Home LiteratureArticle Details
PMID: 10629055 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors.

Molecular and cellular biology ·Vol. 20 ·No. 3 ·2000-02-00 ·Pages 979-89

Ong SH, Guy GR, Hadari YR, Laks S, Gotoh N, Schlessinger J, Lax I

Abstract

The docking protein FRS2 was implicated in the transmission of extracellular signals from the fibroblast growth factor (FGF) or nerve growth factor (NGF) receptors to the Ras/mitogen-activated protein kinase signaling cascade. The two members of the FRS2 family, FRS2alpha and FRS2beta, are structurally very similar. Each is composed of an N-terminal myristylation signal, a phosphotyrosine-binding (PTB) domain, and a C-terminal tail containing multiple binding sites for the SH2 domains of the adapter protein Grb2 and the protein tyrosine phosphatase Shp2. Here we show that the PTB domains of both the alpha and beta isoforms of FRS2 bind directly to the FGF or NGF receptors. The PTB domains of the FRS2 proteins bind to a highly conserved sequence in the juxtamembrane region of FGFR1. While FGFR1 interacts with FRS2 constitutively, independent of ligand stimulation and tyrosine phosphorylation, NGF receptor (TrkA) binding to FRS2 is strongly dependent on receptor activation. Complex formation with TrkA is dependent on phosphorylation of Y490, a canonical PTB domain binding site that also functions as a binding site for Shc (NPXpY). Using deletion and alanine scanning mutagenesis as well as peptide competition assays, we demonstrate that the PTB domains of the FRS2 proteins specifically recognize two different primary structures in two different receptors in a phosphorylation-dependent or -independent manner. In addition, NGF-induced tyrosine phosphorylation of FRS2alpha is diminished in cells that overexpress a kinase-inactive mutant of FGFR1. This experiment suggests that FGFR1 may regulate signaling via NGF receptors by sequestering a common key element which both receptors utilize for transmitting their signals. The multiple interactions mediated by FRS2 appear to play an important role in target selection and in defining the specificity of several families of receptor tyrosine kinases.

MeSH Terms
Adaptor Proteins, Signal Transducing Amino Acid Sequence Animals Binding Sites Cell Line GRB2 Adaptor Protein Humans Intracellular Signaling Peptides and Proteins Membrane Proteins/metabolism Molecular Sequence Data Mutagenesis Phosphoproteins/metabolism Protein Tyrosine Phosphatase, Non-Receptor Type 1 Protein Tyrosine Phosphatase, Non-Receptor Type 11 Protein Tyrosine Phosphatase, Non-Receptor Type 6 Protein Tyrosine Phosphatases/chemistry,metabolism Proteins/chemistry,metabolism Receptor Protein-Tyrosine Kinases/chemistry,genetics,metabolism Receptor, Fibroblast Growth Factor, Type 1 Receptors, Fibroblast Growth Factor/chemistry,genetics,metabolism Receptors, Nerve Growth Factor/chemistry,metabolism Recombinant Proteins/chemistry,metabolism SH2 Domain-Containing Protein Tyrosine Phosphatases Sequence Alignment Sequence Deletion Sequence Homology, Amino Acid Signal Transduction/physiology Transfection src Homology Domains
Chemicals
Adaptor Proteins, Signal Transducing FRS2 protein, human GRB2 Adaptor Protein GRB2 protein, human Intracellular Signaling Peptides and Proteins Membrane Proteins Phosphoproteins Proteins Receptors, Fibroblast Growth Factor Receptors, Nerve Growth Factor Recombinant Proteins FGFR1 protein, human Receptor Protein-Tyrosine Kinases Receptor, Fibroblast Growth Factor, Type 1 PTPN11 protein, human PTPN6 protein, human Protein Tyrosine Phosphatase, Non-Receptor Type 1 Protein Tyrosine Phosphatase, Non-Receptor Type 11 Protein Tyrosine Phosphatase, Non-Receptor Type 6 Protein Tyrosine Phosphatases SH2 Domain-Containing Protein Tyrosine Phosphatases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ong S H
Signal Transduction Laboratory, Institute of Molecular and Cell Biology, Singapore 117609, Singapore.
Guy G R
Hadari Y R
Laks S
Gotoh N
Schlessinger J
Lax I
References (44)
44 references, click to expand
  1. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway.
    Cell. 1997 May 30;89(5):693-702 PMID: 9182757
  2. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor.
    Mol Cell Biol. 1995 Aug;15(8):4403-9 PMID: 7542744
  3. High-affinity binding of the Drosophila Numb phosphotyrosine-binding domain to peptides containing a Gly-Pro-(p)Tyr motif.
    Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7204-9 PMID: 9207069
  4. The PTB domain: a new protein module implicated in signal transduction.
    Trends Biochem Sci. 1995 Jul;20(7):277-80 PMID: 7545337
  5. Cloning of a fibroblast growth factor receptor 1 splice variant from Xenopus embryos that lacks a protein kinase C site important for the regulation of receptor activity.
    J Biol Chem. 1995 Sep 29;270(39):22758-63 PMID: 7559402
  6. Affinity, specificity, and kinetics of the interaction of the SHC phosphotyrosine binding domain with asparagine-X-X-phosphotyrosine motifs of growth factor receptors.
    J Biol Chem. 1996 Jan 5;271(1):264-9 PMID: 8550571
  7. A Grb2-associated docking protein in EGF- and insulin-receptor signalling.
    Nature. 1996 Feb 8;379(6565):560-4 PMID: 8596638
  8. Thermodynamic studies of SHC phosphotyrosine interaction domain recognition of the NPXpY motif.
    J Biol Chem. 1996 Mar 1;271(9):4770-5 PMID: 8617744
  9. Peptide-surface association: the case of PDZ and PTB domains.
    Cell. 1996 Aug 9;86(3):341-3 PMID: 8756715
  10. The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein.
    Mol Cell Biol. 1996 Nov;16(11):6229-41 PMID: 8887653
  11. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis.
    Nature. 1996 Nov 14;384(6605):173-6 PMID: 8906793
  12. Ligand stimulation of a Ret chimeric receptor carrying the activating mutation responsible for the multiple endocrine neoplasia type 2B.
    J Biol Chem. 1996 Nov 15;271(46):29497-501 PMID: 8910618
  13. p62(dok): a constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells.
    Cell. 1997 Jan 24;88(2):197-204 PMID: 9008160
  14. Identification of the Abl- and rasGAP-associated 62 kDa protein as a docking protein, Dok.
    Cell. 1997 Jan 24;88(2):205-11 PMID: 9008161
  15. Functions of fibroblast growth factors in vertebrate development.
    Cytokine Growth Factor Rev. 1996 Dec;7(4):311-25 PMID: 9023055
  16. Interaction of the phosphotyrosine interaction/phosphotyrosine binding-related domains of Fe65 with wild-type and mutant Alzheimer's beta-amyloid precursor proteins.
    J Biol Chem. 1997 Mar 7;272(10):6399-405 PMID: 9045663
  17. Identification of Shc docking site on Ret tyrosine kinase.
    Oncogene. 1997 Feb 20;14(7):773-82 PMID: 9047384
  18. Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells.
    EMBO J. 1997 Jul 1;16(13):3877-88 PMID: 9233798
  19. A dominant role of the juxtamembrane region of the TrkA nerve growth factor receptor during neuronal cell differentiation.
    J Biol Chem. 1997 Sep 12;272(37):23231-8 PMID: 9287331
  20. SHP2 associates directly with tyrosine phosphorylated p90 (SNT) protein in FGF-stimulated cells.
    Biochem Biophys Res Commun. 1997 Sep 8;238(1):261-6 PMID: 9299490
  21. Sequence-specific recognition of the internalization motif of the Alzheimer's amyloid precursor protein by the X11 PTB domain.
    EMBO J. 1997 Oct 15;16(20):6141-50 PMID: 9321393
  22. Signaling through scaffold, anchoring, and adaptor proteins.
    Science. 1997 Dec 19;278(5346):2075-80 PMID: 9405336
  23. Numb-associated kinase interacts with the phosphotyrosine binding domain of Numb and antagonizes the function of Numb in vivo.
    Mol Cell Biol. 1998 Jan;18(1):598-607 PMID: 9418906
  24. Peptide recognition by PTB and PDZ domains.
    Curr Opin Struct Biol. 1997 Dec;7(6):835-8 PMID: 9434904
  25. The mammalian numb phosphotyrosine-binding domain. Characterization of binding specificity and identification of a novel PDZ domain-containing numb binding protein, LNX.
    J Biol Chem. 1998 Apr 10;273(15):9179-87 PMID: 9535908
  26. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation.
    Mol Cell Biol. 1998 Jul;18(7):3966-73 PMID: 9632781
  27. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase.
    Mol Cell Biol. 1998 Jul;18(7):4109-17 PMID: 9632795
  28. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins.
    J Biol Chem. 1998 Jul 17;273(29):17987-90 PMID: 9660748
  29. Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity.
    Nat Struct Biol. 1998 Dec;5(12):1075-83 PMID: 9846878
  30. The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation.
    J Biol Chem. 1999 Apr 2;274(14):9861-70 PMID: 10092678
  31. Brain-derived neurotrophic factor induces phosphorylation of fibroblast growth factor receptor substrate 2.
    J Biol Chem. 1999 Apr 16;274(16):11321-7 PMID: 10196222
  32. A Drosophila shc gene product is implicated in signaling by the DER receptor tyrosine kinase.
    Mol Cell Biol. 1995 Sep;15(9):4810-8 PMID: 7651398
  33. Trophic factors and neuronal survival.
    Neuron. 1989 Jun;2(6):1525-34 PMID: 2697237
  34. Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis.
    Nature. 1992 Aug 20;358(6388):681-4 PMID: 1379698
  35. Growth factor signaling by receptor tyrosine kinases.
    Neuron. 1992 Sep;9(3):383-91 PMID: 1326293
  36. SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells.
    Mol Cell Biol. 1993 Apr;13(4):2203-13 PMID: 7681142
  37. Identification of Trk binding sites for SHC and phosphatidylinositol 3'-kinase and formation of a multimeric signaling complex.
    J Biol Chem. 1993 Nov 5;268(31):22963-6 PMID: 8226808
  38. How receptor tyrosine kinases activate Ras.
    Trends Biochem Sci. 1993 Aug;18(8):273-5 PMID: 8236435
  39. Ras-dependent growth factor regulation of MEK kinase in PC12 cells.
    Science. 1994 Sep 2;265(5177):1458-61 PMID: 8073291
  40. Phosphotyrosine-dependent interaction of SHC and insulin receptor substrate 1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain.
    Mol Cell Biol. 1995 May;15(5):2500-8 PMID: 7537849
  41. PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine.
    Science. 1995 May 26;268(5214):1177-9 PMID: 7539155
  42. The phosphotyrosine interaction domain of SHC recognizes tyrosine-phosphorylated NPXY motif.
    J Biol Chem. 1995 Jun 23;270(25):14863-6 PMID: 7541030
  43. Shc binding to nerve growth factor receptor is mediated by the phosphotyrosine interaction domain.
    J Biol Chem. 1995 Jun 23;270(25):15125-9 PMID: 7541035
  44. The IRS-signalling system during insulin and cytokine action.
    Bioessays. 1997 Jun;19(6):491-500 PMID: 9204766
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2000-02-00
Pages
979-89
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC85215
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