Functional analysis of protein kinase CK2 of the human malaria parasite Pasmodium falciparum

Eukaryotic Cell

Volumn 8, Issue 3, 2009, Pages 388-397

  Holland, Zoë ^a   Prudent, Renaud ^b,c   Reiser, Jean Baptiste ^d   Cochet, Claude ^b,c   Doerig, Christian ^a,e  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b INSERM   (France)

^c UNIV GRENOBLE ALPES   (France)

^d CEA GRENOBLE   (France)

^e EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; MAMMALIA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 61949442464     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00334-08     Document Type: Article

References (57)

1. Ahmed, K., D. A. Gerber, and C. Cochet. 2002. Joining the cell survival squad: an emerging role for protein kinase CK2. Trends Cell Biol. 12:226-230.
2. Allende, J. E., and C. C. Allende. 1995. Protein kinases 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J. 9:313-323.
3. Anamika, N. Srinivasan, and A. Krupa. 2005. A genomic perspective of protein kinases in Plasmodium falciparum. Proteins 58:180-189.
4. Armstrong, C. M., and D. E. Goldberg. 2007. An FKBP destabilization domain modulates protein levels in Plasmodium falciparum. Nat. Methods 4:1007-1009.
5. Bain, J., L. Plater, M. Elliott, N. Shpiro, C. J. Hastie, H. McLauchlan, I. Klevernic, J. S. Arthur, D. R. Alessi, and P. Cohen. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408:297-315.
6. Bibby, A. C., and D. W. Litchfield. 2005. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2β. Int. J. Biol. Sci. 1:67-79.
7. Bozdech, Z., M. Llinas, B. L. Pulliam, E. D. Wong, J. Zhu, and J. L. DeRisi. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:E5.
8. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Breman, J. G. 2001. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am. J. Trop. Med. Hyg. 64:1-11.
10. Breman, J. G., M. S. Alilio, and A. Mills. 2004. Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am. J. Trop. Med. Hyg. 71:1-15.
11. Chan, P. K., M. Aldrich, R. G. Cook, and H. Busch. 1986. Amino acid sequence of protein B23 phosphorylation site. J. Biol. Chem. 261:1868-1872.
12. Chantalat, L., D. Leroy, O. Filhol, A. Nueda, M. J. Benitez, E. M. Chambaz, C. Cochet, and O. Dideberg. 1999. Crystal structure of the human protein kinase CK2 regulatory subunit reveals its zinc finger-mediated dimerization. EMBO J. 18:2930-2940.
13. Cohen, P. 2002. Protein kinases - the major drug targets of the twenty-first century? Nat. Rev. Drug Discov. 1:309-315.
14. Doerig, C. 2004. Protein kinases as targets for anti-parasitic chemotherapy. Biochim. Biophys. Acta 1697:155-168.
15. Doerig, C., and L. Meijer. 2007. Antimalarial drug discovery: targeting protein kinases. Expert Opin. Ther. Targets. 11:279-290.
16. Fidock, D. A., T. Nomura, R. A. Cooper, X. Su, A. K. Talley, and T. E. Wellems. 2000. Allelic modifications of the cg2 and cg1 genes do not alter the chloroquine response of drug-resistant Plasmodium falciparum. Mol. Biochem. Parasitol. 110:1-10.
17. Fidock, D. A., and T. E. Wellems. 1997. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc. Natl. Acad. Sci. USA 94:10931-10936.
18. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, I. T. Paulsen, K. James, J. A. Eisen, K. Rutherford, S. L. Salzberg, A. Craig, S. Kyes, M. S. Chan, V. Nene, S. J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M. W. Mather, A. B. Vaidya, D. M. Martin, A. H. Fairlamb, M. J. Fraunholz, D. S. Roos, S. A. Ralph, G. I. McFadden, L. M. Cummings, G. M. Subramanian, C. Mungall, J. C. Venter, D. J. Carucci, S. L. Hoffman, C. Newbold, R. W. Davis, C. M. Fraser, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
19. Gietz, R. D., K. C. Graham, and D. W. Litchfield. 1995. Interactions between the subunits of casein kinase II. J. Biol. Chem. 270:13017-13021.
20. Glass, D. B., R. A. Masaracchia, J. R. Feramisco, and B. E. Kemp. 1978. Isolation of phosphorylated peptides and proteins on ion exchange papers. Anal. Biochem. 87:566-575.
21. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
22. Hanks, S. K., and A. M. Quinn. 1991. Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Methods Enzymol. 200:38-62.
23. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
24. Kikkawa, U., S. K. O. Mann, R. A. Firtel, and T. Hunter. 1992. Molecular cloning of casein kinase II α subunit from Dictyostelium discoideum and its expression in the life cycle. Mol. Cell. Biol. 12:5711-5723.
25. Kuenzel, E. A., J. A. Mulligan, J. Sommercorn, and E. G. Krebs. 1987. Substrate specificity determinants for casein kinase II as deduced from studies with synthetic peptides. J. Biol. Chem. 262:9136-9140.
26. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
27. Laudet, B. A., C. Barette, V. Dulery, O. Renaudet, P. Dumy, A. Metz, R. Prudent, A. Deshiere, O. Dideberg, O. Filhol, and C. Cochet. 2007. Structure-based design of small peptide inhibitors of protein kinase CK2 subunit interaction. Biochem. J. 408:363-373.
28. Le Roch, K. G., Y. Zhou, P. L. Blair, M. Grainger, J. K. Moch, J. D. Haynes, P. De La Vega, A. A. Holder, S. Batalov, D. J. Carucci, and E. A. Winzeler. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503-1508.
29. Leroy, D., O. Filhol, N. Quintaine, D. Sarrouilhe, P. Loue-Mackenbach, E. M. Chambaz, and C. Cochet. 1999. Dissecting subdomains involved in multiple functions of the CK2β subunit. Mol. Cell. Biochem. 191:43-50.
30. Litchfield, D. W., F. J. Lozeman, M. F. Cicirelli, M. Harrylock, L. H. Ericsson, C. J. Piening, and E. G. Krebs. 1991. Phosphorylation of the beta subunit of casein kinase II in human A431 cells. Identification of the autophosphorylation site and a site phosphorylated by p34cdc2. J. Biol. Chem. 266:20380-20389.
31. Lou, D. Y., I. Dominguez, P. Toselli, E. Landesman-Bollag, C. O'Brien, and D. C. Seldin. 2008. The alpha catalytic subunit of protein kinase CK2 is required for mouse embryonic development. Mol. Cell. Biol. 28:131-139.
32. Meggio, F., B. Boldyreff, O. G. Issinger, and L. A. Pinna. 1994. Casein kinase 2 down-regulation and activation by polybasic peptides are mediated by acidic residues in the 55-64 region of the beta-subunit. A study with calmodulin as phosphorylatable substrate. Biochemistry 33:4336-4342.
33. Meggio, F., B. Boldyreff, O. Marin, O. G. Issinger, and L. A. Pinna. 1995. Phosphorylation and activation of protein kinase CK2 by p34cdc2 are independent events. Eur. J. Biochem. 230:1025-1031.
34. Meggio, F., and L. A. Pinna. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368.
35. Niefind, K., B. Guerra, I. Ermakowa, and O. G. Issinger. 2001. Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme. EMBO J. 20:5320-5331.
36. Olsten, M. E., and D. W. Litchfield. 2004. Order or chaos? An evaluation of the regulation of protein kinase CK2. Biochem. Cell Biol. 82:681-693.
37. Padmanabha, R., J. L. Chen-Wu, D. E. Hanna, and C. V. Glover. 1990. Isolation, sequencing, and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:4089-4099.
38. Pinna, L. A. 2002. Protein kinase CK2: a challenge to canons. J. Cell Sci. 115:3873-3878.
39. Pinna, L. A., A. Donella-Deana, and F. Meggio. 1979. Structural features determining the site specificity of a rat liver cAMP-independent protein kinase. Biochem. Biophys. Res. Commun. 87:114-120.
40. Poletto, G., J. Vilardell, O. Marin, M. A. Pagano, G. Cozza, S. Sarno, A. Falques, E. Itarte, L. A. Pinna, and F. Meggio. 2008. The regulatory beta subunit of protein kinase CK2 contributes to the recognition of the substrate consensus sequence. A study with an eIF2 beta-derived peptide. Biochemistry 47:8317-8325.
41. Redwood, C., S. L. Davies, N. J. Wells, A. M. Fry, and I. D. Hickson. 1998. Casein kinase II stabilizes the activity of human topoisomerase IIalpha in a phosphorylation-independent manner. J. Biol. Chem. 273:3635-3642.
42. Reininger, L., O. Billker, R. Tewari, A. Mukhopadhyay, C. Fennell, D. Dorin-Semblat, C. Doerig, D. Goldring, L. Harmse, L. Ranford-Cartwright, J. Packer, and C. Doerig. 2005. A NIMA-related protein kinase is essential for completion of the sexual cycle of malaria parasites. J. Biol. Chem. 280:31957-31964.
43. Ridley, R. G. 2002. Medical need, scientific opportunity and the drive for antimalarial drugs. Nature 415:686-693.
44. Rodriguez, F. A., C. Contreras, V. Bolanos-Garcia, and J. E. Allende. 2008. Protein kinase CK2 as an ectokinase: the role of the regulatory CK2beta subunit. Proc. Natl. Acad. Sci. USA 105:5693-5698.
45. Salvi, M., S. Sarno, O. Marin, F. Meggio, E. Itarte, and L. A. Pinna. 2006. Discrimination between the activity of protein kinase CK2 holoenzyme and its catalytic subunits. FEBS Lett. 580:3948-3952.
46. Sarno, S., S. Moro, F. Meggio, G. Zagotto, D. Dal Ben, P. Ghisellini, R. Battistutta, G. Zanotti, and L. A. Pinna. 2002. Toward the rational design of protein kinase casein kinase-2 inhibitors. Pharmacol. Ther. 93:159-168.
47. Sidhu, A. B., S. G. Valderramos, and D. A. Fidock. 2005. pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol. Microbiol. 57:913-926.
48. Singh, G. P., B. R. Chandra, A. Bhattacharya, R. R. Akhouri, S. K. Singh, and A. Sharma. 2004. Hyper-expansion of asparagines correlates with an abundance of proteins with prion-like domains in Plasmodium falciparum. Mol. Biochem. Parasitol. 137:307-319.
49. Snow, R. W., C. A. Guerra, A. M. Noor, H. Y. Myint, and S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217.
50. Tellez, R., M. Gatica, C. C. Allende, and J. E. Allende. 1990. Copolymers of glutamic acid and tyrosine are potent inhibitors of oocyte casein kinase II. FEBS Lett. 265:113-116.
51. Tonkin, C. J., G. G. van Dooren, T. P. Spurck, N. S. Struck, R. T. Good, E. Handman, A. F. Cowman, and G. I. McFadden. 2004. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol. 137:13-21.
52. Tuazon, P. T., E. W. Bingham, and J. A. Traugh. 1979. Cyclic nucleotide-independent protein kinases from rabbit reticulocytes. Site-specific phosphorylation of casein variants. Eur. J. Biochem. 94:497-504.
53. Uhle, S., O. Medalia, R. Waldron, R. Dumdey, P. Henklein, D. Bech-Otschir, X. Huang, M. Berse, J. Sperling, R. Schade, and W. Dubiel. 2003. Protein kinase CK2 and protein kinase D are associated with the COP9 signalosome. EMBO J. 22:1302-1312.
54. Walliker, D., I. A. Quakyi, T. E. Wellems, T. F. McCutchan, A. Szarfman, W. T. London, L. M. Corcoran, T. R. Burkot, and R. Carter. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236:1661-1666.
55. Walter, J., M. Schnolzer, W. Pyerin, V. Kinzel, and D. Kubler. 1996. Induced release of cell surface protein kinase yields CK1- and CK2-like enzymes in tandem. J. Biol. Chem. 271:111-119.
56. Walton, G. M., J. Spiess, and G. N. Gill. 1985. Phosphorylation of high mobility group protein 14 by casein kinase II. J. Biol. Chem. 260:4745-4750.
57. Ward, P., L. Equinet, J. Packer, and C. Doerig. 2004. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5:79.