Home LiteratureArticle Details
PMID: 7791764 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Interactions of Cbl with Grb2 and phosphatidylinositol 3'-kinase in activated Jurkat cells.

Molecular and cellular biology ·Vol. 15 ·No. 7 ·1995-07-00 ·Pages 3571-8

Meisner H, Conway BR, Hartley D, Czech MP

Abstract

T-cell receptor (TCR) cross-linking increases tyrosine phosphorylation of multiple proteins, only a few of which have been identified. One of the most rapidly tyrosine-phosphorylated polypeptides is the 120-kDa product of the proto-oncogene c-cbl, a cytosolic and cytoskeletal protein containing multiple proline-rich motifs that are potential binding sites for proteins containing Src homology 3 (SH3) domains. We report here that in cultured Jurkat T cells, Cbl is coprecipitated with antibody against the adapter protein Grb2. Upon activation of Jurkat T cells via the TCR-CD3 complex, we find that high-affinity binding of Cbl requires the N-terminal SH3 domain of GST-Grb2 fusion protein but after cross-linking of the TCR-CD3 and CD4 receptors, Cbl binds equally to its SH2 domain. Grb2 antisera also precipitated p85 from serum-starved cells, while TCR activation increased p85 and tyrosine-phosphorylated Cbl but not Cbl protein in Grb2 immunocomplexes. Phosphatidylinositol (PI) 3-kinase activity was immunoprecipitated from serum-starved cells with Cbl and to a lesser extent with Grb2 antisera, and TCR cross-linking increased this activity severalfold. The PI 3-kinase activity associated with Cbl amounted to 5 to 10% of the total cellular activity that could be precipitated by p85 antisera. The Ras exchange factor Son-of-sevenless 1 (Sos-1) was not found in anti-Cbl immunoprecipitates from activated cells, and Cbl was not detectable in anti-Sos-1 precipitates, supporting the likelihood that Sos-Grb2 and Cbl-Grb2 are present as distinct complexes. Taken together, these data suggest that Cbl function in Jurkat T cells involves its constitutive association with Grb2 and its recruitment of PI 3-kinase in response to TCR activation.

MeSH Terms
Adaptor Proteins, Signal Transducing Base Sequence Blotting, Western CD3 Complex/metabolism GRB2 Adaptor Protein Lymphocyte Activation/physiology Membrane Proteins/analysis Molecular Sequence Data Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor)/metabolism Precipitin Tests Protein Binding Proteins/genetics,metabolism Proto-Oncogene Proteins/metabolism Proto-Oncogene Proteins c-cbl Receptors, Antigen, T-Cell/metabolism Recombinant Fusion Proteins/metabolism Signal Transduction Son of Sevenless Proteins T-Lymphocytes/metabolism Ubiquitin-Protein Ligases
Chemicals
Adaptor Proteins, Signal Transducing CD3 Complex GRB2 Adaptor Protein Membrane Proteins Proteins Proto-Oncogene Proteins Receptors, Antigen, T-Cell Recombinant Fusion Proteins Son of Sevenless Proteins Proto-Oncogene Proteins c-cbl Ubiquitin-Protein Ligases Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor)
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Meisner H
Department of Biochemistry and Molecular Biology, University of Massachusetts Medical School, Worcester 01605, USA.
Conway B R
Hartley D
Czech M P
References (46)
46 references, click to expand
  1. The SH3 domain of p56lck is involved in binding to phosphatidylinositol 3'-kinase from T lymphocytes.
    Mol Cell Biol. 1993 Dec;13(12):7408-17 PMID: 7504174
  2. Increases in tyrosine phosphorylation are detectable before phospholipase C activation after T cell receptor stimulation.
    J Immunol. 1990 Mar 1;144(5):1591-9 PMID: 1689750
  3. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal.
    Cell. 1990 Sep 7;62(5):1019-29 PMID: 2203532
  4. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling.
    Nature. 1993 May 6;363(6424):85-8 PMID: 8479541
  5. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor.
    Mol Cell Biol. 1994 Aug;14(8):5192-201 PMID: 7518560
  6. Multiple kinases mediate T-cell-receptor signaling.
    Trends Biochem Sci. 1995 Feb;20(2):59-64 PMID: 7701563
  7. GRB2 and phospholipase C-gamma 1 associate with a 36- to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation.
    Mol Cell Biol. 1994 Jul;14(7):4435-42 PMID: 7516467
  8. Two-step TCR zeta/CD3-CD4 and CD28 signaling in T cells: SH2/SH3 domains, protein-tyrosine and lipid kinases.
    Immunol Today. 1994 May;15(5):225-34 PMID: 8024683
  9. The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor.
    J Biol Chem. 1994 Sep 16;269(37):22921-4 PMID: 8083187
  10. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3443-7 PMID: 7512734
  11. Association of the fyn protein-tyrosine kinase with the T-cell antigen receptor.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4358-62 PMID: 2190221
  12. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav.
    Mol Cell Biol. 1994 Apr;14(4):2777-85 PMID: 7511210
  13. Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2.
    J Biol Chem. 1994 Jun 10;269(23):16009-14 PMID: 8206897
  14. The CD3 chains of the T cell antigen receptor associate with the ZAP-70 tyrosine kinase and are tyrosine phosphorylated after receptor stimulation.
    J Exp Med. 1993 Nov 1;178(5):1523-30 PMID: 7693848
  15. In vivo association of Grb2 with pp116, a substrate of the T cell antigen receptor-activated protein tyrosine kinase.
    J Biol Chem. 1994 Aug 26;269(34):21608-13 PMID: 8063801
  16. The sequences of the human and mouse c-cbl proto-oncogenes show v-cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif.
    Oncogene. 1991 Apr;6(4):653-7 PMID: 2030914
  17. The truncation that generated the v-cbl oncogene reveals an ability for nuclear transport, DNA binding and acute transformation.
    EMBO J. 1993 May;12(5):2017-26 PMID: 8491192
  18. Phosphatidylinositol 3'-kinase is activated by association with IRS-1 during insulin stimulation.
    EMBO J. 1992 Sep;11(9):3469-79 PMID: 1380456
  19. Involvement of phosphatidylinositol 3-kinase in Fc gamma receptor signaling.
    J Biol Chem. 1994 Sep 9;269(36):22732-7 PMID: 7521331
  20. p56lck-independent activation and tyrosine phosphorylation of p72syk by T-cell antigen receptor/CD3 stimulation.
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5301-5 PMID: 7515496
  21. Rapid T-cell receptor-mediated tyrosine phosphorylation of p120, an Fyn/Lck Src homology 3 domain-binding protein.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4135-9 PMID: 7514295
  22. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases.
    Nature. 1992 Dec 17;360(6405):689-92 PMID: 1465135
  23. Disruption of PDGF receptor trafficking by mutation of its PI-3 kinase binding sites.
    Science. 1994 Feb 4;263(5147):684-7 PMID: 8303278
  24. Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation.
    Science. 1993 Nov 5;262(5135):902-5 PMID: 8235613
  25. Signal transduction by lymphocyte antigen receptors.
    Cell. 1994 Jan 28;76(2):263-74 PMID: 8293463
  26. Src-homology 3 domain of protein kinase p59fyn mediates binding to phosphatidylinositol 3-kinase in T cells.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7366-70 PMID: 8394019
  27. SH2 and SH3 domains: from structure to function.
    Cell. 1992 Oct 30;71(3):359-62 PMID: 1423600
  28. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells.
    Cell. 1989 Apr 7;57(1):167-75 PMID: 2467744
  29. Tumour induction by activated abl involves tyrosine phosphorylation of the product of the cbl oncogene.
    EMBO J. 1994 Oct 3;13(19):4515-23 PMID: 7925293
  30. Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Dec;10(12):6742-54 PMID: 2247081
  31. The IRS-1 signaling system.
    Trends Biochem Sci. 1994 Jul;19(7):289-93 PMID: 8048169
  32. Physical association between Src homology 3 elements and the protein product of the c-cbl proto-oncogene.
    J Biol Chem. 1994 Jul 1;269(26):17363-6 PMID: 7517397
  33. Regulation of src family tyrosine kinases in lymphocytes.
    Trends Biochem Sci. 1993 Jun;18(6):215-20 PMID: 7688486
  34. Antigen receptor tail clue.
    Nature. 1989 Mar 30;338(6214):383-4 PMID: 2927501
  35. Binding of the Ras activator son of sevenless to insulin receptor substrate-1 signaling complexes.
    Science. 1993 Jun 25;260(5116):1950-2 PMID: 8391166
  36. Association of phosphatidylinositol 3-kinase with a specific sequence of the T cell receptor zeta chain is dependent on T cell activation.
    J Biol Chem. 1994 May 27;269(21):15140-6 PMID: 8195151
  37. Cell surface molecules and early events involved in human T lymphocyte activation.
    Adv Immunol. 1987;41:1-38 PMID: 2961214
  38. Regulation of D-3 phosphoinositides during T cell activation via the T cell antigen receptor/CD3 complex and CD2 antigens.
    Eur J Immunol. 1992 Jan;22(1):45-9 PMID: 1346114
  39. Signalling through SH2 and SH3 domains.
    Trends Cell Biol. 1993 Jan;3(1):8-13 PMID: 14731533
  40. SH3 domains of the adapter molecule Grb2 complex with two proteins in T cells: the guanine nucleotide exchange protein Sos and a 75-kDa protein that is a substrate for T cell antigen receptor-activated tyrosine kinases.
    J Biol Chem. 1994 May 13;269(19):14081-7 PMID: 8188688
  41. Phosphatidylinositol 3-kinase.
    Bioessays. 1994 Aug;16(8):565-76 PMID: 8086005
  42. Common elements in interleukin 4 and insulin signaling pathways in factor-dependent hematopoietic cells.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4032-6 PMID: 7683417
  43. Physical and functional interactions between SH2 and SH3 domains of the Src family protein tyrosine kinase p59fyn.
    Mol Cell Biol. 1994 Sep;14(9):6372-85 PMID: 7520528
  44. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation.
    Nature. 1993 May 6;363(6424):45-51 PMID: 8479536
  45. Tyrosine kinases and tyrosine-based activation motifs. Current research on activation via the T cell antigen receptor.
    J Biol Chem. 1992 Dec 15;267(35):24913-6 PMID: 1459994
  46. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction.
    Cell. 1992 Jul 10;70(1):93-104 PMID: 1623525
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1995-07-00
Pages
3571-8
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC230594
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com