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PMID: 1372092 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

SH2 domains of the p85 alpha subunit of phosphatidylinositol 3-kinase regulate binding to growth factor receptors.

Molecular and cellular biology ·Vol. 12 ·No. 3 ·1992-03-00 ·Pages 991-7

McGlade CJ, Ellis C, Reedijk M, Anderson D, Mbamalu G, Reith AD, Panayotou G, End P, Bernstein A, Kazlauskas A

Abstract

The binding of cytoplasmic signaling proteins such as phospholipase C-gamma 1 and Ras GTPase-activating protein to autophosphorylated growth factor receptors is directed by their noncatalytic Src homology region 2 (SH2) domains. The p85 alpha regulatory subunit of phosphatidylinositol (PI) 3-kinase, which associates with several receptor protein-tyrosine kinases, also contains two SH2 domains. Both p85 alpha SH2 domains, when expressed individually as fusion proteins in bacteria, bound stably to the activated beta receptor for platelet-derived growth factor (PDGF). Complex formation required PDGF stimulation and was dependent on receptor tyrosine kinase activity. The bacterial p85 alpha SH2 domains recognized activated beta PDGF receptor which had been immobilized on a filter, indicating that SH2 domains contact autophosphorylated receptors directly. Several receptor tyrosine kinases within the PDGF receptor subfamily, including the colony-stimulating factor 1 receptor and the Steel factor receptor (Kit), also associate with PI 3-kinase in vivo. Bacterially expressed SH2 domains derived from the p85 alpha subunit of PI 3-kinase bound in vitro to the activated colony-stimulating factor 1 receptor and to Kit. We infer that the SH2 domains of p85 alpha bind to high-affinity sites on these receptors, whose creation is dependent on receptor autophosphorylation. The SH2 domains of p85 are therefore primarily responsible for the binding of PI 3-kinase to activated growth factor receptors.

MeSH Terms
Animals Cell Line Hematopoietic Cell Growth Factors/metabolism Humans Immunoblotting Phosphatidylinositol 3-Kinases Phosphorylation Phosphotransferases/chemistry,metabolism Platelet-Derived Growth Factor/metabolism Rats Receptor, Macrophage Colony-Stimulating Factor/metabolism Receptors, Cell Surface/metabolism Receptors, Platelet-Derived Growth Factor Stem Cell Factor Sulfhydryl Compounds/metabolism
Chemicals
Hematopoietic Cell Growth Factors Platelet-Derived Growth Factor Receptors, Cell Surface Stem Cell Factor Sulfhydryl Compounds Phosphotransferases Phosphatidylinositol 3-Kinases Receptor, Macrophage Colony-Stimulating Factor Receptors, Platelet-Derived Growth Factor
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
McGlade C J
Division of Molecular and Developmental Biology, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada.
Ellis C
Reedijk M
Anderson D
Mbamalu G
Reith A D
Panayotou G
End P
Bernstein A
Kazlauskas A
References (55)
55 references, click to expand
  1. Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms.
    Cell. 1990 Oct 5;63(1):235-43 PMID: 1698558
  2. A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps.
    Mol Cell Biol. 1986 Dec;6(12):4396-408 PMID: 3025655
  3. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254.
    Cell. 1991 May 3;65(3):435-41 PMID: 1708307
  4. The Steel/W transduction pathway: kit autophosphorylation and its association with a unique subset of cytoplasmic signaling proteins is induced by the Steel factor.
    Mol Cell Biol. 1991 Jun;11(6):3043-51 PMID: 1710023
  5. Oncogenes and signal transduction.
    Cell. 1991 Jan 25;64(2):281-302 PMID: 1846320
  6. Cloning of PI3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases.
    Cell. 1991 Apr 5;65(1):83-90 PMID: 1849461
  7. Platelet-derived growth factor increases the in vivo activity of phospholipase C-gamma 1 and phospholipase C-gamma 2.
    Mol Cell Biol. 1991 Apr;11(4):2018-25 PMID: 2005895
  8. PDGF beta-receptor stimulates tyrosine phosphorylation of GAP and association of GAP with a signaling complex.
    Cell. 1990 Apr 6;61(1):125-33 PMID: 2156626
  9. Signal transduction by receptors with tyrosine kinase activity.
    Cell. 1990 Apr 20;61(2):203-12 PMID: 2158859
  10. Purification and characterization of bovine brain type I phosphatidylinositol kinase.
    Eur J Biochem. 1990 Aug 17;191(3):761-7 PMID: 2167854
  11. Interactions of phosphatidylinositol kinase, GTPase-activating protein (GAP), and GAP-associated proteins with the colony-stimulating factor 1 receptor.
    Mol Cell Biol. 1990 Nov;10(11):5601-8 PMID: 2172781
  12. Common elements in growth factor stimulation and oncogenic transformation: 85 kd phosphoprotein and phosphatidylinositol kinase activity.
    Cell. 1987 Sep 25;50(7):1021-9 PMID: 2441878
  13. Epidermal growth factor stimulates tyrosine phosphorylation of phospholipase C-II independently of receptor internalization and extracellular calcium.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1568-72 PMID: 2466293
  14. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells.
    Cell. 1989 Apr 7;57(1):167-75 PMID: 2467744
  15. vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells.
    EMBO J. 1989 Aug;8(8):2283-90 PMID: 2477241
  16. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins.
    Cell. 1989 Sep 22;58(6):1121-33 PMID: 2550144
  17. The colony stimulating factor-1 receptor associates with and activates phosphatidylinositol-3 kinase.
    Nature. 1989 Dec 7;342(6250):699-702 PMID: 2556641
  18. Structure of the receptor for platelet-derived growth factor helps define a family of closely related growth factor receptors.
    Nature. 1986 Sep 18-24;323(6085):226-32 PMID: 3020426
  19. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase.
    Gene. 1988 Jul 15;67(1):31-40 PMID: 3047011
  20. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases.
    Nature. 1990 Jan 25;343(6256):377-81 PMID: 1689011
  21. Tyrosine mutations within the alpha platelet-derived growth factor receptor kinase insert domain abrogate receptor-associated phosphatidylinositol-3 kinase activity without affecting mitogenic or chemotactic signal transduction.
    Mol Cell Biol. 1991 Jul;11(7):3780-5 PMID: 1646396
  22. Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor.
    Cell. 1990 Oct 5;63(1):213-24 PMID: 1698556
  23. The tyrosine phosphorylated carboxyterminus of the EGF receptor is a binding site for GAP and PLC-gamma.
    EMBO J. 1990 Dec;9(13):4375-80 PMID: 2176151
  24. Effect of phospholipase C-gamma overexpression on PDGF-induced second messengers and mitogenesis.
    Science. 1990 May 4;248(4955):607-10 PMID: 2333512
  25. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins.
    Science. 1990 Jun 22;248(4962):1537-9 PMID: 1694307
  26. Association between the PDGF receptor and members of the src family of tyrosine kinases.
    Cell. 1990 Aug 10;62(3):481-92 PMID: 1696179
  27. The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus.
    Cell. 1990 Oct 5;63(1):225-33 PMID: 1698557
  28. The noncatalytic src homology region 2 segment of abl tyrosine kinase binds to tyrosine-phosphorylated cellular proteins with high affinity.
    Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):627-31 PMID: 1703304
  29. A phosphatidylinositol-3 kinase binds to platelet-derived growth factor receptors through a specific receptor sequence containing phosphotyrosine.
    Mol Cell Biol. 1991 Feb;11(2):1125-32 PMID: 1703628
  30. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes, and PI3-kinase.
    Cell. 1991 Apr 5;65(1):91-104 PMID: 1707345
  31. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins.
    Science. 1991 May 3;252(5006):668-74 PMID: 1708916
  32. The SH2 and SH3 domains of pp60src direct stable association with tyrosine phosphorylated proteins p130 and p110.
    EMBO J. 1991 Jul;10(7):1689-98 PMID: 1710979
  33. BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner.
    Cell. 1991 Jul 12;66(1):161-71 PMID: 1712671
  34. cDNA cloning of a novel 85 kd protein that has SH2 domains and regulates binding of PI3-kinase to the PDGF beta-receptor.
    Cell. 1991 Apr 5;65(1):75-82 PMID: 1849460
  35. The epidermal growth factor receptor phosphorylates GTPase-activating protein (GAP) at Tyr-460, adjacent to the GAP SH2 domains.
    Mol Cell Biol. 1991 May;11(5):2511-6 PMID: 1850098
  36. Protein-tyrosine kinases regulate the phosphorylation, protein interactions, subcellular distribution, and activity of p21ras GTPase-activating protein.
    Mol Cell Biol. 1991 Apr;11(4):1804-12 PMID: 2005883
  37. 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
  38. Binding of GAP to activated PDGF receptors.
    Science. 1990 Mar 30;247(4950):1578-81 PMID: 2157284
  39. Activated type I phosphatidylinositol kinase is associated with the epidermal growth factor (EGF) receptor following EGF stimulation.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3816-20 PMID: 2160078
  40. Structural features of the colony-stimulating factor 1 receptor that affect its association with phosphatidylinositol 3-kinase.
    EMBO J. 1990 Aug;9(8):2415-21 PMID: 2164469
  41. Phosphorylation of the PDGF receptor beta subunit creates a tight binding site for phosphatidylinositol 3 kinase.
    EMBO J. 1990 Oct;9(10):3279-86 PMID: 2170111
  42. Binding of SH2 domains of phospholipase C gamma 1, GAP, and Src to activated growth factor receptors.
    Science. 1990 Nov 16;250(4983):979-82 PMID: 2173144
  43. Purification and characterization of phosphoinositide 3-kinase from rat liver.
    J Biol Chem. 1990 Nov 15;265(32):19704-11 PMID: 2174051
  44. Src homology region 2 domains direct protein-protein interactions in signal transduction.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8622-6 PMID: 2236073
  45. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus.
    Nature. 1986 Mar 20-26;320(6059):277-80 PMID: 2421165
  46. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand.
    EMBO J. 1987 Nov;6(11):3341-51 PMID: 2448137
  47. A novel viral oncogene with structural similarity to phospholipase C.
    Nature. 1988 Mar 17;332(6161):272-5 PMID: 2450282
  48. Role of phosphatidylinositol kinase in PDGF receptor signal transduction.
    Science. 1989 Mar 3;243(4895):1191-4 PMID: 2466336
  49. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling.
    Cell. 1989 Jun 30;57(7):1101-7 PMID: 2472218
  50. Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro.
    Cell. 1989 Jun 30;57(7):1109-22 PMID: 2472219
  51. PDGF induction of tyrosine phosphorylation of GTPase activating protein.
    Nature. 1989 Dec 7;342(6250):711-4 PMID: 2480526
  52. Phospholipase C-gamma, a substrate for PDGF receptor kinase, is not phosphorylated on tyrosine during the mitogenic response to CSF-1.
    EMBO J. 1989 Nov;8(11):3345-50 PMID: 2555162
  53. The common src homology region 2 domain of cytoplasmic signaling proteins is a positive effector of v-fps tyrosine kinase function.
    Mol Cell Biol. 1989 Oct;9(10):4131-40 PMID: 2685548
  54. Murine c-fms cDNA: cloning, sequence analysis and retroviral expression.
    Oncogene Res. 1987 Sep-Oct;1(4):311-24 PMID: 2966922
  55. A specific combination of substrates is involved in signal transduction by the kit-encoded receptor.
    EMBO J. 1991 Mar;10(3):647-54 PMID: 1705885
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1992-03-00
Pages
991-7
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC369531
Subset
IM
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