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Is Casein Kinase 2 Able to Phosphorylate Plant α-Tubulin?

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Abstract

Results of classical and structural bioinformatical research allow to predict casein kinase 2 dependent phosphorylation of conservative residues of Ser94 and Ser419 in Trypanosoma and Arabidopsis α-tubulin. Location of these residues in the region of internal contact of α-/β-tubulin heterodimer has been demonstrated. It is hypothesized that phosphorylation of Ser94 can affect dimerization of α-/β-tubulin in Trypanosoma and Arabidopsis. Most likely, potential phosphorylation of Ser419 does not have a direct effect on microtubule structure but is related to interaction with associated proteins, in particular with kinesins.

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References

  1. Litchfield, D.W., Protein kinase CK2: structure, regulation and role in cellular decisions of life and death, Biochem. J., 2003, vol. 369, pp. 1–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Litchfield, D.W., Bosc, D.G., Canton, D.A., Saulnier, R.B., Vilk, G., and Zhang, C., Functional specialization of CK2 isoforms and characterization of isoform-specific binding partners, Mol. Cell. Biochem., 2001, vol. 227, pp. 21–29.

    Article  CAS  PubMed  Google Scholar 

  3. Shi, X., Potvin, B., Huang, T., Hilgard, P., Spray, D.C., Suadicani, S.O., Wolkoff, A.W., Stanley, P., and Stockert, R.J., A novel casein kinase 2 alpha subunit regulates membrane protein traffic in the human hepatoma cell line HuH-7, J. Biol. Chem., 2001, vol. 276, no. 3, pp. 2075–2082.

    Article  CAS  PubMed  Google Scholar 

  4. Hanif, I.M., Hanif, I.M., Shazib, M.A., Ahmad, K.A., and Pervaiz, S., Casein kinase II: an attractive target for anti-cancer drug design, Int. J. Biochem. Cell. Biol., 2010, vol. 42, no. 10, pp. 1602–1605.

    Article  CAS  PubMed  Google Scholar 

  5. Volodina, Iu.L. and Shtil’, A.A., Casein kinase 2, the versatile regulator of cell survival, Mol. Biol. (Moscow), 2012, vol. 46, no. 3, pp. 423–433.

    Article  Google Scholar 

  6. Canton, D.A. and Litchfield, D.W., The shape of things to come: an emerging role for protein kinase CK2 in the regulation of cell morphology and the cytoskeleton, Cell Signal., 2006, vol. 18, no. 3, pp. 267–275.

    Article  CAS  PubMed  Google Scholar 

  7. Karpov, P.A., Nadezhdina, E.S., Yemets, A.I., and Blume, Ya.B., Results of the clusterization of human microtubule and cell-cycle related serine/threonine protein kinases and their plant homologues, Moscow Univ. Biol. Sci. Bull., 2010, vol. 65, no. 4, pp. 213–216.

    Article  Google Scholar 

  8. Delorme, V., Cayla, X., Faure, G., Garcia, A., and Tardieux, I., Actin dynamics is controlled by a casein kinase II and phosphatase 2C interplay on Toxoplasma gondii toxofilin, Mol. Biol. Cell, 2003, vol. 14, no. 5, pp. 1900–1912.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Li, H., Liu, X.S., Yang, X., Wang, Y., Wang, Y., Turner, J.R., and Liu, X., Phosphorylation of CLIP-170 by Plk1 and CK2 promotes timely formation of kinetochore–microtubule attachments, EMBO J., 2010, vol. 29, no. 17, pp. 2953–2965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lim, A.C., Tiu, S.Y., Li, Q., and Qi, R.Z., Direct regulation of microtubule dynamics by protein kinase CK2, J. Biol. Chem., 2004, vol. 279, no. 6, pp. 4433–4439.

    Article  CAS  PubMed  Google Scholar 

  11. Sanchez-Ponce, D., Munoz, A., and Garrido, J.J., Casein kinase 2 and microtubules control axon initial segment formation, Mol. Cell Neurosci., 2011, vol. 46, no. 1, pp. 222–234.

    Article  CAS  PubMed  Google Scholar 

  12. Serrano, L., Hernandez, M.A., Diaz-Nido, J., and Avila, J., Association of casein kinase II with microtubules, Exp. Cell Res., 1989, vol. 181, no. 1, pp. 263–272.

    Article  CAS  PubMed  Google Scholar 

  13. Wang, Z.Y., Shi, Q., Wang, S.B., Tian, C., Xu, Y., Guo, Y., Chen, C., Zhang, J., and Dong, X.P., Coexpressions of casein kinase 2 (CK2) subunits restore the down-regulation of tubulin levels and disruption of microtubule structures caused by PrP mutants, J. Mol. Neurosci., 2013, vol. 50, no. 1, pp. 14–22.

    Article  PubMed  Google Scholar 

  14. Dıaz-Nido, J. and Avila, J., Protein kinases associated with isolated mitotic spindles from mammalian cells: identification of a casein kinase II-like enzyme, Second Messengers Phosphoproteins, 1992, vol. 14, nos. 1–2, pp. 39–53.

    PubMed  Google Scholar 

  15. Faust, M., Schuster, N., and Montenarh, M., Specific binding of protein kinase CK2 catalytic subunits to tubulin, FEBS Lett., 1999, vol. 462, nos. 1–2, pp. 51–56.

    Article  CAS  PubMed  Google Scholar 

  16. Carneiro, A.C., Fragel-Madeira, L., Silva-Neto, M.A., and Linden, R., A role for CK2 upon interkinetic nuclear migration in the cell cycle of retinal progenitor cells, Dev. Neurobiol., 2008, vol. 68, no. 5, pp. 620–631.

    Article  PubMed  Google Scholar 

  17. Kramerov, A.A., Golub, A.G., Bdzhola, V.G., Yarmoluk, S.M., Ahmed, K., Bretner, M., and Ljubimov, A.V., Treatment of cultured human astrocytes and vascular endothelial cells with protein kinase CK2 inhibitors induces early changes in cell shape and cytoskeleton, Mol. Cell Biochem., 2011, vol. 349, nos. 1–2, pp. 125–137.

    Article  CAS  PubMed  Google Scholar 

  18. Boscan, B.E., Uzcanga, G.L., Calabokis, M., Camargo, R., Aponte, F., and Bubis, J., Interaction of tubulin and protein kinase CK2 in Trypanosoma equiperdum, Z. Naturforsch., A: Phys. Sci., vol. 72, nos. 11–12, pp. 459–465.

  19. Mulekar, J.J. and Huq, E., Expanding roles of protein kinase CK2 in regulating plant growth and development, J. Exp. Bot., 2014, vol. 65, no. 11, pp. 2883–2893.

    Article  PubMed  Google Scholar 

  20. Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N., Kamada, H., and Shinozaki, K., Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana, Plant. Mol. Biol., 1993, vol. 21, no. 2, pp. 279–289.

    Article  CAS  PubMed  Google Scholar 

  21. Klimczak, L.J., Collinge, M.A., Farini, D., Giuliano, G., Walker, J.C., and Cashmore, A.R., Reconstitution of Arabidopsis casein kinase II from recombinant subunits and phosphorylation of transcription factor GBF1, Plant Cell, 1995, vol. 7, no. 1, pp. 105–115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bu, Q., Zhu, L., Dennis, M.D., Yu, L., Lu, S.X., Person, M.D., Tobin, E.M., Browning, K.S., and Huq, E., Phosphorylation by CK2 enhances the rapid lightinduced degradation of phytochrome interacting factor 1 in Arabidopsis, J. Biol. Chem., 2011, vol. 286, no. 14, pp. 12066–12074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dennis, M.D. and Browning, K.S., Differential phosphorylation of plant translation initiation factors by Arabidopsis thaliana CK2 holoenzymes, J. Biol. Chem., 2009, vol. 284, pp. 20602–20614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dennis, M.D., Person, M.D., and Browning, K.S., Phosphorylation of plant translation initiation factors by CK2 enhances the in vitro interaction of multifactor complex components, J. Biol. Chem., 2009, vol. 284, no. 31, pp. 20615–20628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lu, S.X., Liu, H., Knowles, S.M., Li, J., Ma, L., Tobin, E.M., and Lin, C., A role for protein kinase casein kinase2 alpha-subunits in the Arabidopsis circadian clock, Plant Physiol., 2011, vol. 157, no. 3, pp. 1537–1545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Moreno-Romero, J., Armengot, L., Mar Marques-Bueno, M., Britt, A., and Carmen Martinez, M., CK2-defective Arabidopsis plants exhibit enhanced doublestrand break repair rates and reduced survival after exposure to ionizing radiation, Plant J., 2012, vol. 71, no. 4, pp. 627–638.

    Article  CAS  PubMed  Google Scholar 

  27. Liu, B.Q., Jin, L., Zhu, L., Li, J., Huang, S., and Yuan, M., Phosphorylation of microtubule-associated protein SB401 from Solanum berthaultii regulates its effect on microtubules, J. Integr. Plant Biol., 2009, vol. 51, no. 3, pp. 235–242.

    Article  CAS  PubMed  Google Scholar 

  28. The Universal Protein Resource (UniProt), Nucl. Acids Res., 2008, vol. 36, pp. D190–D195.

  29. Claverie, J.-M. and Notredame, C., Bioinformatics for Dummies, New York: Wiley Publ., 2007.

    Google Scholar 

  30. Korf, I., Bedell, J., and Yandell, M., BLAST, Sebastopol: O’Reilly and Ass., 2003.

    Google Scholar 

  31. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., and Higgins, D.G., Clustal W and Clustal X version 2.0, Bioinformatics, 2007, vol. 23, no. 21, pp. 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  32. Atteson, K., The performance of neighbor-joining algorithms of phylogeny reconstruction, in Lecture Notes in Computer Science, Jiang, T. and Lee, D., Eds., Berlin: Springer-Verlag, 1997, vol. 1276, pp. 101–110.

    Google Scholar 

  33. Nei, M. and Kumar, S., Molecular Evolution and Phylogenetics, New York: Oxford Univ. Press, 2000.

    Google Scholar 

  34. Kumar, S., Stecher, G., and Tamura, K., MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1870–1874.

    Article  CAS  PubMed  Google Scholar 

  35. Cheng, H., Wang, Y., Liu, Z., and Xue, Y., Computational identification of protein kinases and kinase-specific substrates in plants, Methods Mol. Biol., 2015, vol. 1306, pp. 195–205.

    Article  CAS  PubMed  Google Scholar 

  36. Xue, Y., Liu, Z., Cao, J., Ma, Q., Gao, X., Wang, Q., Jin, C., Zhou, Y., Wen, L., and Ren, J., GPS 2.1: enhanced prediction of kinase-specific phosphorylation sites with an algorithm of motif length selection, Protein Eng. Des. Sel., 2011, vol. 24, no. 3, pp. 255–260.

    Article  CAS  PubMed  Google Scholar 

  37. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Gallo Cassarino, T., Bertoni, M., Bordoli, L., and Schwede, T., SWISSMODEL: modelling protein tertiary and quaternary structure using evolutionary information, Nucleic Acids Res., 2014, vol. 42, pp. W252–W258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Leverett, C.A., Sukuru, S.C., Vetelino, B.C., Musto, S., Parris, K., Pandit, J., Loganzo, F., Varghese, A.H., Bai, G., Liu, B., Liu, D., Hudson, S., Doppalapudi, V.R., Stock, J., O’Donnell, C.J., and Subramanyam, C., Design, synthesis, and cytotoxic evaluation of novel tubulysin analogues as ADC payloads, ACS Med. Chem. Lett., 2016, vol. 7, no. 11, pp. 999–1004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cormier, A., Marchand, M., Ravelli, R.B., Knossow, M., and Gigant, B., Structural insight into the inhibition of tubulin by vinca domain peptide ligands, EMBO Rep., 2008, vol. 9, no. 11, pp. 1101–1106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hornbeck, P.V., Zhang, B., Murray, B., Kornhauser, J.M., Latham, V., and Skrzypek, E., Phospho-SitePlus. 2014: mutations, PTMs and recalibrations, Nucleic Acids Res., 2014, vol. 43, pp. D512–D520.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tian, G., Jaglin, X.H., Keays, D.A., Francis, F., Chelly, J., and Cowan, N.J., Disease-associated mutations in tuba1a result in a spectrum of defects in the tubulin folding and heterodimer assembly pathway, Hum. Mol. Genet., 2010, vol. 19, no. 18, pp. 3599–3613.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Uchimura, S., Oguchi, Y., Hachikubo, Y., Ishiwata, S., and Muto, E., Key residues on microtubule responsible for activation of kinesin ATPase, EMBO J., 2010, vol. 29, no. 7, pp. 1167–1175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mertins, P., Mani, D.R., Ruggles, K.V., Gillette, M.A., Clauser, K.R., Wang, P., Wang, X., Qiao, J.W., Cao, S., Petralia, F., Kawaler, E., Mundt, F., Krug, K., Tu, Z., Lei, J.T., Gatza, M.L., Wilkerson, M., Perou, C.M., Yellapantula, V., Huang, K.L., Lin, C., McLellan, M.D., Yan, P., Davies, S.R., Townsend, R.R., Skates, S.J., Wang, J., Zhang, B., Kinsinger, C.R., Mesri, M., Rodriguez, H., Ding, L., Paulovich, A.G., Fenyo, D., Ellis, M.J., and Carr, S.A., NCI CPTAC, Proteogenomics connects somatic mutations to signalling in breast cancer, Nature, 2016, vol. 534, no. 7605, pp. 55–62.

    CAS  PubMed  Google Scholar 

  44. Tsai, C.F., Wang, Y.T., Yen, H.Y., Tsou, C.C., Ku, W.C., Lin, P.Y., Chen, H.Y., Nesvizhskii, A.I., Ishihama, Y., and Chen, Y.J., Large-scale determination of absolute phosphorylation stoichiometries in human cells by motif-targeting quantitative proteomics, Nat. Commun., 2015, vol. 6. doi 10.1038/ncomms7622

  45. Liu, N., Sun, N., Gao, X., and Li, Z., Phosphosite mapping of HIP-55 protein in mammalian cells, Int. J. Mol. Sci., 2014, vol. 15, no. 3, pp. 4903–4914.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine

    P. A. Karpov & Ya. B. Blume

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  1. P. A. Karpov
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  2. Ya. B. Blume
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Correspondence to P. A. Karpov.

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Original Russian Text © P.A. Karpov, Ya.B. Blume, 2018, published in Tsitologiya i Genetika, 2018, Vol. 52, No. 2, pp. 22–32.

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Karpov, P.A., Blume, Y.B. Is Casein Kinase 2 Able to Phosphorylate Plant α-Tubulin?. Cytol. Genet. 52, 103–111 (2018). https://doi.org/10.3103/S0095452718020044

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