A receptor/cytoskeletal movement triggered by costimulation during T cell activation

Science

Volumn 282, Issue 5397, 1998, Pages 2266-2269

  Wülfing, Christoph ^a   Davis, Mark M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; MYOSIN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL INTERACTION; CELL MIGRATION; CYTOSKELETON; GENE EXPRESSION; IMMUNE RESPONSE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, CD86; BIOTINYLATION; CALCIUM; CHO CELLS; CRICETINAE; CYTOSKELETON; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MEMBRANE GLYCOPROTEINS; MICE; MICROSPHERES; MOLECULAR MOTOR PROTEINS; MYOSINS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0032545218     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.282.5397.2266     Document Type: Article

References (66)

1. S. Demotz, H. M. Grey, A. Sette, Science 249, 1028 (1990); C. V. Harding and E. R. Unanue, Nature 346, 574 (1990); R. C. Brower et al., Mol. Immunol. 31, 1285 (1994); Y. Sykulev, M. Joo, I. Vturina, T. J. Tsomides, H. N. Eisen, Immunity 4, 565 (1996); J. Delon, N. Bercovici, G. Raposo, R. Liblau, A. Trautmann, J. Exp. Med. 188, 1473 (1998).
2. S. Demotz, H. M. Grey, A. Sette, Science 249, 1028 (1990); C. V. Harding and E. R. Unanue, Nature 346, 574 (1990); R. C. Brower et al., Mol. Immunol. 31, 1285 (1994); Y. Sykulev, M. Joo, I. Vturina, T. J. Tsomides, H. N. Eisen, Immunity 4, 565 (1996); J. Delon, N. Bercovici, G. Raposo, R. Liblau, A. Trautmann, J. Exp. Med. 188, 1473 (1998).
3. S. Demotz, H. M. Grey, A. Sette, Science 249, 1028 (1990); C. V. Harding and E. R. Unanue, Nature 346, 574 (1990); R. C. Brower et al., Mol. Immunol. 31, 1285 (1994); Y. Sykulev, M. Joo, I. Vturina, T. J. Tsomides, H. N. Eisen, Immunity 4, 565 (1996); J. Delon, N. Bercovici, G. Raposo, R. Liblau, A. Trautmann, J. Exp. Med. 188, 1473 (1998).
4. S. Demotz, H. M. Grey, A. Sette, Science 249, 1028 (1990); C. V. Harding and E. R. Unanue, Nature 346, 574 (1990); R. C. Brower et al., Mol. Immunol. 31, 1285 (1994); Y. Sykulev, M. Joo, I. Vturina, T. J. Tsomides, H. N. Eisen, Immunity 4, 565 (1996); J. Delon, N. Bercovici, G. Raposo, R. Liblau, A. Trautmann, J. Exp. Med. 188, 1473 (1998).
5. S. Demotz, H. M. Grey, A. Sette, Science 249, 1028 (1990); C. V. Harding and E. R. Unanue, Nature 346, 574 (1990); R. C. Brower et al., Mol. Immunol. 31, 1285 (1994); Y. Sykulev, M. Joo, I. Vturina, T. J. Tsomides, H. N. Eisen, Immunity 4, 565 (1996); J. Delon, N. Bercovici, G. Raposo, R. Liblau, A. Trautmann, J. Exp. Med. 188, 1473 (1998).
6. S. Valitutti, S. Müller, M. Cella, E. Padovan, A. Lanzavecchia, Nature 375, 148 (1995); S. Valitutti, S. Müller, M. Salio, A. Lanzavecchia, J. Exp. Med. 185, 1859 (1997).
7. S. Valitutti, S. Müller, M. Cella, E. Padovan, A. Lanzavecchia, Nature 375, 148 (1995); S. Valitutti, S. Müller, M. Salio, A. Lanzavecchia, J. Exp. Med. 185, 1859 (1997).
8. S. Valitutti, M. Dessing, K. Aktories, H. Gallati, A. Lanzavecchia, J. Exp. Med. 181, 577 (1995).
9. G. Iezzi, K. Karjalainen, A. Lanzavecchia, Immunity 8, 89 (1998); L. J. Holsinger et al., Curr. Biol. 8, 563 (1998).
10. G. Iezzi, K. Karjalainen, A. Lanzavecchia, Immunity 8, 89 (1998); L. J. Holsinger et al., Curr. Biol. 8, 563 (1998).
11. C. G. Sagerstrom, E. M. Kerr, J. P. Allison, M. M. Davis, Proc. Natl. Acad. Sci. U.S.A. 90, 8987 (1993); M. Croft and C. Dubey, Crit. Rev. Immunol. 17, 89 (1997); S. L. Swain et al., Immunol. Rev. 150, 143 (1996); M. F. Bachmam et al., Immunity 7, 549 (1997).
12. C. G. Sagerstrom, E. M. Kerr, J. P. Allison, M. M. Davis, Proc. Natl. Acad. Sci. U.S.A. 90, 8987 (1993); M. Croft and C. Dubey, Crit. Rev. Immunol. 17, 89 (1997); S. L. Swain et al., Immunol. Rev. 150, 143 (1996); M. F. Bachmam et al., Immunity 7, 549 (1997).
13. C. G. Sagerstrom, E. M. Kerr, J. P. Allison, M. M. Davis, Proc. Natl. Acad. Sci. U.S.A. 90, 8987 (1993); M. Croft and C. Dubey, Crit. Rev. Immunol. 17, 89 (1997); S. L. Swain et al., Immunol. Rev. 150, 143 (1996); M. F. Bachmam et al., Immunity 7, 549 (1997).
14. C. G. Sagerstrom, E. M. Kerr, J. P. Allison, M. M. Davis, Proc. Natl. Acad. Sci. U.S.A. 90, 8987 (1993); M. Croft and C. Dubey, Crit. Rev. Immunol. 17, 89 (1997); S. L. Swain et al., Immunol. Rev. 150, 143 (1996); M. F. Bachmam et al., Immunity 7, 549 (1997).
15. C. A. Chambers and J. P. Allison, Curr. Opin. Immunol. 9, 396 (1997); P. J. Blair et al., Biochem. Soc. Trans. 25, 651 (1997);
16. C. A. Chambers and J. P. Allison, Curr. Opin. Immunol. 9, 396 (1997); P. J. Blair et al., Biochem. Soc. Trans. 25, 651 (1997);
17. A. I. Sperling and J. A. Bluestone, Immunol. Rev. 153, 155 (1996).
18. M. L. Dustin and T. A. Springer, Nature 341, 619 (1989); Y. van Kooyk and C. G. Figdor, Biochem. Soc. Trans. 25, 515 (1997); M. Stewart and N. Hogg, J. Cell. Biochem. 61, 554 (1996).
19. M. L. Dustin and T. A. Springer, Nature 341, 619 (1989); Y. van Kooyk and C. G. Figdor, Biochem. Soc. Trans. 25, 515 (1997); M. Stewart and N. Hogg, J. Cell. Biochem. 61, 554 (1996).
20. M. L. Dustin and T. A. Springer, Nature 341, 619 (1989); Y. van Kooyk and C. G. Figdor, Biochem. Soc. Trans. 25, 515 (1997); M. Stewart and N. Hogg, J. Cell. Biochem. 61, 554 (1996).
21. A. Kupfer and S. J. Singer, Annu. Rev. Immunol. 7, 309 (1989); C. R. Monks, B. A. Freiberg, H. Kupfer, N. Sciaky, A. Kupfer, Nature 395, 82 (1998).
22. A. Kupfer and S. J. Singer, Annu. Rev. Immunol. 7, 309 (1989); C. R. Monks, B. A. Freiberg, H. Kupfer, N. Sciaky, A. Kupfer, Nature 395, 82 (1998).
23. C. Wülfing, M. D. Sjaastad, M. M. Davis, Proc. Natl. Acad. Sci. U.S.A. 95, 6302 (1998).
24. S. J. Singer, Science 255, 1671 (1992).
25. As reviewed by M. D. Sheets, R. Simson, K. Jacobson, Curr. Opin. Cell Biol. 7, 707 (1995); M. S. Bretscher, Cell 87, 601 (1996).
26. As reviewed by M. D. Sheets, R. Simson, K. Jacobson, Curr. Opin. Cell Biol. 7, 707 (1995); M. S. Bretscher, Cell 87, 601 (1996).
27. 7 beads. For microscopy, beads were used at a 2:1 ratio over T cells. Half of the beads were preincubated with the T cells at 4°C; the other half were added to the T cells on the microscopy stage.
28. H. Xu et al., J. Exp. Med. 180, 95 (1994); J. E. Sligh Jr. et al., Proc. Natl. Acad. Sci. U.S.A. 90, 8529 (1993).
29. H. Xu et al., J. Exp. Med. 180, 95 (1994); J. E. Sligh Jr. et al., Proc. Natl. Acad. Sci. U.S.A. 90, 8529 (1993).
30. B. F. Holifield, A. Ishinara, K. Jacobson, J. Cell Biol. 111, 2499 (1990); D. A. Lauffenberger and A. F. Horwitz, Cell 84, 359 (1996).
31. B. F. Holifield, A. Ishinara, K. Jacobson, J. Cell Biol. 111, 2499 (1990); D. A. Lauffenberger and A. F. Horwitz, Cell 84, 359 (1996).
32. R. A. Seder, W. E. Paul, M. M. Davis, B. Fazekas de St. Groth, J. Exp. Med. 176, 1091 (1992).
33. C. Wülfing and M. M. Davis, data not shown.
34. P. A. Negulescu, T. B. Krasieva, A. Khan, H. H. Kerschbaum, M. D. Cahalan, Immunity 4, 421 (1996).
35. 2 at 4°C, they were used within 2 hours. Streptavidin-coated Dynabeads (M280; Dynal) were used as described for the YN1-coated beads.
36. A. E. Ting and R. E. Pagano, J. Biol. Chem. 265, 5337 (1990).
37. 2.
38. J. P. Heath and B. F. Holifield, Symp. Soc. Exp. Biol. 47, 35 (1993).
39. C. Wülfing and M. M. Davis, unpublished data.
40. P. Kuhlman, V. T. Moy, B. A. Lollo, A. A. Brian, J. Immunol. 146, 1773 (1991); S. B. Kanner, L. S. Grosmaire, J. A. Ledbetter, N. K. Damle, Proc. Natl. Acad. Sci. U.S.A. 90, 7099 (1993).
41. P. Kuhlman, V. T. Moy, B. A. Lollo, A. A. Brian, J. Immunol. 146, 1773 (1991); S. B. Kanner, L. S. Grosmaire, J. A. Ledbetter, N. K. Damle, Proc. Natl. Acad. Sci. U.S.A. 90, 7099 (1993).
42. S. C. Ward, C. H. June, D. Olive, Immunol. Today 17, 187 (1996); A. Toker and L. C. Cantley, Nature 387, 673 (1997).
43. S. C. Ward, C. H. June, D. Olive, Immunol. Today 17, 187 (1996); A. Toker and L. C. Cantley, Nature 387, 673 (1997).
44. H. Yano et al., J. Biol. Chem. 268, 25846 (1993); R. Woscholski, T. Kodaki, M. McKinnon, M. D. Waterfield, P. J. Parker, FEBS Lett. 342, 109 (1994).
45. H. Yano et al., J. Biol. Chem. 268, 25846 (1993); R. Woscholski, T. Kodaki, M. McKinnon, M. D. Waterfield, P. J. Parker, FEBS Lett. 342, 109 (1994).
46. As reviewed by M. F. Cartier and D. Pantaloni, J. Mol. Biol. 269, 459 (1997); S. K. Maciver, Bioessays 18, 179 (1996).
47. As reviewed by M. F. Cartier and D. Pantaloni, J. Mol. Biol. 269, 459 (1997); S. K. Maciver, Bioessays 18, 179 (1996).
48. L. P. Cramer and T. J. Mitchison, J. Cell Biol. 131, 179 (1995).
49. L. C. Schlichter, P. A. Pahapill, I. Chung, J. Pharmacol. Exp. Ther. 261, 438 (1992).
50. S. Grissmer et al., Mol. Pharmacol. 45, 1227 (1994).
51. J. A. Verbeugen, F. Le Deist, V. Devignot, H. Korn, Cell Calcium 21, 1 (1997) and references therein.
52. F. Takei, J. Immunol. 134, 1403 (1985).
53. J. T. Groves, C. Wülfing, S. G. Boxer, Biophys. J. 71, 2716 (1996).
54. K. Miyake et al., J. Cell Biol. 114, 557 (1991); K. Miyake, I. L. Weissman, J. S. Greenberger, P. W. Kincade, J. Exp. Med. 173, 599 (1991).
55. K. Miyake et al., J. Cell Biol. 114, 557 (1991); K. Miyake, I. L. Weissman, J. S. Greenberger, P. W. Kincade, J. Exp. Med. 173, 599 (1991).
56. The results are derived from a composite analysis of at least seven experiments (11 on average) performed on at least two different days (four on average) for each condition. We show a composite analysis because on average only three or four cells per experiment could be analyzed. To ensure consistency within the data set at least one positive control experiment was included during each day of experiments.
57. The CH27 cells used in this particular experiment were ICAM-1-GFP transfected. ICAM-1-GFP transfection of the CH27 cells has no effect on the bead movement (16). The ICAM-1-GFP fluorescence is not shown.
58. Peptide loading of APCs using 10 μM moth cytochrome c peptide 82-103, Fura-2 loading of T cells, and microscopy (using the Zeiss/Attoftuor system) were performed as in (9).
59. Movie 1: Bead movement toward the interface. The interaction of 5C.C7 T cells, loaded with 4.5-μm anti-ICAM-1 (YN1) beads, with peptide-loaded CH27 B cell lymphoma cells (35) is shown. The CH27 cell is substantially larger than the T cells. Although the beads are bound to the posterior end of the top T cell before and at the time of its activation, they can be seen to move toward the T cell-B cell interface in subsequent frames. The T cell intracellular calcium concentration is overlaid in a false color scale. Two closely related calcium-sensitive dyes that differ in their calcium dissociation constant, Fura-PE in movie 1 and Fura-2 in movie 2, have been used. Therefore, blue indicates low calcium concentration in both movies, whereas high calcium concentration is encoded in yellow in movie 1 and in red in movie 2. For reasons of simplicity, in Fig. 1 the calcium color scale has been changed from the original one of movie 1 to match that of movie 2/Fig. 2. The movie compresses 20 min of experiment into 1 min of movie.
60. Movie 2: T cell-APC interaction with blocked myosin motor proteins. The interaction of 5C.C7 T cells, loaded with 4.5-μm anti-ICAM-1 (YN1) beads, with peptide-loaded, ICAM-1-GFP-transfected CH27 B cell lymphoma in the presence of 2 mM BDM is shown. A bright-field series of images has been duplicated and is overlaid with false-color encoded fluorescence information. The top panel is overlaid with a false-color representation of the intracellular calcium concentration of the T cell, ranging from blue (low concentration) to red (high concentration). In the bottom panel, the ICAM-1-GFP fluorescence of the B cell lymphoma is overlaid in a false color scale from green (low fluorescence) to blue (high fluorescence) to allow the simultaneous investigation of an additional cellular parameter. The movie shows that in the presence of 2 μM BDM, although the calcium signal is elevated in a stable manner and ICAM-1-GFP accumulates at the T cell-B cell interface, this interface is narrow (as most easily seen by the tightly concentrated ICAM-1-GFP accumulation) and no bead movement is seen. The movie compresses 20 min of experiment into 1 min of movie.
61. Three categories of bead movement were observed. Movement toward the interface was defined as bead movement at least one-fourth of a T cell circumference toward the interface (as shown in Fig. 1). Movement away from the interface was defined as bead movement at least one-fourth of a T cell circumference away from the interface, indicative of random bead movement Beads located at the interface at the moment of T cell activation constituted <25% of all beads bound to T cells, consistent with the observation that migrating T cells move the beads toward their posterior. The only exception occurs after treatment with the Pl 3-kinase inhibitor wortmannin, when 75% of the beads are already at the interface at the time of T cell activation, indicative of a lack of polarization. In this case, the beads are likely to initiate the cell-cell interaction by binding to ICAM-1 on both cells simultaneously. Beads that started at the interface stay there without exception. Beads that are scored "no movement" are those that move less than one-fourth of a T cell circumference in at least 5 min (Fig. 2).
62. 2+ at 5 mM. and both were added directly to the microscopy dish. T cells were preloaded with BAPTA in parallel with Fura-2 at 20 μM. The ICAM-1-GFP construct has been described (9); the B7-2-GFP construct is strictly analogous, with the GFP attached to the cytoplasmic tail. Stable transfectants were selected for GFP expression using flow cytometry, and single cells were cloned.
63. Lack of T cell polarization is indicated by the fact that few activated cells had beads at the interface, by the lack of uropods and extended lamellipodia, and by the failure to migrate (16).
64. BDM (Sigma) was added to the T cells at the indicated concentrations 5 min before the start of the microscopy experiment from a fresh 200 μM stock in PBS. Noxius toxin (Alomone Labs, Jerusalem, Israel) was added to the T cells at 100 nM, that is, a 100-fold excess over the apparent dissociation concentration of blocking peak potassium channels 5 min before the start of the microscopy experiment.
65. The results were derived from a composite analysis of at least five experiments (nine on average) performed on at least three different days for each condition. As discussed in (34), composite data sets are shown because of the small number of cells per experiment that could be analyzed for some parameters. Positive controls were run on each day of the experiments to ensure uniformity.
66. We thank M. D. Sjaastad, W. J. Nelson, R. S. Lewis, and D. A. Lauffenberger for helpful discussions. Supported by the Howard Hughes Medical Institute and the European Molecular Biology Organization (C.W.).