Abstract
Protein kinase CK2 is a highly conserved Ser/Thr protein kinase involved in cell cycle control, transcription, signal transduction and cell proliferation. It is upregulated in several diseases and by oxidative stress. CK2 is generally composed of two catalytic subunits and two regulatory subunits and utilizes either ATP or GTP as a phosphate donor. CK2 was isolated from the sea mussel Mytilus galloprovincialis, a biomarker of marine pollution, and the Mediterranean fly Ceratitis capitata, an insect capable of wreaking extensive damage to a wide range of fruit crops with great economical importance. The catalytic CK2α and regulatory CK2β subunits of M. galloprovincialis and C. capitata show similar properties. The mussel and fly catalytic subunits and holoenzymes were capable of phosphorylating the recombinant ribosomal stalk P1 protein, implying functional conservation. They also demonstrate the characteristics of a typical CK2: use of ATP and GTP as phosphate donors, inhibition by known modulators of CK2 activity (like benzotriazole derivatives and heparin), and stimulation by polycations. Both organisms seem to be ideal models for the analysis of CK2 in the control of gene expression in response to cellular stress.
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References
Meggio F., Pinna L.A., One-thousand-and-one substrates of protein kinase CK2?, FASEB J., 2003, 17, 349–368
Litchfield D.W., Protein kinase CK2: Structure, regulation and role in cellular decisions of life and death, Biochem. J., 2003, 369, 1–15
Ahmad K.A., Wang G., Slaton J., Unger G., Ahmed K., Targeting CK2 for cancer therapy, Anticancer Drugs, 2005, 16, 1037–1043
Pinna L.A., Protein kinase CK2, Int. J. Biochem. Cell Biol., 1997, 29, 551–554
Glover C.V.C, On the physiological role of casein kinase II in Saccharomyces cerevisiae, Prog. Nucleic Acid Res. Mol. Biol., 1998, 59, 95–133
Abramczyk O., Zień P., Zieliński R., Pilecki M., Helman U., Szyszka R., The protein kinase 60S is a free catalytic CK2α′ subunit and form an inactive complex with superoxide dismutase SOD1, Biochem. Biophys. Res. Commun., 2003, 307, 31–40
Saxena A., Padmanabha R., Glover C.V.C, Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II, Mol Cell Biol., 1987, 7, 3409–3417
Theodoraki M.A., Mintzas A.C., cDNA cloning, heat shock regulation and developmental expression of the hsp83 gene in the Mediterranean fruit fly Ceratitis capitata, Insect Mol. Biol., 2006, 15, 839–852
Kalpaxis D.L., Theos C., Xaplanteri M.A., Dinos G.P., Catsiki A.V., Leotsinidis M., Biomonitoring of Gulf of Patras, N. Peloponnesus, Greece. Application of a biomarker suite including evaluation of translation efficiency in Mytilus galloprovincialis cells, Environ. Res., 2004, 94, 211–220
Muttray A.F., O’Toole T.F., Morrill W., Van Beneden R.J., Baldwin S.A., An invertebrate mdm homolog interacts with p53 and is differentially expressed together with p53 and ras in neoplastic Mytilus trossulus haemocytes, Comp. Biochem. Physiol., 2010, 156, 298–308
Pantzartzi C., Drosopoulou E., Yiangou M., Drozdov I., Tsoka S., Ouzounis C.A., et al., Promoter complexity and tissue-specific expression of stress response components in Mytilus galloprovincialis, a sessile marine invertebrate species, PLoS Comput. Biol., 2010, 6, e1000847
Watabe M., Nakaki T., Protein kinase CK2 regulates the formation and clearance of aggresomes in response to stress, J. Cell Sci., 2011, 124, 1519–1532
Dotan I., Ziv E., Dafni N., Beckman J.S., McCann R.O., Glover C.V.C., et al., Functional conservation between the human, nematode and yeast CK2 cell cycle genes, Biochem. Biophys. Res. Commun., 2001, 288, 603–609
Kolaiti R.M., Baier A., Szyszka R., Kouyanou-Koutsoukou S., Isolation of a CK2α Subunit and the holoenzyme from the mussel Mytilus galloprovincialis and construction of the CK2α and CK2β cDNAs, Mar. Biotechnol., 2011, 13, 505–516
Kouyanou-Koutsoukou S., Baier A., Kolaitis R.M., Maniatopoulou E., Thanopoulou K., Szyszka R., Cloning and purification of protein kinase CK2 recombinant alpha and beta subunits from the Mediterranean fly Ceratitis capitata, Mol. Cell. Biochem., 2011, 356, 261–267
Sarno S. Ghisellini P., Pinna L.A., Unique activation mechanism of protein kinase CK2. The N-terminal segment is essential for constitutive activity of the catalytic subunit but not of the holoenzyme, J. Biol. Chem., 2002, 277, 22509–22514
Cozza G., Bortolato A., Moro S., How druggable is protein kinase CK2?, Med. Res. Rev., 2009, 30, 1–44
Sarno S., Vaglio P., Meggio F., Issinger O.-G., Pinna L.A., Protein kinase CK2 mutants defective in substrate recognition. Purification and kinetic analysis., J. Biol. Chem., 1996, 271, 10595–10601
Sarno S., Vaglio P., Marin O., Meggio F., Issinger O.-G., Pinna L.A., Basic residues in the 74–83 and 191–198 segments of protein kinase CK2 catalytic subunit are implicated in the negative but not in the positive regulation by the beta-subunit, Eur. J. Biochem., 1997, 248, 290–295
Salinas P., Fuentes D., Vidal E., Jordana X., Echeverria M., Holuigue L., An extensive survey of CK2 α and β subunits in Arabidopsis: Multiple isoforms exhibit differential subcellular localization, Plant Cell. Physiol., 2006, 47, 1295–1308
Bibby A.C., Litchfield D.W., 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., 2005, 1, 67–79
Boldyreff B., Meggio F., Pinna L.A, Issinger O.-G., Reconstitution of normal and hyperactivated forms of casein kinase-2 by variably mutated betasubunits, Biochemistry, 1993, 32, 12672–12677
Zhang C., Vilk G., Canton D.A., Litchfield D.W., Phosphorylation regulates the stability of the regulatory CK2beta subunit, Oncogene, 2002, 21, 3754–3764
Allende J.E., Allende, C.C., Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation, FASEB J., 1995, 9, 313–323
Bolanos-Garcia V.M., Fernandez-Recio J., Allende J.E., Blundell, T.L., Identifying interaction motifs in CK2β — a ubiquitous kinase regulatory subunit, TRENDS Biochem. Sci., 2006, 31, 654–660
Soderling T.R., Protein kinases and phosphatases: regulation by autoinhibitory domains, Biotechnol. Appl. Biochem., 1993, 18, 185–200
Meggio F., Boldyreff B., Issinger O.-G. Pinna L.A., Casein kinase 2 down-regulation and activation by polybasic peptides aremediated by acidic residues in the 55–64 region of the beta-subunit. A study by the calmodulin as phosphorylatable substrate, Biochemistry, 1994, 33, 6998–7004
Chantalat L., Leroy D., Filhol O., Nueda A., Benitez M.J., Chambaz E.M., et al., Crystal structure of the human protein kinase CK2 regulatory subunit reveals its zinc finger-mediated dimerization, EMBO J., 1999, 18, 2930–2940
Niefind K., Guerra B., Ermakowa I., Issinger O.-G., Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme, EMBO J., 2001, 20, 5320–5331
Hagemann C., Kalmes A., Wixler V., Wixler L., Schuster T., Rapp U.R., The regulatory subunit of protein kinase CK2 is a specific A-Raf activator, FEBS Lett., 1997, 403, 200–202
Chen M., Li D., Krebs E.G., Cooper J.A., The casein kinase II beta subunit binds to Mos and inhibits Mos activity, Mol. Cell. Biol., 1997, 17, 1904–1912
Guerra B., Issinger O.-G., Wang J.Y., Modulation of human checkpoint kinase Chk1 by the regulatory beta-subunit of protein kinase CK2, Oncogene, 2003, 22, 4933–4942
Bjørling-Poulsen M., Siehler S., Wiesmüller L., Meek D., Niefind K., Issinger O.-G., The ‘regulatory’ beta-subunit of protein kinase CK2 negatively influences p53-mediated allosteric effects on Chk2 activation, Oncogene, 2005, 24, 6194–6200
Litchfield D.W., Bosc D.G., Slominski E., The protein kinase from mitotic human cells that phosphorylates Ser-209 on the casein kinase II beta-subunit is p34cdc2, Biochim. Biophys. Acta, 1995, 1269, 69–78
Olsen, B.B., Niefind, K., Issinger, O.-G., Inter- and supramolecular interactions of protein kinase CK2 and their relevance for genome integrity. In: D.-H. Lankeman (Ed.) Genome Dynamics and Stability: Genome Integrity, Springer Berlin Heidelberg, 2007
Kristensen L.P., Larsen M.R., Højrup P., Issinger O.G., Guerra B., Phosphorylation of the regulatory beta-subunit of protein kinase CK2 by checkpoint kinase Chk1: identification of the in vitro CK2beta phosphorylation site, FEBS Lett., 2004, 569, 217–223
Russo G.L., Tosto M., Mupo A., Castellano I., Cuomo A., Tosti E., Biochemical and functional characterization of protein kinase CK2 in ascidian Ciona intestinalis oocytes at fertilization, J. Biol. Chem., 2004, 279, 33012–33023
Riera M., Pages M., Issinger O.-G., Guerra B., Purification and characterization of recombinant protein kinase CK2 from Zea mays expressed in Escherichia coli, Protein Expr. Purif., 2003, 29, 24–32
Jensen B.C., Kifer C.T., Brekken D.L., Randall A.C., Wang Q., Drees B.L., et al., Characterization of protein kinase CK2 from Trypanosoma brucei, Mol. Biochem. Parasitol., 2007, 151, 28–40
Meggio F., Grankowski N., Kudlicki W., Szyszka R., Gąsior E., Pinna L.A., Structure and properties of casein kinase-2 from Saccharomyces cerevisiae. A comparison with the liver enzyme, Eur. J. Biochem., 1986, 159, 31–38
Domańska K., Zieliński R., Kubiński K., Sajnaga E., Masłyk M., Bretner M., et al., Protein kinase CK2 from Saccharomyces cerevisiae, Acta Biochim. Polon., 2005, 52, 947–951
Ballesta J.P.G., Remacha M., The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery, Prog. Nucleic Acid Res. Mol. Biol., 1996, 55, 157–193
Kolaiti R.M., Lucas J.M., Kouyanou-Koutsoukou S., Molecular cloning of the ribosomal P-proteins MgP1, MgP2, MgP0, and superoxide dismutase (SOD) in the mussel Mytilus galloprovincialis and analysis of MgP0 at stress conditions, Gene, 2009, 430, 77–85
Guerra B., Issinger O.-G., Protein kinase CK2 in human diseases, Curr. Med. Chem., 2008, 15, 1870–1886
Arnold K., Bordoli L., Kopp J., Schwede T., The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling, Bioinformatics, 2006, 22, 195–201
Kopp J., Schwede T., Automated protein structure homology modeling: a progress report, Pharmacogenomics, 2004, 5, 405–416
Battistutta R., Sarno S., De Moliner E., Marin O., Issinger O.-G., Zanotti G., et al., The crystal structure of the complex of Zea mays alpha subunit with a fragment of human beta subunit provides the clue to the architecture of protein kinase CK2 holoenzyme, Eur. J. Biochem., 2000, 267, 5184–5190
Raaf J., Brunstein E., Issinger O.-G., Niefind K., The interaction of CK2alpha and CK2beta, the subunits of protein kinase CK2, requires CK2beta in a preformed conformation and is enthalpically driven, Protein Sci., 2008, 17, 2180–2186
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Kouyanou-Koutsoukou, S., Baier, A., Kolaitis, RM. et al. Protein kinase CK2 from two higher eukaryotes of economical importance, the mussel Mytilus galloprovincialis and the medfly Ceratitis capitata . cent.eur.j.biol. 7, 185–191 (2012). https://doi.org/10.2478/s11535-012-0019-2
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DOI: https://doi.org/10.2478/s11535-012-0019-2