SUMMARY. It was identified 18 isotypes of CK1-like protein kinases in A. thaliana. Comparison of catalytic domains in rat CK1 (α, β, γ1-3, δ, and ε) and 18 plant homologs from A. thaliana, confirm high structural similarity for 13 CK1-like kinases: CKL1 (CK1δ), CKL2, CKL3, CKL4, CKL5, CKL6, CKL7, CKL8, CKL9, CKL10, CKL11, CKL12 and CKL13. It was found that CK1-specific inhibitor D4476 interact with rat KС1D and 13 plant homologes in similar ATP-competitive manner. Ligand binding were confirmed by docking scoring functions, molecular dynamics and chemogenomic analysis. The specific binding of CK1 kinases with substrate proteins depend on specific motifs located in their C-end region. The specific motifs of EB1 binding was identified in plant СKL1 and CKL2. Also, it was confirmed the role of C-end region in CKL6-β-tubulin interaction.
Keywords: Casein kinase 1, plant homologues, tubulin, EB1, phosphorylation, inhibitor, D4476, Arabidopsis
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References
1. Cheong, J.K. and Virshup, D.M., Casein kinase 1: complexity in the family, Int. J. Biochem. Cell Biol., 2011, vol. 43, no. 4, pp. 465–469.
2. Elmore, Z.C., Guillen, R.X., and Gould, K.L., The kinase domain of CK1 enzymes contains the localization cue essential for compartmentalized signaling at the spindle pole, Mol. Biol. Cell, 2018, vol. 29, no. 13, pp. 1664–1674.
3. Qiao, Y., Chen, T., Yang, H., Chen, Y, Lin, H., Qu, W., Feng, F., Liu, W., Guo, Q., Liu, Z., and Sun, H., Small molecule modulators targeting protein kinase CK1 and CK2, Eur. J. Med. Chem., 2019, vol. 181, p. 111 581. doi.org/10.10l6/j.ejmech.2019.111581
4. Ben-Nissan, G., Cui, W., Kim, D.J., Yang, Y., Yoo, B.C., and Lee, J.Y., Arabidopsis Casein kinase 1-Like 6 contains a microtubule-binding domain and affects the organization of cortical microtubules, Plant Physiol., 2008, vol. 148, pp. 1897–1907.
5. Ben-Nissan, G., Yang, Y., and Lee, J.Y., Partitioning of casein kinase 1-like 6 to late endosome-like vesicles, Protoplasma, 2010, vol. 240, pp. 45–56.
6. Karpov, P.A., Sheremet, Ya.A., Blume, Ya.B., and Yemets, A.I., Studying the role of protein kinases CK1 in organization of cortical microtubules in Arabidopsis thaliana root cells, Cytol. Genet., 2019, vol. 53, no. 6, pp. 441–450.
7. Yemets, A., Sheremet, Y, Vissenberg, K., Van Orden, J., Verbelen, J.-P., and Blume, Y.B., Effects of tyrosine kinase and phosphatase inhibitors on microtubules in Arabidopsis root cells, Cell Biol. Int., 2008, vol. 32, pp. 630–637.
8. Cozza, G., Gianoncelli, A., Montopoli, M., Caparrotta, L., Venerando, A., Meggio, F., Pinna, L.A., Zagotto, G., and Moro, S., Identification of novel protein kinase CK1 delta (CKldelta) inhibitors through structure-based virtual screening, Bioorg. Med. Chem. Lett., 2008, vol. 18, pp. 5672–5675.
9. Perez, D.I., Gil, C., and Martinez, A., Protein kinases CK1 and CK2 as new targets for neurodegenerative diseases, Med. Res. Rev., 2011, vol. 31, vol. 924–954.
10. Rena, G., Bain, J., Elliot, M., and Cohen, P., D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXOla, EMBO Rept., 2004, vol. 5, pp. 60–5.
11. Aud, D.E., Peng, S.L.-Y., Methods of treating inflammatory diseases, US Patent no. US 2008/0146617 Al, 2008.
12. Zelenak, C, Eberhard, M., Jilani, K., Qadri, S.M., Macek, B., and Lang, F., Protein kinase CKla regulates erythrocyte survival, Cell Physiol. Biochem., 2012, vol. 29, pp. 171–180.
13. Benson, D.A, Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., and Sayers, E.W., GenBank, Nucleic Acids Res., 2011, vol. 39 (database issue), pp. D32–D37.
14. Manning, G, Whyte, D.B., Martinez, R., Hunter, T., and Sudarsanam, S., The protein kinase complement of the human genome, Science, 2002, vol. 298, pp. 1912–1934.
15. Wittau, M., Wolff, S., Xiao, Z., Henne-Bruns, D., and Knippschild, U., Die stressinduzierte Casein Kinase 1 delta kann die Spindeldynamik durch direkte Interaktion mit dem Mikrotubuli assoziierten Protein MAP1A beeinflussen, in Chirurgisches Forum 2005, Rothmund, M. Jauch, KW., and Bauer, H., Eds., Deutsche Gesellschaft fer Chirurgie, Berlin: Springer, 2005, vol. 34, ch. 13, pp. 37–39.
16. Albornoz, A., Yacez, J.M., Foerster, C, Aguirre, C, Pereiro, L., Burzio, V., Moraga, M., Reyes, A.E., and Antonelli, M., The CK1 gene family: expression patterning in zebrafish development, Biol. Res., 2007, vol. 40, pp. 251–266.
17. Löhler, J., Hirner, H., Schmidt, B., Kramer, K., Fischer, D., Thai, D.R., Leithäuser, F., and Knippschild, U., Immunohistochemical characterisation of cell-type specific expression of CK15 in various tissues of young adult BALB/c mice, PLoS One, 2009, vol. 4, no. 1, e4174.
18. Ikeda, K., Zhapparova, O., Brodsky, I., Semenova, I., Tirnauer, J.S., Zaliapin, I., and Rodionov, V., CK1 activates minus-end-directed transport of membrane organelles along microtubules, Mol. Biol. Cell, 2011, vol. 22, pp. 1321–9.
19. The UniProt Consortium, UniProt: the universal protein knowledgebase, Nucleic Acids Res., 2017, vol. 45, pp. D158–D169.
20. Claverie, J-M. and Notredame, C., Bioinformatics for Dummies, 2nd ed., New York: Wiley, 2007.
21. Korf, I., Yandell, M., and Bedell, J., BLAST, Sebastopol: O’Reilly and Associates, 2003.
22. 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. 2947–8. https://doi.org/10.1093/bioinformatics/btm404
23. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E., WebLogo: a sequence logo generator, Genome Res., 2004; vol. 14, pp. 1188–1190.
24. 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.
25. Hall, B.G., Phylogenetic Trees Made Easy, 3rd ed., Sinauer Ass. Inc., 2008.
26. Letunic, I., Doerks, T., and Bork, P., SMART 7: recent updates to the protein domain annotation resource, Nucleic Acids Res., 2012, vol. 40 (D1), pp. D302–D305.
27. Page, R.D., TREEVIEW: an application to display phylogenetic trees on personal computers, Comput. Appl. Biosci., 1996, vol. 12, pp. 357–358.
28. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S., MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 28, no. 10, pp. 2731–2739. https://doi.org/10.1093/molbev/msr121
29. Jacoby, E., Chemogenomics, Methods and Applications, Methods Mol. Biol., Springer, Humana Press, 2009, vol. 575, p. 315.
30. Huang, D., Zhou, T., Lafleur, K., Nevado, C., and Caflisch, A., Kinase selectivity potential for inhibitors targeting the ATP binding site: a network analysis, Bioinformatics, 2010, vol. 26, no. 2, pp. 198–204.
31. Baron, R., Computational Drug Discovery and Design, Methods Mol. Biol., Springer, 2012, vol. 819.
32. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.Y., Pieper U., and Sali, A., Comparative protein structure modeling with Modeller, Curr. Prot. Bioinform., 2006. https://doi.org/10.1002/0471250953.bi0506s15
33. Xu, R.M., Carmel, G., Sweet, R.M., Kuret, J., and Cheng, X., Crystal structure of casein kinase-1, a phosphate-directed protein kinase, EMBO J., 1995, vol. 14, no. 5, pp. 1015–1023.
34. Mashhoon, N., DeMaggio, A.J., Tereshko, V., Bergmeier, S.C., Egli, M., Hoekstra, M.F., and Kuret, J., Crystal structure of a conformation-selective casein kinase-1 inhibitor, J. Biol. Chem., 2000, vol. 275, no. 26, pp. 20 052–20 060. https://doi.org/10.1074/jbc.M001713200
35. Gu, J. and Bourne, P.E., Structural Bioinformatics, 2nd ed., New Jersey: Wiley, 2009.
36. Melo, F. and Feytmans, E., Assessing protein structures with a non-local atomic interaction energy, J. Mol. Biol., 1998, vol. 277, pp. 1141–1152.
37. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M., PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Cryst., 1993, vol. 26, pp. 283–291.
38. Chen, V.B., Arendall, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S., and Richardson, D.C., MolProbity: all-atom structure validation for macromolecular crystallography, Acta Crystallogr. D. Biol. Crystallogr., 2010, vol. 66, no. 1, pp. 12–21. https://doi.org/10.1107/S09074449-09042073
39. Eisenberg, D., Lüthy, R., and Bowie, J.U., VERIFY3D: assessment of protein models with three-dimensional profiles, Methods Enzymol., 1997, vol. 277, pp. 396–404.
40. Zoete, V., Cuendet, M.A., Grosdidier, A., and Michielin, O., SwissParam: a fast force field generation tool for small organic molecules, J. Comput. Chem., 2011, vol. 32, no. 11, pp. 2359–2368.
41. Hartshorn, M.J., Verdonk, M.L., Chessari, G., Brewerton, S.C., Mooij, W.T., Mortenson, P.N., and Murray C.W., Diverse, high-quality test set for the validation of protein-ligand docking performance, J. Med. Chem., 2007, vol. 50, no. 4, pp. 726–741. https://doi.org/10.1021/jm061277y
42. Stacklies, W., Seifert, C., and Graeter, F., Implementation of force distribution analysis for molecular dynamics simulations, BMC Bioinformatics, 2011, vol. 12, no. 101, pp. 1–5.
43. MacKerell, Jr.A.D., Banavali, N., and Foloppe, N., Development and current status of the CHARMM force field for nucleic acids, Biopolymers, 2001, vol. 56, no. 4, pp. 257–65.
44. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., and Mackerell, A.D., Jr., CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields, J. Comp. Chem., 2010, vol. 31, no. 4, pp. 671–690. https://doi.org/10.1002/jcc.21367
45. Biro, J.C., Amino acid size, charge, hydropathy indices and matrices for protein structure analysis, Theor. Biol. Med. Model., 2006, vol. 3, no. 15. https://doi.org/10.1186/1742-4682-3-15
46. Zyss, D., Ebrahimi, H., and Gergely, F., Casein kinase I delta controls centrosome positioning during T cell activation, J. Cell Biol., 2011, vol. 195, pp. 781–797.
47. Wolff, S., Xiao, Z., Wittau, M., Sossner, N., Stuter, M., and Knippschild, U., Interaction of casein kinase 1 delta (CK1 delta) with the light chain LC2 of microtubule associated protein 1A (MAP1A), Biochem. Biophys. Acta, 2005, no. 1745, pp. 196– 206.
48. Lӧhler, J., Hirner, H., Schmidt, B., Kramer, K., Fischer, D., Thal, D.R., Leithдuser, F., and Knippschild, U., Immunohistochemical characterisation of cell-type specific expression of CK1delta in various tissues of young adult BALB/c mice, PLoS One, 2009, vol. 4, e4174. https://doi.org/. 0004174https://doi.org/10.1371/journal.pone
49. Hamada, T., Microtubule-associated proteins in higher plants, J. Plant Res., 2007, vol. 120, pp. 79–98.
50. Karpov, P.A., and Blume, Y.B., Baird, W.V., Yemets, A.I., Breviario, D., Bioinformatic search for plant homologues of animal structural MAPs in the Arabidopsis thaliana genome, in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, Netherlands: Springer, 2008, pp. 373–394. https://doi.org/10.1007/978-1-4020-8843-8_18
51. Honnappa, S., Gouveia, S.M., Weisbrich, A., Dam-berger, F.F., Bhavesh, N.S., et al. An EB1-binding motif acts as a microtubule tip localization signal, Cell, 2009, vol. 138, pp. 366–376.