Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse

Journal of Experimental Medicine

Volumn 207, Issue 12, 2010, Pages 2719-2732

  Pulecio, Julian ^a   Petrovic, Jelena ^a   Prete, Francesca ^a   Chiaruttini, Giulia ^a   Lennon Dumenil, Ana Maria ^b   Desdouets, Chantal ^c   Gasman, Stephane ^d   Burrone, Oscar R ^a   Benvenuti, Federica ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b INSERM   (France)

^c INSTITUT COCHIN   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; PROTEIN CDC42; STAT4 PROTEIN; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; IN VITRO STUDY; MICROTUBULE ORGANIZING CENTER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL COMMUNICATION; CELL POLARITY; DENDRITIC CELLS; ESCHERICHIA COLI INFECTIONS; FEMALE; IMMUNOLOGICAL SYNAPSES; INTERFERON-GAMMA; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICROTUBULE-ORGANIZING CENTER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 78649439527     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100007     Document Type: Article

References (49)

1. Al-Alwan, M.M., R.S. Liwski, S.M. Haeryfar, W.H. Baldridge, D.W. Hoskin, G. Rowden, and K.A. West. 2003. Cutting edge: dendritic cell actin cytoskeletal polarization during immunological synapse formation is highly antigen-dependent. J. Immunol. 171:4479-4483.
2. Bacon, C.M., D.W. McVicar, J.R. Ortaldo, R.C. Rees, J.J. O'Shea, and J.A. Johnston. 1995. Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J. Exp. Med. 181:399-404. doi:10.1084/jem.181.1.399
3. Banerjee, P.P., R. Pandey, R. Zheng, M.M. Suhoski, L. Monaco-Shawver, and J.S. Orange. 2007. Cdc42-interacting protein-4 functionally links actin and microtubule networks at the cytolytic NK cell immunological synapse. J. Exp. Med. 204:2305-2320. doi:10.1084/jem.20061893
4. Benvenuti, F., S. Hugues, M. Walmsley, S. Ruf, L. Fetler, M. Popoff, V.L. Tybulewicz, and S. Amigorena. 2004a. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science. 305:1150-1153. doi:10.1126/science.1099159 (Pubitemid 39100327)
5. Benvenuti, F., C. Lagaudrière-Gesbert, I. Grandjean, C. Jancic, C. Hivroz, A. Trautmann, O. Lantz, and S. Amigorena. 2004b. Dendritic cell maturation controls adhesion, synapse formation, and the duration of the interactions with naive T lymphocytes. J. Immunol. 172:292-301.
6. Blanchard, N., V. Di Bartolo, and C. Hivroz. 2002. In the immune synapse, ZAP-70 controls T cell polarization and recruitment of signaling proteins but not formation of the synaptic pattern. Immunity. 17:389-399. doi:10.1016/S1074-7613(02)00421-1
7. Bloom, O., J.J. Unternaehrer, A. Jiang, J.S. Shin, L. Delamarre, P. Allen, and I. Mellman. 2008. Spinophilin participates in information transfer at immunological synapses. J. Cell Biol. 181:203-211. doi:10.1083/jcb.200711149
8. Boes, M., J. Cerny, R. Massol, M. Op den Brouw, T. Kirchhausen, J. Chen, and H.L. Ploegh. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature. 418:983-988. doi:10.1038/nature01004
9. Borg, C., J. Taieb, M. Terme, K. Maruyama, C. Flament, E. Angevin, and L. Zitvogel. 2003. NK cell-based immunotherapy: new prospects and involvement of dendritic cells. Bull. Cancer. 90:699-705.
10. Braun, V., V. Fraisier, G. Raposo, I. Hurbain, J.B. Sibarita, P. Chavrier, T. Galli, and F. Niedergang. 2004. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J. 23:4166-4176. doi:10.1038/sj.emboj.7600427 (Pubitemid 39546155)
11. Celli, S., F. Lemaître, and P. Bousso. 2007. Real-time manipulation of T cell-dendritic cell interactions in vivo reveals the importance of prolonged contacts for CD4+ T cell activation. Immunity. 27:625-634. doi:10.1016/j.immuni.2007.08.018
12. Chen, X., D.S. Allan, K. Krzewski, B. Ge, H. Kopcow, and J.L. Strominger. 2006. CD28-stimulated ERK2 phosphorylation is required for polarization of the microtubule organizing center and granules in YTS NK cells. Proc. Natl. Acad. Sci. USA. 103:10346-10351. doi:10.1073/pnas.0604236103
13. Curtsinger, J.M., D.C. Lins, and M.F. Mescher. 2003. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J. Exp. Med. 197:1141-1151. doi:10.1084/jem.20021910
14. de la Fuente, H., M. Mittelbrunn, L. Sánchez-Martín, M. Vicente-Manzanares, A. Lamana, R. Pardi, C. Cabañas, and F. Sánchez-Madrid. 2005. Synaptic clusters of MHC class II molecules induced on DCs by adhesion molecule-mediated initial T-cell scanning. Mol. Biol. Cell. 16:3314-3322. doi:10.1091/mbc.E05-01-0005
15. Dustin, M.L., M.W. Olszowy, A.D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P.A. van der Merwe, P.M. Allen, and A.S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell. 94:667-677. doi:10.1016/S0092-8674(00)81608-6
16. Eng, E.W., A. Bettio, J. Ibrahim, and R.E. Harrison. 2007. MTOC reorientation occurs during FcgammaR-mediated phagocytosis in macrophages. Mol. Biol. Cell. 18:2389-2399. doi:10.1091/mbc.E06-12-1128
17. Etienne-Manneville, S. 2004. Cdc42 - the centre of polarity. J. Cell Sci. 117:1291-1300. doi:10.1242/jcs.01115
18. Etienne-Manneville, S., and A. Hall. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell. 106:489-498. doi:10.1016/S0092-8674(01)00471-8
19. Gardella, S., C. Andrei, L.V. Lotti, A. Poggi, M.R. Torrisi, M.R. Zocchi, and A. Rubartelli. 2001. CD8(+) T lymphocytes induce polarized exocytosis of secretory lysosomes by dendritic cells with release of interleukin-1beta and cathepsin D. Blood. 98:2152-2159. doi:10.1182/blood.V98.7.2152
20. Gasman, S., S. Chasserot-Golaz, M. Malacombe, M. Way, and M.F. Bader. 2004. Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol. Biol. Cell. 15: 520-531. doi:10.1091/mbc.E03-06-0402
21. Henrickson, S.E., T.R. Mempel, I.B. Mazo, B. Liu, M.N. Artyomov, H. Zheng, A. Peixoto, M.P. Flynn, B. Senman, T. Junt, et al. 2008. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9:282-291. doi:10.1038/ni1559
22. Henry, C.J., D.A. Ornelles, L.M. Mitchell, K.L. Brzoza-Lewis, and E.M. Hiltbold. 2008. IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J. Immunol. 181:8576-8584.
23. Hugues, S., L. Fetler, L. Bonifaz, J. Helft, F. Amblard, and S. Amigorena. 2004. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat. Immunol. 5:1235-1242. doi:10.1038/ni1134
24. Huse, M., B.F. Lillemeier, M.S. Kuhns, D.S. Chen, and M.M. Davis. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7:247-255. doi:10.1038/ni1304
25. Krummel, M.F., and I. Macara. 2006. Maintenance and modulation of T cell polarity. Nat. Immunol. 7:1143-1149. doi:10.1038/ni1404
26. Kupfer, A., G. Dennert, and S.J. Singer. 1985. The reorientation of the Golgi apparatus and the microtubule-organizing center in the cytotoxic effector cell is a prerequisite in the lysis of bound target cells. J. Mol. Cell. Immunol. 2:37-49.
27. Kupfer, A., T.R. Mosmann, and H. Kupfer. 1991. Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. USA. 88:775-779. doi:10.1073/pnas.88.3.775
28. Lämmermann, T., J. Renkawitz, X. Wu, K. Hirsch, C. Brakebusch, and M. Sixt. 2009. Cdc42-dependent leading edge coordination is essential for interstitial dendritic cell migration. Blood. 113:5703-5710. doi:10.1182/blood-2008-11-191882
29. Li, Q., C. Eppolito, K. Odunsi, and P.A. Shrikant. 2006. IL-12- programmed long-term CD8+ T cell responses require STAT4. J. Immunol. 177:7618-7625.
30. Lund, R.J., Z. Chen, J. Scheinin, and R. Lahesmaa. 2004. Early target genes of IL-12 and STAT4 signaling in th cells. J. Immunol. 172:6775-6782.
31. Malacombe, M., M. Ceridono, V. Calco, S. Chasserot-Golaz, P.S. McPherson, M.F. Bader, and S. Gasman. 2006. Intersectin-1L nucleotide exchange factor regulates secretory granule exocytosis by activating Cdc42. EMBO J. 25:3494-3503. doi:10.1038/sj.emboj.7601247
32. Martín-Cófreces, N.B., J. Robles-Valero, J.R. Cabrero, M. Mittelbrunn, M. Gordón-Alonso, C.H. Sung, B. Alarcón, J. Vázquez, and F. Sánchez-Madrid. 2008. MTOC translocation modulates IS formation and controls sustained T cell signaling. J. Cell Biol. 182:951-962. doi:10.1083/jcb.200801014
33. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135-145. doi:10.1038/35100529
34. Medzhitov, R., P. Preston-Hurlburt, and C.A. Janeway Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 388:394-397. doi:10.1038/41131
35. Momboisse, F., S. Ory, V. Calco, M. Malacombe, M.F. Bader, and S. Gasman. 2009. Calcium-regulated exocytosis in neuroendocrine cells: intersectin-1L stimulates actin polymerization and exocytosis by activating Cdc42. Ann. N. Y. Acad. Sci. 1152:209-214. doi:10.1111/j.1749-6632.2008.03998.x
36. Moon, J.J., H.H. Chu, M. Pepper, S.J. McSorley, S.C. Jameson, R.M. Kedl, and M.K. Jenkins. 2007. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity. 27:203-213. doi:10.1016/j.immuni.2007.07.007
37. Obar, J.J., K.M. Khanna, and L. Lefrançois. 2008. Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity. 28:859-869. doi:10.1016/ j.immuni.2008.04.010
38. Orange, J.S., N. Ramesh, E. Remold-O'Donnell, Y. Sasahara, L. Koopman, M. Byrne, F.A. Bonilla, F.S. Rosen, R.S. Geha, and J.L. Strominger. 2002. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA. 99:11351-11356. doi:10.1073/pnas.162376099
39. Pearce, E.L., and H. Shen. 2007. Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179:2074-2081.
40. Reefman, E., J.G. Kay, S.M. Wood, C. Offenhäuser, D.L. Brown, S. Roy, A.C. Stanley, P.C. Low, A.P. Manderson, and J.L. Stow. 2010. Cytokine secretion is distinct from secretion of cytotoxic granules in NK cells. J. Immunol. 184:4852-4862. doi:10.4049/jimmunol.0803954
41. Riol-Blanco, L., C. Delgado-Martín, N. Sánchez- Sánchez, L.M. Alonso-C, M.D. Gutiérrez-López, G.M. Del Hoyo, J. Navarro, F. Sánchez-Madrid, C. Cabañas, P. Sánchez-Mateos, and J.L. Rodríguez-Fernández. 2009. Immunological synapse formation inhibits, via NF-kappaB and FOXO1, the apoptosis of dendritic cells. Nat. Immunol. 10:753-760. doi:10.1038/ni.1750
42. Rodríguez-Fernández, J.L., M. Gómez, A. Luque, N. Hogg, F. Sánchez-Madrid, and C. Cabañas. 1999. The interaction of activated integrin lymphocyte function-associated antigen 1 with ligand intercellular adhesion molecule 1 induces activation and redistribution of focal adhesion kinase and proline-rich tyrosine kinase 2 in T lymphocytes. Mol. Biol. Cell. 10:1891-1907.
43. Scholer, A., S. Hugues, A. Boissonnas, L. Fetler, and S. Amigorena. 2008. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity. 28:258-270. doi:10.1016/j.immuni.2007.12.016 (Pubitemid 351222655)
44. Semino, C., G. Angelini, A. Poggi, and A. Rubartelli. 2005. NK/iDC interaction results in IL-18 secretion by DCs at the synaptic cleft followed by NK cell activation and release of the DC maturation factor HMGB1. Blood. 106:609-616. doi:10.1182/blood-2004-10-3906
45. Stinchcombe, J.C., and G.M. Griffiths. 2003. The role of the secretory immunological synapse in killing by CD8+ CTL. Semin. Immunol. 15:301-305. doi:10.1016/j.smim.2003.09.003
46. Stinchcombe, J.C., E. Majorovits, G. Bossi, S. Fuller, and G.M. Griffiths. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature. 443:462-465. doi:10.1038/nature05071
47. Trinchieri, G., S. Pflanz, and R.A. Kastelein. 2003. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity. 19:641-644. doi:10.1016/S1074-7613(03)00296-6
48. Valenzuela, J., C. Schmidt, and M. Mescher. 2002. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J. Immunol. 169:6842-6849.
49. West, M.A., R.P. Wallin, S.P. Matthews, H.G. Svensson, R. Zaru, H.G. Ljunggren, A.R. Prescott, and C. Watts. 2004. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science. 305:1153-1157. doi:10.1126/science.1099153