Microtubule nucleation in mouse bone marrow-derived mast cells is regulated by the concerted action of GIT1/βPIX proteins and calcium

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4099-4111

  Sulimenko, Vadym ^a   Hájková, Zuzana ^a,b   Černohorská, Markéta ^a,b   Sulimenko, Tetyana ^a   Sládková, Vladimíra ^a   Dráberová, Lubica ^a   Vinopal, Stanislav ^a   Dráberová, Eduarda ^a   Dráber, Pavel ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM ION; G PROTEIN COUPLED RECEPTOR KINASE; GAMMA TUBULIN; P21 ACTIVATED KINASE; PROTEIN BETAPIX; PROTEIN GIT1; UNCLASSIFIED DRUG; ARHGEF7 PROTEIN, MOUSE; CELL CYCLE PROTEIN; GIT1 PROTEIN, MOUSE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED MAST CELL; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL GROWTH; CENTROSOME; CYTOSOL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IMMUNOREGULATION; MICROTUBULE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUBULIN POLYMERIZATION ASSAY; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; CYTOLOGY; MAST CELL; METABOLISM;

ANIMALS; BONE MARROW CELLS; CALCIUM; CELL CYCLE PROTEINS; GTPASE-ACTIVATING PROTEINS; MAST CELLS; MICE; MICE, INBRED BALB C; MICROTUBULES; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS;

EID: 84928484964     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402459     Document Type: Article

References (57)

1. Gilfillan, A. M., and J. Rivera. 2009. The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228: 149-169.
2. Smith, A. J., J. R. Pfeiffer, J. Zhang, A. M. Martinez, G. M. Griffiths, and B. S. Wilson. 2003. Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic 4: 302-312.
3. Nishida, K., S. Yamasaki, Y. Ito, K. Kabu, K. Hattori, T. Tezuka, H. Nishizumi, D. Kitamura, R. Goitsuka, R. S. Geha, et al. 2005. FcεRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell Biol. 170: 115-126.
4. Martin-Verdeaux, S., I. Pombo, B. Iannascoli, M. Roa, N. Varin-Blank, J. Rivera, and U. Blank. 2003. Evidence of a role for Munc18-2 and microtubules in mast cell granule exocytosis. J. Cell Sci. 116: 325-334.
5. Sulimenko, V., E. Dráberová, T. Sulimenko, L. Macu˚rek, V. Richterová, P. Dráber, and P. Dráber. 2006. Regulation of microtubule formation in activated mast cells by complexes of γ-tubulin with Fyn and Syk kinases. J. Immunol. 176: 7243-7253.
6. Hájková, Z., V. Bugajev, E. Dráberová, S. Vinopal, L. Dráberová, J. Janácek, P. Dráber, and P. Dráber. 2011. STIM1-directed reorganization of microtubules in activated mast cells. J. Immunol. 186: 913-923.
7. Cruse, G., M. A. Beaven, I. Ashmole, P. Bradding, A. M. Gilfillan, and D. D. Metcalfe. 2013. A truncated splice-variant of the FcεRIb receptor subunit is critical for microtubule formation and degranulation in mast cells. Immunity 38: 906-917.
8. Grigoriev, I., S. M. Gouveia, B. van der Vaart, J. Demmers, J. T. Smyth, S. Honnappa, D. Splinter, M. O. Steinmetz, J. W. Putney, Jr., C. C. Hoogenraad, and A. Akhmanova. 2008. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18: 177-182.
9. Oakley, C. E., and B. R. Oakley. 1989. Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338: 662-664.
10. Oegema, K., C. Wiese, O. C. Martin, R. A. Milligan, A. Iwamatsu, T. J. Mitchison, and Y. Zheng. 1999. Characterization of two related Drosophila g-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 144: 721-733.
11. Vogel, J., B. Drapkin, J. Oomen, D. Beach, K. Bloom, and M. Snyder. 2001. Phosphorylation of γ-tubulin regulates microtubule organization in budding yeast. Dev. Cell 1: 621-631.
12. Keck, J. M., M. H. Jones, C. C. Wong, J. Binkley, D. Chen, S. L. Jaspersen, E. P. Holinger, T. Xu, M. Niepel, M. P. Rout, et al. 2011. A cell cycle phosphoproteome of the yeast centrosome. Science 332: 1557-1561.
13. Colello, D., C. G. Reverte, R. Ward, C. W. Jones, V. Magidson, A. Khodjakov, and S. E. LaFlamme. 2010. Androgen and Src signaling regulate centrosome activity. J. Cell Sci. 123: 2094-2102.
14. Nováková, M., E. Dráberová, W. Schürmann, G. Czihak, V. Viklický, and P. Dráber. 1996. γ-Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil. Cytoskeleton 33: 38-51.
15. Hořejší, B., S. Vinopal, V. Sládková, E. Dráberová, V. Sulimenko, T. Sulimenko, V. Vosecká, A. Philimonenko, P. Hozák, C. D. Katsetos, and P. Dráber. 2012. Nuclear γ-tubulin associates with nucleoli and interacts with tumor suppressor protein C53. J. Cell. Physiol. 227: 367-382.
16. Dráberová, E., V. Sulimenko, V. Kukharskyy, and P. Dráber. 1999. Monoclonal antibody NF-09 specific for neurofilament protein NF-M. Folia Biol. (Praha) 45: 163-165.
17. Hibbs, M. L., D. M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S. A. Stacker, and A. R. R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
18. Kovárová, M., P. Tolar, R. Arudchandran, L. Dráberová, J. Rivera, and P. Dráber. 2001. Structure-function analysis of Lyn kinase association with lipid rafts and initiation of early signaling events after Fcε receptor I aggregation. Mol. Cell. Biol. 21: 8318-8328.
19. Zheng, Y., M. K. Jung, and B. R. Oakley. 1991. γ-Tubulin is present in Drosophila melanogaster and Homo sapiens and is associated with the centrosome. Cell 65: 817-823.
20. Vinopal, S., M. Cernohorská, V. Sulimenko, T. Sulimenko, V. Vosecká, M. Flemr, E. Dráberová, and P. Dráber. 2012. γ-Tubulin 2 nucleates microtubules and is downregulated in mouse early embryogenesis. PLoS ONE 7: e29919.
21. ten Klooster, J. P., Z. M. Jaffer, J. Chernoff, and P. L. Hordijk. 2006. Targeting and activation of Rac1 are mediated by the exchange factor b-Pix. J. Cell Biol. 172: 759-769.
22. Dráber, P. 1991. Quantification of proteins in sample buffer for sodium dodecyl sulfate-polyacrylamide gel electrophoresis using colloidal silver. Electrophoresis 12: 453-456.
23. Kukharskyy, V., V. Sulimenko, L. Macu˚rek, T. Sulimenko, E. Dráberová, and P. Dráber. 2004. Complexes of γ-tubulin with nonreceptor protein tyrosine kinases Src and Fyn in differentiating P19 embryonal carcinoma cells. Exp. Cell Res. 298: 218-228.
24. Dráber, P., L. A. Lagunowich, E. Dráberová, V. Viklický, and I. Damjanov. 1988. Heterogeneity of tubulin epitopes in mouse fetal tissues. Histochemistry 89: 485-492.
25. Surviladze, Z., L. Dráberová, M. Kovářová, M. Boubelík, and P. Dráber. 2001. Differential sensitivity to acute cholesterol lowering of activation mediated via the high-affinity IgE receptor and Thy-1 glycoprotein. Eur. J. Immunol. 31: 1-10.
26. Polakovicova, I., L. Draberova, M. Simicek, and P. Draber. 2014. Multiple regulatory roles of the mouse transmembrane adaptor protein NTAL in gene transcription and mast cell physiology. PLoS ONE 9: e105539.
27. Dráberová, E., and P. Dráber. 1993. A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J. Cell Sci. 106: 1263-1273.
28. Hoefen, R. J., and B. C. Berk. 2006. The multifunctional GIT family of proteins. J. Cell Sci. 119: 1469-1475.
29. Frank, S. R., and S. H. Hansen. 2008. The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin. Cell Dev. Biol. 19: 234-244.
30. Webb, D. J., M. W. Mayhew, M. Kovalenko, M. J. Schroeder, E. D. Jeffery, L. Whitmore, J. Shabanowitz, D. F. Hunt, and A. F. Horwitz. 2006. Identification of phosphorylation sites in GIT1. J. Cell Sci. 119: 2847-2850.
31. Teshima, R., H. Ikebuchi, M. Nakanishi, and J. Sawada. 1994. Stimulatory effect of pervanadate on calcium signals and histamine secretion of RBL-2H3 cells. Biochem. J. 302: 867-874.
32. Komarova, Y. A., I. A. Vorobjev, and G. G. Borisy. 2002. Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J. Cell Sci. 115: 3527-3539.
33. Delgehyr, N., J. Sillibourne, and M. Bornens. 2005. Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J. Cell Sci. 118: 1565-1575.
34. 2+release from the endoplasmic reticulum and associated histamine release from rat peritoneal mast cells. Biochem. Pharmacol. 41: 1031-1037.
35. Dráberová, L., E. Dráberová, Z. Surviladze, P. Dráber, and P. Dráber. 1999. Protein tyrosine kinase p53/p56(lyn) forms complexes with γ-tubulin in rat basophilic leukemia cells. Int. Immunol. 11: 1829-1839.
36. Schmalzigaug, R., H. Phee, C. E. Davidson, A. Weiss, and R. T. Premont. 2007. Differential expression of the ARF GAP genes GIT1 and GIT2 in mouse tissues. J. Histochem. Cytochem. 55: 1039-1048.
37. Bagrodia, S., D. Bailey, Z. Lenard, M. Hart, J. L. Guan, R. T. Premont, S. J. Taylor, and R. A. Cerione. 1999. A tyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J. Biol. Chem. 274: 22393-22400.
38. Totaro, A., V. Astro, D. Tonoli, and I. de Curtis. 2014. Identification of two tyrosine residues required for the intramolecular mechanism implicated in GIT1 activation. PLoS ONE 9: e93199.
39. Ren, Y., L. Yu, J. Fan, Z. Rui, Z. Hua, Z. Zhang, N. Zhang, and G. Yin. 2012. Phosphorylation of GIT1 tyrosine 321 is required for association with FAK at focal adhesions and for PDGF-activated migration of osteoblasts. Mol. Cell. Biochem. 365: 109-118.
40. Wang, J., G. Yin, P. Menon, J. Pang, E. M. Smolock, C. Yan, and B. C. Berk. 2010. Phosphorylation of G protein-coupled receptor kinase 2-interacting protein 1 tyrosine 392 is required for phospholipase C-g activation and podosome formation in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 30: 1976-1982.
41. Feng, Q., D. Baird, S. Yoo, M. Antonyak, and R. A. Cerione. 2010. Phosphorylation of the cool-1/b-Pix protein serves as a regulatory signal for the migration and invasive activity of Src-transformed cells. J. Biol. Chem. 285: 18806-18816.
42. Macurek, L., E. Dráberová, V. Richterová, V. Sulimenko, T. Sulimenko, L. Dráberová, V. Marková, and P. Dráber. 2008. Regulation of microtubule nucleation from membranes by complexes of membrane-bound γ-tubulin with Fyn kinase and phosphoinositide 3-kinase. Biochem. J. 416: 421-430.
43. Katagiri, K., T. Katagiri, K. Kajiyama, T. Yamamoto, and T. Yoshida. 1993. Tyrosine-phosphorylation of tubulin during monocytic differentiation of HL-60 cells. J. Immunol. 150: 585-593.
44. Ley, S. C., M. Marsh, C. R. Bebbington, K. Proudfoot, and P. Jordan. 1994. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125: 639-649.
45. Colello, D., S. Mathew, R. Ward, K. Pumiglia, and S. E. LaFlamme. 2012. Integrins regulate microtubule nucleating activity of centrosome through mitogen-activated protein kinase/extracellular signal-regulated kinase kinase/extracellular signal-regulated kinase (MEK/ERK) signaling. J. Biol. Chem. 287: 2520-2530.
46. Fargier, G., C. Favard, A. Parmeggiani, A. Sahuquet, F. Mérezègue, A. Morel, M. Denis, N. Molinari, P. H. Mangeat, P. J. Coopman, and P. Montcourrier. 2013. Centrosomal targeting of Syk kinase is controlled by its catalytic activity and depends on microtubules and the dynein motor. FASEB J. 27: 109-122.
47. Dráber, P., V. Sulimenko, and E. Dráberová. 2012. Cytoskeleton in mast cell signaling. Front. Immunol. 3: 130.
48. Singh, V. K., K. Munro, and Z. Jia. 2012. A novel calmodulin-b-PIX interaction and its implication in receptor tyrosine kinase regulation. Cell. Signal. 24: 1790-1796.
49. Psatha, M. I., M. Razi, A. Koffer, S. E. Moss, D. B. Sacks, and S. R. Bolsover. 2007. Targeting of calcium:calmodulin signals to the cytoskeleton by IQGAP1. Cell Calcium 41: 593-605.
50. Sibilano, R., B. Frossi, R. Suzuki, F. D'Incá, G. Gri, S. Piconese, M. P. Colombo, J. Rivera, and C. E. Pucillo. 2012. Modulation of FcεRI-dependent mast cell response by OX40L via Fyn, PI3K, and RhoA. J. Allergy Clin. Immunol. 130: 751-760, e2.
51. Lefèvre, J., K. G. Chernov, V. Joshi, S. Delga, F. Toma, D. Pastré, P. A. Curmi, and P. Savarin. 2011. The C terminus of tubulin, a versatile partner for cationic molecules: binding of Tau, polyamines, and calcium. J. Biol. Chem. 286: 3065-3078.
52. Zhao, Z. S., J. P. Lim, Y. W. Ng, L. Lim, and E. Manser. 2005. The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol. Cell 20: 237-249.
53. Lüders, J., U. K. Patel, and T. Stearns. 2006. GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8: 137-147.
54. Teixidó-Travesa, N., J. Roig, and J. Lüders. 2012. The where, when and how of microtubule nucleation - one ring to rule them all. J. Cell Sci. 125: 4445-4456.
55. Frank, S. R., M. R. Adelstein, and S. H. Hansen. 2006. GIT2 represses Crk- and Rac1-regulated cell spreading and Cdc42-mediated focal adhesion turnover. EMBO J. 25: 1848-1859.
56. Gavina, M., L. Za, R. Molteni, R. Pardi, and I. de Curtis. 2010. The GIT-PIX complexes regulate the chemotactic response of rat basophilic leukaemia cells. Biol. Cell 102: 231-244.
57. Ganguly, A., H. Yang, R. Sharma, K. D. Patel, and F. Cabral. 2012. The role of microtubules and their dynamics in cell migration. J. Biol. Chem. 287: 43359-43369.