Protein interactions between CD2 and Lck are required for the lipid raft distribution of CD2

Journal of Immunology

Volumn 180, Issue 2, 2008, Pages 988-997

  Nunes, Raquel J ^a,b   Castro, Mónica A A ^a   Gonçalves, Carine M ^a   Bamberger, Martina ^a,b   Pereira, Carlos F ^b,d   Bismuth, Georges ^c   Carmo, Alexandre M ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSERM   (France)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CD2 ANTIGEN; CYSTINE; LIPID; MUTANT PROTEIN; PALMITIC ACID; PROTEIN KINASE FYN; PROTEIN KINASE LCK; CYSTEINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ISOTOPE LABELING; LEUKEMIA CELL LINE; LIPID RAFT; MALE; MUTANT; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; ANIMAL; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; T LYMPHOCYTE; THYMOMA; TUMOR CELL LINE; WISTAR RAT;

ANIMALS; ANTIGENS, CD2; CELL LINE, TUMOR; CELL MEMBRANE; CYSTEINE; HUMANS; JURKAT CELLS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE MICRODOMAINS; MICE; PALMITIC ACID; RATS; RATS, WISTAR; T-LYMPHOCYTES; THYMOMA;

EID: 40449133966     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.2.988     Document Type: Article

References (57)

1. Barclay, A. N., M. H. Brown, S. K. A. Law, A. J. McKnight, M. G. Tomlinson, and P. A. van der Merwe. 1997. The Leukocyte Antigen Factsbook. Academic Press, San Diego.
2. Jones, E. Y., S. J. Davis, A. F. Williams, K. Harlos, and D. I. Stuart. 1992. Crystal structure at 2.8 A resolution of a soluble form of the cell adhesion molecule CD2. Nature 360: 232-239.
3. Davis, S. J., and P. A. van der Merwe. 1996. The structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today 17: 177-187.
4. Evans, E. J., M. A. A. Castro, R. O'Brien, A. Kearney, H. Walsh, L. M. Sparks, M. G. Tucknott, E. A. Davies, A. M. Carmo, P. A. van der Merwe, et al. 2006. Crystal structure and binding properties of the CD2 and CD244 (2B4)-binding protein, CD48. J. Biol. Chem. 281: 29309-29320.
5. Kearney, A., A. Avramovic, M. A. A. Castro, A. M. Carmo, S. J. Davis, and P. A. van der Merwe. 2007. The contribution of conformational adjustments and long-range electrostatic forces to the CD2/CD58 interaction. J. Biol. Chem. 282: 13160-13166.
6. Wang, J. H., A. Smolyar, K. Tan, J. H. Liu, M. Kim, Z. Y. Sun, G. Wagner, and E. L. Reinherz. 1999. Structure of a heterophilic adhesion complex between the human CD2 and CD58 (LFA-3) counterreceptors. Cell 97: 791-803.
7. Meuer, S. C., R. E. Hussey, M. Fabbi, D. Fox, O. Acuto, K. A. Fitzgerald, J. C. Hodgdon, J. P. Protentis, S. F. Schlossman, and E. L. Reinherz. 1984. An alternative pathway of T-cell activation: a functional role for the 50 kd T11 sheep erythrocyte receptor protein. Cell 36: 897-906.
8. Clark, S. J., D. A. Law, D. J. Paterson, M. Puklavec, and A. F. Williams. 1988. Activation of rat T lymphocytes by anti-CD2 monoclonal antibodies. J. Exp. Med. 167: 1861-1872.
9. Gollob, J. A., J. Li, H. Kawasaki, J. F. Daley, C. Groves, E. L. Reinherz, and J. Ritz. 1996. Molecular interaction between CD58 and CD2 counter-receptors mediates the ability of monocytes to augment T cell activation by IL-12. J. Immunol. 157: 1886-1893.
10. Boussiotis, V. A., G. J. Freeman, J. D. Griffin, G. S. Gray, J. G. Gribben, and L. M. Nadler. 1994. CD2 is involved in maintenance and reversal of human alloantigen- specific clonal anergy. J. Exp. Med. 180: 1665-1673.
11. Carmo, A. M., M. A. A. Castro, and F. A. Arosa. 1999. CD2 and CD3 associate independently with CD5 and differentially regulate signaling through CD5 in Jurkat T cells. J. Immunol. 163: 4238-4245.
12. Castro, M. A. A., P. A. Tavares, M. S. Almeida, R. J. Nunes, M. D. Wright, D. Mason, A. Moreira, and A. M. Carmo. 2002. CD2 physically associates with CD5 in rat T lymphocytes with the involvement of both extracellular and intracellular domains. Eur. J. Immunol. 32: 1509-1518.
13. + T cells. Blood 89: 1308-1318.
14. Bierer, B. E., J. Barbosa, S. Herrmann, and S. J. Burakoff. 1988. Interaction of CD2 with its ligand, LFA-3, in human T cell proliferation. J. Immunol. 140: 3358-3363.
15. Chang, H. C., P. Moingeon, P. Lopez, H. Krasnow, C. Stebbins, and E. L. Reinherz. 1989. Dissection of the human CD2 intracellular domain. Identification of a segment required for signal transduction and interleukin 2 production. J. Exp. Med. 169: 2073-2083.
16. Chang, H. C., P. Moingeon, R. Pedersen, J. Lucich, C. Stebbins, and E. L. Reinherz. 1990. Involvement of the PPPGHR motif in T cell activation via CD2. J. Exp. Med. 172: 351-355.
17. He, Q., A. D. Beyers, A. N. Barclay, and A. F. Williams. 1988. A role in transmembrane signaling for the cytoplasmic domain of the CD2 T lymphocyte surface antigen. Cell 54: 979-984.
18. Bell, G. M., J. B. Bolen, and J. B. Imboden. 1992. Association of Src-like protein tyrosine kinases with the CD2 cell surface molecule in rat T lymphocytes and natural killer cells. Mol. Cell Biol. 12: 5548-5554.
19. fyn. Eur. J. Immunol. 23: 2196-2201.
20. fyn with the T lymphocyte costimulatory receptor CD2: binding of the Fyn Src homology (SH) 3 domain is regulated by the Fyn SH2 domain. J. Biol. Chem. 273: 19914-19921.
21. lck binds to proline-rich sequences in the cytoplasmic domain of CD2. J. Exp. Med. 183: 169-178.
22. Freund, C., R. Kuhne, H. Yang, S. Park, E. L. Reinherz, and G. Wagner. 2002. Dynamic interaction of CD2 with the GYF and the SH3 domain of compartmentalized effector molecules. EMBO J. 21: 5985-5995.
23. 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.
24. Li, J., K. Nishizawa, W. An, R. E. Hussey, F. E. Lialios, R. Salgia, R. Sunder-Plassmann, and E. L. Reinherz. 1998. A cdc15-like adaptor protein (CD2BP1) interacts with the CD2 cytoplasmic domain and regulates CD2-triggered adhesion. EMBO J. 17: 7320-7336.
25. Nishizawa, K., C. Freund, J. Li, G. Wagner, and E. L. Reinherz. 1998. Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc. Natl. Acad. Sci. USA 95: 14897-14902.
26. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387: 569-572.
27. Zhang, W., R. P. Trible, and L. E. Samelson. 1998. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9: 239-246.
28. Brdicka, T., D. Pavlistová, A. Leo, E. Bruyns, V. Korínek, P. Angelisová, J. Scherer, A. Shevchenko, I. Hilgert, J. Cerný, et al. 2000. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 191: 1591-1604.
29. Filipp, D., J. Zhang, B. L. Leung, A. Shaw, S. D. Levin, A. Veillette, and M. Julius. 2003. Regulation of Fyn through translocation of activated Lck into lipid rafts. J. Exp. Med. 197: 1221-1227.
30. Alonso, M. A., and J. Millan. 2001. The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J. Cell Sci. 114: 3957-3965.
31. Mestas, J., and C. C. W. Hughes. 2001. Endothelial cell costimulation of T cell activation through CD58-CD2 interactions involves lipid raft aggregation. J. Immunol. 167: 4378-4385.
32. Yashiro-Ohtani, Y., X.-Y. Zhou, K. Toyo-oka, X.-G. Tai, C.-S. Park, T. Hamaoka, R. Abe, K. Miyake, and H. Fujiwara. 2000. Non-CD28 costimulatory molecules present in T cell rafts induce T cell costimulation by enhancing the association of TCR with rafts. J. Immunol. 164: 1251-1259.
33. Viola, A., S. Schroeder, Y. Sakakibara, and A. Lanzavecchia. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283: 680-682.
34. Yang, H., and E. L. Reinherz. 2001. Dynamic recruitment of human CD2 into lipid rafts: linkage to T cell signal transduction. J. Biol. Chem. 276: 18775-18785.
35. Jefferies, W. A., J. R. Green, and A. F. Williams. 1985. Authentic T helper CD4 (W3/25) antigen on rat peritoneal macrophages. J. Exp. Med. 162: 117-127.
36. Conzelmann, A., P. Corthesy, M. Cianfriglia, A. Silva, and M. Nabholz. 1982. Hybrids between rat lymphoma and mouse T cells with inducible cytolytic activity. Nature 298: 170-172.
37. Weiss, A., R. L. Wiskocil, and J. D. Stobo. 1984. The role of T3 surface molecules in the activation of human T cells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J. Immunol. 133: 123-128.
38. Beyers, A. D., A. N. Barclay, D. A. Law, Q. He, and A. F. Williams. 1989. Activation of T lymphocytes via monoclonal antibodies against rat cell surface antigens with particular reference to CD2 antigen. Immunol. Rev. 111: 59-77.
39. Straus, D. B., and A. Weiss. 1992. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 70: 585-593.
40. lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60: 755-765.
41. Kabouridis, P. S., A. I. Magee, and S. C. Ley. 1997. S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO J. 16: 4983-4998.
42. Castro, M. A. A., R. J. Nunes, M. I. Oliveira, P. A. Tavares, C. Simões, J. R. Parnes, A. Moreira, and A. M. Carmo. 2003. OX52 is the rat homologue of CD6: evidence for an effector function in the regulation of CD5 phosphorylation. J. Leukocyte Biol. 73: 183-190.
43. McGlade, C. J., M. L. Tremblay, S. P. Yee, R. Ross, and P. E. Branton. 1987. Acylation of the 176R (19-kilodalton) early region 1B protein of human adenovirus type 5. J. Virol. 61: 3227-3234.
44. lck. J. Biol. Chem. 268: 8669-8674.
45. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17: 5334-5348.
46. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8: 723-732.
47. Nunes, R. J., M. A. A. Castro, and A. M. Carmo. 2006. Protein crosstalk in lipid rafts. Adv. Exp. Med. Biol. 584: 127-136.
48. Xavier, R., and B. Seed. 1999. Membrane compartmentation and the response to antigen. Curr. Opin. Immunol. 11: 265-269.
49. Sharma, P., R. Varma, R. C. Sarasij Ira, K. Gousset, G. Krishnamoorthy, M. Rao, and S. Mayor. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-589.
50. Douglass, A. D., and R. D. Vale. 2005. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121: 937-950.
51. Bierer, B. E., R. E. Bogart, and S. J. Burakoff. 1990. Partial deletions of the cytoplasmic domain of CD2 result in a partial defect in signal transduction. J. Immunol. 144: 785-789.
52. Yang, H., and E. L. Reinherz. 2006. CD2BP1 modulates CD2-dependent T cell activation via linkage to protein tyrosine phosphatase (PTP)-PEST. J. Immunol. 176: 5898-5907.
53. Zeyda, M., G. Staffler, V. Horejsi, W. Waldhausl, and T. M. Stulnig. 2002. LAT displacement from lipid rafts as a molecular mechanism for the inhibition of T cell signaling by polyunsaturated fatty acids. J. Biol. Chem. 277: 28418-28423.
54. s protein α subunit after activation by the β-adrenergic receptor or cholera toxin. J. Biol. Chem. 268: 23769-23772.
55. 7 receptors. J. Neurosci. 24: 10502-10510.
56. Omary, M. B., and I. S. Trowbridge. 1981. Covalent binding of fatty acid to the transferrin receptor in cultured human cells. J. Biol. Chem. 256: 4715-4718.
57. 2+ ion links the cytoplasmic tail of CD4 and the N-terminal region of Lck. J. Biol. Chem. 273: 18729-18733.