T-cell stimulation through the T-cell receptor/CD3 complex regulates CD2 lateral mobility by a calcium/calmodulin-dependent mechanism

Biophysical Journal

Volumn 76, Issue 3, 1999, Pages 1679-1692

  Liu, Si Qiong J ^a   Golan, David E ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM; CALMODULIN INHIBITOR; CD2 ANTIGEN; CD3 ANTIGEN; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE INHIBITOR; T LYMPHOCYTE RECEPTOR;

ARTICLE; BINDING AFFINITY; CALCIUM CELL LEVEL; CELL ADHESION; CELL STIMULATION; CELL SURFACE; CONTROLLED STUDY; CROSS LINKING; DEPHOSPHORYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIGAND BINDING; PHOSPHORYLATION; PROTEIN IMMOBILIZATION; REGULATORY MECHANISM; T LYMPHOCYTE;

EID: 0033021690     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77327-3     Document Type: Article

References (70)

1. Alexander, D., J. Goris, R. Marais, J. Rothbard, W. Merlevede, and M. J. Crumpton. 1989. Dephosphorylation of the human T lymphocyle CD3 antigen. Eur. J. Biochem. 181:55-65.
2. Arulanandam, A. R., P. Moingeon, M. F. Concino, M. A. Recny, K. Kato, H. Yagita, S. Koyasu, and E. L. Reinherz. 1993. A soluble multimeric recombinant CD2 protein identifies CD48 as a low affinity ligand for human CD2: divergence of CD2 ligands during the evolution of humans and mice. J. Exp. Med. 177:1439-1450.
3. Axelrod, D., D. E. Koppel, J. Schlessinger, E. Elson, and W. W. Webb. 1976. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1055-1069.
4. Bernard, A., R. W. Knowles, K. Naito, B. Dupont, B. Raynal, H. C. Tran, and L. Boumsell. 1986. A unique epitope on the CD2 molecule defined by the monoclonal antibody 9-1: epitope-specific modulation of the E-rosette receptor and effects on T-cell functions. Hum. Immunol. 17: 388-405.
5. Bierer, B. E., S. H. Herrmann, C. S. Brown, D. E. Golan, and S. J. Burakoff. 1989. A monoclonal antibody to LFA-3, the CD-2 ligand, specifically immobilizes major histocompatibility complex proteins. Eur. J. Immunol. 19:661-5.
6. Bierer, B. E., G. Holländer, D. Fruman, and S. J. Burakoff. 1993. Cyclosporin A and FK506: molecular mechanisms of immunosuppression and probe for transplantation biology. Curr. Opin. Immunol. 5:763-773.
7. Bierer, B. E., S. L. Schreiber, and S. J. Burakoff. 1991. The effects of the immunosuppressant FK-506 on alternate pathways of T cell activation. Eur. J. Immunol. 21:439-445.
8. 2+/calmodulin-dependent protein kinase type II. Biochem. Biophys. Res. Commun. 198:67-73.
9. Boniface, J. J., and M. M. Davis. 1995. T cell recognition of antigen: a process controlled by transient intermolecular interactions. Ann. N.Y. Acad. Sci. 766:62-69.
10. Chan, P.-Y., M. B. Lawrence, M. L. Dustin, L. M. Ferguson, D. E. Golan, and T. A. Springer. 1991. Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2. J. Cell Biol. 115:245-255.
11. Clipstone, N. A., and G. R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature. 357: 695-697.
12. Cohen, P. 1989. The structure and regulation of protein phosphatases. Annu. Rev. Biochem. 58:453-508.
13. 2+-ATPase activity. J. Clin. Invest. 71:579-586.
14. Deckert, M., J. Kubar, D. Zoccola, G. Bernard-Pomier, P. Angelisova, V. Horejsi, and A. Bernard. 1992. CD59 molecule: a second ligand for CD2 in T cell adhesion. Eur. J. Immunol. 22:2943-2947.
15. Donnadieu, E., G. Bismuth, and A. Trautmann. 1994. Antigen recognition by helper T cells elicits a sequence of distinct changes of their shape and intracellular calcium. Curr. Biol. 4:584-595.
16. Dustin, M. L., L. M. Ferguson, P.-Y. Chan, T. A. Springer, and D. E. Golan. 1996. Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area. J. Cell Biol. 132:465-474.
17. Dustin, M. L., and T. A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 341: 619-624.
18. Dutz, J. P., D. A. Fruman, S. J. Burakoff, and B. E. Bierer. 1993. A role for calcineurin in degranulation of murine cytotoxic T lymphocytes. J. Immunol. 150:2591-2598.
19. Elliott, J. F., Y. Lin, S. B. Mizel, R. C. Bleackley, D. G. Harnish, and V. Paetkau. 1984. Induction of interleukin 2 messenger RNA inhibited by cyclosporin A. Science. 226:1439-1441.
20. Emmel, E. A., C. L. Verweij, D. B. Durand, K. M. Higgins, E. Lacy, and G. R. Crabtree. 1989. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science. 246:1617-1620.
21. Flanagan, W. M., B. Corthesy, R. J. Bram, and G. R. Crabtree. 1991. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature. 352:803-807.
22. Fruman, D. A., C. B. Klee, B. E. Bierer, and S. J. Burakoff. 1992. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc. Natl. Acad. Sci. USA. 89:3686-3690.
23. Golan, D. E., C. S. Brown, C. M. L. Cianci, S. T. Furlong, and J. P. Caulfield. 1986. Schistosomula of Schistosoma mansoni use lysophosphatidylcholine to lyse adherent human red blood cells and immobilize red cell membrane components. J. Cell Biol. 103:819-828.
24. Golding, J. W. 1976. Conjugation of antibodies with fluorochromes: modifications to the standard methods. J. Immunol. Methods. 13:215-226.
25. Granelli-Piperno, A., L. Andrus, and R. M. Steinman. 1986. Lymphokine and nonlymphokine mRNA levels in stimulated human T cells: kinetics, mitogen requirements, and effects of cyclosporin A. J. Exp. Med. 163: 922-937.
26. Hahn, W. C., S. J. Burakoff, and B. E. Bierer. 1993. Signal transduction pathways involved in T cell receptor-induced regulation of CD2 avidity for CD58. J. Immunol. 150:2607-2619.
27. Hahn, W. C., E. Menu, A. L. M. Bothwell, P. J. Sims, and B. E. Bierer. 1992. Overlapping but nonidentical binding sites on CD2 for CD58 and a second ligand CD59. Science. 256:1805-1807.
28. 1+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61:559-601.
29. Hashemi, B., T. J. Feder, W. W. Webb, D. Holowka, and B. A. Baird. 1992. Diffusion and distribution measurements of the T cell receptor complex under stimulating and non-stimulating conditions. Biophys. J. 61:A147.
30. Hashimoto, Y., and T. R. Soderling. 1989. Regulation of calcineurin by phosphorylation. J. Biol. Chem. 264:16524-16529.
31. Hendey, B., C. B. Klee, and F. R. Maxfield. 1992. Inhibition of neutrophil chemokinesis on vitronectin by inhibitors of calcineurin. Science. 258: 296-299.
32. Hubbard, M. J., and C. B. Klee. 1989. Functional domain structure of calcineurin A: mapping by limited proteolysis. Biochemistry. 28: 1868-1874.
33. Ingerbritsen, T. S., and P. Cohen. 1983. Protein phosphatases: properties and role in cellular regulation. Science. 221:331-338.
34. 2+-calmodulin-dependent protein kinase II inhibitor on GABA release in cerebrospinal fluid of the rat. J. Pharmacol. Exp. Ther. 154:598-602.
35. Johansson, B., M. P. Wymann, K. Holmgren-Peterson, and K. E. Magnusson. 1993. N-Formyl peptide receptors in human neutrophils display distinct membrane distribution and lateral mobility when labeled with agonist and antagonist. J. Cell Biol. 121:1281-1289.
36. Kao, J. P. Y., A. T. Harootunian, and R. Y. Tsien. 1989. Photochemically generated cytosolic calcium pulses and their detection by fluo-3. J. Biol. Chem. 264:8179-8184.
37. Kato, K., M. Koyanagi, H. Okada, T. Takanashi, Y. Wong, A. Williams, K. Okumura, and H. Yagita. 1992. CD48 is a counter-receptor for mouse CD2 and is involved in T cell activation. J. Exp. Med. 176:1241-1249.
38. Kino, T., H. Hatanaka, M. Hashimoto, M. Nishiyama, T. Goto, M. Okuhara, M. Kohsaka, H. Aoki, and H. Imanaka. 1987a. FK-506, novel immunosuppressant isolated from a Streptomyces. I. Fermentation, isolation, and physico-chemical and biological characteristics. J. Antibiot. (Tokyo). 40:1249-1255.
39. Kino, T., H. Hatanaka, S. Miyata, N. Inamura, M. Nishiyama, T. Yajima, T. Goto, M. Okuhara, M. Kohsaka, H. Aoki, and H. Imanaka. 1987b. FK-506, novel immunosuppressant isolated from a Streptomyces. II. Immunosuppressive effect of FK-506 in vitro. J. Antibiot. (Tokyo). 40:1256-1265.
40. Klee, C. B. 1991. Concerted regulation of protein phosphorylation and dephosphorylation by calmodulin. Neurochem. Res. 16:1059-1065.
41. Klee, C. B., G. F. Draetta, and M. J. Hubbard. 1988. Calcineurin. Adv. Enzymol. Relat. Areas Mol. Biol. 61:149-200.
42. Koyasu, S., T. Lawton, D. Novick, M. A. Recny, R. F. Siliciano, B. P. Wallner, and E. L. Reinherz. 1990. Role of interaction of CD2 molecules with lymphocyte function-associated antigen 3 in T-cell recognition of nominal antigen. Proc. Natl. Acad. Sci. USA. 87:2603-2607.
43. Kronke, M., W. J. Leonard, J. M. Depper, S. K. Arya, F. Wong-Staal, R. C. Gallo, T. A. Waldmann, and W. C. Greene. 1984. Cyclosporin A inhibits T-cell growth factor gene expression at the level of mRNA transcription. Proc. Natl Acad. Sci. USA. 81:5214-5218.
44. 2+- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature. 377:75-797
45. Lee, T.-P., J. Venuti, I. Macara, R. Kawauchi, P. J. Davis, and B. K. Mookerjee. 1987. Characteristics of calmodulin binding to purified human lymphocyte plasma membranes. J. Immunol. 139:42-48.
46. Liu, J., M. W. Albers, T. J. Wandless, S. Luan, D. G. Alberg, P. J. Belshaw, P. Cohen, C. MacKintosh, C. B. Klee, and S. L. Schreiber. 1992. Inhibition of T cell signalling by immunophilin-ligand complexes correlates with loss of calcineurin phosphatase activity. Biochemistry. 31: 3896-3901.
47. Liu, J., J. D. Farmer, W. S. Lane, J. Friedman, I. Weissman, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66:807-815.
48. 2+ mobilization upon CD2-mediated T cell activation. Biophys. J. 68:459-470.
49. Martz, E. 1977. Mechanism of specific tumor-cell lysis by alloimmune T lymphocytes: resolution and characterization of discrete steps in the cellular interaction. Contemp. Top. Immunobiol. 7:301-361.
50. Martz, E., W. Heagy, and S. H. Gromkowski. 1983. The mechanism of CTL-mediated killing: monoclonal antibody analysis of the roles of killer and target-cell membrane proteins. Immunol. Rev. 72:73-96.
51. Negulescu, P. A., T. B. Krasieva, A. Khan, H. H. Kerschbaum, and M. D. Cahalan. 1996. Polarity of T cell shape, mobility, and sensibility to antigen. Immunity. 4:421-430.
52. 2+/calmodulin-dependent protein kinase: expression in multiple tissues. J. Biol. Chem. 268:5471-5479.
53. i in individual cytolytic T cells and targets. EMBO J 6:2223-2232.
54. Premack, B. A., and P. Gardner. 1992. Signal transduction by T-cell receptors: mobilization of Ca and regulation of Ca-dependent effector molecules. Am. J. Physiol. 263:C1119-C1140.
55. Sanchez-Madrid, F., A. M. Krensky, C. F. Ware, E. Robbins, J. L. Strominger, S. J. Burakoff, and T. A. Springer. 1982. Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3. Proc. Natl. Acad. Sci. USA. 79:7489-7493.
56. Schreiber, S. L. 1991. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science. 251:283-287.
57. Schreiber, S. L., and G. R. Crabtree. 1992. The mechanism of action of cyclosporin A and FK506. Immunol. Today. 13:136-142.
58. 2+/calmodulin-dependent protein kinases. Curr. Opin. Cell Biol. 5:247-253.
59. Schulman, H., P. I. Hanson, and T. Meyer. 1992. Decoding calcium signals by multifunctional CaM kinase. Cell Calcium. 13:401-411.
60. Shaw, A. S., and M. L. Dustin. 1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:361-369.
61. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature. 346:425-434.
62. Stolpen, A. H., D. E. Golan, and J. S. Pober. 1988. Tumor necrosis factor and immune interferon act in concert to slow the lateral diffusion of proteins and lipids in human endothelial cell membranes. J. Cell Biol. 107:781-789.
63. Thatte, H. S., K. R. Bridges, and D. E. Golan. 1994. Microtubule inhibitors differentially affect translational movement, cell surface expression, and endocytosis of transferrin receptors in K562 cells. J. Cell. Physiol. 160:345-357.
64. Thomson, A. W. 1989. FK-506: how much potential? Immunol. Today. 10:6-9.
65. Tocci, M. J., D. A. Matkovich, K. A. Collier, P. Kwok, F. Dumont, S. Lin, S. Degudicibus, J. J. Siekierka, J. Chin, and N. I. Jutchinson. 1989. The immunosuppressant FK506 selectively inhibits expression of early T cell activation genes. J. Immunol. 143:718-726.
66. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 265:4315-4320.
67. Valverde, I., A. Sener, P. Lebrun, A. Herchuelz, and W. J. Malaisse. 1981. The stimulus-secretion coupling of glucose-induced insulin release. XLVII. The possible role of calmodulin. Endocrinology. 108:1305-1312.
68. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell. 76:263-274.
69. Wulfing, C., J. D. Rabinowitz, C. Beeson, M. D. Sjaastad, H. M. McConnell, and M. M. Davis. 1997. Kinetics and extent of T cell activation as measured with the calcium signal. J. Exp. Med. 185:1815-1825.
70. Yang, S. Y., S. Rhee, G. Angelos, and B. Dupont. 1987. Functional analysis of CD2 (T, p50) epitopes detected by 24 CD2 antibodies. In Leucocyte Typing III. White Cell Differentiation Antigens. A. J. McMichael, P. C. L. Beverley, S. Cobbold, M. J. Crumpton, W. Gilks, F. M. Gotch, N. Hogg, M. Horton, N. Ling, I. C. M. MacLennan, D. Y. Mason, C. Milstein, D. Spiegelhalter, and H. Waldmann, editors. Oxford University Press, Oxford. 113-116.