Home LiteratureArticle Details
PMID: 9560226 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Activation of protein tyrosine kinase PYK2 by the m1 muscarinic acetylcholine receptor.

Felsch JS, Cachero TG, Peralta EG

Abstract

Several G protein-coupled receptors are known to direct the tyrosine phosphorylation, and in some cases the activation, of diverse tyrosine kinases. Using a stable cell line approach, we characterize the activation of PYK2, a tyrosine kinase structurally related to focal adhesion kinase, by the G protein-coupled m1 muscarinic acetylcholine receptor. We find that PYK2 tyrosine kinase activity is critical for the m1 receptor-stimulated tyrosine phosphorylation of PYK2. Furthermore, we identify two tyrosine residues that are subject to phosphorylation in response to muscarinic signaling and show that this phosphorylation induces two cytosolic proteins, c-Src and Grb2, to bind to PYK2. This is the first demonstration of the significance played by distinct PYK2 tyrosine residues in G protein-coupled signaling to this kinase. By comparison, though m1 receptors induce the tyrosine phosphorylation of the cytoskeletal protein paxillin, the association of paxillin with PYK2 is unaffected by muscarinic signaling. We also provide evidence that PYK2 specifically phosphorylates the carboxyl-terminal cytosolic portion of the potassium channel Kv1.2 in a manner regulated by the m1 receptor. These results delineate molecular events attending the m1 muscarinic receptor stimulation of this tyrosine kinase and establish PYK2 as an effector of the m1 muscarinic receptor in the regulation of multiple cell functions.

MeSH Terms
Adaptor Proteins, Signal Transducing Cytoplasm/metabolism Enzyme Activation Focal Adhesion Kinase 2 GRB2 Adaptor Protein Humans Kv1.2 Potassium Channel Phosphotyrosine/metabolism Potassium Channels/metabolism Potassium Channels, Voltage-Gated Protein-Tyrosine Kinases/metabolism Proteins/metabolism Proto-Oncogene Proteins pp60(c-src)/metabolism Receptor, Muscarinic M1 Receptors, Muscarinic/metabolism Signal Transduction Structure-Activity Relationship
Chemicals
Adaptor Proteins, Signal Transducing GRB2 Adaptor Protein GRB2 protein, human KCNA2 protein, human Kv1.2 Potassium Channel Potassium Channels Potassium Channels, Voltage-Gated Proteins Receptor, Muscarinic M1 Receptors, Muscarinic Phosphotyrosine Protein-Tyrosine Kinases Focal Adhesion Kinase 2 Proto-Oncogene Proteins pp60(c-src)
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Felsch J S
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
Cachero T G
Peralta E G
References (35)
35 references, click to expand
  1. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C.
    J Biol Chem. 1991 Aug 25;266(24):15771-81 PMID: 1874734
  2. Human homologue of the Drosophila discs large tumor suppressor binds to p56lck tyrosine kinase and Shaker type Kv1.3 potassium channel in T lymphocytes.
    J Biol Chem. 1997 Oct 24;272(43):26899-904 PMID: 9341123
  3. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation.
    Nature. 1992 Aug 20;358(6388):690-2 PMID: 1379699
  4. Bombesin, vasopressin, and endothelin stimulation of tyrosine phosphorylation in Swiss 3T3 cells. Identification of a novel tyrosine kinase as a major substrate.
    J Biol Chem. 1992 Sep 25;267(27):19031-4 PMID: 1382065
  5. Focal adhesion kinase (p125FAK): a point of convergence in the action of neuropeptides, integrins, and oncogenes.
    Cell. 1992 Dec 11;71(6):891-4 PMID: 1458538
  6. The when and how of Src regulation.
    Cell. 1993 Jun 18;73(6):1051-4 PMID: 7685656
  7. Tyrosine kinase-dependent suppression of a potassium channel by the G protein-coupled m1 muscarinic acetylcholine receptor.
    Cell. 1993 Dec 17;75(6):1145-56 PMID: 8261514
  8. Molecular basis of cardiac potassium channel stimulation by protein kinase A.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):624-8 PMID: 8290574
  9. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src.
    Mol Cell Biol. 1994 Mar;14(3):1680-8 PMID: 7509446
  10. Tyrosine phosphorylation of pp125FAK in platelets requires coordinated signaling through integrin and agonist receptors.
    J Biol Chem. 1994 May 20;269(20):14738-45 PMID: 7514181
  11. A transmembrane-anchored chimeric focal adhesion kinase is constitutively activated and phosphorylated at tyrosine residues identical to pp125FAK.
    J Biol Chem. 1994 Aug 12;269(32):20567-74 PMID: 8051157
  12. Activation of Src family kinase activity by the G protein-coupled thrombin receptor in growth-responsive fibroblasts.
    J Biol Chem. 1994 Nov 4;269(44):27372-7 PMID: 7525555
  13. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases.
    Mol Cell Biol. 1995 Feb;15(2):954-63 PMID: 7529876
  14. Integrins and signal transduction pathways: the road taken.
    Science. 1995 Apr 14;268(5208):233-9 PMID: 7716514
  15. Identification of Tyr-397 as the primary site of tyrosine phosphorylation and pp60src association in the focal adhesion kinase, pp125FAK.
    Mol Cell Biol. 1995 May;15(5):2819-27 PMID: 7739563
  16. Signal transduction through integrins: a central role for focal adhesion kinase?
    Bioessays. 1995 Mar;17(3):229-36 PMID: 7748177
  17. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase.
    J Biol Chem. 1995 Jul 21;270(29):17437-41 PMID: 7615549
  18. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions.
    Nature. 1995 Aug 31;376(6543):737-45 PMID: 7544443
  19. Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily.
    J Biol Chem. 1995 Sep 8;270(36):21206-19 PMID: 7673154
  20. Paxillin, a tyrosine phosphorylated focal adhesion-associated protein binds to the carboxyl terminal domain of focal adhesion kinase.
    Mol Biol Cell. 1995 Jun;6(6):637-47 PMID: 7579684
  21. Identification of domains conferring G protein regulation on inward rectifier potassium channels.
    Cell. 1995 Nov 3;83(3):443-9 PMID: 8521474
  22. Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain.
    J Biol Chem. 1995 Nov 17;270(46):27742-51 PMID: 7499242
  23. Integrin-mediated activation of MEK and mitogen-activated protein kinase is independent of Ras [corrected].
    J Biol Chem. 1996 Jul 26;271(30):18122-7 PMID: 8663436
  24. Characterization of RAFTK, a novel focal adhesion kinase, and its integrin-dependent phosphorylation and activation in megakaryocytes.
    Blood. 1996 Jul 15;88(2):417-28 PMID: 8695788
  25. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation.
    Nature. 1996 Oct 10;383(6600):547-50 PMID: 8849729
  26. Differential regulation of proline-rich tyrosine kinase 2/cell adhesion kinase beta (PYK2/CAKbeta) and pp125(FAK) by glutamate and depolarization in rat hippocampus.
    J Biol Chem. 1996 Nov 15;271(46):28942-6 PMID: 8910543
  27. Activation of a novel calcium-dependent protein-tyrosine kinase. Correlation with c-Jun N-terminal kinase but not mitogen-activated protein kinase activation.
    J Biol Chem. 1996 Nov 22;271(47):29993-8 PMID: 8939945
  28. The related adhesion focal tyrosine kinase forms a complex with paxillin in hematopoietic cells.
    J Biol Chem. 1996 Dec 6;271(49):31222-6 PMID: 8940124
  29. Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain.
    Science. 1996 Dec 20;274(5295):2089-91 PMID: 8953041
  30. The related adhesion focal tyrosine kinase is tyrosine-phosphorylated after beta1-integrin stimulation in B cells and binds to p130cas.
    J Biol Chem. 1997 Jan 3;272(1):228-32 PMID: 8995252
  31. Involvement of p130(Cas) and p105(HEF1), a novel Cas-like docking protein, in a cytoskeleton-dependent signaling pathway initiated by ligation of integrin or antigen receptor on human B cells.
    J Biol Chem. 1997 Feb 14;272(7):4230-6 PMID: 9020138
  32. Paxillin is tyrosine-phosphorylated by and preferentially associates with the calcium-dependent tyrosine kinase in rat liver epithelial cells.
    J Biol Chem. 1997 May 30;272(22):14341-8 PMID: 9162070
  33. Ras-dependent mitogen-activated protein kinase activation by G protein-coupled receptors. Convergence of Gi- and Gq-mediated pathways on calcium/calmodulin, Pyk2, and Src kinase.
    J Biol Chem. 1997 Aug 1;272(31):19125-32 PMID: 9235901
  34. The m1 muscarinic acetylcholine receptor transactivates the EGF receptor to modulate ion channel activity.
    EMBO J. 1997 Aug 1;16(15):4597-605 PMID: 9303304
  35. Cloning and expression of a rat cardiac delayed rectifier potassium channel.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7892-5 PMID: 1715584
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
1998-04-28
Pages
5051-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC20211
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