The gatekeeper residue and beyond: Homologous calcium-dependent protein kinases as drug development targets for veterinarian Apicomplexa parasites

Parasitology

Volumn 141, Issue 11, 2014, Pages 1499-1509

  Keyloun, Katelyn R ^a   Reid, Molly C ^a   Choi, Ryan ^a   Song, Yifan ^b   Fox, Anna M W ^a   Hillesland, Heidi K ^a   Zhang, Zhongsheng ^b   Vidadala, Ramasubbarao ^a   Merritt, Ethan A ^b   Lau, Audrey O T ^c   Maly, Dustin J ^a   Fan, Erkang ^b   Barrett, Lynn K ^a   Van Voorhis, Wesley C ^a   Ojo, Kayode K ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Apicomplexa; Bumped kinase inhibitors; Calcium dependent protein kinases

Indexed keywords

GLYCINE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE C; PROTOZOAL PROTEIN; SERINE; THREONINE; CALCIUM-DEPENDENT PROTEIN KINASE; MOLECULAR LIBRARY; PROTEIN KINASE; PROTEIN KINASE INHIBITOR;

BABESIA BOVIS; BINDING SITE; CONFERENCE PAPER; CONTROLLED STUDY; CRYPTOSPORIDIUM PARVUM; CRYSTAL STRUCTURE; CYTOTOXICITY; EIMERIA TENELLA; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NEOSPORA CANINUM; NONHUMAN; PARASITE SURVIVAL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN TARGETING; STRUCTURE ACTIVITY RELATION; TOXOPLASMA GONDII; VETERINARY MEDICINE; WILD TYPE; ANIMAL; APICOMPLEXA; CATERING SERVICE; CELL LINE; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR LIBRARY; NEOSPORA; PARASITOLOGY; PROTOZOAN INFECTIONS;

ANIMALS; APICOMPLEXA; BABESIA BOVIS; CELL LINE; CELL SURVIVAL; EIMERIA TENELLA; FOOD SUPPLY; HUMANS; MODELS, MOLECULAR; NEOSPORA; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTOZOAN INFECTIONS; PROTOZOAN PROTEINS; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP; VETERINARY MEDICINE;

EID: 84906789900     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014000857     Document Type: Conference Paper

References (28)

1. Alexandrov, A., Vignali, M., LaCount, D. J., Quartley, E., de Vries, C., De Rosa, D., Babulski, J., Mitchell, S. F., Schoenfeld, L.W., Fields, S., Hol,W. G., Dumont, M. E., Phizicky, E. M. and Grayhack, E. J. (2004). A facile method for high-throughput co-expression of protein pairs. Molecular and Cellular Proteomics 3, 934-938. doi: 10.1074/mcp.T400008-MCP200.
2. Castellanos-Gonzalez, A., White, A. C., Ojo, K. K., Vidadala, R. S., Zhang, Z., Reid, M. C., Fox, A. M., Keyloun, K. R., Rivas, K., Irani, A., Dann, S. M., Fan, E., Maly, D. J. and Van Voorhis,W. C. (2013). A novel calcium-dependent protein kinase inhibitor as a lead compound for treating cryptosporidiosis. Journal of Infectious Diseases 208, 1342-1348. doi: 10.1093/infdis/jit327.
3. Doggett, J. S., Ojo, K. K., Fan, E., Maly, D. J. and Van Voorhis, W. C. (2014). Bumped kinase inhibitor 1294 treats established Toxoplasma gondii infection. Antimicrobial Agents and Chemotherapy 58, 3547-3549. AAC 01823-13.
4. Guinovart, C., Navia, M. M., Tanner, M. and Alonso, P. L. (2006). Malaria: burden of disease. Current Molecular Medicine 6, 137-140.
5. Johnson, S. M., Murphy, R. C., Geiger, J. A., DeRocher, A. E., Zhang, Z., Ojo, K. K., Larson, E. T., Perera, B. G., Dale, E. J., He, P., Reid, M. C., Fox, A. M., Mueller, N. R., Merritt, E. A., Fan, E., Parsons, M., Van Voorhis, W. C. and Maly, D. J. (2012). Development of Toxoplasma gondii calcium-dependent protein kinase 1 (TgCDPK1) inhibitors with potent anti-toxoplasma activity. Journal of Medicinal Chemistry 55, 2416-2426. doi: 10.1021/jm201713h.
6. Katlama, C., De Wit, S., O'Doherty, E., Van Glabeke, M. and Clumeck, N. (1996). Pyrimethamine-clindamycin vs. pyrimethaminesulfadiazine as acute and long-term therapy for toxoplasmic encephalitis in patients with AIDS. Clinical Infectious Diseases 22, 268-275.
7. Larson, E. T., Ojo, K. K., Murphy, R. C., Johnson, S. M., Zhang, Z., Kim, J. E., Leibly, D. J., Fox, A. M., Reid, M. C., Dale, E. J., Perera, B. G., Kim, J., Hewitt, S. N., Hol, W. G., Verlinde, C. L., Fan, E., Van Voorhis, W. C., Maly, D. J. and Merritt, E. A. (2012). Multiple determinants for selective inhibition of apicomplexan calciumdependent protein kinase CDPK1. Journal of Medicinal Chemistry 55, 2803-2810. doi: 10.1021/jm201725v.
8. Livingstone, C. D. and Barton, G. J. (1993). Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Computer Applications in the Biosciences 9, 745-756.
9. (2+) release from inositol 1,4,5-triphosphate (IP(3))/ryanodine-sensitive stores. Journal of Biological Chemistry 277, 25870-25876. doi: 10.1074/jbc. M202553200.
10. Luft, B. J., Hafner, R., Korzun, A. H., Leport, C., Antoniskis, D., Bosler, E. M., Bourland, D. D., Uttamchandani, R., Fuhrer, J. and Jacobson, J. (1993). Toxoplasmic encephalitis in patients with the acquired immunodeficiency syndrome. Members of the ACTG 077p/ANRS 009 Study Team. New England Journal of Medicine 329, 995-1000. doi: 10.1056/ NEJM199309303291403.
11. Mehlin, C., Boni, E., Buckner, F. S., Engel, L., Feist, T., Gelb, M. H., Haji, L., Kim, D., Liu, C., Mueller, N., Myler, P. J., Reddy, J. T., Sampson, J. N., Subramanian, E., Van Voorhis, W. C., Worthey, E., Zucker, F. and Hol, W. G. (2006). Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes. Molecular and Biochemical Parasitology 148, 144-160. doi: 10.1016/j.molbiopara. 2006.03.011.
12. Morrissette, N. S. and Sibley, L.D. (2002). Cytoskeleton of apicomplexan parasites. Microbiology and Molecular Biology Reviews 66, 21-38.
13. Murphy, R. C., Ojo, K. K., Larson, E. T., Castellanos-Gonzalez, A., Perera, B. G., Keyloun, K. R., Kim, J. E., Bhandari, J. G., Muller, N. R., Verlinde, C. L., White, A. C., Merritt, E. A., Van Voorhis, W. C. and Maly, D. J. (2010). Discovery of potent and selective inhibitors of calcium-dependent protein kinase 1 (CDPK1) from C. parvum and T. gondii. ACS Medicinal Chemistry Letters 1, 331-335. doi: 10.1021/ ml100096t.
14. Nair, S. C., Brooks, C. F., Goodman, C. D., Strurm, A., McFadden, G. I., Sundriyal, S., Anglin, J. L., Song, Y., Moreno, S. N. J. and Striepen, B. (2011). Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. Journal of Experimental Medicine 208, 1547-1559. doi: 10.1084/ jem.20110039.
15. Norrby, R. (1978). A review of the penetration of antibiotics into CSF and its clinical significance. Scandinavian Journal of Infectious Diseases (Suppl. 4), 296-309.
16. Ojo, K. K., Larson, E. T., Keyloun, K. R., Castaneda, L. J., Derocher, A. E., Inampudi, K. K., Kim, J. E., Arakaki, T. L., Murphy, R. C., Zhang, L., Napuli, A. J., Maly, D. J., Verlinde, C. L., Buckner, F. S., Parsons, M., Hol, W. G., Merritt, E. A. and Van Voorhis, W. C. (2010). Toxoplasma gondii calcium-dependent protein kinase 1 is a target for selective kinase inhibitors. Nature Structural and Molecular Biology 17, 602-607. doi: 10.1038/nsmb.1818.
17. Ojo, K. K., Arakaki, T. L., Napuli, A. J., Inampudi, K. K., Keyloun, K. R., Zhang, L., Hol, W. G., Verlinde, C. L., Merritt, E. A. and Van Voorhis, W. C. (2011). Structure determination of glycogen synthase kinase-3 from Leishmania major and comparative inhibitor structure-activity relationships with Trypanosoma brucei GSK-3. Molecular and Biochemical Parasitology 176, 98-108. doi: 10.1016/j. molbiopara.2010.12.009.
18. Ojo, K. K., Pfander, C., Mueller, N. R., Burstroem, C., Larson, E. T., Bryan, C. M., Fox, A. M., Reid, M. C., Johnson, S. M., Murphy, R. C., Kennedy, M., Mann, H., Leibly, D. J., Hewitt, S. N., Verlinde, C. L., Kappe, S., Merritt, E. A., Maly, D. J., Billker, O. and Van Voorhis, W. C. (2012). Transmission of malaria to mosquitoes blocked by bumped kinase inhibitors. Journal of Clinical Investigation 122, 2301-2305. doi: 10.1172/JCI61822.
19. Ojo, K. K., Merritt, E. A., Maly, D. J. and Van Voorhis, W. C. (2013). Calcium-dependent protein kinases of Apicomplexan parasites as drug targets. In Protein Phosphorylation in Parasites: Novel Targets for Antiparasitic Intervention (ed. Doerig, C., Späth, G. and Wiese, M.), pp. 293-316. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany. doi: 10.1002/9783527675401.ch14.
20. Ojo, K. K., Eastman, R. T., Vidadala, R., Zhang, Z., Rivas, K. L., Choi, R., Lutz, J. D., Reid, M. C., Fox, A. M., Hulverson, M. A., Kennedy, M., Isoherranen, N., Kim, L. M., Comess, K. M., Kempf, D. J., Verlinde, C. L., Su, X. Z., Kappe, S. H., Maly, D. J., Fan, E. and Van Voorhis, W. C. (2014). A specific inhibitor of PfCDPK4 blocks malaria transmission: chemicalgenetic validation. Journal of Infectious Diseases 209, 275-284. doi: 10.1093/ infdis/jit522.
21. Reeves, D. S. and Wilkinson, P. J. (1979). The pharmacokinetics of trimethoprim and trimethoprim/sulphonamide combinations, including penetration into body tissues. Infection 7 (Suppl. 4), S330-S341.
22. Seeliger, M. A., Young, M., Henderson, M. N., Pellicena, P., King, D. S., Falick, A. M. and Kuriyan, J. (2005). High yield bacterial expression of active c-Abl and c-Src tyrosine kinases. Protein Science 14, 3135-3139. doi: 10.1110/ps.051750905.
23. Studier, F.W. (2005). Protein production by auto-induction in high density shaking cultures. Protein Expression and Purification 41, 207-234.
24. Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217-1258.
25. Vidadala, R. S., Ojo, K. K., Johnson, S. M., Zhang, Z., Leonard, S. E., Mitra, A., Choi, R., Reid, M. C., Keyloun, K. R., Fox, A. M., Kennedy, M., Silver-Brace, T., Hume, J. C., Kappe, S., Verlinde, C. L., Fan, E., Merritt, E. A., Van Voorhis, W. C. and Maly, D. J. (2014). Development of potent and selective Plasmodium falciparum calcium-dependent protein kinase 4 (PfCDPK4) inhibitors that block the transmission of malaria to mosquitoes. European Journal of Medicinal Chemistry 74C, 562-573.
26. World Health Organization. 2013, World Malaria Report 2013. 1-2. Publications of the World Health Organization, Geneva, Switzerland.
27. Zhang, J. H., Chung, T. D. and Oldenburg, K. R. (1999). A simple statistical parameter for use in evaluation and validation of high throughput screening assays. Journal of Biomolecular Screening 4, 67-73.
28. Zhang, Z., Ojo, K. K., Johnson, S. M., Larson, E. T., He, P., Geiger, J. A., Castellanos-Gonzalez, A., White, A. C., Parsons, M., Merritt, E. A., Maly, D. J., Verlinde, C. L., Van Voorhis, W. C. and Fan, E. (2012). Benzoylbenzimidazole-based selective inhibitors targeting Cryptosporidium parvum and Toxoplasma gondii calcium-dependent protein kinase-1. Bioorganic and Medicinal Chemistry Letters 22, 5264-5267. doi: 10.1016/j.bmcl.2012.06.050.