Complexes of γ-tubulin with nonreceptor protein tyrosine kinases Src and Fyn in differentiating P19 embryonal carcinoma cells

Experimental Cell Research

Volumn 298, Issue 1, 2004, Pages 218-228

  Kukharskyy, Vitaliy ^a   Sulimenko, Vadym ^a   Macůrek, Libor ^a   Sulimenko, Tetyana ^a   Dráberová, Eduarda ^a   Dráber, Pavel ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Antibodies; EC; embryonal carcinoma; Fyn; Fyn kinase; Gamma tubulin; glutathione S transferase; GST; microtubule organizing center; microtubule stabilizing buffer; MSB; MTOC; Neuronal differentiation; P19 cells; protein tyrosine kinase p59fyn; Src kinase

Indexed keywords

GAMMA TUBULIN; PROTEIN ANTIBODY; PROTEIN KINASE FYN; PROTEIN SH2; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYONAL CARCINOMA; ENZYME ACTIVITY; ENZYME ASSAY; IMMUNOPRECIPITATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 3042704345     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.04.016     Document Type: Article

References (46)

1. Maness P.F., Aubry M., Shores C.G., Frame L., Pfenninger K.H. c-src gene product in developing rat brain is enriched in nerve growth cone membranes. Proc. Natl. Acad. Sci. U. S. A. 85:1988;5001-5005
2. Beggs H.E., Soriano P., Maness P.F. NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J. Cell Biol. 127:1994;825-833
3. Ignelzi M.A. Jr., Miller D.R., Soriano P., Maness P.F. Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron. 12:1994;873-884
4. Matten W.T., Aubry M., West J., Maness P.F. Tubulin is phosphorylated at tyrosine by pp60c-src in nerve growth cone membranes. J. Cell Biol. 111:1990;1959-1970
5. Atashi J.R., Klinz S.G., Ingraham C.A., Matten W.T., Schachner M., Maness P.F. Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron. 8:1992;831-842
6. Kinnunen T., Kaksonen M., Saarinen J., Kalkkinen N., Peng H.B., Rauvala H. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J. Biol. Chem. 273:1998;10702-10708
7. Jones-Villeneuve E.M., McBurney M.W., Rogers K.A., Kalnins V.I. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol. 94:1982;253-262
8. Tanaka Y., Kawahata K., Nakata T., Hirokawa N. Chronological expression of microtubule-associated proteins (MAPs) in EC cell P19 after neuronal induction by retinoic acid. Brain Res. 596:1992;269-278
9. Vaillant A.R., Brown D.L. Accumulation of microtubule-associated protein 1A (MAP1A) in differentiating P19 embryonal carcinoma cells. Biochem. Cell Biol. 73:1995;695-702
10. Zíková M., Sulimenko V., Dráber P., Dráberová E. Accumulation of 210 kDa microtubule-interacting protein in differentiating P19 embryonal carcinoma cells. FEBS Lett. 473:2000;19-23
11. Takayama Y., Nada S., Nagai K., Okada M. Role of Csk in neural differentiation of the embryonic carcinoma cell line P19. FEBS Lett. 406:1997;11-16
12. Oakley C.E., Oakley B.R. Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature. 338:1989;662-664
13. Oakley B.R., Oakley C.E., Yoon Y., Jung M. γ-Tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell. 61:1990;1289-1301
14. Zheng Y., Wong M.L., Alberts B., Mitchison T. Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature. 378:1995;578-583
15. Moritz M., Braunfeld M.B., Fung J.C., Sedat J.W., Alberts B.M., Agard D.A. Three-dimensional structural characterization of centrosomes from Drosophila embryos. J. Cell Biol. 130:1995;1149-1159
16. Moritz M., Zheng Y., Alberts B.M., Oegema K. Recruitment of the γ-tubulin ring complex to Drosophila salt-stripped centrosome scaffolds. J. Cell Biol. 142:1998;775-786
17. Murphy S.M., Urbani L., Stearns T. The mammalian γ-tubulin complex contains homologues of the yeast spindle pole body components Spc97p and Spc98p. J. Cell Biol. 141:1998;663-674
18. Oegema K., Wiese C., Martin O.C., Milligan R.A., Iwamatsu A., Mitchison T.J., Zheng Y. Characterization of two related Drosophila γ-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144:1999;721-733
19. Wiese C., Zheng Y. A new function for the γ-tubulin ring complex as a microtubule minus-end cap. Nat. Cell Biol. 2:2000;358-364
20. Leguy R., Melki R., Pantaloni D., Carlier M.F. Monomeric γ-tubulin nucleates microtubules. J. Biol. Chem. 275:2000;21975-21980
21. Llanos R., Chevrier V., Ronjat M., Meurer-Grob P., Martinez P., Frank R., Bornens M., Wade R.H., Wehland J., Job D. Tubulin binding sites on γ-tubulin: identification and molecular characterization. Biochemistry. 38:1999;15712-15720
22. Sulimenko V., Sulimenko T., Poznanovic S., Nechiporuk-Zloy V., Böhm J.K., Macůrek L., Unger E., Dráber P. Association of brain γ-tubulins with αβ-tubulin dimers. Biochem. J. 365:2002;889-895
23. Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., Pous C. The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell. 12:2001;2047-2060
24. Dryková D., Sulimenko V., Cenklová V., Volc J., Dráber P., Binarová P. Plant γ-tubulin interacts with αβ-tubulin dimers and forms membrane-associated complexes. Plant Cell. 15:2003;465-480
25. Westermann S., Weber K. Post-translational modifications regulate microtubule function. Nat. Rev. 4:2003;938-945
26. Vogel J., Drapkin B., Oomen J., Beach D., Bloom K., Snyder M. Phosphorylation of γ-tubulin regulates microtubule organization in budding yeast. Dev. Cell. 1:2001;621-631
27. lyn forms complexes with γ-tubulin in rat basophilic leukemia cells. Int. Immunol. 11:1999;1829-1839
28. Bibbins K.B., Boeuf H., Varmus H.E. Binding of the Src SH2 domain to phosphopeptides is determined by residues in both the SH2 domain and the phosphopeptides. Mol. Cell. Biol. 13:1993;7278-7287
29. Dráber P., Malý P. Mutants of embryonal carcinoma cells defective in the expression of embryoglycan. Proc. Natl. Acad. Sci. U. S. A. 84:1987;5798-5802
30. Nováková M., Dráberová E., Schürmann W., Czihak G., Viklický V., Dráber P. γ-Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil. Cytoskeleton. 33:1996;38-51
31. Dráber P., Dráberová E., Linhartová I., Viklický V. Differences in the exposure of C- and N-terminal tubulin domains in cytoplasmic microtubules detected with domain-specific monoclonal antibodies. J. Cell Sci. 92:1989;519-528
32. Dráberová E., Lukáš Z., Ivanyi D., Viklický V., Dráber P. Expression of class III β-tubulin in normal and neoplastic human tissues. Histochem. Cell Biol. 109:1998;231-239
33. Dráber P., Dráberová E., Viklický V. Immunostaining of human spermatozoa with tubulin domain-specific monoclonal antibodies. Histochemistry. 195:1991;519-524
34. Dráberová E., Sulimenko V., Kukharskyy V., Dráber P. Monoclonal antibody NF-09 specific for neurofilament protein NF-M. Folia Biol. (Praha). 45:1999;163-165
35. 4. Nature. 227:1970;680-685
36. Dráber P. Quantitation of proteins in sample buffer for sodium dodecyl sulfate-polyacrylamide gel electrophoresis using colloidal silver. Electrophoresis. 12:1991;453-456
37. Dráberová E., Dráber P. A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J. Cell Sci. 106:1993;1263-1273
38. Dráber P., Lagunowich L.A., Dráberová E., Viklický V., Damjanov I. Heterogeneity of tubulin epitopes in mouse fetal tissues. Histochemistry. 89:1988;485-492
39. Görg A., Obermaier C., Boguth G., Weiss W. Recent developments in two-dimensional gel electrophoresis with immobilized pH gradients: wide pH gradients up to pH 12, longer separation distances and simplified procedures. Electrophoresis. 20:1999;712-717
40. Feng Y., Hodge D.R., Palmieri G., Chase D.L., Longo D.L., Ferris D.K. Association of polo-like kinase with α-, β- and γ-tubulins in a stable complex. Biochem. J. 339:1999;435-442
41. Kapeller R., Toker A., Cantley L.C., Carpenter C.L. Phosphoinositide 3-kinase binds constitutively to α/β-tubulin and binds to γ-tubulin in response to insulin. J. Biol. Chem. 270:1995;25985-25991
42. Inukai K., Funaki M., Nawano M., Katagiri H., Ogihara T., Anai M., Onishi Y., Sakoda H., Ono H., Fukushima Y., Kikuchi M., Oka Y., Asano T. The N-terminal 34 residues of the 55 kDa regulatory subunits of phosphoinositide 3-kinase interact with tubulin. Biochem. J. 346:2000;483-489
43. Wise D.O., Krahe R., Oakley B.R. The γ-tubulin gene family in humans. Genomics. 67:2000;164-170
44. Détraves C., Mazarguil H., Lajoie-Mazenc I., Julian M., Raynaud-Messina B., Wright M. Protein complexes containing gamma-tubulin are present in mammalian brain microtubule protein preparations. Cell Motil. Cytoskeleton. 36:1997;179-189
45. Linhartová I., Novotná B., Sulimenko V., Dráberová E., Dráber P. Gamma-tubulin in chicken erythrocytes: changes in localization during cell differentiation and characterization of cytoplasmic complexes. Dev. Dyn. 223:2002;229-240
46. Job D., Valiron O., Oakley B. Microtubule nucleation. Curr. Opin. Cell Biol. 15:2003;111-117