Home LiteratureArticle Details
PMID: 9032297 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor proteins.

Molecular and cellular biology ·Vol. 17 ·No. 3 ·1997-03-00 ·Pages 1702-13

Schlaepfer DD, Broome MA, Hunter T

Abstract

The focal adhesion kinase (FAK), a protein-tyrosine kinase (PTK), associates with integrin receptors and is activated by cell binding to extracellular matrix proteins, such as fibronectin (FN). FAK autophosphorylation at Tyr-397 promotes Src homology 2 (SH2) domain binding of Src family PTKs, and c-Src phosphorylation of FAK at Tyr-925 creates an SH2 binding site for the Grb2 SH2-SH3 adaptor protein. FN-stimulated Grb2 binding to FAK may facilitate intracellular signaling to targets such as ERK2-mitogen-activated protein kinase. We examined FN-stimulated signaling to ERK2 and found that ERK2 activation was reduced 10-fold in Src- fibroblasts, compared to that of Src- fibroblasts stably reexpressing wild-type c-Src. FN-stimulated FAK phosphotyrosine (P.Tyr) and Grb2 binding to FAK were reduced, whereas the tyrosine phosphorylation of another signaling protein, p130cas, was not detected in the Src- cells. Stable expression of residues 1 to 298 of Src (Src 1-298, which encompass the SH3 and SH2 domains of c-Src) in the Src- cells blocked Grb2 binding to FAK; but surprisingly, Src 1-298 expression also resulted in elevated p130cas P.Tyr levels and a two- to threefold increase in FN-stimulated ERK2 activity compared to levels in Src- cells. Src 1-298 bound to both FAK and p130cas and promoted FAK association with p130cas in vivo. FAK was observed to phosphorylate p130cas in vitro and could thus phosphorylate p130cas upon FN stimulation of the Src 1-298-expressing cells. FAK-induced phosphorylation of p130cas in the Src 1-298 cells promoted the SH2 domain-dependent binding of the Nck adaptor protein to p130cas, which may facilitate signaling to ERK2. These results show that there are additional FN-stimulated pathways to ERK2 that do not involve Grb2 binding to FAK.

MeSH Terms
Adaptor Proteins, Signal Transducing Animals Calcium-Calmodulin-Dependent Protein Kinases/metabolism Cell Adhesion Molecules/metabolism Cells, Cultured Crk-Associated Substrate Protein Enzyme Activation Fibroblasts Fibronectins/pharmacology Focal Adhesion Kinase 1 Focal Adhesion Protein-Tyrosine Kinases GRB2 Adaptor Protein Integrins/physiology Mice Mice, Knockout Mitogen-Activated Protein Kinase 1 Oncogene Proteins/metabolism Peptide Mapping Phosphoproteins/metabolism Phosphorylation Protein-Tyrosine Kinases/metabolism Proteins/metabolism Proto-Oncogene Proteins pp60(c-src)/metabolism Retinoblastoma-Like Protein p130 Signal Transduction/physiology src Homology Domains
Chemicals
Adaptor Proteins, Signal Transducing Bcar1 protein, mouse Cell Adhesion Molecules Crk-Associated Substrate Protein Fibronectins GRB2 Adaptor Protein Grb2 protein, mouse Integrins Nck protein Oncogene Proteins Phosphoproteins Proteins Retinoblastoma-Like Protein p130 Protein-Tyrosine Kinases Focal Adhesion Kinase 1 Focal Adhesion Protein-Tyrosine Kinases Proto-Oncogene Proteins pp60(c-src) Ptk2 protein, mouse Calcium-Calmodulin-Dependent Protein Kinases Mitogen-Activated Protein Kinase 1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Schlaepfer D D
Molecular Biology and Virology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037, USA.
Broome M A
Hunter T
References (70)
70 references, click to expand
  1. 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
  2. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8487-91 PMID: 1528852
  3. SH2 domains recognize specific phosphopeptide sequences.
    Cell. 1993 Mar 12;72(5):767-78 PMID: 7680959
  4. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions.
    J Cell Biol. 1993 Nov;123(4):993-1005 PMID: 8227154
  5. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK.
    Mol Cell Biol. 1994 Jan;14(1):147-55 PMID: 7505391
  6. Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn.
    J Cell Sci. 1996 Jul;109 ( Pt 7):1787-94 PMID: 8832401
  7. Isolation of a NCK-associated kinase, PRK2, an SH3-binding protein and potential effector of Rho protein signaling.
    J Biol Chem. 1996 Nov 15;271(46):28772-6 PMID: 8910519
  8. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression.
    Cell. 1996 Nov 15;87(4):733-43 PMID: 8929541
  9. The PDGF receptor phosphorylates Tyr 138 in the c-Src SH3 domain in vivo reducing peptide ligand binding.
    Oncogene. 1997 Jan 9;14(1):17-34 PMID: 9010229
  10. 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
  11. Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates the anchorage-dependent expression of cyclin D1.
    Mol Biol Cell. 1996 Jan;7(1):101-111 PMID: 8741843
  12. The insulin signaling system.
    J Biol Chem. 1994 Jan 7;269(1):1-4 PMID: 8276779
  13. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin.
    Development. 1993 Dec;119(4):1079-91 PMID: 8306876
  14. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src.
    Mol Cell Biol. 1994 Mar;14(3):1680-8 PMID: 7509446
  15. Transmembrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras.
    J Biol Chem. 1994 Jun 10;269(23):15961-4 PMID: 7515874
  16. Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed beta 1 integrin cytoplasmic domain.
    J Biol Chem. 1994 Jul 15;269(28):18311-4 PMID: 7518428
  17. Csk suppression of Src involves movement of Csk to sites of Src activity.
    Mol Cell Biol. 1994 Aug;14(8):5402-11 PMID: 7518562
  18. 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
  19. Direct interaction of v-Src with the focal adhesion kinase mediated by the Src SH2 domain.
    Mol Biol Cell. 1994 Apr;5(4):413-21 PMID: 8054685
  20. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner.
    EMBO J. 1994 Aug 15;13(16):3748-56 PMID: 8070403
  21. Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen.
    Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8856-60 PMID: 7522323
  22. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527.
    EMBO J. 1994 Oct 17;13(20):4745-56 PMID: 7525268
  23. Association of insulin receptor substrate-1 with integrins.
    Science. 1994 Dec 2;266(5190):1576-8 PMID: 7527156
  24. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase.
    Nature. 1994 Dec 22-29;372(6508):786-91 PMID: 7997267
  25. 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
  26. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation.
    Cell. 1995 Jan 27;80(2):179-85 PMID: 7834738
  27. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix.
    Science. 1995 Feb 10;267(5199):891-3 PMID: 7531366
  28. Binding of NCK to SOS and activation of ras-dependent gene expression.
    Mol Cell Biol. 1995 Mar;15(3):1169-74 PMID: 7862111
  29. Integrins and signal transduction pathways: the road taken.
    Science. 1995 Apr 14;268(5208):233-9 PMID: 7716514
  30. Cooperative signaling by alpha 5 beta 1 and alpha 4 beta 1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin.
    J Cell Biol. 1995 May;129(3):867-79 PMID: 7537277
  31. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases.
    Curr Biol. 1995 Mar 1;5(3):296-305 PMID: 7780740
  32. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs.
    J Biol Chem. 1995 Jun 23;270(25):15398-402 PMID: 7541040
  33. The alpha 5 beta 1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):6161-5 PMID: 7541142
  34. c-Src enhances the spreading of src-/- fibroblasts on fibronectin by a kinase-independent mechanism.
    Genes Dev. 1995 Jun 15;9(12):1505-17 PMID: 7541382
  35. Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation.
    Mol Biol Cell. 1995 Mar;6(3):273-82 PMID: 7612963
  36. Requirement of the NPXY motif in the integrin beta 3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo.
    J Cell Biol. 1995 Jul;130(2):441-50 PMID: 7542248
  37. Adhesion-induced tyrosine phosphorylation of the p130 src substrate.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1371-9 PMID: 7542255
  38. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton.
    Nature. 1995 Jul 20;376(6537):267-71 PMID: 7617039
  39. Focal adhesion kinase in the brain: novel subcellular localization and specific regulation by Fyn tyrosine kinase in mutant mice.
    Genes Dev. 1995 Aug 1;9(15):1909-21 PMID: 7544314
  40. 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
  41. 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
  42. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix.
    J Biol Chem. 1995 Sep 22;270(38):22259-62 PMID: 7545676
  43. An examination of focal adhesion formation and tyrosine phosphorylation in fibroblasts isolated from src-, fyn-, and yes- mice.
    Cell Adhes Commun. 1995 May;3(2):91-100 PMID: 7583009
  44. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules.
    J Cell Biol. 1995 Nov;131(3):791-805 PMID: 7593197
  45. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10678-82 PMID: 7479864
  46. Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins.
    Mol Cell Biol. 1995 Dec;15(12):6829-37 PMID: 8524249
  47. 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
  48. Integrin transmembrane signaling and cytoskeletal control.
    Curr Opin Cell Biol. 1995 Oct;7(5):681-9 PMID: 8573343
  49. Calcium influx induces neurite growth through a Src-Ras signaling cassette.
    Neuron. 1995 Dec;15(6):1415-25 PMID: 8845164
  50. Dependence of cyclin E-CDK2 kinase activity on cell anchorage.
    Science. 1996 Jan 26;271(5248):499-502 PMID: 8560263
  51. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice.
    Nature. 1995 Oct 12;377(6549):539-44 PMID: 7566154
  52. Impaired migration but not differentiation of haematopoietic stem cells in the absence of beta1 integrins.
    Nature. 1996 Mar 14;380(6570):171-5 PMID: 8600394
  53. Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases.
    Mol Cell Biol. 1996 Jun;16(6):2606-13 PMID: 8649368
  54. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase.
    Mol Cell Biol. 1996 Jun;16(6):3169-78 PMID: 8649427
  55. Direct binding of C-terminal region of p130Cas to SH2 and SH3 domains of Src kinase.
    J Biol Chem. 1996 Apr 12;271(15):8959-65 PMID: 8621540
  56. The molecular architecture of focal adhesions.
    Annu Rev Cell Dev Biol. 1995;11:379-416 PMID: 8689563
  57. Integrins: emerging paradigms of signal transduction.
    Annu Rev Cell Dev Biol. 1995;11:549-99 PMID: 8689569
  58. Human enhancer of filamentation 1, a novel p130cas-like docking protein, associates with focal adhesion kinase and induces pseudohyphal growth in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Jul;16(7):3327-37 PMID: 8668148
  59. p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase.
    J Biol Chem. 1996 Jun 7;271(23):13649-55 PMID: 8662921
  60. Ras activation is necessary for integrin-mediated activation of extracellular signal-regulated kinase 2 and cytosolic phospholipase A2 but not for cytoskeletal organization.
    J Biol Chem. 1996 Jun 21;271(25):14814-8 PMID: 8663348
  61. Requirement for c-Src catalytic activity and the SH3 domain in platelet-derived growth factor BB and epidermal growth factor mitogenic signaling.
    J Biol Chem. 1996 Jul 12;271(28):16798-806 PMID: 8663329
  62. 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
  63. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases.
    Mol Cell Biol. 1996 Oct;16(10):5623-33 PMID: 8816475
  64. Interaction of the Nck adapter protein with p21-activated kinase (PAK1).
    J Biol Chem. 1996 Oct 18;271(42):25746-9 PMID: 8824201
  65. The adaptor protein Nck links receptor tyrosine kinases with the serine-threonine kinase Pak1.
    J Biol Chem. 1996 Aug 30;271(35):20997-1000 PMID: 8798379
  66. Nck, a melanoma cDNA encoding a cytoplasmic protein consisting of the src homology units SH2 and SH3.
    Nucleic Acids Res. 1990 Feb 25;18(4):1048 PMID: 2107526
  67. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice.
    Cell. 1991 Feb 22;64(4):693-702 PMID: 1997203
  68. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates.
    Methods Enzymol. 1991;201:110-49 PMID: 1943760
  69. Phosphorylation of c-Src on tyrosine 527 by another protein tyrosine kinase.
    Science. 1991 Oct 25;254(5031):568-71 PMID: 1719633
  70. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions.
    Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5192-6 PMID: 1594631
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-03-00
Pages
1702-13
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC231895
Subset
IM
Grants
NCI NIH HHS · CA14195 · United States
NCI NIH HHS · CA39780 · 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