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Protein kinase KIN10 from Arabidopsis thaliana as a potential regulator of primary microtubule nucleation centers in plants

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Abstract

The nearest plant homologues of animal protein kinase BRSK were identified using the methods of classical and structural bioinformatics. The selection was performed based on the sequence comparison, results of phylogenetic clustering, and analysis of domain architecture. Spatial structures of human BRSK1 and KIN10 from A. thaliana were compared. The relationship between KIN10 and the regulation of primary microtubule nucleation centers in A. thaliana was revealed. Obvious homology of plant KIN10 and mammalian BRSK1 evidence to suggest that this plant protein kinase is associated with the regulation of the structure and function of primary microtubule nucleation centers and is able to phosphorylate γ-tubulin from Arabidopsis (TUBG1 and TUBG2) at Ser131, affecting the γTuSC monomer structure as well as the γTuRC complex assembly. The effect of the modification on the TUBG1-GACP3 interaction was suggested.

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References

  1. Amos, L.A., http://www.els.net/09.04.2010.

  2. Kollman, J.M., Merdes, A., Mourey, L., and Agard, D.A., Microtubule nucleation by-tubulin complexes, Nat. Rev. Mol. Cell Biol., 2011, vol. 12, no. 11, pp. 709–721.

    Article  CAS  PubMed  Google Scholar 

  3. Nyporko, A.Yu., Demchuk, O.N., and Blume, Ya.B., Cold adaptation of plant microtubules: structural interpretation of primary sequence changes in a highly conserved region of-tubulin, Cell Biol. Int., 2003, vol. 27, no. 3, pp. 241–243.

    Article  CAS  PubMed  Google Scholar 

  4. Karpov, P.A. and Blume, Y.B., Bioinformatic search for plant homologues of animal structural maps in the arabidopsis thaliana genome, in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, Blume, Y.B., Baird, W.V., Yemets, A.I., and Breviario, D., Eds, Netherlands: Springer, 2008, pp. 373–397.

    Google Scholar 

  5. Blume, Ya.B., Plant tubulin phosphorylation and its role in cell cycle progression, in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, Blume, Y.B., Baird, W.V., Yemets, A.I., and Breviario, D., Eds, Netherlands: Springer, 2008, pp. 145–159.

    Chapter  Google Scholar 

  6. Karpov, P.A., Nadezhdina, E.S., Yemets, A.I., Matusov, V.G., Nyporko, A.Yu., Shashina, N.Yu., and Blume, Ya.B., Bioinformatic search of plant protein kinases, participating in microtubule protein phosphorylation and cell division regulation, Tsitol. Genet., 2009, vol. 43, no. 3, pp. 63–79.

    CAS  PubMed  Google Scholar 

  7. Karpov, P.A., Yemets, A.I., Matusov, V.G., Nyporko, A.Yu., Nadezhdina, E.S., and Blume, Ya.B., Bioinformatic search for plant homologs of Ste20-like serine/threonine protein kinases, Tsitol. Genet., 2009, vol. 43, no. 6, pp. 68–71.

    CAS  PubMed  Google Scholar 

  8. Bryantseva, S.A., Gavryushina, E.S., Yemets, A.I., Karpov, P.A., Blume, Ya.B., Drygin, Yu.F., and Nadezhdina, E.S., MAST2-like protein kinase from grape Vitis vinifera: cloning of catalytic domain cDNA, Cytol. Genet, 2010, vol. 44, no. 4, pp. 227–232.

    Article  Google Scholar 

  9. Karpov, P.A., Nadezhdina, E.S., Yemets, A.I., Matusov, V.G., Nyporko, A.Yu., Shashina, N.Yu., and Blume, Ya.B., Bioinformatic search of plant microtubule- and cell cycle related serine-threonine protein kinases, BMC Genom., 2010, vol. 11, suppl. 1, p. 14. doi 10.1186/1471-2164-11-S1-S14

    Google Scholar 

  10. Karpov, P.A., Rayevsky, A.V., and Blume, Ya.B., Bioinformatic search for plant homologs of the protein kinase Bub1—a key component of the mitotic spindle assembly checkpoint, Cytol. Genet, 2010, vol. 44, no. 6, pp. 376–388.

    Article  Google Scholar 

  11. Karpov, P., Raevsky, A., Korablyov, M., and Blume, Ya., Identification of plant homologues of dual specificity Yak1-related kinases, Comp. Biol. J., 2014.

    Google Scholar 

  12. Chen, D. and Vogel, J., SAD kinase keeps centrosomes lonely, Nat. Cell Biol., 2009, vol. 11, no. 9, pp. 1047–1048.

    Article  CAS  PubMed  Google Scholar 

  13. Alvarado-Kristensson, M., Rodriguez, M.J., Silio, V., Valpuesta, J.M., and Carrera, A.C., SADB phosphorylation of γ-tubulin regulates centrosome duplication, Nat. Cell Biol., 2009, vol. 11, no. 9, pp. 1081–1092.

    Article  CAS  PubMed  Google Scholar 

  14. Eklund, G., Lang, S., Glindre, J., Ehlen, A., and Alvarado-Kristensson, M., The nuclear localization of γ-tubulin is regulated by SadB-mediated phosphorylation, J. Biol. Chem., 2014, vol. 289, no. 31, pp. 21360–21373.

    Article  PubMed  PubMed Central  Google Scholar 

  15. UniProt Consortium, The Universal Protein Resource (UniProt), Nucleic Acids Res., 2, vol. 35, pp. D193–D197.

  16. Claverie, J.-M. and Notredame, C., Bioinformatics for Dummies, 2nd ed., New York: Wiley Publ., 2006.

    Google Scholar 

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

    Google Scholar 

  18. 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 

  19. Letunic, I., Doerks, T., and Bork, P., Smart: recent updates, new developments and status in 2015, Nucleic Acids Res., 2015, vol. 43, pp. D257–260.

    Article  CAS  PubMed  Google Scholar 

  20. Letunic, I., Copley, R.R., Pils, B., Pinkert, S., Schultz, J., and Bork, P., SMART 5: domains in the context of genomes and networks, Nucleic Acids Res., 2006, vol. 34, pp. D257–D260. doi 10.1093/nar/gkj079

    Article  CAS  PubMed  Google Scholar 

  21. Finn, R.D., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Mistry, J., Mitchell, A.L., Potter, S.C., Punta, M., Qureshi, M., Sangrador-Vegas, A., Salazar, G.A., Tate, J., and Bateman, A., The Pfam protein families database: towards a more sustainable future, Nucleic Acids Res., 2016, vol. 44, pp. D279–D285.

    Article  CAS  PubMed  Google Scholar 

  22. DeCastro, E., Sigrist, C.J.A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P.S., Gasteiger, E., Bairoch, A., and Hulo, N., ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins, Nucleic Acids Res., 2006, vol. 34, pp. W362–W365.

    Article  CAS  Google Scholar 

  23. Finn, R.D., Attwood, T.K., Babbitt, P.C., Bateman, A., Bork, P., Bridge, A.J., et al., InterPro in 2017—beyond protein family and domain annotations, Nucleic Acids Res., 2017, vol. 45, pp. D190–199.

    Article  PubMed  Google Scholar 

  24. Hanks, S.K. and Quinn, A.M., Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members, Methods Enzymol., 1991, vol. 200, pp. 38–62.

    Article  CAS  PubMed  Google Scholar 

  25. 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 

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

    Google Scholar 

  27. 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 

  28. Huang, H.D., Lee, T.Y., Tseng, S.W., and Horng, J.T., KinasePhos: a web tool for identifying protein kinasespecific phosphorylation sites, Nucleic Acids Res., 2005, vol. 33, pp. W226–W229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., and Zhang, Y., The I-TASSER suite: protein structure and function prediction, Nature Methods, 2015, vol. 12, no. 1, pp. 7–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M., Pieper, U., and Sali, A., Comparative protein structure modeling using MODELLER, Curr. Prot. Bioinform, 2006, suppl. 15, pp. 5.6.1–5.6.30. doi 10.1002/0471250953.bi0506s15.

    Google Scholar 

  31. Kuntal, B.K., Aparoy, P., and Reddanna, P., Easy- Modeller: a graphical interface to MODELLER, BMC Res. Notes, 2010, vol. 3, p. 226.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hildebrand, P.W., Goede, A., Bauer, R.A., Gruening, B., Ismer, J., Michalsky, E., and Preissner, R., Super- Looper—a prediction server for the modeling of loops in globular and membrane proteins, Nucleic Acids Res., 2009, vol. 37, pp. W571–W574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Dominguez, C., Boelens, R., and Bonvin, A.M., HADDOCK: a protein-protein docking approach based on biochemical and/or biophysical information, J. Am. Chem. Soc., 2003, vol. 125, no. 7, pp. 1731–1737.

    Article  CAS  PubMed  Google Scholar 

  34. Kollman, J.M., Zelter, A., Muller, E.G., Fox, B., Rice, L.M., Davis, T.N., and Agard, D.A., The structure of the gamma-tubulin small complex: implications of its architecture and flexibility for microtubule nucleation, Mol. Biol. Cell, 2008, vol. 19, no. 1, pp. 207–215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kollman, J.M., Greenberg, C.H., Li, S., Moritz, M., Zelter, A., Fong, K.K., Fernandez, J.-J., Sali, A., Kilmartin, J., Davis, T.N., and Agard, D.A., Ring closure activates yeast TuRC for species-specific microtubule nucleation, Nat. Struct. Mol. Biol., 2015, vol. 22, no. 2, pp. 132–137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stacklies, W., Seifert, C., and Graeter, F., Implementation of force distribution analysis for molecular dynamics simulations, BMC Bioinform., 2011, vol. 12, no. 1. doi 10.1186/1471-2105-12-101

    Google Scholar 

  37. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B.III., Snoeyink, J., Richardson, J.S., and Richardson, D.C., MolProbity: all-atom contacts and structure validation for proteins and nucleic acids, Nucleic Acids Res., 2007, vol. 35, pp. W375–383.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Benkert, P., Kunzli, M., and Schwede, T., QMEAN server for protein model quality estimation, Nucleic Acids Res., 2009, vol. 37, pp. W510–W514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Karpov, P.A., Bryrsun, V.M., Demchuk, O.M., Pydiura, N.O., Ozheredov, S.P., Samofalova, D.A., Spivak, S.I., Yemets, A.I., Kalchenko, V.I., Blume, Ya.B., and Rayevsky, A.V., High-throughput screening of new antimitotic compounds based on CSLabGrid virtual organization, Sci. Innov., 2015, vol. 11, no. 1, pp. 92–100.

    Article  Google Scholar 

  40. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E., UCSF chimera—a visualization system for exploratory research and analysis, J. Comput. Chem., 2004, vol. 25, no. 13, pp. 1605–1612.

    Article  CAS  PubMed  Google Scholar 

  41. Marx, A., Nugoor, C., Panneerselvam, S., and Mandelkow, E., Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases, FASEB J., 2010, vol. 24, no. 6, pp. 1637–1648.

    Article  CAS  PubMed  Google Scholar 

  42. Naz, F., Anjum, F., Islam, A., Ahmad, F., and Hassan, M.I., Microtubule affinity-regulating kinase 4: structure, function, and regulation, Cell Biochem. Biophys., 2013, vol. 67, no. 2, pp. 485–499.

    Article  CAS  PubMed  Google Scholar 

  43. Tassan, J.P. and Le Goff, X., An overview of the KIN1/PAR-1/MARK kinase family, Biol. Cell., 2004, vol. 96, no. 3, pp. 193–199.

    Article  CAS  PubMed  Google Scholar 

  44. Elbert, M., Rossi, G., and Brennwald, P., The yeast par-1 homologs kin1 and kin2 show genetic and physical interactions with components of the exocytic machinery, Mol. Biol. Cell, 2005, vol. 16, no. 2, pp. 532–549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to P. A. Karpov.

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Original Russian Text © P.A. Karpov, A.V. Rayevsky, E.E. Krasnoperova, S.V. Isayenkov, A.I. Yemets, Ya.B. Blume, 2017, published in Tsitologiya i Genetika, 2017, Vol. 51, No. 6, pp. 3–11.

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Karpov, P.A., Rayevsky, A.V., Krasnoperova, E.E. et al. Protein kinase KIN10 from Arabidopsis thaliana as a potential regulator of primary microtubule nucleation centers in plants. Cytol. Genet. 51, 415–421 (2017). https://doi.org/10.3103/S0095452717060056

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