A large T cell invagination with CD2 enrichment resets receptor engagement in the immunological synapse

Journal of Immunology

Volumn 177, Issue 7, 2006, Pages 4402-4413

  Singleton, Kentner ^a   Parvaze, Nadia ^a   Dama, Kavyya R ^a   Chen, Kenneth S ^a   Jennings, Paula ^a   Purtic, Bozidar ^a   Sjaastad, Michael D ^b   Gilpin, Christopher ^a   Davis, Mark M ^c   Wülfing, Christoph ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD2 ANTIGEN; CD48 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL MEMBRANE TRANSPORT; ELECTRON MICROSCOPY; INTERNALIZATION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 33749147602     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.7.4402     Document Type: Article

References (56)

1. Davis, M. M., I. J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, and Y. Chien. 1998. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16: 523-544.
2. Davis, S. J., S. Ikemizu, E. J. Evans, L. Fugger, T. R. Bakker, and P. A. van der Merwe. 2003. The nature of molecular recognition by T cells. Nat. Immunol. 4: 217-224.
3. Sprent, J. 1999. Presidential address to the American Association of Immunologists: stimulating naive T cells. J. Immunol. 163: 4629-4636.
4. Reinherz, E. L., H. C. Chang, L. K. Clayton, P. Gardner, F. D. Howard, S. Koyasu, Y. J. Jin, P. Moingeon, and P. H. Sayre. 1989. The biology of human CD2. Cold Spring Harb. Symp. Quant. Biol. 54(Pt. 2): 611-625.
5. Meuer, S. C., B. Schraven, and Y. Samstag. 1994. An 'alternative' pathway of T cell activation. Int. Arch. Allergy Immunol. 104: 216-221.
6. lck on endosomes of CD2-triggered T cells, colocalization with ZAP-70. J. Biol. Chem. 271: 20734-20739.
7. fyn in T lymphocytes. Eur. J. Immunol. 24: 139-144.
8. Breitmeyer, J. B., J. F. Daley, H. B. Levine, and S. F. Schlossman. 1987. The T11 (CD2) molecule is functionally linked to the T3/Ti T cell receptor in the majority of T cells. J. Immunol. 139: 2899-2905.
9. Kivens, W. J., S. W. Hunt III, J. L. Mobley, T. Zell, C. L. Dell, B. E. Bierer, and Y. Shimizu. 1998. Identification of a proline-rich sequence in the CD2 cytoplasmic domain critical for regulation of integrin-mediated adhesion and activation of phosphoinositide 3-kinase. Mol. Cell Biol. 18: 5291-5307.
10. Nishizawa, K., C. Freund, J. Li, G. Wagner, and E. L. Reinhera. 1998. Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc. Natl. Acad. Sci. USA 95: 14897-14902.
11. Dustin, M. L., M. W. Olszowy, A. D. Holdotf, 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.
12. Killeen, N., S. G. Stuart, and D. R. Littman. 1992. Development and function of T cells in mice with a disrupted CD2 gene. EMBO J. 11: 4329-4336.
13. Purtic, B., L. A. Pitcher, N. S. van Oers, and C. Wülfing. 2005. T cell receptor (TCR) clustering in the immunological synapse integrates TCR and costimulatory signaling in selected T cells. Proc. Natl. Acad. Sci. USA 102: 2904-2909.
14. Wülfing, C., C. Sumen, M. D. Sjaastad, L. C. Wu, M. L. Dustin, and M. M. Davis. 2002. Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat. Immunol. 3: 42-47.
15. Wülfing, C., M. D. Sjaastad, and M. M. Davis. 1998. Visualizing the dynamics of T cell activation: ICAM-1 migrates rapidly to the T cell:B cell interface and acts to sustain calcium levels. Proc. Natl. Acad. Sci. USA 95: 6302-6307.
16. 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.
17. Tskvitaria-Fuller, I., A. L. Rozelle, H. L. Yin, and C. Wülfing. 2003. Regulation of sustained actin dynamics by the TCR and costimulation as a mechanism of receptor localization. J. Immunol. 171: 2287-2295.
18. 2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86: 233-242.
19. Yang, Z., R. K. Vadlamudi, and R. Kumar. 2005. Dynein light chain 1 phosphorylation controls macropinocytosis. J. Biol. Chem. 280: 654-659.
20. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
21. Shaner, N. C., R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, and R. Y. Tsien. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22: 1567-1572.
22. Randazzo, P. A., and H. M. Fales. 2002. Preparation of myristoylated Arf1 and Arf6 proteins. Methods Mol. Biol. 189: 169-179.
23. Frank, S., S. Upender, S. H. Hansen, and J. E. Casanova. 1998. ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6. J. Biol. Chem. 273: 23-27.
24. Wild, M. K., A. Cambiaggi, M. H. Brown, E. A. Davies, H. Ohno, T. Saito, and P. A. van der Merwe. 1999. Dependence of T cell antigen recognition on the dimensions of an accessory receptor-ligand complex. J. Exp. Med. 190: 31-41.
25. Leupin, O., R. Zaru, T. Laroche, S. Muller, and S. Valitutti. 2000. Exclusion of CD45 from the T-cell receptor signaling area in antigen-stimulated T lymphocytes. Curr. Biol. 10: 277-280.
26. Krummel, M. F., M. D. Sjaastad, C. Wülfing, and M. M. Davis. 2000. Differential clustering of CD4 and CD3ζ during T cell recognition. Science 289: 1349-1352.
27. Conner, S. D., and S. L. Schmid. 2003. Regulated portals of entry into the cell. Nature 422: 37-44.
28. Amyere, M., M. Mettlen, P. Van Der Smissen, A. Platek, B. Payrastre, A. Veithen, and P. J. Courtoy. 2002. Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int. J. Med. Microbiol. 291: 487-494.
29. Greenberg, S., and S. Grinstein. 2002. Phagocytosis and innate immunity. Curr. Opin. Immunol. 14: 136-145.
30. Donaldson, J. G. 2003. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278: 41573-41576.
31. Niedergang, F., E. Colucci-Guyon, T. Dubois, G. Raposo, and P. Chavrier. 2003. ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell Biol. 161: 1143-1150.
32. Radhakrishna, H., R. D. Klausner, and J. G. Donaldson. 1996. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol. 134: 935-947.
33. Langille, S. E., V. Patki, J. K. Klarlund, J. M. Buxton, J. J. Holik, A. Chawla, S. Corvera, and M. P. Czech. 1999. ADP-ribosylation factor 6 as a target of guanine nucleotide exchange factor GRP1. J. Biol. Chem. 274: 27099-27104.
34. Wadia, J. S., and S. F. Dowdy. 2002. Protein transduction technology. Curr. Opin. Biotechnol. 13: 52-56.
35. Knorr, T., W. Nagel, and W. Kolanus. 2000. Phosphoinositides determine specificity of the guanine-nucleotide exchange activity of cytohesin-1 for ADP-ribosylation factors derived from a mammalian expression system. Eur. J. Biochem. 267: 3784-3791.
36. Soga, N., N. Namba, S. McAllister, L. Cornelius, S. L. Teitelbaum, S. F. Dowdy, J. Kawamura, and K. A. Hruska. 2001. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp. Cell Res. 269: 73-87.
37. Tskvitaria-Fuller, I., A. Seth, N. Mistry, H. Gu, M. K. Rosen, and C. Wülfing. 2006. Specific patterns of Cdc42 activity are related to distinct elements of T cell polarization. J. Immunol. 177: 1708-1720.
38. Leverrier, Y., and A. J. Ridley. 2001. Requirement for Rho GTPases and PI3-kinases during apoptotic cell phagocytosis by macrophages. Curr. Biol. 11: 195-199.
39. Marshall, J. G., J. W. Booth, V. Stambolic, T. Mak, T. Balla, A. D. Schreiber, T. Meyer, and S. Grinstein. 2001. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fcγy receptor-mediated phagocytosis. J. Cell Biol. 153: 1369-1380.
40. Amyere, M., B. Payrastre, U. Krause, P. Van Der Smissen, A. Veithen, and P. J. Courtoy. 2000. Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol. Biol. Cell 11: 3453-3467.
41. Navarro-Lérida, I., M. Martinez Moreno, F. Roncal, F. Gavilanes, J. P. Albar, and I. Rodríguez-Crespo. 2004. Proteomic identification of brain proteins that interact with dynein light chain LC8. Proteomics 4: 339-346.
42. Ghosh-Roy, A., B. S. Desai, and K. Ray. 2005. Dynein light chain 1 regulates dynamin-mediated F-actin assembly during sperm individualization in Drosophila. Mol. Biol. Cell 16: 3107-3116.
43. Gomez, T. S., M. J. Hamann, S. McCarney, D. N. Savoy, C. M. Lubking, M. P. Heldebrant, C. M. Labno, D. J. McKean, M. A. McNiven, J. K. Burkhardt, and D. D. Billadeau. 2005. Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat. Immunol. 6: 261-270.
44. Fiorentini, C., L. Falzano, A. Fabbri, A. Stringaro, M. Logozzi, S. Travaglione, S. Contamin, G. Arancia, W. Malomi, and S. Fais. 2001. Activation of rho GT-Pases by cytotoxic necrotizing factor 1 induces macropinocytosis and scavenging activity in epithelial cells. Mol. Biol. Cell 12: 2061-2073.
45. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92: 83-92.
46. Lyons, D. S., S. A. Lieberman, J. Hampl, J. J. Boniface, P. A. Reay, Y. Chien, L. J. Berg, and M. M. Davis. 1996. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 5: 53-61.
47. Hwang, I., J. F. Huang, H. Kishimoto, A. Brunmark, P. A. Peterson, M. R. Jackson, C. D. Surh, Z. Cai, and J. Sprent. 2000. T cells can use either T cell receptor or CD28 receptors to absorb and internalize cell surface molecules derived from antigen-presenting cells. J. Exp. Med. 191: 1137-1148.
48. Patel, D. M., P. Y. Arnold, G. A. White, J. P. Nardella, and M. D. Mannie. 1999. Class II MHC/peptide complexes are released from APC and are acquired by T cell responders during specific antigen recognition. J. Immunol. 163: 5201-5210.
49. Borgonovo, B., E. Cocucci, G. Racchetti, P. Podini, A. Bachi, and J. Meldolesi. 2002. Regulated exocytosis: a novel, widely expressed system. Nat. Cell Biol. 4: 955-962.
50. 2+- dependent tyrosine phosphorylation and microtubules. J. Immunol. 168: 5287-5296.
51. Marston, D. J., S. Dickinson, and C. D. Nobes. 2003. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat. Cell Biol. 5: 879-888.
52. Zimmer, M., A. Palmer, J. Köhler, and R. Klein. 2003. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat. Cell Biol. 5: 869-878,
53. Freiberg, B. A., H. Kupfer, W. Maslanik, J. Delli, J. Kappler, D. M. Zaller, and A. Kupfer. 2002. Staging and resetting T cell activation in SMACs. Nat. Immunol. 3: 911-917.
54. Stefanova, I., J. R. Dorfman, M. Tsukamoto, and R. N. Germain. 2003. On the role of self-recognition in T cell responses to foreign antigen. Immunol. Rev. 191: 97-106.
55. Sloan-Lancaster, J., and P. M. Allen. 1996. Altered peptide ligand induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 14: 1-27.
56. Irvine, D. J., M. A. Purbhoo, M. Krogsgaard, and M. M. Davis. 2002. Direct observation of ligand recognition by T cells. Nature 419: 845-849.