The actin-bundling protein L-plastin dissociates CCR7 proximal signaling from CCR7-induced motility

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3628-3638

  Morley, Sharon Celeste ^a   Wang, Chen ^b   Lo, Wan Lin ^a   Lio, Chan Wang J ^a   Zinselmeyer, Bernd H ^a,c   Miller, Mark J ^a   Brown, Eric J ^b   Allen, Paul M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GENENTECH INC   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; CD24 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR7; F ACTIN; PROTEIN L PLASTIN; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG; CCR7 PROTEIN, MOUSE; LCP1 PROTEIN, MOUSE; PHOSPHOPROTEIN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL LINEAGE; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CHEMOTAXIS; DISSOCIATION; IN VIVO STUDY; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; THYMOCYTE; ANIMAL; CELL SEPARATION; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NEUTROPHIL CHEMOTAXIS; TRANSGENIC MOUSE;

ANIMALS; CELL ADHESION; CELL POLARITY; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PHOSPHOPROTEINS; RECEPTORS, CCR7; SIGNAL TRANSDUCTION;

EID: 77951630203     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903851     Document Type: Article

References (51)

1. Ladi, E., T. A. Schwickert, T. Chtanova, Y. Chen, P. Herzmark, X. Yin, H. Aaron, S. W. Chan, M. Lipp, B. Roysam, and E. A. Robey. 2008. Thymocyte-dendritic cell interactions near sources of CCR7 ligands in the thymic cortex. J. Immunol. 181: 7014-7023.
2. Yin, X., E. Ladi, S. W. Chan, O. Li, N. Killeen, D. J. Kappes, and E. A. Robey. 2007. CCR7 expression in developing thymocytes is linked to the CD4 versus CD8 lineage decision. J. Immunol. 179: 7358-7364.
3. Davalos-Misslitz, A. C., T. Worbs, S. Willenzon, G. Bernhardt, and R. Förster. 2007. Impaired responsiveness to T-cell receptor stimulation and defective negative selection of thymocytes in CCR7-deficient mice. Blood 110: 4351-4359.
4. Ueno, T., K. Hara, M. S. Willis, M. A. Malin, U. E. Höpken, D. H. Gray, K. Matsushima, M. Lipp, T. A. Springer, R. L. Boyd, et al. 2002. Role for CCR7 ligands in the emigration of newly generated T lymphocytes from the neonatal thymus. Immunity 16: 205-218. (Pubitemid 34211961)
5. Asperti-Boursin, F., E. Real, G. Bismuth, A. Trautmann, and E. Donnadieu. 2007. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase-independent manner. J. Exp. Med. 204: 1167-1179.
6. Worbs, T., T. R. Mempel, J. Bölter, U. H. von Andrian, and R. Förster. 2007. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J. Exp. Med. 204: 489-495.
7. Yagi, H., R. Kamba, K. Chiba, H. Soga, K. Yaguchi, M. Nakamura, and T. Itoh. 2000. Immunosuppressant FTY720 inhibits thymocyte emigration. Eur. J. Immunol. 30: 1435-1444.
8. Matloubian, M., C. G. Lo, G. Cinamon, M. J. Lesneski, Y. Xu, V. Brinkmann, M. L. Allende, R. L. Proia, and J. G. Cyster. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427: 355-360. (Pubitemid 38133663)
9. Wei, S. H., H. Rosen, M. P. Matheu, M. G. Sanna, S. K. Wang, E. Jo, C. H. Wong, I. Parker, and M. D. Cahalan. 2005. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6: 1228-1235.
10. Alfonso, C., M. G. McHeyzer-Williams, and H. Rosen. 2006. CD69 down-modulation and inhibition of thymic egress by short- and long-term selective chemical agonism of sphingosine 1-phosphate receptors. Eur. J. Immunol. 36: 149-159.
11. Okada, T., and J. G. Cyster. 2007. CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J. Immunol. 178: 2973-2978. (Pubitemid 46333176)
12. Woolf, E., I. Grigorova, A. Sagiv, V. Grabovsky, S. W. Feigelson, Z. Shulman, T. Hartmann, M. Sixt, J. G. Cyster, and R. Alon. 2007. Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat. Immunol. 8: 1076-1085.
13. Friedman, R. S., J. Jacobelli, and M. F. Krummel. 2006. Surface-bound chemokines capture and prime T cells for synapse formation. Nat. Immunol. 7: 1101-1108.
14. Gollmer, K., F. Asperti-Boursin, Y. Tanaka, K. Okkenhaug, B. Vanhaesebroeck, J. R. Peterson, Y. Fukui, E. Donnadieu, and J. V. Stein. 2009. CCL21 mediates CD4+ T-cell costimulation via a DOCK2/Rac-dependent pathway. Blood 114: 580-588.
15. Vicente-Manzanares, M., and F. Sánchez-Madrid. 2004. Role of the cytoskeleton during leukocyte responses. Nat. Rev. Immunol. 4: 110-122.
16. Real, E., S. Faure, E. Donnadieu, and J. Delon. 2007. Cutting edge: Atypical PKCs regulate T lymphocyte polarity and scanning behavior. J. Immunol. 179: 5649-5652.
17. Thelen, M., and J. V. Stein. 2008. How chemokines invite leukocytes to dance. Nat. Immunol. 9: 953-959.
18. Vicente-Manzanares, M., M. Rey, M. Pérez-Martínez, M. Yáñez-Mó , D. Sancho, J. R. Cabrero, O. Barreiro, H. de la Fuente, K. Itoh, and F. Sánchez-Madrid. 2003. The RhoA effector mDia is induced during T cell activation and regulates actin polymerization and cell migration in T lymphocytes. J. Immunol. 171: 1023-1034. (Pubitemid 36871419)
19. Föger, N., L. Rangell, D. M. Danilenko, and A. C. Chan. 2006. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 313: 839-842. (Pubitemid 44223353)
20. Sakata, D., H. Taniguchi, S. Yasuda, A. Adachi-Morishima, Y. Hamazaki, R. Nakayama, T. Miki, N. Minato, and S. Narumiya. 2007. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J. Exp. Med. 204: 2031-2038.
21. Burkhardt, J. K., E. Carrizosa, and M. H. Shaffer. 2008. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26: 233-259.
22. Shiow, L. R., D. W. Roadcap, K. Paris, S. R. Watson, I. L. Grigorova, T. Lebet, J. An, Y. Xu, C. N. Jenne, N. Föger, et al. 2008. The actin regulator coronin 1A is mutant in a thymic egress-deficient mouse strain and in a patient with severe combined immunodeficiency. Nat. Immunol. 9: 1307-1315.
23. Mick, V. E., T. K. Starr, T. M. McCaughtry, L. K. McNeil, and K. A. Hogquist. 2004. The regulated expression of a diverse set of genes during thymocyte positive selection in vivo. J. Immunol. 173: 5434-5444.
24. Jones, S. L., and E. J. Brown. 1996. FcgammaRII-mediated adhesion and phagocytosis induce L-plastin phosphorylation in human neutrophils. J. Biol. Chem. 271: 14623-14630.
25. Arpin, M., E. Friederich, M. Algrain, F. Vernel, and D. Louvard. 1994. Functional differences between L- and T-plastin isoforms. J. Cell Biol. 127: 1995-2008.
26. Chen, H., A. Mocsai, H. Zhang, R. X. Ding, J. H. Morisaki, M. White, J. M. Rothfork, P. Heiser, E. Colucci-Guyon, C. A. Lowell, et al. 2003. Role for plastin in host defense distinguishes integrin signaling from cell adhesion and spreading. Immunity 19: 95-104.
27. Delanote, V., B. Vanloo, M. Catillon, E. Friederich, J. Vandekerckhove, and J. Gettemans. 2009. An alpaca single-domain antibody blocks filopodia formation by obstructing L-plastin-mediated F-actin bundling. FASEB J. 24: 105-118.
28. Hailman, E., W. R. Burack, A. S. Shaw, M. L. Dustin, and P. M. Allen. 2002. Immature CD4(+)CD8(+) thymocytes form a multifocal immunological synapse with sustained tyrosine phosphorylation. Immunity 16: 839-848. (Pubitemid 34786482)
29. Lindquist, R. L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M. L. Dustin, and M. C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5: 1243-1250.
30. Lo, C. G., Y. Xu, R. L. Proia, and J. G. Cyster. 2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201: 291-301.
31. Kersh, G. J., D. L. Donermeyer, K. E. Frederick, J. M. White, B. L. Hsu, and P. M. Allen. 1998. TCR transgenic mice in which usage of transgenic alpha- and beta-chains is highly dependent on the level of selecting ligand. J. Immunol. 161: 585-593.
32. Yagi, H., M. Matsumoto, M. Nakamura, S. Makino, R. Suzuki, M. Harada, and T. Itoh. 1996. Defect of thymocyte emigration in a T cell deficiency strain (CTS) of the mouse. J. Immunol. 157: 3412-3419. (Pubitemid 126449153)
33. Fukui, Y., O. Hashimoto, T. Sanui, T. Oono, H. Koga, M. Abe, A. Inayoshi, M. Noda, M. Oike, T. Shirai, and T. Sasazuki. 2001. Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 412: 826-831. (Pubitemid 32801465)
34. Felix, N. J., D. L. Donermeyer, S. Horvath, J. J. Walters, M. L. Gross, A. Suri, and P. M. Allen. 2007. Alloreactive T cells respond specifically to multiple distinct peptide-MHC complexes. Nat. Immunol. 8: 388-397.
35. Carlson, C. M., B. T. Endrizzi, J. Wu, X. Ding, M. A. Weinreich, E. R. Walsh, M. A. Wani, J. B. Lingrel, K. A. Hogquist, and S. C. Jameson. 2006. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442: 299-302.
36. Campbell, J. J., J. Pan, and E. C. Butcher. 1999. Cutting edge: developmental switches in chemokine responses during T cell maturation. J. Immunol. 163: 2353-2357.
37. Takesono, A., R. Horai, M. Mandai, D. Dombroski, and P. L. Schwartzberg. 2004. Requirement for Tec kinases in chemokine-induced migration and activation of Cdc42 and Rac. Curr. Biol. 14: 917-922.
38. Nombela-Arrieta, C., T. R. Mempel, S. F. Soriano, I. Mazo, M. P. Wymann, E. Hirsch, C. Martínez-A, Y. Fukui, U. H. von Andrian, and J. V. Stein. 2007. A central role for DOCK2 during interstitial lymphocyte motility and sphingosine-1-phosphate-mediated egress. J. Exp. Med. 204: 497-510.
39. Flanagan, K., D. Moroziewicz, H. Kwak, H. Hörig, and H. L. Kaufman. 2004. The lymphoid chemokine CCL21 costimulates naive T cell expansion and Th1 polarization of non-regulatory CD4+ T cells. Cell. Immunol. 231: 75-84.
40. del Pozo, M. A., P. Sanchez-Mateos, and F. Sanchez-Madrid. 1996. Cellular polarization induced by chemokines: a mechanism for leukocyte recruitment? Immunol. Today 17: 127-131. (Pubitemid 26074501)
41. Nieto, M., J. M. Frade, D. Sancho, M. Mellado, C. Martinez-A, and F. Sánchez-Madrid. 1997. Polarization of chemokine receptors to the leading edge during lymphocyte chemotaxis. J. Exp. Med. 186: 153-158.
42. Sánchez-Madrid, F., and M. A. del Pozo. 1999. Leukocyte polarization in cell migration and immune interactions. EMBO J. 18: 501-511. (Pubitemid 29057235)
43. Gérard, A., A. E. Mertens, R. A. van der Kammen, and J. G. Collard. 2007. The Par polarity complex regulates Rap1- and chemokine-induced T cell polarization. J. Cell Biol. 176: 863-875. (Pubitemid 46425546)
44. Luo, C., H. Pan, M. Mines, K. Watson, J. Zhang, and G. H. Fan. 2006. CXCL12 induces tyrosine phosphorylation of cortactin, which plays a role in CXC chemokine receptor 4-mediated extracellular signal-regulated kinase activation and chemotaxis. J. Biol. Chem. 281: 30081-30093.
45. Kwan, J., and N. Killeen. 2004. CCR7 directs the migration of thymocytes into the thymic medulla. J. Immunol. 172: 3999-4007. (Pubitemid 38375211)
46. Ueno, T., F. Saito, D. H. Gray, S. Kuse, K. Hieshima, H. Nakano, T. Kakiuchi, M. Lipp, R. L. Boyd, and Y. Takahama. 2004. CCR7 signals are essential for cortex-medulla migration of developing thymocytes. J. Exp. Med. 200: 493-505.
47. Kurobe, H., C. Liu, T. Ueno, F. Saito, I. Ohigashi, N. Seach, R. Arakaki, Y. Hayashi, T. Kitagawa, M. Lipp, et al. 2006. CCR7-dependent cortex-tomedulla migration of positively selected thymocytes is essential for establishing central tolerance. Immunity 24: 165-177.
48. Davalos-Misslitz, A. C., J. Rieckenberg, S. Willenzon, T. Worbs, E. Kremmer, G. Bernhardt, and R. Förster. 2007. Generalized multi-organ autoimmunity in CCR7-deficient mice. Eur. J. Immunol. 37: 613-622.
49. Krummel, M. F., and I. Macara. 2006. Maintenance and modulation of T cell polarity. Nat. Immunol. 7: 1143-1149.
50. Wabnitz, G. H., T. Köcher, P. Lohneis, C. Stober, M. H. Konstandin, B. Funk, U. Sester, M. Wilm, M. Klemke, and Y. Samstag. 2007. Costimulation induced phosphorylation of L-plastin facilitates surface transport of the T cell activation molecules CD69 and CD25. Eur. J. Immunol. 37: 649-662.
51. Gomez, T. S., and D. D. Billadeau. 2008. T cell activation and the cytoskeleton: you can't have one without the other. Adv. Immunol. 97: 1-64.