Home LiteratureArticle Details
PMID: 7524079 Published · ppublish English Comparative Study Journal Article

Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement.

Saouaf SJ, Mahajan S, Rowley RB, Kut SA, Fargnoli J, Burkhardt AL, Tsukada S, Witte ON, Bolen JB

Abstract

We evaluated in WEHI 231 B cells the time-dependent responses of Lyn, Blk, Btk, Syk, and three members of the Jak family of protein tyrosine kinases following antibody-mediated surface engagement of the B-cell antigen receptor. Our results show that the enzyme activities of Lyn and Blk were stimulated within seconds of antigen receptor engagement and correlated with the initial tyrosine phosphorylation of the Ig alpha and Ig beta subunits of the B-cell antigen receptor. Btk enzyme activity was also transiently stimulated and was maximal at approximately 5 min after B-cell receptor surface binding. Syk activity gradually increased to a maximum at 10-30 min following receptor ligation and was found to parallel the association of Syk with the tyrosine phosphorylated Ig alpha and Ig beta subunits of the receptor. While the specific activities of the Jak1, Jak2, and Tyk2 protein tyrosine kinases were unaltered following B-cell receptor ligation, the abundance of Jak1 and Jak2 were increased 3- to 4-fold within 10 min of receptor engagement. These results demonstrate that multiple families of non-transmembrane protein tyrosine kinases are temporally regulated during the process of B-cell antigen receptor-initiated intracellular signal transduction.

MeSH Terms
Amino Acid Sequence Animals B-Lymphocytes/enzymology,immunology Cell Line Conserved Sequence Enzyme Activation Immunoglobulin G/pharmacology Kinetics Mice Molecular Sequence Data Phosphoproteins/isolation & purification,metabolism Phosphotyrosine Protein-Tyrosine Kinases/metabolism Receptors, Antigen, B-Cell/physiology Time Factors Tyrosine/analogs & derivatives,analysis,metabolism
Chemicals
Immunoglobulin G Phosphoproteins Receptors, Antigen, B-Cell Phosphotyrosine Tyrosine Protein-Tyrosine Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Saouaf S J
Department of Molecular Biology, Bristol-Myers Squibb Pharmaceutical Research Institute, Princeton, NJ 08543.
Mahajan S
Rowley R B
Kut S A
Fargnoli J
Burkhardt A L
Tsukada S
Witte O N
Bolen J B
References (41)
41 references, click to expand
  1. Cross-linking of surface immunoglobulin activates src-related tyrosine kinases in WEHI 231 cells.
    Biochem Biophys Res Commun. 1992 Sep 30;187(3):1536-44 PMID: 1384474
  2. Signaling by the cytokine receptor superfamily: JAKs and STATs.
    Trends Biochem Sci. 1994 May;19(5):222-7 PMID: 8048164
  3. The B cell antigen receptor complex: association of Ig-alpha and Ig-beta with distinct cytoplasmic effectors.
    Science. 1992 Oct 2;258(5079):123-6 PMID: 1439759
  4. 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
  5. Human genetics. Becoming B cells.
    Nature. 1993 Jan 21;361(6409):202-3 PMID: 7678697
  6. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases.
    Nature. 1993 Jan 21;361(6409):226-33 PMID: 8380905
  7. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia.
    Cell. 1993 Jan 29;72(2):279-90 PMID: 8425221
  8. Association with B-cell-antigen receptor with protein-tyrosine kinase p72syk and activation by engagement of membrane IgM.
    Eur J Biochem. 1993 Apr 1;213(1):455-9 PMID: 8477717
  9. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes.
    Science. 1993 Jul 16;261(5119):355-8 PMID: 8332900
  10. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice.
    Science. 1993 Jul 16;261(5119):358-61 PMID: 8332901
  11. Signal transduction by immunoglobulin is mediated through Ig alpha and Ig beta.
    J Exp Med. 1993 Sep 1;178(3):1049-55 PMID: 7688784
  12. Antisense oligodeoxynucleotides to the blk tyrosine kinase prevent anti-mu-chain-mediated growth inhibition and apoptosis in a B-cell lymphoma.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7946-50 PMID: 7690139
  13. Cross-linking of Fc gamma receptor I (Fc gamma RI) and receptor II (Fc gamma RII) on monocytic cells activates a signal transduction pathway common to both Fc receptors that involves the stimulation of p72 Syk protein tyrosine kinase.
    J Biol Chem. 1993 Nov 15;268(32):24442-8 PMID: 8226994
  14. Alterations of the lymphocyte-specific protein tyrosine kinase (p56lck) during T-cell activation.
    Mol Cell Biol. 1988 Oct;8(10):4353-61 PMID: 3141789
  15. Specific expression of a tyrosine kinase gene, blk, in B lymphoid cells.
    Science. 1990 Jan 19;247(4940):332-6 PMID: 2404338
  16. Protein tyrosine phosphorylation is induced in murine B lymphocytes in response to stimulation with anti-immunoglobulin.
    EMBO J. 1990 Jul;9(7):2125-31 PMID: 2357961
  17. Stimulation of protein tyrosine phosphorylation by the B-lymphocyte antigen receptor.
    Nature. 1990 Jun 28;345(6278):810-3 PMID: 1694265
  18. Association of B cell antigen receptor with protein tyrosine kinase Lyn.
    Science. 1991 Jan 11;251(4990):192-4 PMID: 1702903
  19. Mutational analysis of antigen receptor regulation of B lymphocyte growth. Evidence for involvement of the phosphoinositide signaling pathway.
    J Biol Chem. 1991 Mar 25;266(9):5563-74 PMID: 1848555
  20. Tyrosine phosphorylation of components of the B-cell antigen receptors following receptor crosslinking.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3436-40 PMID: 1707541
  21. IgM antigen receptor complex contains phosphoprotein products of B29 and mb-1 genes.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3982-6 PMID: 2023945
  22. 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
  23. 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
  24. Activation of Src-like protein-tyrosine kinase Lyn and its association with phosphatidylinositol 3-kinase upon B-cell antigen receptor-mediated signaling.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1118-22 PMID: 1371009
  25. Structure and developmental regulation of the B-lymphoid tyrosine kinase gene blk.
    J Biol Chem. 1992 Mar 5;267(7):4815-23 PMID: 1537861
  26. Association of the 72-kDa protein-tyrosine kinase PTK72 with the B cell antigen receptor.
    J Biol Chem. 1992 Apr 25;267(12):8613-9 PMID: 1569106
  27. Association between B-lymphocyte membrane immunoglobulin and multiple members of the Src family of protein tyrosine kinases.
    Mol Cell Biol. 1992 May;12(5):2315-21 PMID: 1569953
  28. Multichain immune recognition receptors: similarities in structure and signaling pathways.
    Immunol Today. 1992 Feb;13(2):63-8 PMID: 1575894
  29. Functional reconstitution of an immunoglobulin antigen receptor in T cells.
    J Exp Med. 1992 Jun 1;175(6):1669-76 PMID: 1588287
  30. 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
  31. Membrane immunoglobulin and its accomplices: new lessons from an old receptor.
    FASEB J. 1992 Oct;6(13):3207-17 PMID: 1397843
  32. Interaction of tyrosine kinase oncoproteins with cellular membranes.
    Biochim Biophys Acta. 1993 Dec 23;1155(3):307-22 PMID: 8268189
  33. Structure and function of the B cell antigen receptor.
    Annu Rev Cell Biol. 1993;9:377-410 PMID: 8280466
  34. Ig alpha and Ig beta are functionally homologous to the signaling proteins of the T-cell receptor.
    Mol Cell Biol. 1994 Feb;14(2):1095-103 PMID: 8289790
  35. The alpha/beta sheath and its cytoplasmic tyrosines are required for signaling by the B-cell antigen receptor but not for capping or for serine/threonine-kinase recruitment.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):474-8 PMID: 8290550
  36. Signal transduction by lymphocyte antigen receptors.
    Cell. 1994 Jan 28;76(2):263-74 PMID: 8293463
  37. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases.
    Science. 1994 Feb 25;263(5150):1136-9 PMID: 7509083
  38. Activation of phosphatidylinositol-3' kinase by Src-family kinase SH3 binding to the p85 subunit.
    Science. 1994 Mar 18;263(5153):1609-12 PMID: 8128248
  39. 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
  40. Point mutations define a mIgM transmembrane region motif that determines intersubunit signal transduction in the antigen receptor.
    J Immunol. 1994 Mar 15;152(6):2837-44 PMID: 8144885
  41. 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
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
1994-09-27
Pages
9524-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC44845
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