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PMID: 7628439 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Reconstitution of interactions between tyrosine kinases and the high affinity IgE receptor which are controlled by receptor clustering.

The EMBO journal ·Vol. 14 ·No. 14 ·1995-07-17 ·Pages 3385-94

Scharenberg AM, Lin S, Cuenod B, Yamamura H, Kinet JP

Abstract

High affinity IgE receptor (Fc epsilon RI) signaling after contact with antigen occurs in response to receptor clustering. This paper describes methodology, based on vaccinia virus driven protein expression, for probing signaling pathways and its application to Fc epsilon RI interactions with the lyn and syk tyrosine kinases. Reconstitution of the complete tetrameric Fc epsilon RI receptor, lyn and syk in a non-hematopoietic 'null' cell line is sufficient to reconstruct clustering-controlled receptor tyrosine phosphorylation and activation of syk, without apparent requirement for hematopoietic specific phosphatases. The src family kinase lyn phosphorylates Fc epsilon RI in response to receptor clustering, resulting in syk binding to the phosphorylated Fc epsilon RI. Lyn also participates in the tyrosine phosphorylation and activation of syk in a manner which is dependent on phosphorylated Fc epsilon RI. Using overexpression of active and dominant negative syk proteins in a mast cell line which naturally expresses Fc epsilon RI, we corroborate syk's role downstream of receptor phosphorylation, and demonstrate that syk SH2 domains protect receptor ITAMs from ongoing dephosphorylation. Based on these results, we propose that receptor clustering controls lyn-mediated Fc epsilon RI tyrosine phosphorylation by shifting a balance between phosphorylation and dephosphorylation towards accumulation of tyrosine phosphorylated Fc epsilon RI. Fc epsilon RI tyrosine phosphorylation functions to bring syk into a microenvironment where it becomes tyrosine phosphorylated and activated, thereby allowing clustering to indirectly control syk activity.

Related Genes
MeSH Terms
3T3 Cells Amino Acid Sequence Animals Cell Line Enzyme Activation Enzyme Precursors/genetics,metabolism Intracellular Signaling Peptides and Proteins Mice Molecular Sequence Data Protein-Tyrosine Kinases/genetics,metabolism Rats Receptor Aggregation Receptors, IgE/genetics,metabolism Recombinant Proteins Signal Transduction Swine Syk Kinase Vaccinia virus
Chemicals
Enzyme Precursors Intracellular Signaling Peptides and Proteins Receptors, IgE Recombinant Proteins lynA protein, rat Protein-Tyrosine Kinases Syk Kinase Syk protein, mouse Syk protein, rat
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Scharenberg A M
Molecular Allergy and Immunology Section/NIAID/NIH, Rockville, MD 20852, USA.
Lin S
Cuenod B
Yamamura H
Kinet J P
References (66)
66 references, click to expand
  1. The high-affinity receptor for immunoglobulin E.
    Chem Immunol. 1994;59:173-90 PMID: 7945926
  2. Interaction of p72syk with the gamma and beta subunits of the high-affinity receptor for immunoglobulin E, Fc epsilon RI.
    Mol Cell Biol. 1995 Jan;15(1):272-81 PMID: 7528327
  3. 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
  4. Hematopoietic cells express two forms of lyn kinase differing by 21 amino acids in the amino terminus.
    Mol Cell Biol. 1991 May;11(5):2391-8 PMID: 2017160
  5. Anti-immunoglobulin stimulation of B lymphocytes activates src-related protein-tyrosine kinases.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7410-4 PMID: 1714601
  6. Molecular cloning of a porcine gene syk that encodes a 72-kDa protein-tyrosine kinase showing high susceptibility to proteolysis.
    J Biol Chem. 1991 Aug 25;266(24):15790-6 PMID: 1874735
  7. Fc receptors.
    Annu Rev Immunol. 1991;9:457-92 PMID: 1910686
  8. Phosphorylation and dephosphorylation of the high-affinity receptor for immunoglobulin E immediately after receptor engagement and disengagement.
    Nature. 1991 Oct 31;353(6347):855-8 PMID: 1834946
  9. Expression and interactions of the Src family of tyrosine protein kinases in T lymphocytes.
    Adv Cancer Res. 1991;57:103-49 PMID: 1950702
  10. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases.
    Nature. 1992 Jan 2;355(6355):78-80 PMID: 1370575
  11. The receptor with high affinity for IgE.
    Immunol Rev. 1992 Feb;125:37-48 PMID: 1532373
  12. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon.
    Science. 1992 Jan 3;255(5040):79-82 PMID: 1532456
  13. High-affinity IgE receptor-mediated stimulation of rat basophilic leukemia (RBL-2H3) cells induces early and late protein-tyrosine phosphorylations.
    J Biol Chem. 1992 Apr 15;267(11):7310-4 PMID: 1373133
  14. Epidermal Langerhans cells from normal human skin bind monomeric IgE via Fc epsilon RI.
    J Exp Med. 1992 May 1;175(5):1353-65 PMID: 1533243
  15. The gamma-zeta dimers of Fc receptors as connectors to signal transduction.
    Curr Opin Immunol. 1992 Feb;4(1):43-8 PMID: 1534484
  16. Signal transduction by the cytoplasmic domains of Fc epsilon RI-gamma and TCR-zeta in rat basophilic leukemia cells.
    J Biol Chem. 1992 Oct 15;267(29):21027-32 PMID: 1383215
  17. Cell transformation and activation of pp60c-src by overexpression of a protein tyrosine phosphatase.
    Nature. 1992 Sep 24;359(6393):336-9 PMID: 1383828
  18. 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
  19. p59fyn tyrosine kinase associates with multiple T-cell receptor subunits through its unique amino-terminal domain.
    Mol Cell Biol. 1992 Dec;12(12):5438-46 PMID: 1448076
  20. Correlation between Src family member regulation by the protein-tyrosine-phosphatase CD45 and transmembrane signaling through the T-cell receptor.
    Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1402-6 PMID: 8433999
  21. Differential effects of expression of the CD45 tyrosine protein phosphatase on the tyrosine phosphorylation of the lck, fyn, and c-src tyrosine protein kinases.
    Mol Cell Biol. 1993 Mar;13(3):1651-6 PMID: 8441403
  22. Regulation of TCR signaling by CD45 lacking transmembrane and extracellular domains.
    Science. 1993 Apr 23;260(5107):541-4 PMID: 8475386
  23. Rescue of signaling by a chimeric protein containing the cytoplasmic domain of CD45.
    Science. 1993 Apr 23;260(5107):544-6 PMID: 8475387
  24. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases.
    Cell. 1993 Apr 23;73(2):209-12 PMID: 8477442
  25. Regulation of c-Src tyrosine kinase activity by the Src SH2 domain.
    Oncogene. 1993 May;8(5):1119-26 PMID: 7683128
  26. Signal transduction by Fc receptors: the Fc epsilon RI case.
    Immunol Today. 1993 May;14(5):222-6 PMID: 8517921
  27. T cell activation by clustered tyrosine kinases.
    Cell. 1993 Jul 16;74(1):171-83 PMID: 8334702
  28. Negative regulation of T-cell receptor signalling by tyrosine protein kinase p50csk.
    Nature. 1993 Sep 9;365(6442):156-60 PMID: 8371758
  29. Receptor protein tyrosine phosphatase alpha activates pp60c-src and is involved in neuronal differentiation.
    EMBO J. 1993 Oct;12(10):3789-98 PMID: 7691597
  30. Different roles for the Fc epsilon RI gamma chain as a function of the receptor context.
    J Exp Med. 1995 Jan 1;181(1):247-55 PMID: 7528770
  31. New nomenclature for the Reth motif (or ARH1/TAM/ARAM/YXXL)
    Immunol Today. 1995 Feb;16(2):110 PMID: 7888063
  32. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization.
    J Immunol. 1980 Jun;124(6):2728-37 PMID: 7373045
  33. A cDNA presumptively coding for the alpha subunit of the receptor with high affinity for immunoglobulin E.
    Biochemistry. 1987 Jul 28;26(15):4605-10 PMID: 2959318
  34. SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat.
    Mol Cell Biol. 1988 Jan;8(1):466-72 PMID: 2827008
  35. Isolation and characterization of cDNAs coding for the beta subunit of the high-affinity receptor for immunoglobulin E.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6483-7 PMID: 2970642
  36. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck.
    Cell. 1988 Oct 21;55(2):301-8 PMID: 3262426
  37. Complete structure and expression in transfected cells of high affinity IgE receptor.
    Nature. 1989 Jan 12;337(6203):187-9 PMID: 2521376
  38. Antigen receptor tail clue.
    Nature. 1989 Mar 30;338(6214):383-4 PMID: 2927501
  39. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs.
    Cell. 1990 Mar 9;60(5):755-65 PMID: 2107025
  40. 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
  41. Stimulation of protein tyrosine phosphorylation by the B-lymphocyte antigen receptor.
    Nature. 1990 Jun 28;345(6278):810-3 PMID: 1694265
  42. Expression of T cell antigen receptor heterodimers in a lipid-linked form.
    Science. 1990 Aug 10;249(4969):677-9 PMID: 1696397
  43. 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
  44. Association of B cell antigen receptor with protein tyrosine kinase Lyn.
    Science. 1991 Jan 11;251(4990):192-4 PMID: 1702903
  45. Cellular immunity to HIV activated by CD4 fused to T cell or Fc receptor polypeptides.
    Cell. 1991 Mar 8;64(5):1037-46 PMID: 1900456
  46. T cell antigen receptor activation pathways: the tyrosine kinase connection.
    Cell. 1991 Mar 8;64(5):875-8 PMID: 1848158
  47. Protein-tyrosine kinase p72syk in high affinity IgE receptor signaling. Identification as a component of pp72 and association with the receptor gamma chain after receptor aggregation.
    J Biol Chem. 1993 Nov 5;268(31):23318-24 PMID: 7693687
  48. Functional and physical interaction of protein-tyrosine kinases Fyn and Csk in the T-cell signaling system.
    J Biol Chem. 1993 Dec 25;268(36):27413-9 PMID: 8262983
  49. Signal transduction by lymphocyte antigen receptors.
    Cell. 1994 Jan 28;76(2):263-74 PMID: 8293463
  50. Expression of functional high affinity immunoglobulin E receptors (Fc epsilon RI) on monocytes of atopic individuals.
    J Exp Med. 1994 Feb 1;179(2):745-50 PMID: 8294882
  51. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases.
    Science. 1994 Feb 25;263(5150):1136-9 PMID: 7509083
  52. High-affinity IgE receptor on eosinophils is involved in defence against parasites.
    Nature. 1994 Jan 13;367(6459):183-6 PMID: 8114916
  53. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor.
    J Biol Chem. 1994 Feb 25;269(8):5918-25 PMID: 8119935
  54. Tyrosine kinases Lyn and Syk regulate B cell receptor-coupled Ca2+ mobilization through distinct pathways.
    EMBO J. 1994 Mar 15;13(6):1341-9 PMID: 8137818
  55. Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling.
    J Exp Med. 1994 May 1;179(5):1725-9 PMID: 7513017
  56. Interactions of p59fyn and ZAP-70 with T-cell receptor activation motifs: defining the nature of a signalling motif.
    Mol Cell Biol. 1994 Jun;14(6):3729-41 PMID: 8196616
  57. 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
  58. Fc receptors: rubor redux.
    Cell. 1994 Aug 26;78(4):553-60 PMID: 8069908
  59. Src homology 2 domains of Syk and Lyn bind to tyrosine-phosphorylated subunits of the high affinity IgE receptor.
    J Biol Chem. 1994 Sep 2;269(35):22427-32 PMID: 8071371
  60. The catalytic activity of the CD45 membrane-proximal phosphatase domain is required for TCR signaling and regulation.
    EMBO J. 1994 Sep 1;13(17):4002-10 PMID: 8076596
  61. Temporal regulation of non-transmembrane protein tyrosine kinase enzyme activity following T cell antigen receptor engagement.
    J Biol Chem. 1994 Sep 23;269(38):23642-7 PMID: 7522230
  62. Surface expression of a heterologous phosphatase complements CD45 deficiency in a T cell clone.
    J Exp Med. 1994 Oct 1;180(4):1359-66 PMID: 7931069
  63. Functional analysis of Csk in signal transduction through the B-cell antigen receptor.
    Mol Cell Biol. 1994 Nov;14(11):7306-13 PMID: 7935444
  64. Regulation by CD45 of the tyrosine phosphorylation of high affinity IgE receptor beta- and gamma-chains.
    J Immunol. 1995 Apr 1;154(7):3047-55 PMID: 7897197
  65. A requirement for Syk in the activation of the microtubule-associated protein kinase/phospholipase A2 pathway by Fc epsilon R1 is not shared by a G protein-coupled receptor.
    J Biol Chem. 1995 May 5;270(18):10960-7 PMID: 7537741
  66. Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9524-8 PMID: 7524079
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1995-07-17
Pages
3385-94
Language
English
Region
England
NLM ID
8208664
PMCID
PMC394405
Subset
IM
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