ISSN 0564-3783  

Main page
Information to authors
Editorial board
Mobile version

In Ukrainian

Export citations

Motif-based prediction of plant tubulin phosphorylationby calcium-dependent protein kinases

Karpov P.A., Novozhylov.D.O., Isayenkov.S.V., Blume Ya.B.


Tsitologiya i Genetika 2018, vol. 52, no. 6, pp. 46-60

E-mail: karpov, karpov.p.a, novozhylovd, stan.isayenkov, cellbio

Karpov P.A., Novozhylov.D.O., Isayenkov.S.V., Blume Ya.B. Motif-based prediction of plant tubulin phosphorylationby calcium-dependent protein kinases, Tsitol Genet., 2018, vol. 52, no. 6, pp. 46-60.

In "Cytology and Genetics":
P. A. Karpov, D. O. Novozhylov, S. V. Isayenkov, Ya. B. Blume Motif-Based Prediction of Plant Tubulin Phosphorylation Sites Associated with Calcium-Dependent Protein Kinases in Arabidopsis thaliana, Cytol Genet., 2018, vol. 52, no. 6, pp. 428439
DOI: 10.3103/S0095452718060038


1. Wloga, D. and Gaertig, J., Post-translational modifications of microtubules, J. Cell Sci., 2010, vol. 123, no. 20, pp. 34473455. doi 10.1242/jcs.063727

2. Blume, Ya., Yemets, A., Sulimenko, V., Sulimenko, T., Chan, J., Lloyd, C., and Draber, P., Tyrosine phosphorylation of plant tubulin, Planta, 2008, vol. 229, no. 1, pp. 143150. doi 10.1007/s00425-008-0816-z

3. Fisher, D., Gilroy, S., and Cyr, R., Evidence for opposing effects of calmodulin on cortical microtubules, Plant Physiol., 1996, vol. 112, no. 3, pp. 10791087.

4. 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 Genomics, 2010, vol. 11, suppl. 1, p. S14. doi 10.1186/1471-2164-11-S1-S14

5. Karpov, P.A., Nadezhdina, E.S., Yemets, A.I., and Blume, Ya.B., Results of the clusterization of human microtubule and cel-cycle related serine/threonine protein kinases and their plant homologues, Moscow Univ. Biol. Sci. Bull., 2010, vol. 65, no. 4, pp. 213216. doi 10.3103/S0096392510040267

6. Goodman, D.B., Rasmussen, H., DiBella, F., and Guthrow, C.E., Cyclic adenosine 3':5'-monophosphate-stimulated phosphorylation of isolated neurotubule subunits, Proc. Natl. Acad. Sci. U. S. A., 1970, vol. 67, no. 2, pp. 652659.

7. Eipper, B.A., Rat brain microtubule protein: purification and determination of covalently bound phosphate and carbohydrate, Proc. Natl. Acad. Sci. U. S. A., 1972, vol. 69, no. 8, pp. 22832287.

8. Alvarado-Kristensson, M., Rodriguez, M.J., Silio, V., Valpuesta, J.M., and Carrera, A.C., SADB phosphorylation of gamma-tubulin regulates centrosome duplication, Nat. Cell Biol., 2009, vol. 11, pp. 10811092. doi doi 10.1038/ncb1921

9. McKenney, K.M., McKenney, R.J., Huang, H.H., Li, T., Meltzer, S., Jan, L.Y., Vale, R.D., Wiita, A.P., and Jan, Y.N., Phosphorylation of β-tubulin by the down syndrome kinase, minibrain/DYRK1a, regulates microtubule dynamics and dendrite morphogenesis, Neuron, 2016, vol. 90, no. 3, pp. 551563. doi 10.1016/j.neuron.2016.03.027

10. Boscán, 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. C, 2017, vol. 72, nos. 1112, pp. 4594565. doi 10.1515/znc-2017-0019

11. Goldenring, J.R., Gonzalez, B., McGuire, J.S., Jr., and DeLorenzo, R.J., Purification and characterization of a calmodulin-dependent kinase from rat brain cytosol able to phosphorylate tubulin and microtubule-associated proteins, J. Biol. Chem., 1983, vol. 258, no. 20, pp. 1263212640.

12. 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, Cytol. Genet., 2009, vol. 43, no. 6, pp. 6877.

13. Karpov, P., Raevsky, A., Korablyov, M., and Blume, Ya., Identification of plant homologues of dual specificity Yak1-related kinases, Comput. Biol. J., 2014. doi 10.1155/2014/909268

14. 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. 227232. doi 10.3103/S0095452710040079

15. Chudinova, E.M., Karpov, P.A., Fokin, A.I., Yemets, A.I., Lytvyn, D.I., Nadezhdina, E.S., and Blume, Y.B., MAST-like protein kinase IREH1 from Arabidopsis thaliana co-localizes with the centrosome when expressed in animal cells, Planta, 2017, vol. 246, no. 5, pp. 959969. doi 10.1007/s00425-017-2742-4

16. Sheremet, Ya.A., Yemets, A.I., Vissenberg, K., Verbelen, J.P., and Blume, Ya.B., Effects of inhibitors of serine/threonine protein kinases on Arabidopsis thaliana root morphology and microtubule organization in its cells, Cell Tissue Biol., 2010, vol. 4, no. 4, pp. 399409. doi 10.1134/S1990519X10040139

17. Blume, Ya.B., Lloyd, C.W., and Yemets, A.I., Plant tubulin phosphorylation and its role in cell cycle progression, in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, 2008, pp. 14559. doi 10.1007/978-1-4020-8843-8_7

18. Sathyanarayanan, P. and Poovaiah, B., Decoding Ca2+ signals in plants, Crit. Rev. Plant Sci., 2004, vol. 23, no. 1, pp. 111. org/ doi 10.1080/07352680490273310

19. Harmon, A.C., Calcium-regulated protein kinases of plants, Gravitat. Space Biol. Bull., 2003, vol. 16, no. 2, pp. 8390.

20. Hrabak, E.M., Chan, C.W., Gribskov, M., Harper, J.F., Choi, J.H., Halford, N., Kudla, J., Luan, S., Nimmo, H.G., Sussman, M.R., Thomas, M., Walker-Simmons, K., Zhu, J.K., and Harmon, A.C., The Arabidopsis CDPK-SnRK superfamily of protein kinases, Plant Physiol., 2003, vol. 132, no. 2, pp. 666680. doi 10.1104/pp.102.011999

21. Novozhylov, D.O., Karpov, P.A., and Blume, Ya.B., Bioinformatic search for Ca2+- and calmodulin-dependent protein kinases potentially associated with the regulation of plant cytoskeleton, Cytol. Genet., 2017, vol. 51, no. 4, pp. 239246. doi 10.3103/S0095452717040053

22. Baratier, J., Peris, L., Brocard, J., Gory-Faure, S., Dufour, F., Bosc, C., Fourest-Lieuvin, A., Blanchoin, L., Salin, P., Job, D., and Andrieux, A., Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II, J. Biol. Chem., 2006, vol. 281, no. 28, pp. 1956119569. doi 10.1074/jbc.m509602200

23. Wandosell, F., Serrano, L., Hernandez, M.A., and Avila, J., Phosphorylation of tubulin by a calmodulin-dependent protein kinase, J. Biol. Chem., 1986, vol. 261, no. 22, pp. 1033210339.

24. Holmfeldt, P., Zhang, X., Stenmark, S., Walczak, C.E., and Gullberg, M., CaMKIIgamma-mediated inactivation of the Kin I kinesin MCAK is essential for bipolar spindle formation, EMBO J., 2005, vol. 24, no. 6, pp. 12551266. doi 10.1038/sj.emboj.7600601

25. Hoffman, L., Farley, M.M., and Waxham, M.N., Calcium-calmodulin-dependent protein kinase II isoforms differentially impact the dynamics and structure of the actin cytoskeleton, Biochemistry, 2013, vol. 52, no. 7, pp. 11981207. doi 10.1021/bi3016586

26. Zhao, J.W., Gao, Z.L., Ji, Q.Y., Wang, H., Zhang, H.Y., Yang, Y.D., Xing, F.J., Meng, L.J., and Wang, Y., Regulation of cofilin activity by CaMKII and calcineurin, Am. J. Med. Sci., 2012, vol. 344, no. 6, pp. 46272. doi 10.1097/MAJ.0b013e318244745b

27. Easley, C.A., Faison, M.O., Kirsch, T.L., Lee, J.A., Seward, M.E., and Tombes, R.M., Laminin ctivates CaMK-II to stabilize nascent embryonic axons, Brain Res., 2006, vol. 1092, no. 1, pp. 5968. doi 10.1016/ j.brainres.2006.03.099

28. The UniProt Consortium UniProt: the universal protein knowledgebase, Nucleic Acids Res., 2018, vol. 46, no. 5, p. 2699. org/ doi 10.1093/nar/gky092

29. Lee, M.M., Chan, M.K., and Bundschuh, R., SIBBLAST: a web server for improved delineation of true and false positives in PSI-BLAST searches, Nucleic Acids Res., 2009, vol. 37, nos. 12, pp. W53W56. doi 10.1093/nar/gkp301

30. Korf, I., Yandell, M., and Bedell, J., BLAST, Sebastopol: OReilly and Associates, Inc., 2003.

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., Higgins, D.G., and Clustal, W., Clustal X., version 2.0, Bioinformatics, 2007, vol. 23, no. 21, pp. 29472948. doi 10.1093/bioinformatics/btm404

32. Hornbeck, P.V., Zhang, B., Murray, B., Kornhauser, J.M., Latham, V., and Skrzypek, E., PhosphoSitePlus, 2014: mutations, PTMs and recalibrations, Nucleic Acids Res., 2014, vol. 43, pp. D512D520. doi 10.1093/nar/gku1267

33. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E., WebLogo: A sequence logo generator, Genome Res., 2004, vol. 14, no. 6, pp. 11881190. doi 10.1101/gr.849004

34. Sigrist, C.J.A., de Castro, E., Cerutti, L., Cuche, B.A., Hulo, N., Bridge, A., Bougueleret, L., and Xenarios, I., New and continuing developments at PROSITE, Nucleic Acids Res., 2013, vol. 41, pp. D344D347. doi 10.1093/nar/gks1067

35. Atteson, K., The performance of neighbor-joining algorithms of phylogeny reconstruction, Lecture Notes Comp. Sci., 1997, vol. 1276, pp. 101110.

36. 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. 18701874. doi 10.1093/molbev/msw054

37. Letunic, I., Doerks, T., and Bork, P., SMART: recent updates, new developments and status in 2015, Nucleic Acids Res., 2015, vol. 43, pp. D257D60. doi 10.1093/nar/gku949

38. 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, no. D1, pp. D279D285. doi 10.1093/nar/gkv1344

39. 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. W362W365. doi 10.1093/nar/gkl124

40. Finn, R.D., Attwood, T.K., Babbitt, P.C., Bateman, A., Bork, P., Bridge, A.J., Chang, H.Y., Dosztnyi, Z., El-Gebali, S., Fraser, M., Gough, J., Haft, D., Holliday, G.L., Huang, H., Huang, X., Letunic, I., Lopez, R., Lu, S., Marchler-Bauer, A., Mi, H., Mistry, J., Natale, D.A., Necci, M., Nuka, G., Orengo, C.A., Park, Y., Pesseat, S., Piovesan, D., Potter, S.C., Rawlings, N.D., Redaschi, N., Richardson, L., Rivoire, C., Sangrador-Vegas, A., Sigrist, C., Sillitoe, I., Smithers, B., Squizzato, S., Sutton, G., Thanki, N., Thomas, P.D., Tosatto, S.C., Wu, C.H., Xenarios, I., Yeh, L.S., Young, S.Y., and Mitchell, A.L., InterPro in 2017-beyond protein family and domain annotations, Nucleic Acids Res., 2017, vol. 45, no. D1, pp. D190D199. doi 10.1093/nar/gkw1107

41. Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., and Zhang, Y., The I-TASSER Suite: protein structure and function prediction, Nature Meth., 2015, vol. 12, no. 1, pp. 78. doi 10.1038/nmeth.3213

42. Lee, J.-Y., Yoo, B.-C., and Harmon, A.C., Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean, Biochemistry, 1998, vol. 37, no. 19, pp. 68016809. doi 10.1021/bi980062q

43. Bachmann, M., Shiraishi, N., Campbell, W.H., Yoo, B.-C., Harmon, A.C., and Huber, S.C., Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase, Plant Cell., 1996, vol. 8, no. 3, pp. 505517. doi 10.1105/tpc.8.3.505

44. Huang, J.-Z., Hardin, S.C., and Huber, S.C., Identification of a novel phosphorylation motif for CDPKs: phosphorylation of synthetic peptides lacking basic residues at P-3/P-4, Arch. Biochem. Biophys., 2001, vol. 393, no. 1, pp. 6166. doi 10.1006/abbi.2001.2476

45. Sebastia, C.H., Hardin, S.C., Clouse, S.D., Kieber, J.J., and Huber, S.C., Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate, Arch. Biochem. Biophys., 2004, vol. 428, no. 1, pp. 8191. doi 10.1016/

46. Harmon, A.C., Gribskov, M., Gubrium, E., and Harper, J.F., The CDPK superfamily of protein kinases, New Phytol., 2001, vol. 151, no. 1, pp. 175183. org/ doi 10.1046/j.1469-8137.2001.00171.x

47. McCurdy, D.W. and Harmon, A.C., Calcium-dependent protein kinase in the green alga Chara, Planta, 1992, vol. 188, no. 1, pp. 5461. doi 10.1007/BF00198939

48. Sugiyama, K., Mori, I.C., Takahashi, K., Muto, S., and Shihira-Ishikawa, I., A calcium-dependent protein kinase functions in wound healing in Ventricaria ventricosa (Chlorophyta), J. Phycol., 2000, vol. 36, pp. 11451152. doi 10.1046/j.1529-8817.2000.00050.x

49. Billker, O., Lourido, S., and Sibley, L.D., Calcium-dependent signaling and kinases in Apicomplexan parasites, Cell Host Microbe, 2009, vol. 5, no. 6, pp. 612622. doi 10.1016/j.chom.2009.05.017

50. Fantino, E., Segretin, M.E., Santin, F., Mirkin, F.G., and Ulloa, R.M., Analysis of the potato calciumdependent protein kinase family and characterization of StCDPK7, a member induced upon infection with Phytophthora infestans, Plant Cell Rep., 2017, vol. 36, no. 7, pp. 11371157. doi 10.1007/s00299-017-2144-x

51. Valmonte, G.R., Arthur, K., and Higgins, C.M., MacDiarmid R.M., Calcium-dependent protein kinases in plants: evolution, expression and function, Plant Cell Physiol., 2014, vol. 55, no. 3, pp. 551569. doi 10.1093/pcp/pct200

52. Ren, R., Sun, Y., Zhao, Y., Geiser, D., Ma, H., and Zhou, X., Phylogenetic resolution of deep eukaryotic and fungal relationships using highly conserved low-copy nuclear genes, Genome Biol. Evol., 2016, vol. 8, no. 9, pp. 26832701. doi 10.1093/gbe/evw196

53. Hey, S.J., Mayerhofer, H., Halford, N.G., and Dickinson, J.R., DNA sequences from Arabidopsis, which encode protein kinases and function as upstream regulators of Snf1 in yeast, J. Biol. Chem., 2007, vol. 282, pp. 1047210479. doi 10.1074/jbc.M611244200

54. Shen, W., Reyes, M., and Hanley-Bowdoin, L., Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop, Plant Physiol., 2009, vol. 150, no. 2, pp. 9961005. doi 10.1104/pp.108.132787

55. Crozet, P., Jammes, F., Valot, B., Ambard-Bretteville, F., Nessler, S., Hodges, M., Vidal, J., and Thomas, M., Cross-phosphorylation between Arabidopsis thaliana sucrose nonfermenting 1-related protein kinase 1 (AtSnRK1) and its activating kinase (AtSnAK) determines their catalytic activities, J. Biol. Chem., 2010, vol. 285, no. 16, pp. 1207112077. doi 10.1074/ jbc.M109.079194

56. Karpov, P.A., Raevsky, A.V., Krasnoperova, E.E., Isayenkov, S.V., Yemets, A.I., and Blume, Ya.B., Protein kinase KIN10 from Arabidopsis thaliana as a potential regulator of primary microtubule nucleation centers in plants, Cytol. Genet., 2017, vol. 51, no. 6, pp. 415421. doi 10.3103/S0095452717060056

Copyright© ICBGE 2002-2021 Coded & Designed by Volodymyr Duplij Modified 22.06.21