CD16-mediated p21ras activation is associated with Shc and p36 tyrosine phosphorylation and their binding with Grb2 in human natural killer cells

Journal of Experimental Medicine

Volumn 183, Issue 1, 1996, Pages 179-186

  Galandrini, Ricciarda ^a   Palmieri, Gabriella ^a,b   Piccoli, Mario ^a   Frati, Luigi ^a,d   Santoni, Angela ^a,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Biotechnology Section

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d IRCCS NEUROMED   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CELL PROTEIN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; PHOSPHOPROTEIN; RAS PROTEIN; FC RECEPTOR; GRB2 PROTEIN, HUMAN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HRAS PROTEIN, HUMAN; HYBRID PROTEIN; PROTEIN; PROTEIN P21; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SRC HOMOLOGY 2 DOMAIN CONTAINING, TRANSFORMING PROTEIN 1; SRC HOMOLOGY 2 DOMAIN-CONTAINING, TRANSFORMING PROTEIN 1; TYROSINE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; HUMAN; HUMAN CELL; KINETICS; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; DRUG EFFECT; IMMUNOBLOTTING; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SERODIAGNOSIS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; GRB2 ADAPTOR PROTEIN; HUMANS; IMMUNOBLOTTING; INTERLEUKIN-2; KILLER CELLS, NATURAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN BINDING; PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTORS, IGG; RECEPTORS, INTERLEUKIN-2; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TYROSINE;

EID: 0029671267     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.183.1.179     Document Type: Article

References (54)

1. Trinchieri, G. 1990. Biology of natural killer cells. Adv. Immunol. 47:187-376.
2. Ravetch, J.V., and J.P. Kinet. 1991. Fc receptors. Annu. Rev. Immunol. 9:457-492.
3. Perussia, B., G. Trinchieri, A. Jackson, N.L. Warner, J. Faust, H. Rumpold, D. Kraft, and L. Lanier. 1984. The Fc receptor for IgG on human natural killler cells: phenotypic, functional and comparative studies using monoclonal antibody. J. Immunol. 133:180-189.
4. O'Shea, J.J., A.M. Weissman, I.C.S. Kennedy, and J.R. Ortaldo. 1991. Engagement of the natural killer cell IgG Fc receptor results in tyrosine phosphorylation of the ζ chain. Proc. Natl. Acad. Sci USA. 88:350-354.
5. Vivier, E., P. Morin, C. O'Brian, B. Druker, S.F. Schlossman, and P. Anderson. 1991. Tyrosine phosphorylation of FcγRIII (CD16): ζ complex in human natural killer cells. Induction by Ab-dependent cytotoxicity but not by natural killing. J. Immunol. 146:206-210.
6. Ting, A.T., L.M. Karnitz, R.A. Schoon, R.T. Abraham, and P J. Leibson. 1992. Fcγ receptor activation induces the tyrosine phosphorylation of both phospholipase C (PLC)-γ1 and PLC-γ2 in natural killer cells. J. Exp. Med. 176:1751-1755.
7. lck acavation. J. Exp. Med. 176:1745-1750.
8. Bonnema, B.J.D., L.M. Karnitz, R.A. Schoon, R.T. Abraham, and P. Leibson. 1994. Fc receptor stimulation of phosphatidylinositol-3 kinase in natural killer cells is associated with protein kinase C-independent granule release and cell-mediated cytotoxicity. J. Exp. Med. 180:1427-1435.
9. Kanakaraj, P., B. Duckworth, L. Azzoni, M. Kamoun, L.C. Cantley, and B. Perussia. 1994. Phosphatidylinositol-3 kinase activation induced upon FcγRIIIA-ligand interaction. J. Exp. Med. 179:551-558.
10. Balboa, M.A., J. Balsinde, J. Aramburu, F. Mollinedo, and M. López-Botet. 1992. Phospholipase D activation in human natural killer cells through the Kp43 and CD16 surface antigens takes place by different mechanisms. Involvement of the phospholipase D pathway in tumor necrosis factor α synthesis J Exp. Med. 176:9-17.
11. 2+ in FcγR (CD16)-induced transcription and expression of lymphokine genes. J. Exp. Med. 169:549-567.
12. Downward, J. 1992. Regulatory mechanisms for ras proteins. Bioessays. 14:177-184.
13. Bogusky, M.S., and F. McCormick. 1993. Proteins regulating Ras and its relatives. Nature (Lond.). 366:643-654.
14. Bowtell, D., P. Fu, M. Simon, and P. Senior. 1992. Identification of murine homologues of the Drosophila Son of sevenless: potential activators of Ras. Proc. Natl. Acad. Sci. USA. 89 6511-6515.
15. Downward, J. 1994. The GRB/Sem-5 adaptor protein. FEBS (Fed. Eur. Biochem. Soc.) Lett. 338:113-117.
16. Lammers, R., A. Ullrich, E.Y. Skolnick, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to Ras signaling Cell. 70:431-442.
17. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P.G. Pelicci. 1992. A transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell. 70-93-104.
18. Skolnik, E.Y., C.-H. Lee, A. Batzer, L.M. Vicentini, M. Zhou, R. Daly, M.J. Myers, Jr., J.M. Baker, A. Ullrich, M.F. White, and J. Schlessinger. 1993. The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and Shc: implications for insulin control of Ras signaling. EMBO (Eur. Mol. Biol. Organ.) J. 12:1929-1935.
19. ras. Mol. Cell. Biol. 14:1575-1581.
20. Basu, T., P.H. Warne, and J. Downward. 1994. Role of Shc in the activation of ras in response to epidermal growth ractor and nerve growth factor. Oncogene. 9:3483-3491.
21. Ravichandran, K.S., K.K. Lee, Z. Songyang, L.C. Cantley, P. Burn, and S.J. Burakoff. 1993. Interaction of Shc with the ζ chain of the T cell receptor upon T cell activation. Science (Wash. DC). 262:902-905.
22. Sieh, M., A. Batzer, J. Schlessinger, and A. Weiss. 1994. GRB2 and phospholipase C-γ1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol. Cell. Biol. 14:4435-4442.
23. Smit, L., M.M. de Vries-Smits, J.L. Bos, and J. Borst. 1994. B cell antigen receptor stimulation induces formation of a Shc-Grb2 complex containing multiple tyrosine-phosphorylated proteins. J. Biol. Chem. 269:20209-20212.
24. ras oncoprotein activators SHC and mSos1 as well as assembly of complexes containing SHC, Grb2, mSos1 and a 145-kDa tyrosine-phosphorylated protein. J. Immunol. 153:623-636.
25. shc in T lymphocytes. J. Biol. Chem. 268:17659-17661.
26. Ravichandran, K.S., and S.J. Burakoff. 1994. The adaptor protein Shc interacts with the interleukin-2 (IL-2) receptor upon IL-2 stimulation. J. Biol. Chem. 269:1599-1602.
27. Liu, L., J.E. Damen, R.L. Cutler, and G. Krystal. 1994. Multiple cytokines stimulate the binding of a common 145-kilodalton protein to Shc at the Grb2 recognition site of Shc. Mol. Cell. Biol. 14:6926-6935.
28. Buday, L., S.E. Egan, P.R. Viciana, D.A. Cantrell, and J. Downward. 1994. A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane bound tyrosine phosphoprotein is implicated in Ras activation in T cells. J. Biol. Chem. 269:9019-9023.
29. Gismondi, A., M. Milella, G. Palmieri M. Piccoli, L. Frati, and A. Santoni. 1995. Stimulation of protein tyrosine phosphorylation by interaction of NK cells with fibronectin via α4β1 and α5β1. J. Immunol. 154:3128-3137.
30. ras upon T-cell activation. Nature (Lond.). 346:719-723.
31. Kavanaugh, W.M., and L.T. Williams. 1994. An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science (Wash. DC). 266:1862-1865.
32. Lankester, A.C., G.M.V. van Schijndel, P.M.L. Rood, A.J. Verhoeven, and R.A.W. van Lier. 1994. B cell antigen receptor cross-linking induces tyrosine phosphorylation and membrane translocation ot a multimeric Shc complex that is augmented by CD19 co-ligation. Eur. J. Immunol. 24:2818-2825.
33. Rudd, C.E., J.M. Trevillyand, J.D. Dasgupta, L.L. Wong, and S.F. Schlossman, 1988. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc. Natl. Acad. Sci. USA. 85:5190-5194.
34. lck. Cell. 55:301-308.
35. Van Noesel, C.J.M., A.C. Lankester, G.M.V. Van Schijndel, and R.A.W. Van Lier. 1993. The CR2/CD19 complex on human B cells contains the src-family kinase lyn. Int. Immunol. 5:699-705.
36. Baldari, C.T., G. Pelicci, M.M. Di Somma, E. Milia, S. Giuli, P.G. Pelicci, and J.L. Telford. 1995. Inhibition of CD4/p56lck signaling by a dominant negative mutant of the Shc adaptor protein. Oncogene. 10:1141-1147.
37. Ravichandran, K.S., U. Lorentz, S.E. Shoelson, and S.J. Burakoff. 1995. Interaction of Shc with Grb2 regulates association of Grb2 with mSos. Mol Cell. Biol. 15:593-600.
38. Weng, Z., S.M. Thomas, R.J. Rickles, J.A. Taylor, A.W. Brauer, C. Seidel-Dugan, W.M. Michael, G. Dreyfuss, and G.S. Brudge. 1994. Identification of Src, Fyn, and Lyn SH3-binding proteins: implication for a function of SH3 domains. Mol. Cell. Biol. 14:4509-4521.
39. McGlade, J., A. Cheng, G. Pelicci, P.G. Pelicci, and T. Pawson. 1992. Shc proteins are phosphorylated and regulated by the v-Src and v-Fps protein-tyrosine kinases. Proc. Natl. Acad. Sci. USA. 89:8869-8873.
40. Salcedo, T.W., T. Kurosaki, P Kanakaraj, J.V. Ravetch, and B. Perussia. 1993. Physical and functional association of p56lck with FcγRIIIA (CD16) in natural killer cells. J. Exp. Med. 177:1475-1480.
41. lck: identification of an intermolecular association. Science (Wash. DC). 252:1523-1528.
42. Gilliland, L.K., G.L. Schieven, N.A. Norris, S.B. Kanner, A. Aruffo, and J.A. Ledbetter. 1992. Lymphocyte lineage-restricted tyrosine-phosphorylated proteins that bind PLCγ1 SH2 domains. J. Biol. Chem. 267:13610-13616.
43. Rodewald, H.-R., P. Moingeon, J.L. Lucich, C. Dosiou, P. Lopez, and E.L. Reinherz. 1992. A population of early fetal thymocytes expressing FcγRII/III contains precursors of T lymphocytes and natural killer cells. Cell. 69:139-150.
44. Sánchez, M.J., M.O. Muench, M.G. Roncarolo, L.L. Lanier, and J.H. Phillips. 1994. Identification of a common T/natural killer cell progenitor in human fetal thymus. J Exp. Med. 180:569-576.
45. ras J. Biol. Chem 269.32621-32625.
46. Sasaoka, T., B. Draznin, J.W. Leitner, W.J. Langlois, and J M. Olefsky. 1994. Shc is the predominant signaling molecule coupling insulin receptors to activation of guanine nucleotide releasing factor and p21ras-GTP formation. J. Biol. Chem. 269:10734-10738.
47. Lanier, L.L., D.W. Buck, L. Rhodes, A. Ding, E. Evans, C. Barney, and J.H. Phillips. 1988. Interleukin-2 activation of natural killer cells rapidly induces the expression and phosphorylation of the Leu-23 activation antigen. J. Exp. Med. 167:1572-1585.
48. Borrego, F., J. Pena, and R. Solana. 1993. Regulation of CD69 expression on human natural killer cells: differential involvement of protein kinase C and protein tyrosine kinases. Eur. J. Immunol. 23:1039-1043.
49. Egan, S.E., and R.A. Weinberg. 1993. The pathway to signal achievement. Nature (Lond.). 365:781-783.
50. Bourne, H.R., D.A. Sanders, and F. McCormick. 1991. The GTPase superfamily: conserved structure and molecular mechanisms. Nature (Lond.). 349:117-127.
51. Hill, C.S., and R. Treisman. 1995. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell. 80:199-211.
52. ras mediates control of IL2 gene promoter function in T cell activation. EMBO (Eur. Mol. Biol. Organ.) J. 11:4549-4556.
53. D'Ambrosio, D., D.A. Cantrell, L. Frati, A. Santoni, and R. Testi. 1994. Involvement of p21ras activation in T cell CD69 expression. Eur. J. Immunol. 24:616-620.
54. Izquierdo, M., R. Karin, and D.A. Cantrell. 1995. The regulation and function of p21 ras during T-cell activation and growth. Immunol. Today. 16:159-164.