis PH, et al. Chemical genetics of Plasmodium falciparum. Nature 2010; 465: 311-315. doi:10.1038/nature09099 PMID: 20485428.
5. Guiguemde WA, Shelat AA, Garcia-Bustos JF, Diagana TT, Gamo FJ, Guy RK. Global phenotypic screening for antimalarials. Chem Biol 2012; 19: 116-129. doi:10.1016/j.chembiol.2012.01.004 PMID: 22284359.
6. Cohen P. Targeting protein kinases for the development of anti-inflammatory drugs. Curr Opin Cell Biol 2009; 21: 317-324. doi:10.1016/j.ceb.2009.01.015 PMID: 19217767.
7. Schreiber M, Res I, Matter A. Protein kinases as antibacterial targets. Curr Opin Cell Biol 2009; 21: 325-330. doi:10.1016/j.ceb.2009.01.026 PMID: 19246185.
8. Doerig C, Abdi A, Bland N, Eschenlauer S, Dorin-Semblat D, Fennell C, et al. Malaria: Targeting parasite and host cell kinomes. Biochim Biophys Acta 2010; 1804: 604-612. doi:10.1016/j.bbapap.2009.10.009 PMID: 19840874.
9. Tewari R, Straschil U, Bateman A, Bohme U, Cherevach I, Gong P, et al. The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 2010; 8: 377-387. doi:10.1016/j.chom.2010.09.006 PMID: 20951971.
10. Solyakov L, Halbert J, Alam MM, Semblat JP, Dorin-Semblat D, Reininger L, et al. Global kinomic and phospho-proteomic analyses of the human malaria parasite Plasmodium falciparum. Nat Commun 2011; 2: 565. doi:10.1038/ncomms1558PMID: 22127061.
11. Dorin D, Alano P, Boccaccio I, Ciceron L, Doerig C, Sulpice R, et al. An atypical mitogen-activated protein kinase (MAPK) homologue expressed in gametocytes of the human malaria parasite Plasmodium falciparum. Identification of a MAPK signature. J Biol Chem 1999; 274: 29912-29920. PMID: 10514473.
12. Bracchi-Ricard V, Barik S, Delvecchio C, Doerig C, Chakrabarti R, Chakrabarti D. PfPK6, a novel cyclin-dependent kinase/mitogen-activated protein kinase-related protein kinase from Plasmodium falciparum. Biochem J 2000; 347 Pt 1: 255-263. PMID: 10727426.
13. Dorin D, Semblat JP, Poullet P, Alano P, Goldring JP, Whittle C, et al. PfPK7, an atypical MEK-related protein kinase, reflects the absence of classical three-component MAPK pathways in the human malaria parasite Plasmodium falciparum. Mol Microbiol 2005; 55: 184-196. PMID: 15612927.
14. Ojo KK, Pfander C, Mueller NR, Burstroem C, Larson ET, Bryan CM, et al. Transmission of malaria to mosquitoes blocked by bumped kinase inhibitors. J Clin Invest 2012; 122: 2301-2305. doi:10.1172/JCI61822PMID: 22565309.
15. Alonso PL B Q, Bell D, Berman P, Breman JG, de Savigny D, Drakeley C, Evans T, Block MA, Hanson K, Kachur SP, Kress D, Macdonald M, Newman RD, Nyonator FK, Pagnoni F, Perkins M, Schapira A, Schellenberg D, Slutsker L, Sullivan D, Tanner M, Teklehaimanot A, Teuscher T, Mendis K, Brown G. A research agenda for malaria eradication: health systems and operational research. Plos Med 2011; 8: e1000397. doi:10.1371/journal.pmed.1000397 PMID: 21311588.
16. Kato N, Sakata T, Breton G, Le Roch KG, Nagle A, Andersen C, et al. Gene expression signatures and small-molecule compounds link a protein kinase to Plasmodium falciparum motility. Nat Chem Biol 2008; 4: 347-356. doi:10.1038/nchembio.87 PMID: 18454143.
17. Billker O, Dechamps S, Tewari R, Wenig G, Franke-Fayard B, Brinkmann V. Calcium and a calciumdependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 2004; 117: 503-514. PMID: 15137943.
18. Rangarajan R, Bei AK, Jethwaney D, Maldonado P, Dorin D, Sultan AA, et al. A mitogen-activated protein kinase regulates male gametogenesis and transmission of the malaria parasite Plasmodium berghei. EMBO Rep 2005; 6: 464-469. PMID: 15864297.
19. Tewari R, Dorin D, Moon R, Doerig C, Billker O. An atypical mitogen-activated protein kinase controls cytokinesis and flagellar motility during male gamete formation in a malaria parasite. Mol Microbiol 2005; 58: 1253-1263. PMID: 16313614.
20. Dorin-Semblat D, Quashie N, Halbert J, Sicard A, Doerig C, Peat E, et al. Functional characterization of both MAP kinases of the human malaria parasite Plasmodium falciparum by reverse genetics. Mol Microbiol 2007; 65: 1170-1180. PMID: 17651389.
21. Dorin-Semblat D, Sicard A, Doerig C, Ranford-Cartwright L. Disruption of the PfPK7 gene impairs schizogony and sporogony in the human malaria parasite Plasmodium falciparum. Eukaryot Cell 2008; 7: 279-285. PMID: 18083830.
22. Spangenberg T, Burrows JN, Kowalczyk P, McDonald S, Wells TN, Willis P. The open access malaria box: a drug discovery catalyst for neglected diseases. Plos One 2013; 8: e62906. doi:10.1371/journal.pone.0062906 PMID: 23798988.
23. Vedadi M, Lew J, Artz J, Amani M, Zhao Y, Dong A, et al. Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol Biochem Parasitol 2007; 151: 100-110. PMID: 17125854.
24. Merckx A, Echalier A, Langford K, Sicard A, Langsley G, Joore J, et al. Structures of P. falciparum protein kinase 7 identify an activation motif and leads for inhibitor design. Structure 2008; 16: 228-238. doi:10.1016/j.str.2007.11.014 PMID: 18275814.
25. Bantscheff M, Eberhard D, Abraham Y, Bastuck S, Boesche M, Hobson S, et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nature biotechnology 2007; 25: 1035-1044. PMID: 17721511.
26. Bergamini G, Bell K, Shimamura S, Werner T, Cansfield A, Muller K, et al. A selective inhibitor reveals PI3Kgamma dependence of T(H)17 cell differentiation. Nature chemical biology 2012; 8: 576-582. doi:10.1038/nchembio.957 PMID: 22544264.
27. Bantscheff M, Hopf C, Savitski MM, Dittmann A, Grandi P, Michon AM, et al. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nature biotechnology 2011; 29: 255-265. doi:10.1038/nbt.1759 PMID: 21258344.
28. Savitski MM, Fischer F, Mathieson T, Sweetman G, Lang M, Bantscheff M. Targeted data acquisition for improved reproducibility and robustness of proteomic mass spectrometry assays. Journal of the American Society for Mass Spectrometry 2010; 21: 1668-1679. doi:10.1016/j.jasms.2010.01.012 PMID: 20171116.
29. Savitski MM, Mathieson T, Zinn N, Sweetman G, Doce C, Becher I, et al. Measuring and managing ratio compression for accurate iTRAQ/TMT quantification. Journal of proteome research 2013; 12: 3586-3598. doi:10.1021/pr400098r PMID: 23768245.
30. Savitski MM, Sweetman G, Askenazi M, Marto JA, Lang M, Zinn N, et al. Delayed fragmentation and optimized isolation width settings for improvement of protein identification and accuracy of isobaric mass tag quantification on Orbitrap-type mass spectrometers. Analytical chemistry 2011; 83: 8959- 8967. doi:10.1021/ac201760x PMID: 22017476.
31. Zhang JH, Chung TD, Oldenburg KR. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999; 4: 67-73. PMID: 10838414.
32. Talevich E, Tobin AB, Kannan N, Doerig C. An evolutionary perspective on the kinome of malaria parasites. Philos Trans R Soc Lond B Biol Sci 2012; 367: 2607-2618. doi:10.1098/rstb.2012.0014PMID: 22889911.
33. Bouloc N, Large JM, Smiljanic E, Whalley D, Ansell KH, Edlin CD, et al. Synthesis and in vitro evaluation of imidazopyridazines as novel inhibitors of the malarial kinase PfPK7. Bioorg Med Chem Lett 2008; 18: 5294-5298. doi:10.1016/j.bmcl.2008.08.043 PMID: 18774709.
34. Crowther GJ, He P, Rodenbough PP, Thomas AP, Kovzun KV, Leibly DJ, et al. Use of thermal melt curves to assess the quality of enzyme preparations. Anal Biochem 2010; 399: 268-275. doi:10.1016/j.ab.2009.12.018 PMID: 20018159.
35. Manhani KK, Arcuri HA, da Silveira NJ, Uchoa HB, de Azevedo WF Jr, Canduri F. Molecular models of protein kinase 6 from Plasmodium falciparum. J Mol Model 2005; 12: 42-48. PMID: 16096806.
36. Lemercier G, Fernandez-Montalvan A, Shaw JP, Kugelstadt D, Bomke J, Domostoj M, et al. Identification and characterization of novel small molecules as potent inhibitors of the plasmodial calcium-dependent protein kinase 1. Biochemistry 2009; 48: 6379-6389. doi:10.1021/bi9005122 PMID: 19507895.
37. Larson ET, Ojo KK, Murphy RC, Johnson SM, Zhang Z, Kim JE, et al. Multiple determinants for selective inhibition of apicomplexan calcium-dependent protein kinase CDPK1. J Med Chem 2012; 55: 2803-2810. doi:10.1021/jm201725v PMID: 22369268.
38. Zhang Z, Ojo KK, Johnson SM, Larson ET, He P, Geiger JA, et al. Benzoylbenzimidazole-based selective inhibitors targeting Cryptosporidium parvum and Toxoplasma gondii calcium-dependent protein kinase-1. Bioorg Med Chem Lett 2012; 22: 5264-5267. doi:10.1016/j.bmcl.2012.06.050 PMID: 22795629.
39. Lourido S, Zhang C, Lopez MS, Tang K, Barks J, Wang Q, et al. Optimizing small molecule inhibitors of calcium-dependent protein kinase 1 to prevent infection by Toxoplasma gondii. J Med Chem 2013; 56: 3068-3077. doi:10.1021/jm4001314 PMID: 23470217.
40. Keyloun KR, Reid MC, Choi R, Song Y, Fox AM, Hillesland HK, et al. The gatekeeper residue and beyond: homologous calcium-dependent protein kinases as drug development targets for veterinarian Apicomplexa parasites. Parasitology 2014; 141: 1499-1509. doi:10.1017/S0031182014000857PMID: 24927073.
41. Crowther GJ, Napuli AJ, Gilligan JH, Gagaring K, Borboa R, Francek C, et al. Identification of inhibitors for putative malaria drug targets among novel antimalarial compounds. Mol Biochem Parasitol 2011; 175: 21-29. doi:10.1016/j.molbiopara.2010.08.005 PMID: 20813141.
42. Theobald AJ, Caballero I, Coma I, Colmenarejo G, Cid C, Gamo FJ, et al. Discovery and biochemical characterization of Plasmodium thioredoxin reductase inhibitors from an antimalarial set. Biochemistry 2012; 51: 4764-4771. doi:10.1021/bi3005076PMID: 22612231.
43. Spillman NJ, Allen RJ, McNamara CW, Yeung BK, Winzeler EA, Diagana TT, et al. Na(+) regulation in the malaria parasite Plasmodium falciparum involves the cation ATPase PfATP4 and is a target of the spiroindolone antimalarials. Cell Host Microbe 2013; 13: 227-237. doi:10.1016/j.chom.2012.12.006 PMID: 23414762.
44. Baragana B, Hallyburton I, Lee MC, Norcross NR, Grimaldi R, Otto TD, et al. A novel multiple-stage antimalarial agent that inhibits protein synthesis. Nature 2015; 522: 315-320. doi:10.1038/nature14451 PMID: 26085270 Biochemical Screening of Five Protein Kinases from P. falciparum.