Rho GTPases: Masters of T lymphocyte migration and activation

Immunology Letters

Volumn 142, Issue 1-2, 2012, Pages 1-13

  Rougerie, Pablo ^a   Delon, Jérôme ^a  

^a INSTITUT COCHIN   (France)

Author keywords

Activation; Adhesion; Migration; Morphological polarization; Rho GTPases; Signalling; T cell

Indexed keywords

INTEGRIN; PROTEIN CDC42; RAC1 PROTEIN; RAC2 PROTEIN; RAP1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; ANTIGEN RECOGNITION; CALCIUM TRANSPORT; CELL ADHESION; CELL POLARITY; CELLULAR DISTRIBUTION; HUMAN; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; LYMPHOCYTE STRUCTURE; MICROTUBULE ORGANIZING CENTER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

CELL MOVEMENT; LYMPHOCYTE ACTIVATION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84857192289     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2011.12.003     Document Type: Review

References (122)

1. Stekel D.J., Parker C.E., Nowak M.A. A model of lymphocyte recirculation. Immunol Today 1997, 18:216-221.
2. Wennerberg K., Der C.J. Rho-family GTPases: it's not only Rac and Rho (and I like it). J Cell Sci 2004, 117:1301-1312.
3. Tybulewicz V.L.J., Henderson R.B. Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 2009, 9:630-644.
4. Aspenström P., Ruusala A., Pacholsky D. Taking Rho GTPases to the next level: the cellular functions of atypical Rho GTPases. Exp Cell Res 2007, 313:3673-3679.
5. DerMardirossian C., Bokoch G.M. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 2005, 15:356-363.
6. Bokoch G.M., Bohl B.P., Chuang T.H. Guanine nucleotide exchange regulates membrane translocation of Rac/Rho GTP-binding proteins. J Biol Chem 1994, 269:31674-31679.
7. Fleming I.N., Elliott C.M., Exton J.H. Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor. J Biol Chem 1996, 271:33067-33073.
8. Aoki H., Izumo S., Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ Res 1998, 82:666-676.
9. Putnam A.J., Cunningham J.J., Pillemer B.B.L., Mooney D.J. External mechanical strain regulates membrane targeting of Rho GTPases by controlling microtubule assembly. Am J Physiol Cell Physiol 2003, 284:C627-C639.
10. Birukova A.A., Smurova K., Birukov K.G., Kaibuchi K., Garcia J.G.N., Verin A.D. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 2004, 67:64-77.
11. Chaigne-Delalande B., Deuve L., Reuzeau E., Basoni C., Lafarge D., Varon C., et al. RhoGTPases and p53 are involved in the morphological appearance and interferon-α response of hairy cells. Am J Pathol 2006, 168:562-573.
12. Yonemura S., Hirao-Minakuchi K., Nishimura Y. Rho localization in cells and tissues. Exp Cell Res 2004, 295:300-314.
13. Allal C., Favre G., Couderc B., Salicio S., Sixou S., Hamilton A.D., et al. RhoA prenylation is required for promotion of cell growth and transformation and cytoskeleton organization but not for induction of serum response element transcription. J Biol Chem 2000, 275:31001-31008.
14. Michaelson D., Silletti J., Murphy G., D'Eustachio P., Rush M., Philips M.R. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 2001, 152:111-126.
15. Williams C.L. The polybasic region of Ras and Rho family small GTPases: a regulator of protein interactions and membrane association and a site of nuclear localization signal sequences. Cell Signal 2003, 15:1071-1080.
16. Zaoui K., Honoré S., Isnardon D., Braguer D., Badache A. Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol 2008, 183:401-408.
17. Valderrama F., Cordeiro J.V., Schleich S., Frischknecht F., Way M. Vaccinia virus-induced cell motility requires F11L-mediated inhibition of RhoA signaling. Science 2006, 311:377-381.
18. Allen W.E., Jones G.E., Pollard J.W., Ridley A.J. Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J Cell Sci 1997, 110(Pt 6):707-720.
19. Wells C.M., Walmsley M., Ooi S., Tybulewicz V., Ridley A.J. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci 2004, 117:1259-1268.
20. Bokoch G.M., Zhao T. Regulation of the phagocyte NADPH oxidase by Rac GTPase. Antioxid Redox Signal 2006, 8:1533-1548.
21. Posern G., Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 2006, 16:588-596.
22. Ren X.D., Kiosses W.B., Schwartz M.A. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 1999, 18:578-585.
23. Benard V., Bohl B.P., Bokoch G.M. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J Biol Chem 1999, 274:13198-13204.
24. Pertz O., Hahn K.M. Designing biosensors for Rho family proteins-deciphering the dynamics of Rho family GTPase activation in living cells. J Cell Sci 2004, 117:1313-1318.
25. Nakamura T., Kurokawa K., Kiyokawa E., Matsuda M. Analysis of the spatiotemporal activation of rho GTPases using Raichu probes. Meth Enzymol 2006, 406:315-332.
26. Pertz O., Hodgson L., Klemke R.L., Hahn K.M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006, 440:1069-1072.
27. Machacek M., Hodgson L., Welch C., Elliott H., Pertz O., Nalbant P., et al. Coordination of Rho GTPase activities during cell protrusion. Nature 2009, 461:99-103.
28. Li X., Bu X., Lu B., Avraham H., Flavell R.A., Lim B. The hematopoiesis-specific GTP-binding protein RhoH is GTPase deficient and modulates activities of other Rho GTPases by an inhibitory function. Mol Cell Biol 2002, 22:1158-1171.
29. Cherry L.K., Li X., Schwab P., Lim B., Klickstein L.B. RhoH is required to maintain the integrin LFA-1 in a nonadhesive state on lymphocytes. Nat Immunol 2004, 5:961-967.
30. Dorn T., Kuhn U., Bungartz G., Stiller S., Bauer M., Ellwart J., et al. RhoH is important for positive thymocyte selection and T-cell receptor signaling. Blood 2007, 109:2346-2355.
31. Bolomini-Vittori M., Montresor A., Giagulli C., Staunton D., Rossi B., Martinello M., et al. Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat Immunol 2009, 10:185-194.
32. Katagiri K., Hattori M., Minato N., Irie S.k., Takatsu K., Kinashi T. Rap1 is a potent activation signal for leukocyte function-associated antigen 1 distinct from protein kinase C and phosphatidylinositol-3-OH kinase. Mol Cell Biol 2000, 20:1956-1969.
33. Shimonaka M., Katagiri K., Nakayama T., Fujita N., Tsuruo T., Yoshie O., et al. Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J Cell Biol 2003, 161:417-427.
34. Ghandour H., Cullere X., Alvarez A., Luscinskas F.W., Mayadas T.N. Essential role for Rap1 GTPase and its guanine exchange factor CalDAG-GEFI in LFA-1 but not VLA-4 integrin mediated human T-cell adhesion. Blood 2007, 110:3682-3690.
35. Katagiri K., Maeda A., Shimonaka M., Kinashi T. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat Immunol 2003, 4:741-748.
36. Katagiri K., Ohnishi N., Kabashima K., Iyoda T., Takeda N., Shinkai Y., et al. Crucial functions of the Rap1 effector molecule RAPL in lymphocyte and dendritic cell trafficking. Nat Immunol 2004, 5:1045-1051.
37. D'Souza-Schorey C., Boettner B., Van Aelst L. Rac regulates integrin-mediated spreading and increased adhesion of T lymphocytes. Mol Cell Biol 1998, 18:3936-3946.
38. 1. Mol Biol Cell 2005, 16:3223-3235.
39. Vielkind S., Gallagher-Gambarelli M., Gomez M., Hinton H.J., Cantrell D.A. Integrin regulation by RhoA in thymocytes. J Immunol 2005, 175:350-357.
40. Faroudi M., Hons M., Zachacz A., Dumont C., Lyck R., Stein J.V., et al. Critical roles for Rac GTPases in T-cell migration to and within lymph nodes. Blood 2010, 116:5536-5547.
41. 1. J Immunol 2006, 177:5215-5225.
42. Nombela-Arrieta C., Lacalle R.A., Montoya M.C., Kunisaki Y., Megías D., Marqués M., et al. Differential requirements for DOCK2 and phosphoinositide-3-kinase γ during T and B lymphocyte homing. Immunity 2004, 21:429-441.
43. Giagulli C., Scarpini E., Ottoboni L., Narumiya S., Butcher E.C., Constantin G., et al. RhoA and ζ PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity 2004, 20:25-35.
44. Pasvolsky R., Grabovsky V., Giagulli C., Shulman Z., Shamri R., Feigelson S.W., et al. RhoA is involved in LFA-1 extension triggered by CXCL12 but not in a novel outside-in LFA-1 activation facilitated by CXCL9. J Immunol 2008, 180:2815-2823.
45. Laudanna C., Campbell J.J., Butcher E.C. Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 1996, 271:981-983.
46. Ebisuno Y., Katagiri K., Katakai T., Ueda Y., Nemoto T., Inada H., et al. Rap1 controls lymphocyte adhesion cascade and interstitial migration within lymph nodes in RAPL-dependent and -independent manners. Blood 2010, 115:804-814.
47. Real E., Faure S., Donnadieu E., Delon J. Cutting edge: atypical PKCs regulate T lymphocyte polarity and scanning behavior. J Immunol 2007, 179:5649-5652.
48. Krummel M.F., Macara I. Maintenance and modulation of T cell polarity. Nat Immunol 2006, 7:1143-1149.
49. Lee J.-H., Katakai T., Hara T., Gonda H., Sugai M., Shimizu A. Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation. J Cell Biol 2004, 167:327-337.
50. Takesono A., Heasman S.J., Wojciak-Stothard B., Garg R., Ridley A.J. Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells. PLoS ONE 2010, 5:e8774.
51. Smith A., Bracke M., Leitinger B., Porter J.C., Hogg N. LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J Cell Sci 2003, 116:3123-3133.
52. Renkawitz J., Schumann K., Weber M., Lämmermann T., Pflicke H., Piel M., et al. Adaptive force transmission in amoeboid cell migration. Nat Cell Biol 2009, 11:1438-1443.
53. Campello S., Lacalle R.A., Bettella M., Mañes S., Scorrano L., Viola A. Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J Exp Med 2006, 203:2879-2886.
54. Heasman S.J., Carlin L.M., Cox S., Ng T., Ridley A.J. Coordinated RhoA signaling at the leading edge and uropod is required for T cell transendothelial migration. J Cell Biol 2010, 190:553-563.
55. Iden S., Collard J.G. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 2008, 9:846-859.
56. Ludford-Menting M.J., Oliaro J., Sacirbegovic F., Cheah E.T.-Y., Pedersen N., Thomas S.J., et al. A network of PDZ-containing proteins regulates T cell polarity and morphology during migration and immunological synapse formation. Immunity 2005, 22:737-748.
57. Gérard A., Mertens A.E.E., van der Kammen R.A., Collard J.G. The Par polarity complex regulates Rap1- and chemokine-induced T cell polarization. J Cell Biol 2007, 176:863-875.
58. Gérard A., van der Kammen R.A., Janssen H., Ellenbroek S.I., Collard J.G. The Rac activator Tiam1 controls efficient T-cell trafficking and route of transendothelial migration. Blood 2009, 113:6138-6147.
59. Lämmermann T., Renkawitz J., Wu X., Hirsch K., Brakebusch C., Sixt M. Cdc42-dependent leading edge coordination is essential for interstitial dendritic cell migration. Blood 2009, 113:5703-5710.
60. Srinivasan S., Wang F., Glavas S., Ott A., Hofmann F., Aktories K., et al. Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. J Cell Biol 2003, 160:375-385.
61. Li Z., Hannigan M., Mo Z., Liu B., Lu W., Wu Y., et al. Directional sensing requires Gβγ- mediated PAK1 and PIX α-dependent activation of Cdc42. Cell 2003, 114:215-227.
62. Li Z., Dong X., Dong X., Wang Z., Liu W., Deng N., et al. Regulation of PTEN by Rho small GTPases. Nat Cell Biol 2005, 7:399-404.
63. Asperti-Boursin F., Real E., Bismuth G., Trautmann A., Donnadieu E. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase-independent manner. J Exp Med 2007, 204:1167-1179.
64. Ratner S., Piechocki M.P., Galy A. Role of Rho-family GTPase Cdc42 in polarized expression of lymphocyte appendages. J Leukoc Biol 2003, 73:830-840.
65. Friedl P., Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol 2010, 188:11-19.
66. Renkawitz J., Sixt M. Mechanisms of force generation and force transmission during interstitial leukocyte migration. EMBO Rep 2010, 11:744-750.
67. Fukui Y., Hashimoto O., Sanui T., Oono T., Koga H., Abe M., et al. Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 2001, 412:826-831.
68. Nombela-Arrieta C., Mempel T.R., Soriano S.F., Mazo I., Wymann M.P., Hirsch E., et al. A central role for DOCK2 during interstitial lymphocyte motility and sphingosine-1-phosphate-mediated egress. J Exp Med 2007, 204:497-510.
69. Shulman Z., Pasvolsky R., Woolf E., Grabovsky V., Feigelson S.W., Erez N., et al. DOCK2 regulates chemokine-triggered lateral lymphocyte motility but not transendothelial migration. Blood 2006, 108:2150-2158.
70. Vicente-Manzanares M., Cruz-Adalia A., Martín-Cófreces N.B., Cabrero J.R., Dosil M., Alvarado-Sánchez B., et al. Control of lymphocyte shape and the chemotactic response by the GTP exchange factor Vav. Blood 2005, 105:3026-3034.
71. Wallar B.J., Alberts A.S. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol 2003, 13:435-446.
72. Watanabe N., Madaule P., Reid T., Ishizaki T., Watanabe G., Kakizuka A., et al. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 1997, 16:3044-3056.
73. Eisenmann K.M., West R.A., Hildebrand D., Kitchen S.M., Peng J., Sigler R., et al. T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice. J Biol Chem 2007, 282:25152-25158.
74. Sakata D., Taniguchi H., Yasuda S., Adachi-Morishima A., Hamazaki Y., Nakayama R., et al. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J Exp Med 2007, 204:2031-2038.
75. Jacobelli J., Chmura S.A., Buxton D.B., Davis M.M., Krummel M.F. A single class II myosin modulates T cell motility and stopping, but not synapse formation. Nat Immunol 2004, 5:531-538.
76. Morin N.A., Oakes P.W., Hyun Y.-M., Lee D., Chin Y.E., Chin E.Y., et al. Nonmuscle myosin heavy chain IIA mediates integrin LFA-1 de-adhesion during T lymphocyte migration. J Exp Med 2008, 205:195-205.
77. Sun C.X., Downey G.P., Zhu F., Koh A.L.Y., Thang H., Glogauer M. Rac1 is the small GTPase responsible for regulating the neutrophil chemotaxis compass. Blood 2004, 104:3758-3765.
78. Shulman Z., Shinder V., Klein E., Grabovsky V., Yeger O., Geron E., et al. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 2009, 30:384-396.
79. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
80. Weber K.S., Klickstein L.B., Weber P.C., Weber C. Chemokine-induced monocyte transmigration requires cdc42-mediated cytoskeletal changes. Eur J Immunol 1998, 28:2245-2251.
81. Worthylake R.A., Lemoine S., Watson J.M., Burridge K. RhoA is required for monocyte tail retraction during transendothelial migration. J Cell Biol 2001, 154:147-160.
82. Bajénoff M., Egen J.G., Koo L.Y., Laugier J.P., Brau F., Glaichenhaus N., et al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 2006, 25:989-1001.
83. Woolf E., Grigorova I., Sagiv A., Grabovsky V., Feigelson S.W., Shulman Z., et al. Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat Immunol 2007, 8:1076-1085.
84. Boscacci R.T., Pfeiffer F., Gollmer K., Sevilla A.I.C., Martin A.M., Soriano S.F., et al. Comprehensive analysis of lymph node stroma-expressed Ig superfamily members reveals redundant and nonredundant roles for ICAM-1, ICAM-2, and VCAM-1 in lymphocyte homing. Blood 2010, 116:915-925.
85. Lämmermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Söldner R., Hirsch K., et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453:51-55.
86. Mempel T.R., Henrickson S.E., Von Andrian U.H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004, 427:154-159.
87. Dustin M.L. Hunter to gatherer and back: immunological synapses and kinapses as variations on the theme of amoeboid locomotion. Annu Rev Cell Dev Biol 2008, 24:577-596.
88. Sims T.N., Soos T.J., Xenias H.S., Dubin-Thaler B., Hofman J.M., Waite J.C., et al. Opposing effects of PKCθ and WASp on symmetry breaking and relocation of the immunological synapse. Cell 2007, 129:773-785.
89. Stoll S., Delon J., Brotz T.M., Germain R.N. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 2002, 296:1873-1876.
90. Singleton K.L., Roybal K.T., Sun Y., Fu G., Gascoigne N.R.J., van Oers N.S.C., et al. Spatiotemporal patterning during T cell activation is highly diverse. Sci Signal 2009, 2:ra15.
91. Sanui T., Inayoshi A., Noda M., Iwata E., Oike M., Sasazuki T., et al. DOCK2 is essential for antigen-induced translocation of TCR and lipid rafts, but not PKC-θ and LFA-1, in T cells. Immunity 2003, 19:119-129.
92. Sanui T., Inayoshi A., Noda M., Iwata E., Stein J.V., Sasazuki T., et al. DOCK2 regulates Rac activation and cytoskeletal reorganization through interaction with ELMO1. Blood 2003, 102:2948-2950.
93. Saveliev A., Vanes L., Ksionda O., Rapley J., Smerdon S.J., Rittinger K., et al. Function of the nucleotide exchange activity of vav1 in T cell development and activation. Sci Signal 2009, 2:ra83.
94. Ku G.M., Yablonski D., Manser E., Lim L., Weiss A. A PAK1-PIX-PKL complex is activated by the T-cell receptor independent of Nck, Slp-76 and LAT. EMBO J 2001, 20:457-465.
95. Missy K., Hu B., Schilling K., Harenberg A., Sakk V., Kuchenbecker K., et al. αPIX Rho GTPase guanine nucleotide exchange factor regulates lymphocyte functions and antigen receptor signaling. Mol Cell Biol 2008, 28:3776-3789.
96. Bécart S., Balancio A.J.C., Charvet C., Feau S., Sedwick C.E., Altman A. Tyrosine-phosphorylation-dependent translocation of the SLAT protein to the immunological synapse is required for NFAT transcription factor activation. Immunity 2008, 29:704-719.
97. Martínez-Martín N., Fernández-Arenas E., Cemerski S., Delgado P., Turner M., Heuser J., et al. T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 2011, 35:208-222.
98. Oh-hora M. Calcium signaling in the development and function of T-lineage cells. Immunol Rev 2009, 231:210-224.
99. Arrieumerlou C., Randriamampita C., Bismuth G., Trautmann A. Rac is involved in early TCR signaling. J Immunol 2000, 165:3182-3189.
100. Yu H., Leitenberg D., Li B., Flavell R.A. Deficiency of small GTPase Rac2 affects T cell activation. J Exp Med 2001, 194:915-926.
101. Nolz J.C., Gomez T.S., Zhu P., Li S., Medeiros R.B., Shimizu Y., et al. The WAVE2 complex regulates actin cytoskeletal reorganization and CRAC-mediated calcium entry during T cell activation. Curr Biol 2006, 16:24-34.
102. Bécart S., Charvet C., Canonigo Balancio A.J., De Trez C., Tanaka Y., Duan W., et al. SLAT regulates Th1 and Th2 inflammatory responses by controlling Ca2+/NFAT signaling. J Clin Invest 2007, 117:2164-2175.
103. 2+ signaling in T cells. Immunol Rev 2009, 232:319-333.
104. Stowers L., Yelon D., Berg L.J., Chant J. Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc Natl Acad Sci USA 1995, 92:5027-5031.
105. Bertrand F., Esquerré M., Petit A.-E., Rodrigues M., Duchez S., Delon J., et al. Activation of the ancestral polarity regulator protein kinase C ζ at the immunological synapse drives polarization of Th cell secretory machinery toward APCs. J Immunol 2010, 185:2887-2894.
106. Tourret M., Guégan S., Chemin K., Dogniaux S., Miro F., Bohineust A., et al. T cell polarity at the immunological synapse is required for CD154-dependent IL-12 secretion by dendritic cells. J Immunol 2010, 185:6809-6818.
107. Pulecio J., Petrovic J., Prete F., Chiaruttini G., Lennon-Dumenil A.-M., Desdouets C., et al. Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse. J Exp Med 2010, 207:2719-2732.
108. Sinai P., Nguyen C., Schatzle J.D., Wülfing C. Transience in polarization of cytolytic effectors is required for efficient killing and controlled by Cdc42. Proc Natl Acad Sci USA 2010, 107:11912-11917.
109. Gomez T.S., Kumar K., Medeiros R.B., Shimizu Y., Leibson P.J., Billadeau D.D. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 2007, 26:177-190.
110. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
111. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
112. Valitutti S., Dessing M., Aktories K., Gallati H., Lanzavecchia A. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J Exp Med 1995, 181:577-584.
113. + T cells: compulsory cytoskeletal alterations for the triggering of an intracellular calcium response. Eur J Immunol 1998, 28:716-729.
114. Burkhardt J.K., Carrizosa E., Shaffer M.H. The actin cytoskeleton in T cell activation. Annu Rev Immunol 2008, 26:233-259.
115. Cannon J.L., Burkhardt J.K. Differential roles for Wiskott-Aldrich syndrome protein in immune synapse formation and IL-2 production. J Immunol 2004, 173:1658-1662.
116. Zipfel P.A., Bunnell S.C., Witherow D.S., Gu J.J., Chislock E.M., Ring C., et al. Role for the Abi/wave protein complex in T cell receptor-mediated proliferation and cytoskeletal remodeling. Curr Biol 2006, 16:35-46.
117. Takahashi K., Sasaki T., Mammoto A., Takaishi K., Kameyama T., Tsukita S., et al. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 1997, 272:23371-23375.
118. Henning S.W., Galandrini R., Hall A., Cantrell D.A. The GTPase Rho has a critical regulatory role in thymus development. EMBO J 1997, 16:2397-2407.
119. Corre I., Gomez M., Vielkind S., Cantrell D.A. Analysis of thymocyte development reveals that the GTPase RhoA is a positive regulator of T cell receptor responses in vivo. J Exp Med 2001, 194:903-914.
120. Mullin M., Lightfoot K., Clarke R., Miller M., Lahesmaa R., Cantrell D. The RhoA transcriptional program in pre-T cells. FEBS Lett 2007, 581:4309-4317.
121. Gomez M., Tybulewicz V., Cantrell D.A. Control of pre-T cell proliferation and differentiation by the GTPase Rac-I. Nat Immunol 2000, 1:348-352.
122. Gomez M., Kioussis D., Cantrell D.A. The GTPase Rac-1 controls cell fate in the thymus by diverting thymocytes from positive to negative selection. Immunity 2001, 15:703-713.