The SH2-containing inositol-5'-phosphatase enhances LFA-1-mediated cell adhesion and defines two signaling pathways for LFA-1 activation

Journal of Immunology

Volumn 162, Issue 10, 1999, Pages 5792-5799

  Rey Ladino, Jose A ^a   Huber, Michael ^a   Liu, Ling ^b   Damen, Jacqueline E ^a   Krystal, Gerald ^a,c   Takei, Fumio ^a,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b ELI LILLY AND COMPANY   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 3; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE C; SH2 CONTAINING INOSITOL PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW CULTURE; CELL ADHESION; CONTROLLED STUDY; ENZYME ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL ADHESION; ERYTHROPOIETIN; HEMATOPOIETIC STEM CELLS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-3; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN BINDING; PROTEIN KINASE C; RATS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TETRADECANOYLPHORBOL ACETATE;

EID: 0033563167     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Kishimoto, T. K., R. S. Larsson, A. L. Corbi, M. L. Dustin, D. E. Staunton, and T. A. Springer. 1989. The leukocyte integrins. Adv. Immunol. 46:149.
2. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature 346:425.
3. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76:301.
4. Picker, J. L., and E. C. Butcher. 1996. Lymphocyte homing and homeostasis. Science 272:60.
5. Dustin, M. L., and T. A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341:619.
6. van Kooyk, Y., P. van de Wiel-van Kemenade, P. Weder, T. W. Kuijpers, and C. G. Figdor. 1989. Enhancement of LFA-1-mediated cell adhesion by triggering through CD2 or CD3 on T lymphocytes. Nature 342:811.
7. Dang, L. H., and K. L. Rock. 1991. Stimulation of B lymphocytes through surface Ig receptors induces LFA-1 and ICAM-1 dependent adhesion. J. Immunol. 146: 3273.
8. Koopman, G., Y. van Kooyk, M. de Graaff, C. J. Meyer, C. G. Figdor, and S. T. Pals. 1990. Triggering of the CD44 antigen on T lymphocytes promotes T cells adhesion through the LFA-1 pathway. J. Immunol. 145:3589.
9. Mourad, W., R. S. Geha, and T. Chatila. 1990. Engagement of major histocompatibility complex class II molecules induces sustained, lymphocyte function-associated molecule 1-dependent cell adhesion. J. Exp. Med. 172:1513.
10. Spertini, F., A.V.T. Wang, T. Chatila, and R. S. Geha. 1994. Engagement of the common leukocyte antigen CD45 induces homotipic adhesion of activated human T cells. J. Immunol. 153:1593.
11. Ono, M., S. Holland, P. Tempst, and J. V. Ravetch. 1996. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor FcγRIIB. Nature 383:263.
12. Damen, J. E., L. Liu, P. Rosten, R. K. Humphries, A. B. Jefferson, P. W. Majerus, and G. Krystal. 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 93:1689.
13. Ono, M., H. Okada, S. Bolland, S. Yanagi, T. Kurosaki, and J. V. Ravetch. 1997. Deletion of SHIP or SHIP-1 reveals two distinct pathways for inhibitory signaling. Cell 90:293.
14. Bolland, S., R. N. Pearse, T. Kurosaki, and J. V. Ravetch. 1998. SHIP modulates immune receptors by regulating membrane association of Btk. Immunity 8:509.
15. Huber, M., C. D. Helgason, J. E. Damen, L. Liu, and R. K. Humphries. 1998. The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc. Natl. Acad. Sci. USA 95:11330.
16. SHIP, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10:1084.
17. Kavanaugh, W. M., D. A. Pot, S. M. Chin, M. Deuter-Reinhard, A. B. Jefferson, F. A. Norris, F. R. Masiarz, L. S. Cousens, P. W. Majerus, and L. T. Williams. 1996. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 6:438.
18. Pyszniak, A. M., C. A. Welder, and F. Takei. 1994. Cell surface distribution of high-avidity LFA-1 detected by soluble ICAM-1-coated microspheres. J. Immunol. 152:5241.
19. Liu, L., J. E. Damen, M. R. Hughes, I Babic, F. R. Jirik, and G. Krystal. 1997. The Src homology 2 (SH2) domain of SH2-containing inositol phosphatase (SHIP) is essential for tyrosine phosphorylation of SHIP, its association with Shc, and its induction of apoptosis. J. Biol. Chem. 272:8983.
20. Murthy, S. C. Sorensen, P. H. B., Mui, A. L. F., and G. Krystal. 1989. Interleukin-3 down-regulates its own receptor. Blood 73:1180.
21. Wognum, A. W., P. M. Lansdorp, R. K. Humphries, and G. Krystal. 1990. Detection and isolation of the erythropoietin receptor using biotinylated erythropoietin. Blood 76:696.
22. Damen, J. E., L. Liu, R. L. Cutler, and G. Krystal. 1993. Erythropoietin stimulates the tyrosine phosphorylation of Shc and its association with Grb2 and a 145-Kd tyrosine phosphorylated protein. Blood 82:2296.
23. Jefferson, A. B., and P. W. Majerus. 1996. Mutation of the conserved domains of two inositol polyphosphate 5-phosphatases. Biochemistry 35:7890.
24. Liu, L., R. L. Cutler, A. L.-F. Mutis, and G. Krystal. 1994. Steel factor stimulates the serine/threonine phosphorylation of the interleukin-3 receptor. J. Biol. Chem. 269:16774.
25. Scheid, M. P., and V. Duronio. 1998. Dissociation of cytokine-induced phosphorylation of Bad and activation of PKB/akt: involvement of MEK upstream of Bad phosphorylation. Proc. Natl. Acad. Sci. USA 95:7439.
26. Shimizu, Y., and S. W. Hunt, III. 1996. Regulating integrin-mediated adhesion: one more function for PI3-kinase? Immunol. Today 17:565.
27. Welder, C. H., D. H. S. Lee, and F. Takei. 1993. Inhibition of cell adhesion by microspheres coated with recombinant soluble ICAM-1. J. Immunol. 150:2203.
28. Loftus, J. C., J. W. Smith, and M. H. Ginsberg. 1994. Integrin-mediated adhesion: the extracellular face. J. Biol. Chem. 269:25235.
29. Dransfield, I., C. Cabanas, A. Craig, and N. Hogg. 1992. Divalent cation regulation of the function of the leukocyte integrin LFA-1. J. Cell Biol. 116:219.
30. Herbert, J. M., J. M. Augereau, J. Gleye, and J. P. Maffrand. 1990. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochim. Biophys. Res. Commun. 172:993.
31. Lee, S. K., W. G. Qing, W. Mar, L. Luyengi, R. G. Mehta, K. Kawanishi, H. H. S. Fong, C. W. W. Beecher, A. D. Kinghorn, and J. M. Pezzuto. 1998. Angoline and chelerythrine, benzophenanthridine alkaloids that do not inhibit protein kinase C. J. Biol. Chem. 273:19829.
32. Carrol, M. P., and W. S. May. 1994. Protein kinase C-mediated serine phosphorylation directly activates Raf-1 in murine hematopoietic cells. J. Biol. Chem. 269:1249.
33. Miura, Y., O. Miura, J. N. Ihle, and N. Aoki. 1994. Activation of the mitogen-activated protein kinase pathway by the erythropoietin receptor. J. Biol. Chem. 269:29962.
34. ras GTPase-activating protein. Proc. Natl. Acad. Sci. USA 89:1587.
35. ras activation and p120GAP tyrosine phosphorylation in human erythroleukemia cells. J. Biol. Chem. 267: 8293.
36. Hartwig, J. H., G. M. Bokoch, C. L. Carpenter, P. A. Janmey, L. A. Taylor, A. Toker, and T. P. Stossel. 1995. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82:643.
37. 3 interacts with SH2 domains and modulates PI-3-kinase association with tyrosine-phosphorylated proteins. Cell 83:821.
38. 3. J Biol. Chem. 269:32358.
39. 3: a regulatory nexus between tyrosine kinases and sustained calcium signals. Cell 94:5.
40. Toker, A., and L. C. Cantley. 1997. Signaling through the lipid products of phosphoinositide-3-OH kinase. Nature 187:673.
41. Nielsen, M., A. Svejgaard, S. Skov, P. Dobson, K. Bendtzen, C. Geisler, and N. Odum. 1996. IL-2 induces β2-integrin adhesion via a wortmannin/Ly294002-sensitive rapamycin-resistant pathway. Phosphorylation of a 125-kilodalton protein correlates with induction, but not mitogenesis. J. Immunol. 157:5350.
42. Mazerolles, F., C. Barbat, and A. Fischer. 1997. Down-regulation of LFA-1-mediated T cell adhesion induced by the HIV envelope glycoprotein gp 160 requires phosphatidylinositol-3-kinase activity. Eur. J. Immunol. 27:2457.
43. 2 (LFA-1 CD11a/CD18) cytoplasmic domain/cytoskeleton interaction. J. Exp. Med. 181:315.
44. Hibbs, M. L., H. Xu, S. A. Stacker, and T. A. Springer. 1991. Regulation of adhesion of ICAM-1 by the cytoplasmic domain of LFA-1 integrin β subunit. Science 251:1611.
45. Rey-Ladino, J. A., A. M. Pyszniak, and F. Takei. 1998. Dominant-negative effect of the lymphocyte function-associated antigen-1 β (CD18) cytoplasmic domain on leukocyte adhesion to ICAM-1 and fibronectin. J. Immunol. 160:3494.
46. 2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86:233.
47. Hemings, B. A. 1997. PH domains - a universal membrane adapter. Science 275: 1899.
48. Nagel, W., L. Zeitlmann, P. Schilcher, C. Geiger, J. Kolanus, W. Kolanus. 1998. Phosphoinositide 3-OH kinase activates the β2 integrin adhesion pathway and induces membrane recruitment of cytohesin-1. J. Biol. Chem. 273:14853.
49. Franke, T., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997. Direct regulation of the AKT proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275:665.
50. + T cell adhesion to B cells. Cell. Immunol. 150:439.
51. Tominaga, T., K. Sugie, M. Hirata, N. Morii, J. Fukata, A. Uchida, H. Imura, and S. Narumiya. 1993. Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GT-binding protein, Rho-1. J. Cell Biol. 120:1529.
52. 2+ -permeable channel. Nature 355:356.
53. Stewart, M. P., C. Cabanas, and N. Hogg. 1996. T cell adhesion to intracellular molecular-1 (ICAM-1) is controlled by cell spreading and the activation of integrin LFA-1. J. Immunol. 156:1810.
54. Rothlein, R., and T. A. Springer. 1986. The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester. J. Exp. Med. 163:1132.
55. van Kooyk, Y., E. van de Wiel-van Kemenade, P. Eder, R. J. Huijbens, and C. G. Figdor. 1993. Lymphocyte function-associated antigen 1 dominates very late antigen 4 in binding of activated T cells to endothelium. J. Exp. Med. 177: 185.
56. 2+-dependent protease, calpain. J. Cell Biol. 140:699.