Vinculin arrests motile B cells by stabilizing integrin clustering at the immune synapse

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2742-2751

  De Guinoa, Julia Saez ^a   Barrio, Laura ^a   Carrasco, Yolanda R ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL13 CHEMOKINE; INTEGRIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; PHOSPHATIDYLINOSITOL 4 PHOSPHATE 5 KINASE TYPE I GAMMA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN KINASE SYK; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL MOTILITY; CELLULAR PARAMETERS; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE MIGRATION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PERIPHERAL SUPRAMOLECULAR ACTIVATION CLUSTER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL ADHESION; CHEMOTAXIS, LEUKOCYTE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGICAL SYNAPSES; INTEGRINS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; VINCULIN;

EID: 84883391753     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300684     Document Type: Article

References (55)

1. Cyster, J. G. 2010. B cell follicles and antigen encounters of the third kind. Nat. Immunol. 11: 989-996.
2. Miller, M. J., S. H. Wei, I. Parker, and M. D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296: 1869-1873.
3. Okada, T., M. J. Miller, I. Parker, M. F. Krummel, M. Neighbors, S. B. Hartley, A. O'Garra, M. D. Cahalan, and J. G. Cyster. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3: e150.
4. Bajénoff, M., J. G. Egen, L. Y. Koo, J. P. Laugier, F. Brau, N. Glaichenhaus, and R. N. Germain. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25: 989-1001.
5. Allen, C. D., and J. G. Cyster. 2008. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin. Immunol. 20: 14-25.
6. Carrasco, Y. R., S. J. Fleire, T. Cameron, M. L. Dustin, and F. D. Batista. 2004. LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20: 589-599.
7. Sáez de Guinoa, J., L. Barrio, M. Mellado, and Y. R. Carrasco. 2011. CXCL13/CXCR5 signaling enhances BCR-triggered B-cell activation by shaping cell dynamics. Blood 118: 1560-1569.
8. Fleire, S. J., J. P. Goldman, Y. R. Carrasco, M. Weber, D. Bray, and F. D. Batista. 2006. B cell ligand discrimination through a spreading and contraction response. Science 312: 738-741.
9. Randall, K. L., T. Lambe, A. L. Johnson, B. Treanor, E. Kucharska, H. Domaschenz, B. Whittle, L. E. Tze, A. Enders, T. L. Crockford, et al. 2009. Dock8 mutations cripple B cell immunological synapses, germinal centers and long-lived antibody production. [Published erratum appears in 2010. Nat. Immunol. 11: 644.] Nat. Immunol. 10: 1283-1291.
10. Kinashi, T. 2007. Integrin regulation of lymphocyte trafficking: lessons from structural and signaling studies. Adv. Immunol. 93: 185-227.
11. Batista, F. D., E. Arana, P. Barral, Y. R. Carrasco, D. Depoil, J. Eckl-Dorna, S. Fleire, K. Howe, A. Vehlow, M. Weber, and B. Treanor. 2007. The role of integrins and coreceptors in refining thresholds for B-cell responses. Immunol. Rev. 218: 197-213.
12. Dustin, M. L. 2007. Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr. Opin. Cell Biol. 19: 529-533.
13. Harwood, N. E., and F. D. Batista. 2011. The cytoskeleton coordinates the early events of B-cell activation. Cold Spring Harb. Perspect. Biol. 3: 3.
14. Humphries, J. D., P.Wang, C. Streuli, B. Geiger, M. J. Humphries, and C. Ballestrem. 2007. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179: 1043-1057.
15. Carisey, A., and C. Ballestrem. 2011. Vinculin, an adapter protein in control of cell adhesion signalling. Eur. J. Cell Biol. 90: 157-163.
16. Grashoff, C., B. D. Hoffman, M. D. Brenner, R. Zhou, M. Parsons, M. T. Yang, M. A. McLean, S. G. Sligar, C. S. Chen, T. Ha, and M. A. Schwartz. 2010. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466: 263-266.
17. Carisey, A., R. Tsang, A. M. Greiner, N. Nijenhuis, N. Heath, A. Nazgiewicz, R. Kemkemer, B. Derby, J. Spatz, and C. Ballestrem. 2013. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr. Biol. 23: 271-281.
18. Bakolitsa, C., D. M. Cohen, L. A. Bankston, A. A. Bobkov, G. W. Cadwell, L. Jennings, D. R. Critchley, S. W. Craig, and R. C. Liddington. 2004. Structural basis for vinculin activation at sites of cell adhesion. Nature 430: 583-586.
19. Ling, K., N. J. Schill, M. P.Wagoner, Y. Sun, and R. A. Anderson. 2006. Movin' on up: the role of PtdIns(4,5)P(2) in cell migration. Trends Cell Biol. 16: 276-284.
20. Di Paolo, G., L. Pellegrini, K. Letinic, G. Cestra, R. Zoncu, S. Voronov, S. Chang, J. Guo, M. R. Wenk, and P. De Camilli. 2002. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 420: 85-89.
21. Ling, K., R. L. Doughman, A. J. Firestone, M. W. Bunce, and R. A. Anderson. 2002. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93.
22. Xu, W., H. Baribault, and E. D. Adamson. 1998. Vinculin knockout results in heart and brain defects during embryonic development. Development 125: 327-337.
23. Coll, J. L., A. Ben-Ze'ev, R. M. Ezzell, J. L. Rodríguez Fernández, H. Baribault, R. G. Oshima, and E. D. Adamson. 1995. Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion. Proc. Natl. Acad. Sci. USA 92: 9161-9165.
24. Lifschitz-Mercer, B., B. Czernobilsky, E. Feldberg, and B. Geiger. 1997. Expression of the adherens junction protein vinculin in human basal and squamous cell tumors: relationship to invasiveness and metastatic potential. Hum. Pathol. 28: 1230-1236.
25. Xu, W., J. L. Coll, and E. D. Adamson. 1998. Rescue of the mutant phenotype by reexpression of full-length vinculin in null F9 cells; effects on cell locomotion by domain deleted vinculin. J. Cell Sci. 111: 1535-1544.
26. Rodríguez Fernández, J. L., B. Geiger, D. Salomon, I. Sabanay, M. Zöller, and A. Ben-Ze'ev. 1992. Suppression of tumorigenicity in transformed cells after transfection with vinculin cDNA. J. Cell Biol. 119: 427-438.
27. Lacalle, R. A., R. M. Peregil, J. P. Albar, E. Merino, C. Martínez-A, I. Mérida, and S. Mañes. 2007. Type I phosphatidylinositol 4-phosphate 5-kinase controls neutrophil polarity and directional movement. J. Cell Biol. 179: 1539-1553.
28. Falasca, M., S. K. Logan, V. P. Lehto, G. Baccante, M. A. Lemmon, and J. Schlessinger. 1998. Activation of phospholipase C gamma by PI 3-kinaseinduced PH domain-mediated membrane targeting. EMBO J. 17: 414-422.
29. Shen, K., C. E. Tolbert, C. Guilluy, V. S. Swaminathan, M. E. Berginski, K. Burridge, R. Superfine, and S. L. Campbell. 2011. The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties. J. Biol. Chem. 286: 45103-45115.
30. Riedl, J., A. H. Crevenna, K. Kessenbrock, J. H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T. A. Holak, Z.Werb, et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5: 605-607.
31. Zufferey, R., D. Nagy, R. J. Mandel, L. Naldini, and D. Trono. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15: 871-875.
32. Spaargaren, M., E. A. Beuling, M. L. Rurup, H. P. Meijer, M. D. Klok, S. Middendorp, R. W. Hendriks, and S. T. Pals. 2003. The B cell antigen receptor controls integrin activity through Btk and PLCgamma2. J. Exp. Med. 198: 1539-1550.
33. Pearce, G., T. Audzevich, and R. Jessberger. 2011. SYK regulates B-cell migration by phosphorylation of the F-actin interacting protein SWAP-70. Blood 117: 1574-1584.
34. Pasapera, A. M., I. C. Schneider, E. Rericha, D. D. Schlaepfer, and C.M.Waterman. 2010. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188: 877-890.
35. Nolz, J. C., R. B. Medeiros, J. S. Mitchell, P. Zhu, B. D. Freedman, Y. Shimizu, and D. D. Billadeau. 2007. WAVE2 regulates high-affinity integrin binding by recruiting vinculin and talin to the immunological synapse. Mol. Cell. Biol. 27: 5986-6000.
36. Wernimont, S. A., A. J. Wiemer, D. A. Bennin, S. J. Monkley, T. Ludwig, D. R. Critchley, and A. Huttenlocher. 2011. Contact-dependent T cell activation and T cell stopping require talin1. J. Immunol. 187: 6256-6267.
37. Mace, E. M., J. Zhang, K. A. Siminovitch, and F. Takei. 2010. Elucidation of the integrin LFA-1-mediated signaling pathway of actin polarization in natural killer cells. Blood 116: 1272-1279.
38. Xu, W., P. Wang, B. Petri, Y. Zhang, W. Tang, L. Sun, H. Kress, T. Mann, Y. Shi, P. Kubes, and D. Wu. 2010. Integrin-induced PIP5K1C kinase polarization regulates neutrophil polarization, directionality, and in vivo infiltration. Immunity 33: 340-350.
39. Legate, K. R., S. Takahashi, N. Bonakdar, B. Fabry, D. Boettiger, R. Zent, and R. Fässler. 2011. Integrin adhesion and force coupling are independently regulated by localized PtdIns(4,5)2 synthesis. EMBO J. 30: 4539-4553.
40. Chandrasekar, I., T. E. Stradal, M. R. Holt, F. Entschladen, B. M. Jockusch, and W. H. Ziegler. 2005. Vinculin acts as a sensor in lipid regulation of adhesion-site turnover. J. Cell Sci. 118: 1461-1472.
41. Wernimont, S. A., K. R. Legate, W. T. Simonson, R. Fassler, and A. Huttenlocher. 2010. PIPKI gamma 90 negatively regulates LFA-1-mediated adhesion and activation in antigen-induced CD4+ T cells. J. Immunol. 185: 4714-4723.
42. Sun, Y., R. D. Dandekar, Y. S. Mao, H. L. Yin, and C. Wülfing. 2011. Phosphatidylinositol (4,5) bisphosphate controls T cell activation by regulating T cell rigidity and organization. PLoS ONE 6: e27227.
43. Cai, Y., N. Biais, G. Giannone, M. Tanase, G. Jiang, J. M. Hofman, C. H. Wiggins, P. Silberzan, A. Buguin, B. Ladoux, and M. P. Sheetz. 2006. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives Factin flow. Biophys. J. 91: 3907-3920.
44. van den Dries, K., M. B. Meddens, S. de Keijzer, S. Shekhar, V. Subramaniam, C. G. Figdor, and A. Cambi. 2013. Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat Commun 4: 1412.
45. Jacobelli, J., S. A. Chmura, D. B. Buxton, M. M. Davis, and M. F. Krummel. 2004. A single class II myosin modulates T cell motility and stopping, but not synapse formation. Nat. Immunol. 5: 531-538.
46. Ilani, T., G. Vasiliver-Shamis, S. Vardhana, A. Bretscher, and M. L. Dustin. 2009. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat. Immunol. 10: 531-539.
47. Jacobelli, J., R. S. Friedman, M. A. Conti, A. M. Lennon-Dumenil, M. Piel, C. M. Sorensen, R. S. Adelstein, and M. F. Krummel. 2010. Confinementoptimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nat. Immunol. 11: 953-961.
48. Kumari, S., S. Vardhana, M. Cammer, S. Curado, L. Santos, M. P. Sheetz, and M. L. Dustin. 2012. T Lymphocyte Myosin IIA is Required for Maturation of the Immunological Synapse. Front Immunol 3: 230.
49. Yu, Y., N. C. Fay, A. A. Smoligovets, H. J. Wu, and J. T. Groves. 2012. Myosin IIA modulates T cell receptor transport and CasL phosphorylation during early immunological synapse formation. PLoS ONE 7: e30704.
50. Depoil, D., S. Fleire, B. L. Treanor, M. Weber, N. E. Harwood, K. L. Marchbank, V. L. Tybulewicz, and F. D. Batista. 2008. CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nat. Immunol. 9: 63-72.
51. Yokosuka, T., K. Sakata-Sogawa, W. Kobayashi, M. Hiroshima, A. Hashimoto-Tane, M. Tokunaga, M. L. Dustin, and T. Saito. 2005. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6: 1253-1262.
52. Varma, R., G. Campi, T. Yokosuka, T. Saito, and M. L. Dustin. 2006. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25: 117-127.
53. Cemerski, S., J. Das, E. Giurisato, M. A. Markiewicz, P. M. Allen, A. K. Chakraborty, and A. S. Shaw. 2008. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 29: 414-422.
54. Le Roux, D., D. Lankar, M. I. Yuseff, F. Vascotto, T. Yokozeki, G. Faure-André, E. Mougneau, N. Glaichenhaus, B. Manoury, C. Bonnerot, and A. M. Lennon-Duménil. 2007. Syk-dependent actin dynamics regulate endocytic trafficking and processing of antigens internalized through the B-cell receptor. Mol. Biol. Cell 18: 3451-3462.
55. Saito, K., K. F. Tolias, A. Saci, H. B. Koon, L. A. Humphries, A. Scharenberg, D. J. Rawlings, J. P. Kinet, and C. L. Carpenter. 2003. BTK regulates PtdIns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity 19: 669-678.