Calcium-Dependent Protein Kinases of Apicomplexan Parasites as Drug Targets

Protein Phosphorylation in Parasites: Novel Targets for Antiparasitic Intervention

Volumn , Issue , 2013, Pages 293-315

  Ojo, Kayode K ^a   Merritt, Ethan A ^a   Maly, Dustin J ^b   van Voorhis, Wesley C ^a  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85017366806     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527675401.ch14     Document Type: Chapter

References (46)

1. Pape, J.W., Verdier, R.I., and Johnson, W.D. Jr (1989) Treatment and prophylaxis of Isospora belli infection in patients with the acquired immunodeficiency syndrome. N. Engl.]. Med., 320, 1044-1047.
2. Tram, N.T., Hoang, L.M., Cam, P.D., Chung, P.T., Fyfe, M.W., Isaac-Renton, J.L., and Ong, C.S. (2008) Cyclospora spp. in herbs and water samples collected from markets and farms in Hanoi, Vietnam. Trop. Med. Int. Health, 13, 1415-1420.
3. Breman, J.G., Alilio, M.S., and Mills, A. (2004) Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am. J. Trop. Med. Hyg., 71, 1-15.
4. Carme, B., Bissuel, F., Ajzenberg, D., Bouyne, R., Aznar, C., Demar, M., Bichat, S., Louvel, D., Bourbigot, A.M., Peneau, C., Neron, P., and Darde, M.L. (2002) Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana. J. Clin. Microbiol., 40, 4037-4044.
5. Rossignol, J.F., Ayoub, A., and Ayers, M.S. (2001) Treatment of diarrhea caused by Cryptosporidium parvum: a prospective randomized, double-blind, placebo-controlled study ofNitazoxanide. J. Infect. Dis., 184, 103-106.
6. Miners, J.O. and Birkett, D.J. (1998) Cytochrome P4502C9: an enzyme ofmajor importance in human drug metabolism. Br. J. Clin. Pharmacol., 45, 525-538.
7. Gimnig, J.E., MacArthur, J.R., M'bang'ombe, M., Kramer, M.H., Chizani, N., Stern, R.S., Mkandala, C., Newman, R. D., Steketee, R.W., and Campbell, C.H. (2006) Severe cutaneous reactions to sulfadoxine-pyrimethamine and trimethoprim-sulfamethoxazole in Blantyre District, Malawi. Am. J. Trop. Med. Hyg., 74, 738-743.
8. McFarland, L.V. (1998) Epidemiology, risk factors and treatments for antibiotic-associated diarrhea. Dig. Dis., 16, 292-307.
9. Boothroyd, J.C. and Dubremetz, J.F. (2008) Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat. Rev. Microbiol., 6, 79-88.
10. Carruthers, V.B. and Sibley, L.D. (1997) Sequential protein secretion from three distinct organelles ofToxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol., 73, 114-123.
11. Lovett, J.L., Marchesini, N., Moreno, S.N., and Sibley, L.D. (2002) Toxoplasma gondii microneme secretion involves intracellular Ca(2+) release from inositol 1, 4, 5-triphosphate (IP(3))/ryanodine-sensitive stores. J. Biol. Chem., 277, 25870-25876.
12. Lovett, J.L. and Sibley, L.D. (2003) Intracellular calcium stores in Toxoplasma gondii govern invasion of host cells. J. Cell Sci., 116, 3009-3016.
13. Billker, O., Lourido, S., and Sibley, L.D. (2009) Calcium-dependent signaling and kinases in apicomplexan parasites. Cell Host Microbe, 5, 612-622.
14. Raichaudhuri, A., Bhattacharyya, R., Chaudhuri, S., Chakrabarti, P., and Dasgupta, M. (2006) Domain analysis ofa groundnut calcium-dependent protein kinase: nuclear localization sequence in the junction domain is coupled with nonconsensus calcium binding domains. J. Biol. Chem., 281, 10399-10409.
15. Wernimont, A.K., Artz, J.D., Finerty, P., Lin, Y.H., Amani, M., Allali-Hassani, A., Senisterra, G., Vedadi, M., Tempel, W., Mackenzie, F., Chau, I., Lourido, S., Sibley, L.D., and Hui, R. (2010) Structures of apicomplexan calcium-dependent protein kinases reveal mechanism ofactivation by calcium. Nat. Struct. Mol. Biol., 17, 596-601.
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.M.J., Buckner, F.S., Parsons, M., Hol, W.G.J., Merritt, E.A., and Van Voorhis, W.C. (2010) Toxoplasma gondii calciumdependent protein kinase 1 is a target for selective kinase inhibitors. Nat. Struct. Mol. Biol., 17, 602-607.
17. Murphy, R.C., Ojo, K.K., Larson, E.T., Castellanos-Gonzalez, A., Perera, B.G.K., Keyloun, K.R., Kim, J.E., Bhandari, J.G., Muller, N.R., Verlinde, C.L.M.J., White, A. C., Merritt, E.A., Van Voorhis, W.C., and Maly, D.J. (2010) Discovery of potent and selective inhibitors ofCDPK1 from C. parvum and T. gondii. ACS Med. Chem. Lett., 1, 331-335.
18. Kato, N., Sakata, T., Breton, G., Le Roch, K. G., Nagle, A., Andersen, C., Bursulaya, B., Henson, K., Johnson, J., Kumar, K.A., Marr, F., Mason, D., McNamara, C., Plouffe, D., Ramachandran, V., Spooner, M., Tuntland, T., Zhou, Y., Peters, E.C., Chatterjee, A., Schultz, P.G., Ward, G.E., Gray, N., Harper, J., and Winzeler, E.A. (2008) Gene expression signatures and small-molecule compounds link a protein kinase to Plasmodium falciparum motility. Nat. Chem. Biol., 4, 347-356.
19. Dvorin, J.D., Martyn, D.C., Patel, S.D., Grimley, J.S., Collins, C.R., Hopp, C.S., Bright, A.T., Westenberger, S., Winzeler, E., Blackman, M.J., Baker, D.A., Wandless, T.J., and Duraisingh, M.T. (2010) A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science, 328, 910-912.
20. Siden-Kiamos, I., Ecker, A., Nyback, S., Louis, C., Sinden, R.E., and Billker, O. (2006) Plasmodium berghei calciumdependent protein kinase 3 is required for ookinete gliding motility and mosquito midgut invasion. Mol. Microbiol., 60, 1355-1363.
21. Coppi, A., Tewari, R., Bishop, J.R., Bennett, B.L., Lawrence, R., Esko, J.D., Billker, O., and Sinnis, P. (2007) Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe, 2, 316-327.
22. Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B., and Brinkmann, V. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell, 117, 503-514.
23. 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. J. Clin. Invest., 122 (6), 2301-2305.
24. Ojo, K.K., Gillespie, J.R., Riechers, A.J., Napuli, A.J., Verlinde, C.L., Buckner, F.S., Gelb, M.H., Domostoj, M.M., Wells, S.J., Scheer, A., Wells, T.N., and Van Voorhis, W. C. (2008) Glycogen synthase kinase 3 is a potential drug target for African trypanosomiasis therapy. Antimicrob. Agents Chemother., 52, 3710-3717.
25. Carter, T.A., Wodicka, L.M., Shah, N.P., Velasco, A.M., Fabian, M.A., Treiber, D.K., Milanov, Z.V., Atteridge, C.E., Biggs, W.H. III, Edeen, P.T., Floyd, M., Ford, J.M., Grotzfeld, R.M., Herrgard, S., Insko, D.E., Mehta, S.A., Patel, H.K., Pao, W., Sawyers, C.L., Varmus, H., Zarrinkar, P.P., and Lockhart, D.J. (2005) Inhibition ofdrug-resistant mutants ofABL, KIT, and EGF receptor kinases. Proc. Natl Acad. Sci. USA, 102, 11011-11016.
26. Fabian, M.A., Biggs J III, W.H., Treiber, D. K., Atteridge, C.E., Azimioara, M.D., Benedetti, M.G., Carter, T.A., Ciceri, P., Edeen, P.T., Floyd, M., Ford, J.M., Galvin, M., Gerlach, J.L., Grotzfeld, R.M., Herrgard, S., Insko, D.E., Insko, M.A., Lai, A.G., Lelias, J.M., Mehta, S.A., Milanov, Z.V., Velasco, A.M., Wodicka, L.M., Patel, H.K., Zarrinkar, P.P., and Lockhart, D.J. (2005) A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol., 23, 329-336.
27. Fedorov, O., Marsden, B., Pogacic, V., Rellos, P., Muller, S., Bullock, A.N., Schwaller, J., Sundstrom, M., and Knapp, S. (2007) A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc. Natl Acad. Sci. USA, 104, 20523-20528.
28. Karaman, M.W., Herrgard, S., Treiber, D.K., Gallant, P., Atteridge, C.E., Campbell, B.T., Chan, K.W., Ciceri, P., Davis, M.I., Edeen, P.T., Faraoni, R., Floyd, M., Hunt, J.P., Lockhart, D.J., Milanov, Z.V., Morrison, M.J., Pallares, G., Patel, H.K., Pritchard, S., Wodicka, L.M., andZarrinkar, P.P. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol., 26, 127-132.
29. Blencke, S., Zech, B., Engkvist, O., Greff, Z., Orfi, L., Horvath, Z., Keri, G., Ullrich, A., and Daub, H. (2004) Characterization of a conserved structural determinant controlling protein kinase sensitivity to selective inhibitors. Chem. Biol., 11, 691-701.
30. Liu, Y., Bishop, A., Witucki, L., Kraybill, B., Shimizu, E., Tsien, J., Ubersax, J., Blethrow, J., Morgan, D.O., and Shokat, K.M. (1999) Structural basis for selective inhibition of Src family kinases by PP1. Chem. Biol., 6, 671-678.
31. Gum, R.J., McLaughlin, M.M., Kumar, S., Wang, Z., Bower, M.J., Lee, J.C., Adams, J. L., Livi, G.P., Goldsmith, E.J., and Young, P. R. (1998) Acquisition ofsensitivity ofstress-activated protein kinases to the p38 inhibitor, SB 203580, by alteration ofone or more amino acids within the ATP binding pocket. J. Biol. Chem., 273, 15605-15610.
32. Wang, Z., Canagarajah, B.J., Boehm, J.C., Kassisa, S., Cobb, M.H., Young, P.R., Abdel- Meguid, S., Adams, J.L., and Goldsmith, E.J. (1998) Structural basis ofinhibitor selectivity in MAP kinases. Structure, 6, 1117-1128.
33. Schindler, T., Bornmann, W., Pellicena, P., Miller, W.T., Clarkson, B., and Kuriyan, J. (2000) Structural mechanism for STI-571 inhibition of Abelson tyrosine kinase. Science, 289, 1938-1942.
34. Bishop, A.C., Buzko, O., and Shokat, K.M. (2001) Magic bullets for protein kinases. Trends Cell Biol., 11, 167-172.
35. Bishop, A.C., Kung, C.Y., Shah, K., Witucki, L., Shokat, K.M., and Liu, Y. (1999) Generation of monospecific nanomolar tyrosine kinase inhibitors via a chemical genetic approach. J. Am. Chem. Soc., 121, 627-631.
36. Bishop, A.C., Ubersax, J.A., Petsch, D.T., Matheos, D.P., Gray, N.S., Blethrow, J., Shimizu, E., Tsien, J.Z., Schultz, P.G., Rose, M.D., Wood, J.L., Morgan, D.O., and Shokat, K.M. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature, 407, 395-401.
37. Doerig, C., Meijer, L., and Mottram, J.C. (2002) Protein kinases as drug targets in parasitic protozoa. Trends Parasitol., 18, 366-371.
38. Greenbaum, D.C. (2008) Is chemical genetics the new frontier for malaria biology? Trends Pharmacol. Sci., 29, 51-56.
39. Cohen, P. (2002) Protein kinases - the major drug targets of the twenty-first century? Nat. Rev. Drug Discovery, 1, 309-315.
40. Zhang, J.M., Yang, P.L., and Gray, N.S. (2009) Targeting cancer with small molecule kinase inhibitors. Nat. Rev. Cancer, 9, 28-39.
41. Krishnamurty, R. and Maly, D.J. (2007) Chemical genomic and proteomic methods for determining kinase inhibitor selectivity. Comb. Chem. High-Throughput Screen., 10, 652-666.
42. Noble, M.E., Endicott, J.A., and Johnson, L. N. (2004) Protein kinase inhibitors: insights into drug design from structure. Science, 303, 1800-1805.
43. 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 ofToxoplasma gondii calciumdependent protein kinase 1 (TgCDPK1) inhibitors with potent anti-Toxoplasma activity. J. Med. Chem., 55, 2416-2426.
44. Wang, H., Shimizu, E., Tang, Y.P., Cho, M., Kyin, M., Zuo, W., Robinson, D.A., Alaimo, P.J., Zhang, C., Morimoto, H., Zhuo, M., Feng, R., Shokat, K.M., and Tsien, J.Z. (2003) Inducible protein knockout reveals temporal requirement ofCaMKII reactivation for memory consolidation in the brain. Proc. Natl Acad. Sci. USA, 100, 4287-4292.
45. 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. J. Med. Chem., 55, 2803-2810.
46. Chen, X.M., O'Hara, S.P., Huang, B.Q., Nelson, J.B., Lin, J.J., Zhu, G., Ward, H.D., and LaRusso, N.F. (2004) Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infect. Immun., 72, 6806-6816.