Cofilin-mediated F-actin severing is regulated by the Rap GTPase and controls the cytoskeletal dynamics that drive lymphocyte spreading and BCR microcluster formation

Journal of Immunology

Volumn 187, Issue 11, 2011, Pages 5887-5900

  Freeman, Spencer A ^a   Lei, Victor ^a   Dang Lawson, May ^a   Mizuno, Kensaku ^b   Roskelley, Calvin D ^a   Gold, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; COFILIN; F ACTIN; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; RAP PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CELL INTERACTION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; F ACTIN SEVERING; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; ANTIGEN PRESENTATION; B-LYMPHOCYTES; CHEMOTAXIS, LEUKOCYTE; CYTOSKELETON; DENDRITIC CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GTP PHOSPHOHYDROLASES; IMMUNOBLOTTING; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MULTIGENE FAMILY; RECEPTORS, ANTIGEN, B-CELL; T-LYMPHOCYTES; TRANSFECTION;

EID: 82755189245     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102233     Document Type: Article

References (39)

1. Batista, F. D., and N. E. Harwood. 2009. The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 9: 15-27.
2. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285: 221-227. (Pubitemid 29329988)
3. 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.
4. 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. (Pubitemid 350286205)
5. Campi, G., R. Varma, and M. L. Dustin. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202: 1031-1036.
6. Lee, K. H., A. R. Dinner, C. Tu, G. Campi, S. Raychaudhuri, R. Varma, T. N. Sims, W. R. Burack, H. Wu, J. Wang, et al. 2003. The immunological synapse balances T cell receptor signaling and degradation. Science 302: 1218-1222. (Pubitemid 37421028)
7. 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. (Pubitemid 44066825)
8. Harwood, N. E., and F. D. Batista. 2009. Visualizing the molecular and cellular events underlying the initiation of B-cell activation. Curr. Top. Microbiol. Immunol. 334: 153-177.
9. Batista, F. D., B. Treanor, and N. E. Harwood. 2010. Visualizing a role for the actin cytoskeleton in the regulation of B-cell activation. Immunol. Rev. 237: 191-204.
10. Lin, K. B., S. A. Freeman, S. Zabetian, H. Brugger, M. Weber, V. Lei, M. Dang- Lawson, K. W. Tse, R. Santamaria, F. D. Batista, and M. R. Gold. 2008. The Rap GTPases regulate B cell morphology, immune-synapse formation, and signaling by particulate B cell receptor ligands. Immunity 28: 75-87.
11. Arana, E., A. Vehlow, N. E. Harwood, E. Vigorito, R. Henderson, M. Turner, V. L. Tybulewicz, and F. D. Batista. 2008. Activation of the small GTPase Rac2 via the B cell receptor regulates B cell adhesion and immunological-synapse formation. Immunity 28: 88-99.
12. Bos, J. L. 2005. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 17: 123-128. (Pubitemid 40380934)
13. Hao, S., and A. August. 2005. Actin depolymerization transduces the strength of B-cell receptor stimulation. Mol. Biol. Cell 16: 2275-2284. (Pubitemid 40632211)
14. Ichetovkin, I., W. Grant, and J. Condeelis. 2002. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12: 79-84. (Pubitemid 34063358)
15. Treanor, B., and F. D. Batista. 2010. Organisation and dynamics of antigen receptors: implications for lymphocyte signalling. Curr. Opin. Immunol. 22: 299-307.
16. Treanor, B., D. Depoil, A. Gonzalez-Granja, P. Barral, M. Weber, O. Dushek, A. Bruckbauer, and F. D. Batista. 2010. The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 32: 187-199.
17. Gupta, N., B. Wollscheid, J. D. Watts, B. Scheer, R. Aebersold, and A. L. DeFranco. 2006. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat. Immunol. 7: 625-633. (Pubitemid 43797344)
18. Bretscher, A., K. Edwards, and R. G. Fehon. 2002. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3: 586-599.
19. Treanor, B., D. Depoil, A. Bruckbauer, and F. D. Batista. 2011. Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J. Exp. Med. 208: 1055-1068.
20. Eibert, S. M., K. H. Lee, R. Pipkorn, U. Sester, G. H. Wabnitz, T. Giese, S. C. Meuer, and Y. Samstag. 2004. Cofilin peptide homologs interfere with immunological synapse formation and T cell activation. Proc. Natl. Acad. Sci. USA 101: 1957-1962. (Pubitemid 38228997)
21. McLeod, S. J., A. J. Shum, R. L. Lee, F. Takei, and M. R. Gold. 2004. The Rap GTPases regulate integrin-mediated adhesion, cell spreading, actin polymerization, and Pyk2 tyrosine phosphorylation in B lymphocytes. J. Biol. Chem. 279: 12009-12019. (Pubitemid 38445762)
22. Lankar, D., H. Vincent-Schneider, V. Briken, T. Yokozeki, G. Raposo, and C. Bonnerot. 2002. Dynamics of major histocompatibility complex class II compartments during B cell receptor-mediated cell activation. J. Exp. Med. 195: 461-472. (Pubitemid 34461299)
23. Burkel, B. M., G. von Dassow, and W. M. Bement. 2007. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton 64: 822-832. (Pubitemid 350035031)
24. Nishita, M., C. Tomizawa, M. Yamamoto, Y. Horita, K. Ohashi, and K. Mizuno. 2005. Spatial and temporal regulation of cofilin activity by LIM kinase and Slingshot is critical for directional cell migration. J. Cell Biol. 171: 349-359. (Pubitemid 41540026)
25. Algrain, M., O. Turunen, A. Vaheri, D. Louvard, and M. Arpin. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120: 129-139.
26. June, C. H., J. A. Ledbetter, M. M. Gillespie, T. Lindsten, and C. B. Thompson. 1987. T-cell proliferation involving the CD28 pathway is associated with cyclosporine-resistant interleukin 2 gene expression. Mol. Cell. Biol. 7: 4472-4481. (Pubitemid 17166404)
27. Freeman, S. A., S. J. McLeod, J. Dukowski, P. Austin, C. C. Lee, B. Millen- Martin, P. Kubes, D. M. McCafferty, M. R. Gold, and C. D. Roskelley. 2010. Preventing the activation or cycling of the Rap1 GTPase alters adhesion and cytoskeletal dynamics and blocks metastatic melanoma cell extravasation into the lungs. Cancer Res. 70: 4590-4601.
28. Lorenz, M., V. DesMarais, F. Macaluso, R. H. Singer, and J. Condeelis. 2004. Measurement of barbed ends, actin polymerization, and motility in live carcinoma cells after growth factor stimulation. Cell Motil. Cytoskeleton 57: 207-217. (Pubitemid 38419153)
29. Chan, A. Y., M. Bailly, N. Zebda, J. E. Segall, and J. S. Condeelis. 2000. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J. Cell Biol. 148: 531-542.
30. Chudakov, D. M., V. V. Verkhusha, D. B. Staroverov, E. A. Souslova, S. Lukyanov, and K. A. Lukyanov. 2004. Photoswitchable cyan fluorescent protein for protein tracking. Nat. Biotechnol. 22: 1435-1439. (Pubitemid 39482864)
31. Ait-Azzouzene, D., L. Verkoczy, J. Peters, A. Gavin, P. Skog, J. L. Vela, and D. Nemazee. 2005. An immunoglobulin C kappa-reactive single chain antibody fusion protein induces tolerance through receptor editing in a normal polyclonal immune system. J. Exp. Med. 201: 817-828. (Pubitemid 40395125)
32. Condeelis, J. 2001. How is actin polymerization nucleated in vivo? Trends Cell Biol. 11: 288-293. (Pubitemid 32537774)
33. Van Troys, M., L. Huyck, S. Leyman, S. Dhaese, J. Vandekerkhove, and C. Ampe. 2008. Ins and outs of ADF/cofilin activity and regulation. Eur. J. Cell Biol. 87: 649-667.
34. Faure, S., L. I. Salazar-Fontana, M. Semichon, V. L. Tybulewicz, G. Bismuth, A. Trautmann, R. N. Germain, and J. Delon. 2004. ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nat. Immunol. 5: 272-279. (Pubitemid 38332124)
35. Bakal, C., J. Aach, G. Church, and N. Perrimon. 2007. Quantitative morphological signatures define local signaling networks regulating cell morphology. Science 316: 1753-1756. (Pubitemid 46988551)
36. Davey, E. J., J. Thyberg, D. H. Conrad, and E. Severinson. 1998. Regulation of cell morphology in B lymphocytes by IL-4: evidence for induced cytoskeletal changes. J. Immunol. 160: 5366-5373. (Pubitemid 28267825)
37. Carrasco, Y. R., and F. D. Batista. 2006. B-cell activation by membrane-bound antigens is facilitated by the interaction of VLA-4 with VCAM-1. EMBO J. 25: 889-899. (Pubitemid 43292449)
38. Bernstein, B. W., and J. R. Bamburg. 2010. ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 20: 187-195.
39. Jaqaman, K., H. Kuwata, N. Touret, R. Collins, W. S. Trimble, G. Danuser, and S. Grinstein. 2011. Cytoskeletal control of CD36 diffusion promotes its receptor and signaling function. Cell 146: 593-606.