Home LiteratureArticle Details
PMID: 7623828 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A functional T-cell receptor signaling pathway is required for p95vav activity.

Molecular and cellular biology ·Vol. 15 ·No. 8 ·1995-08-00 ·Pages 4337-46

Wu J, Katzav S, Weiss A

Abstract

Stimulation of the T-cell antigen receptor (TCR) induces activation of multiple tyrosine kinases, resulting in phosphorylation of numerous intracellular substrates. One substrate is p95vav, which is expressed exclusively in hematopoietic and trophoblast cells. It contains a number of structural motifs, including Src homology 2, Src homology 3, and pleckstrin homology domains and a putative guanine nucleotide exchange domain. The role of p95vav in TCR-mediated signaling processes is unclear. Here, we show that overexpression of p95vav alone in Jurkat T cells leads to activation of the nuclear factors, including NFAT, involved in interleukin-2 expression. Furthermore, p95vav synergizes with TCR stimulation in inducing NFAT- and interleukin-2-dependent transcription. In contrast, NFAT activation by a G-protein-coupled receptor is not modulated by p95vav overexpression, suggesting that the effect is specific to the TCR signaling pathways. Although removal of the first 67 amino acids of p95vav activates its transforming potential in NIH 3T3 cells, this region appears to be required for its function in T cells. We further demonstrate that the p95vav-induced NFAT activation is not mimicked by Ras activation, though its function is dependent upon Ras and Raf. Furthermore, the activating function of p95vav is blocked by FK506, suggesting that its activity also depends on calcineurin. To further dissect p95vav involvement in TCR signaling, we analyzed various Jurkat mutants deficient in TCR signaling function or TCR expression and showed that an intact TCR signaling pathway is required for p95vav to function. However, overexpression of p95vav does not appear to influence TCR-induced protein tyrosine phosphorylation or increases in cytoplasmic free calcium. Taken together, our data suggest that p95vav plays an important role at an yet unidentified proximal position in the TCR signaling cascade.

MeSH Terms
Calcineurin Calcium/metabolism Calmodulin-Binding Proteins/metabolism Cell Cycle Proteins DNA-Binding Proteins/metabolism GTP-Binding Proteins/metabolism Humans Interleukin-2/biosynthesis,genetics NFATC Transcription Factors Nuclear Proteins Oncogene Proteins/genetics,metabolism Phosphoprotein Phosphatases/metabolism Promoter Regions, Genetic/genetics Proto-Oncogene Proteins/genetics,metabolism Proto-Oncogene Proteins c-vav Receptors, Antigen, T-Cell/metabolism Recombinant Proteins/metabolism Signal Transduction Structure-Activity Relationship T-Lymphocytes/physiology Transcription Factors/metabolism Transcription, Genetic ras Proteins/metabolism
Chemicals
Calmodulin-Binding Proteins Cell Cycle Proteins DNA-Binding Proteins Interleukin-2 NFATC Transcription Factors Nuclear Proteins Oncogene Proteins Proto-Oncogene Proteins Proto-Oncogene Proteins c-vav Receptors, Antigen, T-Cell Recombinant Proteins Transcription Factors VAV1 protein, human Calcineurin Phosphoprotein Phosphatases GTP-Binding Proteins ras Proteins Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wu J
Department of Microbiology and Immunology, University of California, San Francisco 94143, USA.
Katzav S
Weiss A
References (65)
65 references, click to expand
  1. Mechanism of activation of the vav protooncogene.
    Cell Growth Differ. 1991 Feb;2(2):95-105 PMID: 2069873
  2. Raf-1 is required for T cell IL2 production.
    EMBO J. 1993 Nov;12(11):4367-73 PMID: 8223446
  3. 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
  4. How receptor tyrosine kinases activate Ras.
    Trends Biochem Sci. 1993 Aug;18(8):273-5 PMID: 8236435
  5. The PH domain: a common piece in the structural patchwork of signalling proteins.
    Trends Biochem Sci. 1993 Sep;18(9):343-8 PMID: 8236453
  6. Proteins regulating Ras and its relatives.
    Nature. 1993 Dec 16;366(6456):643-54 PMID: 8259209
  7. 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
  8. Activation of Ras in vitro and in intact fibroblasts by the Vav guanine nucleotide exchange protein.
    Mol Cell Biol. 1994 Feb;14(2):906-13 PMID: 8289830
  9. Signal transduction by lymphocyte antigen receptors.
    Cell. 1994 Jan 28;76(2):263-74 PMID: 8293463
  10. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases.
    Science. 1994 Feb 25;263(5150):1136-9 PMID: 7509083
  11. Tyrosine phosphorylation and activation of Vav GTP/GDP exchange activity in antigen receptor-triggered B cells.
    J Immunol. 1994 Mar 1;152(5):2123-9 PMID: 8133029
  12. Zinc finger domains and phorbol ester pharmacophore. Analysis of binding to mutated form of protein kinase C zeta and the vav and c-raf proto-oncogene products.
    J Biol Chem. 1994 Apr 15;269(15):11590-4 PMID: 8157692
  13. The T-cell antigen receptor utilizes Lck, Raf-1, and MEK-1 for activating mitogen-activated protein kinase. Evidence for the existence of a second protein kinase C-dependent pathway in an Lck-negative Jurkat cell mutant.
    J Biol Chem. 1994 Jun 24;269(25):17349-57 PMID: 7516337
  14. 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
  15. Direct stimulation of Vav guanine nucleotide exchange activity for Ras by phorbol esters and diglycerides.
    Mol Cell Biol. 1994 Jul;14(7):4749-58 PMID: 7516472
  16. 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
  17. Novel signaling pathway suggested by SH3 domain-mediated p95vav/heterogeneous ribonucleoprotein K interaction.
    J Biol Chem. 1994 Aug 12;269(32):20225-8 PMID: 8051112
  18. Calcium signalling in T cells stimulated by a cyclophilin B-binding protein.
    Nature. 1994 Sep 22;371(6495):355-8 PMID: 7522304
  19. 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
  20. The protein tyrosine kinase ZAP-70 can associate with the SH2 domain of proto-Vav.
    J Biol Chem. 1994 Dec 23;269(51):32579-85 PMID: 7798261
  21. Interaction of Shc with Grb2 regulates association of Grb2 with mSOS.
    Mol Cell Biol. 1995 Feb;15(2):593-600 PMID: 7529871
  22. The vav proto-oncogene is required early in embryogenesis but not for hematopoietic development in vitro.
    EMBO J. 1995 Jan 3;14(1):1-11 PMID: 7828581
  23. Association of the vav proto-oncogene product with poly(rC)-specific RNA-binding proteins.
    Mol Cell Biol. 1995 Mar;15(3):1324-32 PMID: 7862126
  24. The small GTPases Rac and Rho as regulators of secretion in mast cells.
    Curr Biol. 1995 Jan 1;5(1):68-73 PMID: 7697350
  25. 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
  26. 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
  27. Defective T-cell receptor signalling and positive selection of Vav-deficient CD4+ CD8+ thymocytes.
    Nature. 1995 Mar 30;374(6521):474-7 PMID: 7700360
  28. Requirement for the coexpression of T3 and the T cell antigen receptor on a malignant human T cell line.
    J Exp Med. 1984 Nov 1;160(5):1284-99 PMID: 6208306
  29. Reconstitution of an active surface T3/T-cell antigen receptor by DNA transfer.
    Nature. 1985 Aug 15-21;316(6029):606-9 PMID: 4033759
  30. Isolation and characterization of a T-lymphocyte somatic mutant with altered signal transduction by the antigen receptor.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6879-83 PMID: 3309950
  31. Characterization of antigen receptor response elements within the interleukin-2 enhancer.
    Mol Cell Biol. 1988 Apr;8(4):1715-24 PMID: 3260003
  32. At least two non-antigen-binding molecules are required for signal transduction by the T-cell antigen receptor.
    Proc Natl Acad Sci U S A. 1988 Nov;85(22):8613-7 PMID: 3263650
  33. vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells.
    EMBO J. 1989 Aug;8(8):2283-90 PMID: 2477241
  34. Function of a heterologous muscarinic receptor in T cell antigen receptor signal transduction mutants.
    J Biol Chem. 1989 Oct 15;264(29):17190-7 PMID: 2529257
  35. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation.
    Science. 1989 Dec 22;246(4937):1617-20 PMID: 2595372
  36. Increase of the catalytic activity of phospholipase C-gamma 1 by tyrosine phosphorylation.
    Science. 1990 Nov 30;250(4985):1253-6 PMID: 1700866
  37. The cytoplasmic domain of the T cell receptor zeta chain is sufficient to couple to receptor-associated signal transduction pathways.
    Cell. 1991 Mar 8;64(5):891-901 PMID: 1705867
  38. Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway.
    Nature. 1990 Jul 5;346(6279):66-8 PMID: 2164155
  39. Stimulation of p21ras upon T-cell activation.
    Nature. 1990 Aug 23;346(6286):719-23 PMID: 2201921
  40. pEF-BOS, a powerful mammalian expression vector.
    Nucleic Acids Res. 1990 Sep 11;18(17):5322 PMID: 1698283
  41. Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7722-6 PMID: 2217205
  42. Stimulation of the phosphatidylinositol pathway can induce T-cell activation.
    Nature. 1990 Nov 1;348(6296):66-9 PMID: 2234059
  43. Product of vav proto-oncogene defines a new class of tyrosine protein kinase substrates.
    Nature. 1992 Mar 5;356(6364):68-71 PMID: 1311423
  44. Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs.
    Nature. 1992 Mar 5;356(6364):71-4 PMID: 1531699
  45. Sequence requirements for induction of cytolysis by the T cell antigen/Fc receptor zeta chain.
    Cell. 1992 Mar 6;68(5):889-97 PMID: 1547489
  46. The products of the mcf-2 and vav proto-oncogenes and of the yeast gene cdc-24 share sequence similarities.
    Oncogene. 1992 Mar;7(3):585-7 PMID: 1549372
  47. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3686-90 PMID: 1373887
  48. Tyrosine phosphorylation of the vav proto-oncogene product in activated B cells.
    Science. 1992 May 22;256(5060):1196-9 PMID: 1375396
  49. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin.
    Nature. 1992 Jun 25;357(6380):692-4 PMID: 1377361
  50. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation.
    Nature. 1992 Jun 25;357(6380):695-7 PMID: 1377362
  51. Proto-vav and gene expression.
    Nature. 1992 Jul 9;358(6382):113 PMID: 1614545
  52. 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
  53. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  54. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling.
    Cell. 1992 Aug 7;70(3):401-10 PMID: 1643658
  55. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor.
    Cell. 1992 Aug 21;70(4):585-93 PMID: 1505025
  56. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain.
    Cell. 1992 Nov 13;71(4):649-62 PMID: 1423621
  57. p21ras mediates control of IL-2 gene promoter function in T cell activation.
    EMBO J. 1992 Dec;11(12):4549-56 PMID: 1425589
  58. CD45 specifically modulates binding of Lck to a phosphopeptide encompassing the negative regulatory tyrosine of Lck.
    EMBO J. 1993 Jan;12(1):315-21 PMID: 8428589
  59. Tyrosine kinase-stimulated guanine nucleotide exchange activity of Vav in T cell activation.
    Science. 1993 May 7;260(5109):822-5 PMID: 8484124
  60. Interleukin-2 induces tyrosine phosphorylation of the vav proto-oncogene product in human T cells: lack of requirement for the tyrosine kinase lck.
    Biochem J. 1993 Sep 1;294 ( Pt 2):339-42 PMID: 7690544
  61. Loss of the amino-terminal helix-loop-helix domain of the vav proto-oncogene activates its transforming potential.
    Mol Cell Biol. 1991 Apr;11(4):1912-20 PMID: 2005887
  62. Tyrosine phosphatase CD45 is required for T-cell antigen receptor and CD2-mediated activation of a protein tyrosine kinase and interleukin 2 production.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2037-41 PMID: 1672451
  63. Signaling via the inositol phospholipid pathway by T cell antigen receptor is limited by receptor number.
    J Immunol. 1991 May 1;146(9):2935-43 PMID: 1826700
  64. A hemopoietic specific gene encoding a small GTP binding protein is overexpressed during T cell activation.
    Biochem Biophys Res Commun. 1991 Mar 15;175(2):451-8 PMID: 1902092
  65. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins.
    Science. 1991 May 3;252(5006):668-74 PMID: 1708916
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1995-08-00
Pages
4337-46
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC230673
Subset
IM
Grants
NIGMS NIH HHS · GM 44493 · 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: product@genelibs.com