Home LiteratureArticle Details
PMID: 7568223 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Signal transduction in T lymphocytes using a conditional allele of Sos.

Holsinger LJ, Spencer DM, Austin DJ, Schreiber SL, Crabtree GR

Abstract

While Ras activation has been shown to play an important role in signal transduction by the T-lymphocyte antigen receptor, the mechanism of its activation in T cells is unclear. Membrane localization of the guanine nucleotide exchange factor Sos, but not Vav or Dbl, was sufficient for Ras-mediated signaling in T lymphocytes. Activation of Sos appears to involve membrane recruitment and not allosteric changes, because interaction of Sos with the linking molecule Grb-2 was not required for Ras activation. To extend this analysis, we constructed a modified Sos that could be localized to the membrane inducibly by using a rationally designed chemical inducer of dimerization, FK1012. The role of Grb-2 in signaling was mimicked with this technique, which induced the association of a modified Sos with the membrane, resulting in rapid activation of Ras-induced signaling. In contrast, inducible localization of Grb-2 to the membrane did not activate signaling and suggests that the interaction of Grb-2 with Sos in T cells is subject to regulation. This conditional allele of Sos demonstrates that membrane localization of Sos is sufficient for Ras activation in T cells and indicates that the role of Grb-2 is to realize the biologic advantages of linker-mediated dimerization: enhanced specificity and favorable kinetics for signaling. This method of generating conditional alleles may also be useful in dissecting other signal transduction pathways regulated by protein localization or protein-protein interactions.

MeSH Terms
Adaptor Proteins, Signal Transducing Alleles Amino Acid Sequence Cell Compartmentation Cell Line Dose-Response Relationship, Drug Fluorescent Antibody Technique GRB2 Adaptor Protein Guanine Nucleotide Exchange Factors Humans Models, Biological Molecular Sequence Data Proteins/genetics,metabolism Recombinant Fusion Proteins Signal Transduction/genetics T-Lymphocytes/drug effects,physiology Tacrolimus/analogs & derivatives,pharmacology Transfection ras Guanine Nucleotide Exchange Factors ras Proteins/metabolism
Chemicals
Adaptor Proteins, Signal Transducing FK 1012 GRB2 Adaptor Protein GRB2 protein, human Guanine Nucleotide Exchange Factors Proteins Recombinant Fusion Proteins ras Guanine Nucleotide Exchange Factors ras Proteins Tacrolimus
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Holsinger L J
Howard Hughes Medical Institute, Stanford University School of Medicine, CA 94305, USA.
Spencer D M
Austin D J
Schreiber S L
Crabtree G R
References (42)
42 references, click to expand
  1. Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav.
    Nature. 1995 Mar 30;374(6521):467-70 PMID: 7700358
  2. 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
  3. Vav cooperates with Ras to transform rodent fibroblasts but is not a Ras GDP/GTP exchange factor.
    Oncogene. 1994 Aug;9(8):2405-13 PMID: 8036025
  4. Tyrosine kinase-stimulated guanine nucleotide exchange activity of Vav in T cell activation.
    Science. 1993 May 7;260(5109):822-5 PMID: 8484124
  5. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2.
    Science. 1993 May 28;260(5112):1338-43 PMID: 8493579
  6. 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
  7. Defective T-cell receptor signalling and positive selection of Vav-deficient CD4+ CD8+ thymocytes.
    Nature. 1995 Mar 30;374(6521):474-7 PMID: 7700360
  8. vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells.
    EMBO J. 1989 Aug;8(8):2283-90 PMID: 2477241
  9. Dbl and Vav mediate transformation via mitogen-activated protein kinase pathways that are distinct from those activated by oncogenic Ras.
    Mol Cell Biol. 1994 Oct;14(10):6848-57 PMID: 7935402
  10. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor.
    Cell. 1993 May 7;73(3):611-20 PMID: 8490966
  11. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1.
    Nature. 1993 May 6;363(6424):83-5 PMID: 8479540
  12. Membrane-targeting potentiates guanine nucleotide exchange factor CDC25 and SOS1 activation of Ras transforming activity.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8512-6 PMID: 8078913
  13. Interaction of Shc with Grb2 regulates association of Grb2 with mSOS.
    Mol Cell Biol. 1995 Feb;15(2):593-600 PMID: 7529871
  14. Stimulation of p21ras upon T-cell activation.
    Nature. 1990 Aug 23;346(6286):719-23 PMID: 2201921
  15. Signal transmission between the plasma membrane and nucleus of T lymphocytes.
    Annu Rev Biochem. 1994;63:1045-83 PMID: 7979236
  16. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene product.
    J Biol Chem. 1994 Jan 7;269(1):62-5 PMID: 8276860
  17. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1.
    Nature. 1993 Jul 22;364(6435):308-13 PMID: 8332187
  18. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos.
    Cell. 1993 Apr 9;73(1):179-91 PMID: 8462098
  19. Controlling signal transduction with synthetic ligands.
    Science. 1993 Nov 12;262(5136):1019-24 PMID: 7694365
  20. Phosphorylation of the Ras nucleotide exchange factor son of sevenless by mitogen-activated protein kinase.
    J Biol Chem. 1994 Feb 18;269(7):4717-20 PMID: 8106439
  21. Vagaries of vav.
    Curr Biol. 1992 May;2(5):275-7 PMID: 15335967
  22. A general strategy for producing conditional alleles of Src-like tyrosine kinases.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9805-9 PMID: 7568222
  23. 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
  24. Role of protein kinase C in T-cell antigen receptor regulation of p21ras: evidence that two p21ras regulatory pathways coexist in T cells.
    Mol Cell Biol. 1992 Jul;12(7):3305-12 PMID: 1620132
  25. Proteins regulating Ras and its relatives.
    Nature. 1993 Dec 16;366(6456):643-54 PMID: 8259209
  26. 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
  27. Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product.
    Nature. 1991 Nov 28;354(6351):311-4 PMID: 1956381
  28. Calcineurin is a key signaling enzyme in T lymphocyte activation and the target of the immunosuppressive drugs cyclosporin A and FK506.
    Ann N Y Acad Sci. 1993 Nov 30;696:20-30 PMID: 7509131
  29. Mammalian Ras interacts directly with the serine/threonine kinase Raf.
    Cell. 1993 Jul 16;74(1):205-14 PMID: 8334704
  30. Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs.
    Nature. 1992 Mar 5;356(6364):71-4 PMID: 1531699
  31. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK.
    Cell. 1992 Mar 20;68(6):1041-50 PMID: 1312393
  32. Membrane targeting of the nucleotide exchange factor Sos is sufficient for activating the Ras signaling pathway.
    Cell. 1994 Sep 23;78(6):949-61 PMID: 7923364
  33. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation.
    Nature. 1992 Jun 25;357(6380):695-7 PMID: 1377362
  34. 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
  35. Defective signalling through the T- and B-cell antigen receptors in lymphoid cells lacking the vav proto-oncogene.
    Nature. 1995 Mar 30;374(6521):470-3 PMID: 7700359
  36. The predicted DBL oncogene product defines a distinct class of transforming proteins.
    Proc Natl Acad Sci U S A. 1988 Apr;85(7):2061-5 PMID: 3281159
  37. 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. 1994 Mar 25;269(12):9019-23 PMID: 7510700
  38. p21ras and calcineurin synergize to regulate the nuclear factor of activated T cells.
    J Exp Med. 1993 Nov 1;178(5):1517-22 PMID: 8228805
  39. Mechanistic studies of a signaling pathway activated by the organic dimerizer FK1012.
    Chem Biol. 1994 Nov;1(3):163-72 PMID: 9383386
  40. Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells (NF-AT) complex.
    J Biol Chem. 1993 Feb 5;268(4):2917-23 PMID: 8428966
  41. The hematopoietically expressed vav proto-oncogene shares homology with the dbl GDP-GTP exchange factor, the bcr gene and a yeast gene (CDC24) involved in cytoskeletal organization.
    Oncogene. 1992 Apr;7(4):611-8 PMID: 1565462
  42. 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
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-10-10
Pages
9810-4
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC40892
Subset
IM
Grants
NCI NIH HHS · CA39612 · United States
NIGMS NIH HHS · GM-52067 · United States
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: [email protected]