Mast cell activation mediated by the high affinity receptor for IgE (FcεRI) is a key event in allergic response and inflammation. Other receptors on mast cells, as c-Kit for stem cell factor and G protein-coupled receptors (GPCRs) synergistically enhance the FcεRI-mediated release of inflammatory mediators. Activation of various signaling pathways in mast cells results in changes in cell morphology, adhesion to substrate, exocytosis, and migration. Reorganization of cytoskeleton is pivotal in all these processes. Cytoskeletal proteins also play an important role in initial stages of FcεRI and other surface receptors induced triggering. Highly dynamic microtubules formed by αβ-tubulin dimers as well as microfilaments build up from polymerized actin are affected in activated cells by kinases/phosphatases, Rho GTPases and changes in concentration of cytosolic Ca(2+). Also important are nucleation proteins; the γ-tubulin complexes in case of microtubules or Arp 2/3 complex with its nucleation promoting factors and formins in case of microfilaments. The dynamic nature of microtubules and microfilaments in activated cells depends on many associated/regulatory proteins. Changes in rigidity of activated mast cells reflect changes in intermediate filaments build up from vimentin. This review offers a critical appraisal of current knowledge on the role of cytoskeleton in mast cells signaling.

Department of Biology of Cytoskeleton Institute of Molecular Genetics Academy of Sciences of the Czech Republic Prague Czech Republic

Zobrazit více v PubMed

Akhmanova A., Steinmetz M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309–322 10.1038/nrm2369 PubMed DOI

Allen J. D., Jaffer Z. M., Park S. J., Burgin S., Hofmann C., Sells M. A., Chen S., Derr-Yellin E., Michels E. G., McDaniel A., Bessler W. K., Ingram D. A., Atkinson S. J., Travers J. B., Chernoff J., Clapp D. W. (2009). p21-Activated kinase regulates mast cell degranulation via effects on calcium mobilization and cytoskeletal dynamics. Blood 113, 2695–2705 10.1182/blood-2008-06-160861 PubMed DOI PMC

Alvarado-Kristensson M., Rodriguez M. J., Silio V., Valpuesta J. M., Carrera A. C. (2009). SADB phosphorylation of gamma-tubulin regulates centrosome duplication. Nat. Cell Biol. 11, 1081–1092 10.1038/ncb1921 PubMed DOI

Amos L. A., Schlieper D. (2005). Microtubules and maps. Adv. Protein Chem. 71, 257–298 10.1016/S0065-3233(04)71007-4 PubMed DOI

Andrews N. L., Lidke K. A., Pfeiffer J. R., Burns A. R., Wilson B. S., Oliver J. M., Lidke D. S. (2008). Actin restricts FcεRI diffusion and facilitates antigen-induced receptor immobilization. Nat. Cell Biol. 10, 955–963 10.1038/ncb1755 PubMed DOI PMC

Apgar J. R. (1994). Polymerization of actin in RBL-2H3 cells can be triggered through either the IgE receptor or the adenosine receptor but different signaling pathways are used. Mol. Biol. Cell 5, 313–322 PubMed PMC

Arthur W. T., Petch L. A., Burridge K. (2000). Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10, 719–722 10.1016/S0960-9822(00)00537-6 PubMed DOI

Baba Y., Hayashi K., Fujii Y., Mizushima A., Watarai H., Wakamori M., Numaga T., Mori Y., Iino M., Hikida M., Kurosaki T. (2006). Coupling of STIM1 to store-operated Ca PubMed DOI PMC

Bakowski D., Glitsch M. D., Parekh A. B. (2001). An examination of the secretion-like coupling model for the activation of the Ca PubMed PMC

Bartolini F., Moseley J. B., Schmoranzer J., Cassimeris L., Goode B. L., Gundersen G. G. (2008). The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J. Cell Biol. 181, 523–536 10.1083/jcb.200709029 PubMed DOI PMC

Bement W. M., Miller A. L., von Dassow G. (2006). Rho GTPase activity zones and transient contractile arrays. Bioessays 28, 983–993 10.1002/bies.20477 PubMed DOI PMC

Bishop A. L., Hall A. (2000). Rho GTPases and their effector proteins. Biochem. J. 348, 241–255 10.1042/0264-6021:3480241 PubMed DOI PMC

Blank U., Rivera J. (2004). The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol. 25, 266–273 10.1016/j.it.2004.03.005 PubMed DOI

Borovikov Y. S., Norman J. C., Price L. S., Weeds A., Koffer A. (1995). Secretion from permeabilised mast cells is enhanced by addition of gelsolin: contrasting effects of endogenous gelsolin. J. Cell Sci. 108, 657–666 PubMed

Brown A. M., O’Sullivan A. J., Gomperts B. D. (1998). Induction of exocytosis from permeabilized mast cells by the guanosine triphosphatases Rac and Cdc42. Mol. Biol. Cell 9, 1053–1063 PubMed PMC

Brown M. J., Hallam J. A., Colucci-Guyon E., Shaw S. (2001). Rigidity of circulating lymphocytes is primarily conferred by vimentin intermediate filaments. J. Immunol. 166, 6640–6646 PubMed

Buccione R., Orth J. D., McNiven M. A. (2004). Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5, 647–657 10.1038/nrm1436 PubMed DOI

Bueb J. L., Da S. A., Mousli M., Landry Y. (1992). Natural polyamines stimulate G-proteins. Biochem. J. 282, 545–550 PubMed PMC

Bugajev V., Bambousková M., Dráberová L., Dráber P. (2010). What precedes the initial tyrosine phosphorylation of the high affinity IgE receptor in antigen-activated mast cell? FEBS Lett. 584, 4949–4955 10.1016/j.febslet.2010.08.045 PubMed DOI

Cahalan M. D. (2009). STIMulating store-operated Ca PubMed DOI PMC

Cai L., Marshall T. W., Uetrecht A. C., Schafer D. A., Bear J. E. (2007). Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128, 915–929 10.1016/j.cell.2007.01.031 PubMed DOI PMC

Calloway N., Vig M., Kinet J. P., Holowka D., Baird B. (2009). Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca PubMed DOI PMC

Carlier M. F. (1991). Nucleotide hydrolysis in cytoskeletal assembly. Curr. Opin. Cell Biol. 3, 12–17 10.1016/0955-0674(91)90160-Z PubMed DOI

Carlier M. F., Nioche P., Broutin-L’Hermite I., Boujemaa R., Le C. C., Egile C., Garbay C., Ducruix A., Sansonetti P., Pantaloni D. (2000). GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex. J. Biol. Chem. 275, 21946–21952 10.1074/jbc.M000687200 PubMed DOI

Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., Pous C. (2001). The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell 12, 2047–2060 PubMed PMC

Chan C., Beltzner C. C., Pollard T. D. (2009). Cofilin dissociates Arp2/3 complex and branches from actin filaments. Curr. Biol. 19, 537–545 10.1016/j.cub.2009.02.060 PubMed DOI PMC

Chou Y. H., Flitney F. W., Chang L., Mendez M., Grin B., Goldman R. D. (2007). The motility and dynamic properties of intermediate filaments and their constituent proteins. Exp. Cell Res. 313, 2236–2243 10.1016/j.yexcr.2007.04.008 PubMed DOI

Colello D., Reverte C. G., Ward R., Jones C. W., Magidson V., Khodjakov A., LaFlamme S. E. (2010). Androgen and Src signaling regulate centrosome activity. J. Cell Sci. 123, 2094–2102 10.1242/jcs.057505 PubMed DOI PMC

Coulombe P. A., Wong P. (2004). Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat. Cell Biol. 6, 699–706 10.1038/ncb0804-699 PubMed DOI

Deng Z., Zink T., Chen H. Y., Walters D., Liu F. T., Liu G. Y. (2009). Impact of actin rearrangement and degranulation on the membrane structure of primary mast cells: a combined atomic force and laser scanning confocal microscopy investigation. Biophys. J. 96, 1629–1639 10.1016/j.bpj.2008.12.1272 PubMed DOI PMC

Desai A., Mitchison T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83–117 10.1146/annurev.cellbio.13.1.83 PubMed DOI

dos Remedios C. G., Chhabra D., Kekic M., Dedova I. V., Tsubakihara M., Berry D. A., Nosworthy N. J. (2003). Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83, 433–473 PubMed

Dráber P., Dráberová E. (2012). “Microtubules,” in Cytoskeleton and Human Disease, ed. Kavallaris M. (New York, NY: Humana Press; ), 29–54

Dráber P., Hálová I., Levi-Schaffer F., Dráberová L. (2012). Transmembrane adaptor proteins in the high-affinity IgE receptor signaling. Front. Immunol. 2:95. 10.3389/fimmu.2011.00095 PubMed DOI PMC

Dráberová E., Dráber P. (1993). A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J. Cell Sci. 106, 1263–1273 PubMed

Dráberová L., Dráberová E., Surviladze Z., Dráber Pe., Dráber P. (1999). Protein tyrosine kinase p53/p56 PubMed DOI

Dryková D., Sulimenko V., Cenklová V., Volc J., Dráber P., Binarová P. (2003). Plant γ-tubulin interacts with αβ-tubulin dimers and forms membrane-associated complexes. Plant Cell 15, 465–480 10.1105/tpc.007005 PubMed DOI PMC

Dziadek M. A., Johnstone L. S. (2007). Biochemical properties and cellular localisation of STIM proteins. Cell Calcium 42, 123–132 10.1016/j.ceca.2007.02.006 PubMed DOI

Eiseman E., Bolen J. B. (1992). Engagement of the high-affinity IgE receptor activates Src protein-related tyrosine kinases. Nature 355, 78–80 10.1038/355078a0 PubMed DOI

Faruki S., Geahlen R. L., Asai D. J. (2000). Syk-dependent phosphorylation of microtubules in activated B-lymphocytes. J. Cell Sci. 113, 2557–2565 PubMed

Fernandez J. A., Keshvara L. M., Peters J. D., Furlong M. T., Harrison M. L., Geahlen R. L. (1999). Phosphorylation- and activation-independent association of the tyrosine kinase Syk and the tyrosine kinase substrates Cbl and Vav with tubulin in B-cells. J. Biol. Chem. 274, 1401–1406 10.1074/jbc.274.3.1401 PubMed DOI

Fifadara N. H., Beer F., Ono S., Ono S. J. (2010). Interaction between activated chemokine receptor 1 and FcepsilonRI at membrane rafts promotes communication and F-actin-rich cytoneme extensions between mast cells. Int. Immunol. 22, 113–128 10.1093/intimm/dxp118 PubMed DOI PMC

Firat-Karalar E. N., Welch M. D. (2011). New mechanisms and functions of actin nucleation. Curr. Opin. Cell Biol. 23, 4–13 10.1016/j.ceb.2010.10.007 PubMed DOI PMC

Foger N., Jenckel A., Orinska Z., Lee K. H., Chan A. C., Bulfone-Paus S. (2011). Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins Coronin1a and Coronin1b. J. Exp. Med. 208, 1777–1787 10.1084/jem.20101757 PubMed DOI PMC

Foster K. G., Fingar D. C. (2010). Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. J. Biol. Chem. 285, 14071–14077 10.1074/jbc.M109.029637 PubMed DOI PMC

Frigeri L., Apgar J. R. (1999). The role of actin microfilaments in the down-regulation of the degranulation response in RBL-2H3 mast cells. J. Immunol. 162, 2243–2250 PubMed

Galan C., Dionisio N., Smani T., Salido G. M., Rosado J. A. (2011). The cytoskeleton plays a modulatory role in the association between STIM1 and the Ca PubMed DOI

Galjart N. (2010). Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 20, R528–R537 10.1016/j.cub.2010.05.022 PubMed DOI

Galli S. J., Tsai M., Piliponsky A. M. (2008). The development of allergic inflammation. Nature 454, 445–454 10.1038/nature07204 PubMed DOI PMC

Gilfillan A. M., Rivera J. (2009). The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228, 149–169 10.1111/j.1600-065X.2008.00742.x PubMed DOI PMC

Goley E. D., Welch M. D. (2006). The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713–726 10.1038/nrm2026 PubMed DOI

Green K. J., Bohringer M., Gocken T., Jones J. C. (2005). Intermediate filament associated proteins. Adv. Protein Chem. 70, 143–202 10.1016/S0065-3233(05)70006-1 PubMed DOI

Grigoriev I., Gouveia S. M., van der Vaart B., Demmers J., Smyth J. T., Honnappa S., Splinter D., Steinmetz M. O., Putney J. W., Jr., Hoogenraad C. C., Akhmanova A. (2008). STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18, 177–182 10.1016/j.cub.2007.12.050 PubMed DOI PMC

Guillemot J. C., Montcourrier P., Vivier E., Davoust J., Chavrier P. (1997). Selective control of membrane ruffling and actin plaque assembly by the Rho GTPases Rac1 and CDC42 in FcεRI-activated rat basophilic leukemia (RBL-2H3) cells. J. Cell Sci. 110, 2215–2225 PubMed

Guzman R. E., Bolanos P., Delgado A., Rojas H., DiPolo R., Caputo C., Jaffe E. H. (2007). Depolymerisation and rearrangement of actin filaments during exocytosis in rat peritoneal mast cells: involvement of ryanodine-sensitive calcium stores. Pflugers Arch. 454, 131–141 10.1007/s00424-006-0177-z PubMed DOI

Hájková Z., Bugajev V., Dráberová E., Vinopal S., Dráberová L., Janáček J., Dráber Pe., Dráber P. (2011). STIM1-directed reorganization of microtubules in activated cells. J. Immunol. 186, 913–923 10.4049/jimmunol.1002074 PubMed DOI

Hamawy M. M., Mergenhagen S. E., Siraganian R. P. (1994). Adhesion molecules as regulators of mast-cell and basophil function. Immunol. Today 15, 62–66 10.1016/0167-5699(94)90135-X PubMed DOI

Hamawy M. M., Oliver C., Mergenhagen S. E., Siraganian R. P. (1992). Adherence of rat basophilic leukemia (RBL-2H3) cells to fibronectin-coated surfaces enhances secretion. J. Immunol. 149, 615–621 PubMed

Heasman S. J., Ridley A. J. (2008). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690–701 10.1038/nrm2476 PubMed DOI

Heneberg P., Dráberová L., Bambousková M., Pompach P., Draber P. (2010). Down-regulation of protein-tyrosine phosphatases activates an immune receptor in the absence of its translocation into lipid rafts. J. Biol. Chem. 285, 12787–12802 10.1074/jbc.M109.052555 PubMed DOI PMC

Holowka D., Sheets E. D., Baird B. (2000). Interactions between FcεRI and lipid raft components are regulated by the actin cytoskeleton. J. Cell Sci. 113, 1009–1019 PubMed

Honnappa S., Gouveia S. M., Weisbrich A., Damberger F. F., Bhavesh N. S., Jawhari H., Grigoriev I., van Rijssel F. J., Buey R. M., Lawera A., Jelesarov I., Winkler F. K., Wuthrich K., Akhmanova A., Steinmetz M. O. (2009). An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366–376 10.1016/j.cell.2009.04.065 PubMed DOI

Horny H. P., Reimann O., Kaiserling E. (1988). Immunoreactivity of normal and neoplastic human tissue mast cells. Am. J. Clin. Pathol. 89, 335–340 PubMed

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. (2000). The N-terminal 34 residues of the 55 kDa regulatory subunits of phosphoinositide 3-kinase interact with tubulin. Biochem. J. 346, 483–489 10.1042/0264-6021:3460483 PubMed DOI PMC

Ishizuka T., Okajima F., Ishiwara M., Iizuka K., Ichimonji I., Kawata T., Tsukagoshi H., Dobashi K., Nakazawa T., Mori M. (2001). Sensitized mast cells migrate toward the antigen: a response regulated by p38 mitogen-activated protein kinase and Rho-associated coiled-coil-forming protein kinase. J. Immunol. 167, 2298–2304 PubMed

Izushi K., Fujiwara Y., Tasaka K. (1992). Identification of vimentin in rat peritoneal mast cells and its phosphorylation in association with histamine release. Immunopharmacology 23, 153–161 10.1016/0162-3109(92)90021-4 PubMed DOI

Janke C., Bulinski J. C. (2011). Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12, 773–786 10.1038/nrm3227 PubMed DOI

Jordan M. A., Kamath K. (2007). How do microtubule-targeted drugs work? An overview. Curr. Cancer Drug Targets 7, 730–742 10.2174/156800907783220417 PubMed DOI

Jouvin M. H. E., Adamczewski M., Numerof R., Letourneur O., Valle A., Kinet J. P. (1994). Differential control of the tyrosine kinases Lyn and Syk by the 2 signaling chains of the high-affinity immunoglobulin-e receptor. J. Biol. Chem. 269, 5918–5925 PubMed

Julian M., Tollon Y., Lajoie-Mazenc I., Moisand A., Mazarguil H., Puget A., Wright M. (1993). γ-Tubulin participates in the formation of midbody during cytokinesis in mammalian cells. J. Cell Sci. 105, 145–156 PubMed

Kalesnikoff J., Galli S. J. (2008). New developments in mast cell biology. Nat. Immunol. 9, 1215–1223 10.1038/ni.f.216 PubMed DOI PMC

Kapeller R., Toker A., Cantley L. C., Carpenter C. L. (1995). Phosphoinositide 3-kinase binds constitutively to α/β-tubulin and binds to γ-tubulin in response to insulin. J. Biol. Chem. 270, 25985–25991 10.1074/jbc.270.43.25985 PubMed DOI

Katagiri K., Katagiri T., Kajiyama K., Yamamoto T., Yoshida T. (1993). Tyrosine-phosphorylation of tubulin during monocytic differentiation of HL-60 cells. J. Immunol. 150, 585–593 PubMed

Katsetos C. D., Dráber P. (2012). Tubulins as therapeutic targets in cancer: from bench to bedside. Curr. Pharm. Des. 18, 2778–2792 PubMed

Kettner A., Kumar L., Anton I. M., Sasahara Y., de la F. M., Pivniouk V. I., Falet H., Hartwig J. H., Geha R. S. (2004). WIP regulates signaling via the high affinity receptor for immunoglobulin E in mast cells. J. Exp. Med. 199, 357–368 10.1084/jem.20030652 PubMed DOI PMC

Kim S., Coulombe P. A. (2007). Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21, 1581–1597 10.1101/gad.1552107 PubMed DOI

Kodaki T., Woscholski R., Hallberg B., Rodriguez-Viciana P., Downward J., Parker P. J. (1994). The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol. 4, 798–806 10.1016/S0960-9822(00)00177-9 PubMed DOI

Koffer A., Tatham P. E., Gomperts B. D. (1990). Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J. Cell Biol. 111, 919–927 10.1083/jcb.111.3.919 PubMed DOI PMC

Kreis T., Vale R. (1999). Guidebook to the Cytoskeletal and Motor Proteins. Oxford: Oxford University Press

Kuehn H. S., Jung M. Y., Beaven M. A., Metcalfe D. D., Gilfillan A. M. (2011). Prostaglandin E2 activates and utilizes mTORC2 as a central signaling locus for the regulation of mast cell chemotaxis and mediator release. J. Biol. Chem. 286, 391–402 10.1074/jbc.M110.164772 PubMed DOI PMC

Kuehn H. S., Radinger M., Brown J. M., Ali K., Vanhaesebroeck B., Beaven M. A., Metcalfe D. D., Gilfillan A. M. (2010). Btk-dependent Rac activation and actin rearrangement following FcεRI aggregation promotes enhanced chemotactic responses of mast cells. J. Cell Sci. 123, 2576–2585 10.1242/jcs.071043 PubMed DOI PMC

Kukharskyy V., Sulimenko V., Macurek L., Sulimenko T., Dráberová E., Dráber P. (2004). Complexes of γ-tubulin with non-receptor protein tyrosine kinases Src and Fyn in differentiating P19 embryonal carcinoma cells. Exp. Cell Res. 298, 218–228 10.1016/j.yexcr.2004.04.016 PubMed DOI

Kustermans G., Piette J., Legrand-Poels S. (2008). Actin-targeting natural compounds as tools to study the role of actin cytoskeleton in signal transduction. Biochem. Pharmacol. 76, 1310–1322 10.1016/j.bcp.2008.08.017 PubMed DOI

Lagunoff D., Martin T. W., Read G. (1983). Agents that release histamine from mast cells. Annu. Rev. Pharmacol. Toxicol. 23, 331–351 10.1146/annurev.pa.23.040183.001555 PubMed DOI

Lam V., Kalesnikoff J., Lee C. W., Hernandez-Hansen V., Wilson B. S., Oliver J. M., Krystal G. (2003). IgE alone stimulates mast cell adhesion to fibronectin via pathways similar to those used by IgE+ antigen but distinct from those used by Steel factor. Blood 102, 1405–1413 10.1182/blood-2002-10-3176 PubMed DOI

Lesourne R., Fridman W. H., Daeron M. (2005). Dynamic interactions of Fcγ receptor IIB with filamin-bound SHIP1 amplify filamentous actin-dependent negative regulation of Fcε receptor I signaling. J. Immunol. 174, 1365–1373 PubMed

Ley S. C., Marsh M., Bebbington C. R., Proudfoot K., Jordan P. (1994). Distinct intracellular-localization of Lck and Fyn protein-tyrosine kinases in human T-lymphocytes. J. Cell Biol. 125, 639–649 10.1083/jcb.125.3.639 PubMed DOI PMC

Lin T. C., Gombos L., Neuner A., Sebastian D., Olsen J. V., Hrle A., Benda C., Schiebel E. (2011). Phosphorylation of the yeast γ-tubulin Tub4 regulates microtubule function. PLoS ONE 6, e19700. 10.1371/journal.pone.0014557 PubMed DOI PMC

Linhartová I., Dráber P., Dráberová E., Viklický V. (1992). Immunological discrimination of β-tubulin isoforms in developing mouse brain. Posttranslational modification of non-class III β-tubulins. Biochem. J. 288, 919–924 PubMed PMC

Liou J., Fivaz M., Inoue T., Meyer T. (2007). Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca PubMed DOI PMC

Liou J., Kim M. L., Heo W. D., Jones J. T., Myers J. W., Ferrell J. E., Jr., Meyer T. (2005). STIM is a Ca PubMed DOI PMC

Liu Y., Zhu M., Nishida K., Hirano T., Zhang W. (2007). An essential role for RasGRP1 in mast cell function and IgE-mediated allergic response. J. Exp. Med. 204, 93–103 10.1084/jem.20061440 PubMed DOI PMC

Logue J. S., Whiting J. L., Tunquist B., Sacks D. B., Langeberg L. K., Wordeman L., Scott J. D. (2011). AKAP220 protein organizes signaling elements that impact cell migration. J. Biol. Chem. 286, 39269–39281 10.1074/jbc.M111.277756 PubMed DOI PMC

Lüders J., Patel U. K., Stearns T. (2006). GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin mediated microtubule nucleation. Nat. Cell Biol. 8, 137–147 10.1038/ncb1349 PubMed DOI

Ludowyke R. I., Elgundi Z., Kranenburg T., Stehn J. R., Schmitz-Peiffer C., Hughes W. E., Biden T. J. (2006). Phosphorylation of nonmuscle myosin heavy chain IIA on Ser PubMed

Luduena R. F., Banerjee A. (2008). “The isotypes of tubulin: distribution and functional significance,” in The Role of Microtubules in Cell Biology, Neurobiology and Oncology, ed. Fojo T. (Totowa, NJ: Humana Press; ), 123–175

Lyle K., Kumar P., Wittmann T. (2009a). SnapShot: microtubule regulators I. Cell 136, 380. 10.1016/j.cell.2009.01.010 PubMed DOI PMC

Lyle K., Kumar P., Wittmann T. (2009b). SnapShot: microtubule regulators II. Cell 136, 566. 10.1016/j.cell.2009.01.010 PubMed DOI PMC

Ma H.-T., Beaven A. (2011). “Regulators of Ca

Ma H. T., Beaven M. A. (2009). Regulation of Ca PubMed PMC

Macurek L., Dráberová E., Richterová V., Sulimenko V., Sulimenko T., Dráberová L., Marková V., Dráber P. (2008). Regulation of microtubule nucleation in differentiating embryonal carcinoma cells by complexes of membrane-bound γ-tubulin with Fyn kinase and phosphoinositide 3-kinase. Biochem. J. 416, 421–430 10.1042/BJ20080909 PubMed DOI

Malacombe M., Bader M. F., Gasman S. (2006). Exocytosis in neuroendocrine cells: new tasks for actin. Biochim. Biophys. Acta 1763, 1175–1183 10.1016/j.bbamcr.2006.09.004 PubMed DOI

Marie-Cardine A., Kirchgessner H., Eckerskorn C., Mener S. C., Schraven B. (1995). Human T lymphocyte activation induces tyrosine phosphorylation of α-tubulin and its association with the SH2 domain of the p59 PubMed DOI

Martin-Verdeaux S., Pombo I., Iannascoli B., Roa M., Varin-Blank N., Rivera J., Blank U. (2003). Evidence of a role for Munc18-2 and microtubules in mast cell granule exocytosis. J. Cell Sci. 116, 325–334 10.1242/jcs.00216 PubMed DOI

Meininger C. J., Yano H., Rottapel R., Bernstein A., Zsebo K. M., Zetter B. R. (1992). The c-kit receptor ligand functions as a mast cell chemoattractant. Blood 79, 958–963 PubMed

Mercer J. C., Dehaven W. I., Smyth J. T., Wedel B., Boyles R. R., Bird G. S., Putney J. W., Jr. (2006). Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J. Biol. Chem. 281, 24979–24990 10.1074/jbc.M604589200 PubMed DOI PMC

Mitchison T., Kirschner M. (1984). Dynamic instability of microtubule growth. Nature 312, 237–242 10.1038/312232a0 PubMed DOI

Mullins F. M., Park C. Y., Dolmetsch R. E., Lewis R. S. (2009). STIM1 and calmodulin interact with Orai1 to induce Ca PubMed DOI PMC

Murphy S. M., Preble A. M., Patel U. K., O’Connell K. L., Dias D. P., Moritz M., Agard D., Stults J. T., Stearns T. (2001). GCP5 and GCP6: two new members of the human γ-tubulin complex. Mol. Biol. Cell 12, 3340–3352 PubMed PMC

Nahm D. H., Tkaczyk C., Fukuishi N., Colucci-Guyon E., Gilfillan A. M., Metcalfe D. D. (2003). Identification of Fyn-binding proteins in MC/9 mast cells using mass spectrometry. Biochem. Biophys. Res. Commun. 310, 202–208 10.1016/j.bbrc.2003.08.132 PubMed DOI

Narasimhan V., Holowka D., Baird B. (1990). Microfilaments regulate the rate of exocytosis in rat basophilic leukemia cells. Biochem. Biophys. Res. Commun. 171, 222–229 10.1016/0006-291X(90)91380-B PubMed DOI

Naumanen P., Lappalainen P., Hotulainen P. (2008). Mechanisms of actin stress fibre assembly. J. Microsc. 231, 446–454 10.1111/j.1365-2818.2008.02057.x PubMed DOI

Navara C. S., Vassilev A. O., Tibbles H. E., Marks B., Uckun F. M. (1999). The spleen tyrosine kinase (Syk) is present at the centrosome in cultured B-cells. Blood 94, 9A.

Neisch A. L., Fehon R. G. (2011). Ezrin, Radixin and Moesin: key regulators of membrane-cortex interactions and signaling. Curr. Opin. Cell Biol. 23, 377–382 10.1016/j.ceb.2011.04.011 PubMed DOI PMC

Nielsen E. H., Braun K., Johansen T. (1989). Reorganization of the subplasmalemmal cytoskeleton in association with exocytosis in rat mast cells. Histol. Histopathol. 4, 473–477 PubMed

Nishida K., Yamasaki S., Ito Y., Kabu K., Hattori K., Tezuka T., Nishizumi H., Kitamura D., Goitsuka R., Geha R. S., Yamamoto T., Yagi T., Hirano T. (2005). FcεRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell Biol. 170, 115–126 10.1083/jcb.200501111 PubMed DOI PMC

Nobes C. D., Hall A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53–62 10.1016/0092-8674(95)90370-4 PubMed DOI

Nogales E., Wang H. W. (2006). Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives. Curr. Opin. Struct. Biol. 16, 221–229 10.1016/j.sbi.2006.03.005 PubMed DOI

Nogales E., Wolf S. G., Downing K. H. (1998). Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199–203 10.1038/34465 PubMed DOI

Norman J. C., Price L. S., Ridley A. J., Hall A., Koffer A. (1994). Actin filament organization in activated mast cells is regulated by heterotrimeric and small GTP-binding proteins. J. Cell Biol. 126, 1005–1015 10.1083/jcb.126.4.1005 PubMed DOI PMC

Norman J. C., Price L. S., Ridley A. J., Koffer A. (1996). The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell 7, 1429–1442 PubMed PMC

Nováková M., Dráberová E., Schürmann W., Czihak G., Viklický V., Dráber P. (1996). γ-Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil. Cytoskeleton 33, 38–51 10.1002/(SICI)1097-0169(1996)33:1<38::AID-CM5>3.0.CO;2-E PubMed DOI

Oakley C. E., Oakley B. R. (1989). Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338, 662–664 10.1038/338662a0 PubMed DOI

Oka T., Hori M., Ozaki H. (2005). Microtubule disruption suppresses allergic response through the inhibition of calcium influx in the mast cell degranulation pathway. J. Immunol. 174, 4584–4589 PubMed

Oka T., Hori M., Tanaka A., Matsuda H., Karaki H., Ozaki H. (2004). IgE alone-induced actin assembly modifies calcium signaling and degranulation in RBL-2H3 mast cells. Am. J. Physiol. Cell Physiol. 286, C256–C263 10.1152/ajpcell.00197.2003 PubMed DOI

Oka T., Sato K., Hori M., Ozaki H., Karaki H. (2002). FcεRI cross-linking-induced actin assembly mediates calcium signalling in RBL-2H3 mast cells. Br. J. Pharmacol. 136, 837–846 10.1038/sj.bjp.0704788 PubMed DOI PMC

Palazzo A. F., Cook T. A., Alberts A. S., Gundersen G. G. (2001). mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3, 723–729 10.1038/35087035 PubMed DOI

Parekh A. B., Putney J. W., Jr. (2005). Store-operated calcium channels. Physiol. Rev. 85, 757–810 10.1152/physrev.00057.2003 PubMed DOI

Parravicini V., Gadina M., Kovarova M., Odom S., Gonzalez-Espinosa C., Furumoto Y., Saitoh S., Samelson L. E., O’Shea J. J., Rivera J. (2002). Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3, 741–748 PubMed

Parsons J. T., Horwitz A. R., Schwartz M. A. (2010). Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11, 633–643 10.1038/nrm2957 PubMed DOI PMC

Pendleton A., Koffer A. (2001). Effects of latrunculin reveal requirements for the actin cytoskeleton during secretion from mast cells. Cell Motil. Cytoskeleton 48, 37–51 10.1002/1097-0169(200101)48:1<37::AID-CM4>3.0.CO;2-0 PubMed DOI

Perrin B. J., Ervasti J. M. (2010). The actin gene family: function follows isoform. Cytoskeleton 67, 630–634 10.1002/cm.20475 PubMed DOI PMC

Peters J. D., Furlong M. T., Asai D. J., Harrison M. L., Geahlen R. L. (1996). Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates α-tubulin on tyrosine. J. Biol. Chem. 271, 4755–4762 10.1074/jbc.271.44.27241 PubMed DOI

Pfeiffer J. R., Seagrave J. C., Davis B. H., Deanin G. G., Oliver J. M. (1985). Membrane and cytoskeletal changes associated with IgE-mediated serotonin release from rat basophilic leukemia cells. J. Cell Biol. 101, 2145–2155 10.1083/jcb.101.6.2145 PubMed DOI PMC

Pivniouk V. I., Snapper S. B., Kettner A., Alenius H., Laouini D., Falet H., Hartwig J., Alt F. W., Geha R. S. (2003). Impaired signaling via the high-affinity IgE receptor in Wiskott-Aldrich syndrome protein-deficient mast cells. Int. Immunol. 15, 1431–1440 10.1093/intimm/dxg148 PubMed DOI

Prakriya M., Feske S., Gwack Y., Srikanth S., Rao A., Hogan P. G. (2006). Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230–233 10.1038/nature05122 PubMed DOI

Price L. S., Langeslag M., ten Klooster J. P., Hordijk P. L., Jalink K., Collard J. G. (2003). Calcium signaling regulates translocation and activation of Rac. J. Biol. Chem. 278, 39413–39421 10.1074/jbc.M304519200 PubMed DOI

Price L. S., Norman J. C., Ridley A. J., Koffer A. (1995). The small GTPases Rac and Rho as regulators of secretion in mast cells. Curr. Biol. 5, 68–73 10.1016/S0960-9822(95)00046-7 PubMed DOI

Psatha M., Koffer A., Erent M., Moss S. E., Bolsover S. (2004). Calmodulin spatial dynamics in RBL-2H3 mast cells. Cell Calcium 36, 51–59 10.1016/j.ceca.2003.11.009 PubMed DOI

Psatha M. I., Razi M., Koffer A., Moss S. E., Sacks D. B., Bolsover S. R. (2007). Targeting of calcium:calmodulin signals to the cytoskeleton by IQGAP1. Cell Calcium 41, 593–605 10.1016/j.ceca.2006.10.009 PubMed DOI

Ramesh N., Geha R. (2009). Recent advances in the biology of WASP and WIP. Immunol. Res. 44, 99–111 10.1007/s12026-008-8086-1 PubMed DOI

Ridley A. J., Hall A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389–399 10.1016/0092-8674(92)90164-8 PubMed DOI

Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., Hall A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401–410 10.1016/0092-8674(92)90164-8 PubMed DOI

Rivera J., Fierro N. A., Olivera A., Suzuki R. (2008). New insights on mast cell activation via the high affinity receptor for IgE. Adv. Immunol. 98, 85–120 10.1016/S0065-2776(08)00403-3 PubMed DOI PMC

Robbens J., Louahed J., De Pestel K., Van Colen I., Ampe C., Vandekerckhove J., Renauld J. C. (1998). Murine adseverin (D5), a novel member of the gelsolin family, and murine adseverin are induced by interleukin-9 in T-helper lymphocytes. Mol. Cell Biol. 18, 4589–4596 PubMed PMC

Roos J., DiGregorio P. J., Yeromin A. V., Ohlsen K., Lioudyno M., Zhang S., Safrina O., Kozak J. A., Wagner S. L., Cahalan M. D., Velicelebi G., Stauderman K. A. (2005). STIM1, an essential and conserved component of store-operated Ca PubMed DOI PMC

Sampieri A., Zepeda A., Asanov A., Vaca L. (2009). Visualizing the store-operated channel complex assembly in real time: identification of SERCA2 as a new member. Cell Calcium 45, 439–446 10.1016/j.ceca.2009.02.010 PubMed DOI

Schwartz M. A., Schaller M. D., Ginsberg M. H. (1995). Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11, 549–599 10.1146/annurev.cb.11.110195.003001 PubMed DOI

Sells M. A., Pfaff A., Chernoff J. (2000). Temporal and spatial distribution of activated Pak1 in fibroblasts. J. Cell Biol. 151, 1449–1458 10.1083/jcb.151.7.1449 PubMed DOI PMC

Shimizu T., Owsianik G., Freichel M., Flockerzi V., Nilius B., Vennekens R. (2009). TRPM4 regulates migration of mast cells in mice. Cell Calcium 45, 226–232 10.1016/j.ceca.2008.10.005 PubMed DOI

Simon J. R., Graff R. D., Maness P. F. (1998). Microtubule dynamics in a cytosolic extract of fetal rat brain. J. Neurocytol. 27, 119–126 10.1023/A:1006999306413 PubMed DOI

Sivalenka R. R., Jessberger R. (2004). SWAP-70 regulates c-kit-induced mast cell activation, cell-cell adhesion, and migration. Mol. Cell Biol. 24, 10277–10288 10.1128/MCB.24.23.10277-10288.2004 PubMed DOI PMC

Smith A. J., Pfeiffer J. R., Zhang J., Martinez A. M., Griffiths G. M., Wilson B. S. (2003). Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic 4, 302–312 10.1034/j.1600-0854.2003.00084.x PubMed DOI

Smyth J. T., Dehaven W. I., Bird G. S., Putney J. W., Jr. (2007). Role of the microtubule cytoskeleton in the function of the store-operated Ca PubMed DOI PMC

Smyth J. T., Dehaven W. I., Jones B. F., Mercer J. C., Trebak M., Vazquez G., Putney J. W., Jr. (2006). Emerging perspectives in store-operated Ca PubMed DOI

Spiering D., Hodgson L. (2011). Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh. Migr. 5, 170–180 10.4161/cam.5.2.14403 PubMed DOI PMC

Srikanth S., Jung H. J., Kim K. D., Souda P., Whitelegge J., Gwack Y. (2010). A novel EF-hand protein, CRACR2A, is a cytosolic Ca PubMed DOI PMC

Stearns T., Evans L., Kirschner M. (1991). γ-Tubulin is highly conserved component of the centrosome. Cell 65, 825–836 10.1016/0092-8674(91)90390-K PubMed DOI

Struckhoff A. P., Vitko J. R., Rana M. K., Davis C. T., Foderingham K. E., Liu C. H., Vanhoy-Rhodes L., Elliot S., Zhu Y., Burow M., Worthylake R. A. (2010). Dynamic regulation of ROCK in tumor cells controls CXCR4-driven adhesion events. J. Cell Sci. 123, 401–412 10.1242/jcs.052167 PubMed DOI PMC

Stumpff J., Duncan T., Homola E., Campbell S. D., Su T. T. (2004). Drosophila Wee1 kinase regulates Cdk1 and mitotic entry during embryogenesis. Curr. Biol. 14, 2143–2148 10.1016/j.cub.2004.11.050 PubMed DOI PMC

Sulimenko V., Dráberová E., Sulimenko T., Macurek L., Richterová V., Dráber Pe., Dráber P. (2006). Regulation of microtubule formation in activated mast cells by complexes of γ-tubulin with Fyn and Syk kinases. J. Immunol. 176, 7243–7253 PubMed

Sulimenko V., Sulimenko T., Poznanovic S., Nechiporuk-Zloy V., Böhm J. K., Macurek L., Unger E., Dráber P. (2002). Association of brain γ-tubulins with αβ-tubulin dimers. Biochem. J. 365, 889–895 PubMed PMC

Sullivan R., Burnham M., Torok K., Koffer A. (2000). Calmodulin regulates the disassembly of cortical F-actin in mast cells but is not required for secretion. Cell Calcium 28, 33–46 10.1054/ceca.2000.0127 PubMed DOI

Sullivan R., Price L. S., Koffer A. (1999). Rho controls cortical F-actin disassembly in addition to, but independently of, secretion in mast cells. J. Biol. Chem. 274, 38140–38146 10.1074/jbc.274.53.38140 PubMed DOI

Suzuki R., Liu X., Olivera A., Aguiniga L., Yamashita Y., Blank U., Ambudkar I., Rivera J. (2010). Loss of TRPC1-mediated Ca PubMed DOI PMC

Tasaka K. (1994). Molecular mechanism of histamine release: the role of intermediate filaments and membrane skeletons. J. Physiol. Pharmacol. 45, 479–492 PubMed

Tasaka K., Mio M., Fujisawa K., Aoki I. (1991). Role of microtubules on Ca PubMed DOI

Teshima R., Ikebuchi H., Nakanishi M., Sawada J. (1994). Stimulatory effect of pervanadate on calcium signals and histamine secretion of RBL-2H3 cells. Biochem. J. 302, 867–874 PubMed PMC

Thastrup O., Cullen P. J., Drobak B. K., Hanley M. R., Dawson A. P. (1990). Thapsigargin, a tumor promoter, discharges intracellular Ca PubMed DOI PMC

Tolarová H., Dráberová L., Heneberg P., Dráber P. (2004). Involvement of filamentous actin in setting the threshold for degranulation in mast cells. Eur. J. Immunol. 34, 1627–1636 10.1002/eji.200424991 PubMed DOI

Tumová M., Koffer A., Šimícek M., Dráberová L., Dráber P. (2010). The transmembrane adaptor protein NTAL signals to mast cell cytoskeleton via the small GTPase Rho. Eur. J. Immunol. 40, 3235–3245 10.1002/eji.201040403 PubMed DOI

Urata C., Siraganian R. P. (1985). Pharmacologic modulation of the IgE or Ca PubMed DOI

Verhey K. J., Gaertig J. (2007). The tubulin code. Cell Cycle 6, 2152–2160 10.4161/cc.6.17.4633 PubMed DOI

Vinopal S., černohorská M., Sulimenko V., Sulimenko T., Vosecká V., Flemr M., Dráberová E., Dráber P. (2012). γ-Tubulin 2 nucleates microtubules and is downregulated in mouse early embryogenesis. PLoS ONE 7, e29919. 10.1371/journal.pone.0029919 PubMed DOI PMC

Vogel J., Drapkin B., Oomen J., Beach D., Bloom K., Snyder M. (2001). Phosphorylation of γ-tubulin regulates microtubule organization in budding yeast. Dev. Cell 1, 621–631 10.1016/S1534-5807(01)00073-9 PubMed DOI

Wade R. H. (2009). On and around microtubules: an overview. Mol. Biotechnol. 43, 177–191 10.1007/s12033-009-9193-5 PubMed DOI

Wade R. H., Hyman A. A. (1997). Microtubule structure and dynamics. Curr. Opin. Cell Biol. 9, 12–17 10.1016/S0955-0674(97)80146-9 PubMed DOI

Weller C. L., Collington S. J., Hartnell A., Conroy D. M., Kaise T., Barker J. E., Wilson M. S., Taylor G. W., Jose P. J., Williams T. J. (2007). Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proc. Natl. Acad. Sci. U.S.A. 104, 11712–11717 10.1073/pnas.0701700104 PubMed DOI PMC

Westermann S., Weber K. (2003). Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4, 938–945 10.1038/nrm1260 PubMed DOI

Wilson B. S., Pfeiffer J. R., Oliver J. M. (2000). Observing FcεRI signaling from the inside of the mast cell membrane. J. Cell Biol. 149, 1131–1142 10.1083/jcb.149.5.1131 PubMed DOI PMC

Wise D. O., Krahe R., Oakley B. R. (2000). The γ-tubulin gene family in humans. Genomics 67, 164–170 10.1006/geno.2000.6247 PubMed DOI

Wolff A., Denoulet P., Jeantet C. (1982). High level of tubulin microheterogeneity in the mouse brain. Neurosci. Lett. 31, 323–328 10.1016/0304-3940(82)90041-6 PubMed DOI

Wu M. M., Buchanan J., Luik R. M., Lewis R. S. (2006). Ca PubMed DOI PMC

Yanase Y., Hide I., Mihara S., Shirai Y., Saito N., Nakata Y., Hide M., Sakai N. (2011). A critical role of conventional protein kinase C in morphological changes of rodent mast cells. Immunol. Cell Biol. 89, 149–159 10.1038/icb.2010.67 PubMed DOI

Yang F. C., Kapur R., King A. J., Tao W., Kim C., Borneo J., Breese R., Marshall M., Dinauer M. C., Williams D. A. (2000). Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity 12, 557–568 10.1016/S1074-7613(00)80207-1 PubMed DOI

Regulation of microtubule nucleation in mouse bone marrow-derived mast cells by ARF GTPase-activating protein GIT2