Regulation of Plasmodium falciparumOrigin Recognition Complex subunit 1 (PfORC1) function through phosphorylation mediated by CDK-like kinase PK5

Molecular Microbiology

Volumn 98, Issue 1, 2015, Pages 17-33

  Deshmukh, Abhijit S ^a,b   Agarwal, Meetu ^a   Mehra, Parul ^a   Gupta, Ashish ^a,d   Gupta, Nidhi ^a   Doerig, Christian D ^c   Dhar, Suman Kumar ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b UNIVERSITY OF HYDERABAD   (India)

^c MONASH UNIVERSITY   (Australia)

^d SHIV NADAR UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CDK LIKE KINASE PK5; CYCLIN DEPENDENT KINASE; DNA; MEMBRANE PROTEIN; PLASMODIUM FALCIPARUM ORIGIN RECOGNITION COMPLEX SUBUNIT 1; PROTEASOME; UNCLASSIFIED DRUG; ORIGIN RECOGNITION COMPLEX; PHOSPHOTRANSFERASE; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE REGULATION; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIMERIZATION; DNA REPLICATION; ENZYME SPECIFICITY; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY; WESTERN BLOTTING; AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SCHIZONT;

AMINO ACID SEQUENCE; DNA REPLICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; ORIGIN RECOGNITION COMPLEX; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SCHIZONTS;

EID: 84942196700     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13099     Document Type: Article

References (48)

1. Araki, M., Yu, H., and Asano, M. (2005) A novel motif governs APC-dependent degradation of Drosophila ORC1 in vivo. Genes Dev 19: 2458-2465.
2. Bell, S.P., and Dutta, A. (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374.
3. Bracchi-Ricard, V., Barik, S., Delvecchio, C., Doerig, C., Chakrabarti, R., and Chakrabarti, D. (2000) PfPK6, a novel cyclin-dependent kinase/mitogen-activated protein kinase-related protein kinase from Plasmodium falciparum. Biochem J 347 (Part 1): 255-263.
4. Chen, S., and Bell, S.P. (2011) CDK prevents Mcm2-7 helicase loading by inhibiting Cdt1 interaction with Orc6. Genes Dev 25: 363-372.
5. Crabb, B.S., Rug, M., Gilberger, T.W., Thompson, J.K., Triglia, T., Maier, A.G., and Cowman, A.F. (2004) Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol Biol 270: 263-276.
6. DePamphilis, M.L. (2005) Cell cycle dependent regulation of the origin recognition complex. Cell Cycle 4: 70-79.
7. Deshmukh, A.S., Srivastava, S., Herrmann, S., Gupta, A., Mitra, P., Gilberger, T.W., and Dhar, S.K. (2012) The role of N-terminus of Plasmodium falciparum ORC1 in telomeric localization and var gene silencing. Nucleic Acids Res 40: 5313-5331.
8. Doerig, C., Billker, O., Haystead, T., Sharma, P., Tobin, A.B., and Waters, N.C. (2008) Protein kinases of malaria parasites: an update. Trends Parasitol 24: 570-577.
9. Dorin-Semblat, D., Sicard, A., Doerig, C., and Ranford-Cartwright, L. (2008) Disruption of the PfPK7 gene impairs schizogony and sporogony in the human malaria parasite Plasmodium falciparum. Eukaryot Cell 7: 279-285.
10. Dorin-Semblat, D., Carvalho, T.G., Nivez, M.P., Halbert, J., Pouller, P., Semblat, J.P., etal. (2013) An atypical cyclin-dependent kinase controls Plasmodium falciparum proliferation rate. Kinome 4-16.
11. Feng, H., and Kipreos, E.T. (2003) Preventing DNA re-replication-divergent safeguards in yeast and metazoa. Cell Cycle 2: 431-434.
12. Fidock, D.A., and Wellems, T.E. (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.
13. Findeisen, M., El-Denary, M., Kapitza, T., Graf, R., and Strausfeld, U. (1999) Cyclin A-dependent kinase activity affects chromatin binding of ORC, Cdc6, and MCM in egg extracts of Xenopus laevis. Eur J Biochem 264: 415-426.
14. Flueck, C., Bartfai, R., Volz, J., Niederwiesser, I., Salcedo-Amaya, A.M., Alako, B.T., Ehlgen, F., Ralph, S.A., Cowman, A.F., Bozdech, Z., Stunnenberg, H.G., and Voss, T.S. (2009) Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 9: e1000569.
15. Freitas-Junior, L.H., Bottius, E., Pirrit, L.A., Deitsch, K.W., Scheidig, C., Guinet, F., etal. (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022.
16. Graeser, R., Franklin, R.M., and Kappes, B. (1996a) Mechanisms of activation of the cdc2-related kinase PfPK5 from Plasmodium falciparum. Mol Biochem Parasitol 79: 125-127.
17. Graeser, R., Wernli, B., Franklin, R.M., and Kappes, B. (1996b) Plasmodium falciparum protein kinase 5 and the malarial nuclear division cycles. Mol Biochem Parasitol 82: 37-49.
18. Gupta, A., Mehra, P., Deshmukh, A., Dar, A., Mitra, P., Roy, N., and Dhar, S.K. (2009) Functional dissection of the catalytic carboxyl-terminal domain of origin recognition complex subunit 1 (PfORC1) of the human malaria parasite Plasmodium falciparum. Eukaryot Cell 8: 1341-1351.
19. Gupta, A., Mehra, P., and Dhar, S.K. (2009) Plasmodium falciparum origin recognition complex subunit5: functional characterization and role in DNA replication foci formation. Mol Microbiol 69: 646-665.
20. Halbert, J., Ayong, L., Equinet, L., Le Roch, K., Hardy, M., Goldring, D., etal. (2010) A Plasmodium falciparum transcriptional cyclin-dependent kinase-related kinase with a crucial role in parasite proliferation associates with histone deacetylase activity. Eukaryot Cell 9: 952-959.
21. Issar, N., Roux, E., Mattei, D., and Scherf, A. (2008) Identification of a novel post-translational modification in Plasmodium falciparum: protein sumoylation in different cellular compartments. Cell Microbiol 10: 1999-2011.
22. Jirage, D., Chen, Y., Caridha, D., O'Neil, M.T., Eyase, F., Witola, W.H., etal. (2010) The malarial CDK Pfmrk and its effector PfMAT1 phosphorylate DNA replication proteins and co-localize in the nucleus. Mol Biochem Parasitol 172: 9-18.
23. Laman, H., Peters, G., and Jones, N. (2001) Cyclin-mediated export of human Orc1. Exp Cell Res 271: 230-237.
24. Le Roch, K., Sestier, C., Dorin, D., Waters, N., Kappes, B., Chakrabarti, D., etal. (2000) Activation of a Plasmodium falciparum cdc2-related kinase by heterologous p25 and cyclin H. Functional characterization of a P. falciparum cyclin homologue. J Biol Chem 275: 8952-8958.
25. Lee, K.Y., Bang, S.W., Yoon, S.W., Lee, S.H., Yoon, J.B., and Hwang, D.S. (2012) Phosphorylation of ORC2 protein dissociates origin recognition complex from chromatin and replication origins. J Biol Chem 287: 11891-11898.
26. Leete, T.H., and Rubin, H. (1996) Malaria and the cell cycle. Parasitol Today 12: 442-444.
27. Leykauf, K., Treeck, M., Gilson, P.R., Nebl, T., Braulke, T., Cowman, A.F., etal. (2010) Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite. PLoS Pathog 6: e1000941.
28. Li, C.J., Vassilev, A., and DePamphilis, M.L. (2004) Role for Cdk1 (Cdc2)/cyclin A in preventing the mammalian origin recognition complex's largest subunit (Orc1) from binding to chromatin during mitosis. Mol Cell Biol 24: 5875-5886.
29. Li, J.L., Robson, K.J., Chen, J.L., Targett, G.A., and Baker, D.A. (1996) Pfmrk, a MO15-related protein kinase from Plasmodium falciparum. Gene cloning, sequence, stage-specific expression and chromosome localization. Eur J Biochem 241: 805-813.
30. Makise, M., Takehara, M., Kuniyasu, A., Matsui, N., Nakayama, H., and Mizushima, T. (2009) Linkage between phosphorylation of the origin recognition complex and its ATP binding activity in Saccharomyces cerevisiae. J Biol Chem 284: 3396-3407.
31. Mancio-Silva, L., Rojas-Meza, A.P., Vargas, M., Scherf, A., and Hernandez-Rivas, R. (2008) Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum. J Cell Sci 121: 2046-2053.
32. Mehra, P., Biswas, A.K., Gupta, A., Gourinath, S., Chitnis, C.E., and Dhar, S.K. (2005) Expression and characterization of human malaria parasite Plasmodium falciparum origin recognition complex subunit 1. Biochem Biophys Res Commun 337: 955-966.
33. Mendez, J., Zou-Yang, X.H., Kim, S.Y., Hidaka, M., Tansey, W.P., Stillman, B., etal. (2002) Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol Cell 9: 481-491.
34. Merckx, A., Le Roch, K., Nivez, M.P., Dorin, D., Alano, P., Gutierrez, G.J., etal. (2003) Identification and initial characterization of three novel cyclin-related proteins of the human malaria parasite Plasmodium falciparum. J Biol Chem 278: 39839-39850.
35. Mimura, S., Seki, T., Tanaka, S., and Diffley, J.F. (2004) Phosphorylation-dependent binding of mitotic cyclins to Cdc6 contributes to DNA replication control. Nature 431: 1118-1123.
36. Morgan, D.O. (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13: 261-291.
37. Narum, D.L., and Thomas, A.W. (1994) Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol Biochem Parasitol 67: 59-68.
38. Perez-Toledo, K., Rojas-Meza, A.P., Mancio-Silva, L., Hernandez-Cuevas, N.A., Delgadillo, D.M., Vargas, M., etal. (2009) Plasmodium falciparum heterochromatin protein 1 binds to tri-methylated histone 3 lysine 9 and is linked to mutually exclusive expression of var genes. Nucleic Acids Res 37: 2596-2606.
39. Perkins, G., Drury, L.S., and Diffley, J.F. (2001) Separate SCF(CDC4) recognition elements target Cdc6 for proteolysis in S phase and mitosis. EMBO J 20: 4836-4845.
40. Petersen, B.O., Lukas, J., Sorensen, C.S., Bartek, J., and Helin, K. (1999) Phosphorylation of mammalian CDC6 by cyclin A/CDK2 regulates its subcellular localization. EMBO J 18: 396-410.
41. Pines, J. (1993) Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem Sci 18: 195-197.
42. Remus, D., Blanchette, M., Rio, D.C., and Botchan, M.R. (2005) CDK phosphorylation inhibits the DNA-binding and ATP-hydrolysis activities of the Drosophila origin recognition complex. J Biol Chem 280: 39740-39751.
43. Ross-Macdonald, P.B., Graeser, R., Kappes, B., Franklin, R., and Williamson, D.H. (1994) Isolation and expression of a gene specifying a cdc2-like protein kinase from the human malaria parasite Plasmodium falciparum. Eur J Biochem 220: 693-701.
44. Trager, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
45. Treeck, M., Sanders, J.L., Elias, J.E., and Boothroyd, J.C. (2011) The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites' boundaries. Cell Host Microbe 10: 410-419.
46. Vas, A., Mok, W., and Leatherwood, J. (2001) Control of DNA rereplication via Cdc2 phosphorylation sites in the origin recognition complex. Mol Cell Biol 21: 5767-5777.
47. Ward, P., Equinet, L., Packer, J., and Doerig, C. (2004) Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 12: 79.
48. Woo, R.A., and Poon, R.Y. (2003) Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle 2: 316-324.