Dendritic cell motility and T cell activation requires regulation of rho-cofilin signaling by the rho-GTPase activating protein myosin IXb

Journal of Immunology

Volumn 192, Issue 8, 2014, Pages 3559-3568

  Xu, Yan ^a   Pektor, Stefanie ^b   Balkow, Sandra ^b   Hemkemeyer, Sandra A ^a   Liu, Zhijun ^a   Grobe, Kay ^a   Hanley, Peter J ^a   Shen, Limei ^b   Bros, Matthias ^b   Schmidt, Talkea ^b   Bähler, Martin ^a   Grabbe, Stephan ^b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; BONE MARROW CELLS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MOVEMENT; DENDRITIC CELLS; DERMATITIS, CONTACT; GTPASE-ACTIVATING PROTEINS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MYOSINS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 84898638459     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300695     Document Type: Article

References (44)

1. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21: 685-711.
2. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
3. Randolph, G. J., V. Angeli, and M. A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5: 617-628.
4. Fukata, M., M. Nakagawa, and K. Kaibuchi. 2003. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr. Opin. Cell Biol. 15: 590-597.
5. Raftopoulou, M., and A. Hall. 2004. Cell migration: Rho GTPases lead the way. Dev. Biol. 265: 23-32.
6. Van Keymeulen, A., K. Wong, Z. A. Knight, C. Govaerts, K. M. Hahn, K. M. Shokat, and H. R. Bourne. 2006. To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J. Cell Biol. 174: 437-445.
7. Jaffe, A. B., and A. Hall. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21: 247-269.
8. Bernstein, B.W., and J. R. Bamburg. 2010. ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 20: 187-195.
9. Lämmermann, T., B. L. Bader, S. J. Monkley, T. Worbs, R. Wedlich-Söldner, K. Hirsch, M. Keller, R. Förster, D. R. Critchley, R. Fässler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453: 51-55.
10. Xu, J., F. Wang, A. Van Keymeulen, P. Herzmark, A. Straight, K. Kelly, Y. Takuwa, N. Sugimoto, T. Mitchison, and H. R. Bourne. 2003. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114: 201-214.
11. Davis, D. M. 2009. Mechanisms and functions for the duration of intercellular contacts made by lymphocytes. Nat. Rev. Immunol. 9: 543-555.
12. Scheele, J. S., R. E. Marks, and G. R. Boss. 2007. Signaling by small GTPases in the immune system. Immunol. Rev. 218: 92-101.
13. Hanley, P. J., Y. Xu, M. Kronlage, K. Grobe, P. Schön, J. Song, L. Sorokin, A. Schwab, and M. Bähler. 2010. Motorized RhoGAP myosin IXb (Myo9b) controls cell shape and motility. Proc. Natl. Acad. Sci. USA 107: 12145-12150.
14. Reinhard, J., A. A. Scheel, D. Diekmann, A. Hall, C. Ruppert, and M. Bähler. 1995. A novel type of myosin implicated in signalling by rho family GTPases. EMBO J. 14: 697-704.
15. Graf, B., M. Bähler, P. Hilpelä, C. Böwe, and T. Adam. 2000. Functional role for the class IX myosin myr5 in epithelial cell infection by Shigella flexneri. Cell. Microbiol. 2: 601-616.
16. Muller, R. T., U. Honnert, J. Reinhard, and M. Bähler. 1997. The rat myosin myr 5 is a GTPase-activating protein for Rho in vivo: essential role of arginine 1695. Mol. Biol. Cell 8: 2039-2053.
17. van den Boom, F., H. Dussmann, K. Uhlenbrock, M. Abouhamed, and M. Bähler. 2007. The Myosin IXb motor activity targets the myosin IXb Rho-GAP domain as cargo to sites of actin polymerization. Mol. Biol. Cell 18: 1507-1518.
18. Wirth, J. A., K. A. Jensen, P. L. Post, W. M. Bement, and M. S. Mooseker. 1996. Human myosin-IXb, an unconventional myosin with a chimerin-like rho/rac GTPase-activating protein domain in its tail. J. Cell Sci. 109: 653-661.
19. Monsuur, A. J., P. I. de Bakker, B. Z. Alizadeh, A. Zhernakova, M. R. Bevova, E. Strengman, L. Franke, R. van't Slot, M. J. van Belzen, I. C. Lavrijsen, et al. 2005. Myosin IXB variant increases the risk of celiac disease and points toward a primary intestinal barrier defect. Nat. Genet. 37: 1341-1344.
20. Persengiev, S., B. P. Koeleman, K. Downes, G. Valdigem, A. R. van der Slik, P. Eerligh, A. Monsuur, G. J. Bruining, C. Wijmenga, J. A. Todd, et al. 2010. Association analysis of myosin IXB and type 1 diabetes. Hum. Immunol. 71: 598-601.
21. Klemke, M., E. Kramer, M. H. Konstandin, G. H. Wabnitz, and Y. Samstag. 2010. An MEK-cofilin signalling module controls migration of human T cells in 3D but not 2D environments. EMBO J. 29: 2915-2929.
22. 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.
23. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
24. Reid, T., T. Furuyashiki, T. Ishizaki, G. Watanabe, N. Watanabe, K. Fujisawa, N. Morii, P. Madaule, and S. Narumiya. 1996. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J. Biol. Chem. 271: 13556-13560.
25. Sander, E. E., S. van Delft, J. P. ten Klooster, T. Reid, R. A. van der Kammen, F. Michiels, and J. G. Collard. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143: 1385-1398.
26. Malliri, A., J. P. ten Klooster, C. Olivio, and J. G. Collard. 2002. Determination of the activity of Rho-like GTPases in cells. Methods Mol. Biol. 189: 99-109.
27. Gunzer, M., A. Schäfer, S. Borgmann, S. Grabbe, K. S. Zänker, E. B. Bröcker, E. Kämpgen, and P. Friedl. 2000. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity 13: 323-332.
28. Sudowe, S., E. Montermann, J. Steitz, T. Tuting, J. Knop, and A. B. Reske-Kunz. 2002. Efficacy of recombinant adenovirus as vector for allergen gene therapy in a mouse model of type I allergy. Gene Ther. 9: 147-156.
29. Shortman, K., and S. H. Naik. 2007. Steady-state and inflammatory dendriticcell development. Nat. Rev. Immunol. 7: 19-30.
30. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Muller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33.
31. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Förster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21: 279-288.
32. Riol-Blanco, L., N. Sánchez-Sánchez, A. Torres, A. Tejedor, S. Narumiya, A. L. Corbí, P. Sánchez-Mateos, and J. L. Rodríguez-Fernández. 2005. The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J. Immunol. 174: 4070-4080.
33. Iijima, N., Y. Yanagawa, J. M. Clingan, and K. Onoé. 2005. CCR7-mediated c-Jun N-terminal kinase activation regulates cell migration in mature dendritic cells. Int. Immunol. 17: 1201-1212.
34. Li, G., S. Basu, M. K. Han, Y. J. Kim, and H. E. Broxmeyer. 2007. Influence of ERK activation on decreased chemotaxis of mature human cord blood monocyte-derived dendritic cells to CCL19 and CXCL12. Blood 109: 3173-3176.
35. Kripke, M. L., C. G. Munn, A. Jeevan, J. M. Tang, and C. Bucana. 1990. Evidence that cutaneous antigen-presenting cells migrate to regional lymph nodes during contact sensitization. J. Immunol. 145: 2833-2838.
36. Jönsson, F., C. B. Gurniak, B. Fleischer, G. Kirfel, and W. Witke. 2012. Immunological responses and actin dynamics in macrophages are controlled by N-cofilin but are independent from ADF. PLoS ONE 7: e36034.
37. Shurin, G. V., I. L. Tourkova, G. S. Chatta, G. Schmidt, S. Wei, J. Y. Djeu, and M. R. Shurin. 2005. Small rho GTPases regulate antigen presentation in dendritic cells. J. Immunol. 174: 3394-3400.
38. Blöcker, D., L. Berod, J. W. Fluhr, J. Orth, M. Idzko, K. Aktories, and J. Norgauer. 2006. Pasteurella multocida toxin (PMT) activates RhoGTPases, induces actin polymerization and inhibits migration of human dendritic cells, but does not influence macropinocytosis. Int. Immunol. 18: 459-464.
39. Liao, W., K. Elfrink, and M. Bähler. 2010. Head of myosin IX binds calmodulin and moves processively toward the plus-end of actin filaments. J. Biol. Chem. 285: 24933-24942.
40. Bennett, C. L., M. Noordegraaf, C. A. Martina, and B. E. Clausen. 2007. Langerhans cells are required for efficient presentation of topically applied hapten to T cells. J. Immunol. 179: 6830-6835.
41. Khelfaoui, M., A. Pavlowsky, A. D. Powell, P. Valnegri, K. W. Cheong, Y. Blandin, M. Passafaro, J. G. Jefferys, J. Chelly, and P. Billuart. 2009. Inhibition of RhoA pathway rescues the endocytosis defects in Oligophrenin1 mouse model of mental retardation. Hum. Mol. Genet. 18: 2575-2583.
42. Verdijk, P., P. A. van Veelen, A. H. de Ru, P. J. Hensbergen, K. Mizuno, H. K. Koerten, F. Koning, C. P. Tensen, and A. M. Mommaas. 2004. Morphological changes during dendritic cell maturation correlate with cofilin activation and translocation to the cell membrane. Eur. J. Immunol. 34: 156-164.
43. Bromley, S. K., A. Iaboni, S. J. Davis, A. Whitty, J. M. Green, A. S. Shaw, A. Weiss, and M. L. Dustin. 2001. The immunological synapse and CD28-CD80 interactions. Nat. Immunol. 2: 1159-1166.
44. Sims, T. N., and M. L. Dustin. 2002. The immunological synapse: integrins take the stage. Immunol. Rev. 186: 100-117.