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PMID: 7698994 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Recruitment of epidermal growth factor receptors into coated pits requires their activated tyrosine kinase.

The Journal of cell biology ·Vol. 129 ·No. 1 ·1995-04-00 ·Pages 47-54

Lamaze C, Schmid SL

Abstract

EGF-receptor (EGF-R) tyrosine kinase is required for the down-regulation of activated EGF-R. However, controversy exists as to whether ligand-induced activation of the EGF-R tyrosine kinase is required for internalization or for lysosomal targeting. We have addressed this issue using a cell-free assay that selectively measures the recruitment of EGF-R into coated pits. Here we show that EGF bound to wild-type receptors is efficiently sequestered in coated pits. In contrast, sequestration of kinase-deficient receptors occurs inefficiently and at the same basal rate of endocytosis of unoccupied receptors or receptors lacking any cytoplasmic domain. Sequestration of deletion mutants of the EGF-R that lack autophosphorylation sites also requires an active tyrosine kinase. This suggests that a tyrosine kinase substrate(s) other than the EGF-R itself, is required for its efficient ligand-induced recruitment into coated pits. Addition of a soluble EGF-R tyrosine kinase fully and specifically restores the recruitment of kinase-deficient EGF-R into coated pits providing a powerful functional assay for identification of these substrate(s).

MeSH Terms
Animals Cell Line, Transformed Coated Pits, Cell-Membrane/metabolism Down-Regulation Endocytosis Epidermal Growth Factor/metabolism ErbB Receptors/biosynthesis,genetics,metabolism Humans Kinetics L Cells Lysine Methionine Mice Mutagenesis, Site-Directed Recombinant Proteins/biosynthesis,metabolism Transfection
Chemicals
Recombinant Proteins Epidermal Growth Factor Methionine ErbB Receptors Lysine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lamaze C
Department of Cell Biology, Scripps Research Institute, La Jolla, California 92037.
Schmid S L
References (36)
36 references, click to expand
  1. Ligand-induced endocytosis of the EGF receptor is blocked by mutational inactivation and by microinjection of anti-phosphotyrosine antibodies.
    Cell. 1988 Mar 11;52(5):675-84 PMID: 2449972
  2. Kinetics of binding, endocytosis, and recycling of EGF receptor mutants.
    J Cell Biol. 1992 Apr;117(1):203-12 PMID: 1556153
  3. 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
  4. Recruitment of epidermal growth factor and transferrin receptors into coated pits in vitro: differing biochemical requirements.
    Mol Biol Cell. 1993 Jul;4(7):715-27 PMID: 8400457
  5. Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation.
    Cell. 1989 Oct 6;59(1):33-43 PMID: 2790960
  6. Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body.
    Cell. 1990 May 18;61(4):623-34 PMID: 2344614
  7. The GTPase dynamin binds to and is activated by a subset of SH3 domains.
    Cell. 1993 Oct 8;75(1):25-36 PMID: 8402898
  8. Endocytosis of growth factor receptors.
    Bioessays. 1993 Jun;15(6):375-82 PMID: 8395172
  9. Point mutation at the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing.
    Cell. 1987 Oct 23;51(2):199-209 PMID: 3499230
  10. Ligand-induced internalization and increased cell calcium are mediated via distinct structural elements in the carboxyl terminus of the epidermal growth factor receptor.
    J Biol Chem. 1991 Dec 5;266(34):23467-70 PMID: 1744139
  11. Requirement for intrinsic protein tyrosine kinase in the immediate and late actions of the EGF receptor.
    Nature. 1987 Aug 27-Sep 2;328(6133):820-3 PMID: 3498122
  12. Oncogenes and signal transduction.
    Cell. 1991 Jan 25;64(2):281-302 PMID: 1846320
  13. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431.
    J Cell Biol. 1979 May;81(2):382-95 PMID: 313931
  14. Internalization and down-regulation of the human epidermal growth factor receptor are regulated by the carboxyl-terminal tyrosines.
    J Biol Chem. 1991 May 5;266(13):8363-8 PMID: 2022652
  15. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation.
    J Cell Biol. 1994 Nov;127(4):915-34 PMID: 7962076
  16. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor.
    Science. 1990 Feb 23;247(4945):962-4 PMID: 2305263
  17. Ligand-induced internalization of the epidermal growth factor receptor is mediated by multiple endocytic codes analogous to the tyrosine motif found in constitutively internalized receptors.
    J Biol Chem. 1993 Sep 15;268(26):19312-20 PMID: 8396132
  18. Mathematical model for the effects of epidermal growth factor receptor trafficking dynamics on fibroblast proliferation responses.
    Biotechnol Prog. 1992 Mar-Apr;8(2):132-43 PMID: 1368006
  19. Epidermal growth factor: receptor and ligand expression in human breast cancer.
    Semin Cancer Biol. 1990 Oct;1(5):305-15 PMID: 2103505
  20. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells.
    J Biol Chem. 1993 Dec 5;268(34):25846-56 PMID: 7503989
  21. Receptor tyrosine kinase substrates: src homology domains and signal transduction.
    FASEB J. 1992 Nov;6(14):3283-9 PMID: 1385243
  22. Growth factor-induced binding of dynamin to signal transduction proteins involves sorting to distinct and separate proline-rich dynamin sequences.
    EMBO J. 1994 Jun 1;13(11):2574-82 PMID: 8013457
  23. Disruption of PDGF receptor trafficking by mutation of its PI-3 kinase binding sites.
    Science. 1994 Feb 4;263(5147):684-7 PMID: 8303278
  24. The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor.
    J Biol Chem. 1991 Jun 15;266(17):11083-94 PMID: 1645724
  25. Monoclonal anti-epidermal growth factor receptor antibodies which are inhibitors of epidermal growth factor binding and antagonists of epidermal growth factor binding and antagonists of epidermal growth factor-stimulated tyrosine protein kinase activity.
    J Biol Chem. 1984 Jun 25;259(12):7755-60 PMID: 6330079
  26. Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. Contrasting significance of tyrosine 992 in the native and truncated receptors.
    J Biol Chem. 1992 Apr 25;267(12):8672-8 PMID: 1314835
  27. Separate endocytic pathways of kinase-defective and -active EGF receptor mutants expressed in same cells.
    J Cell Biol. 1990 May;110(5):1541-8 PMID: 2335562
  28. Microtubules and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11468-72 PMID: 7505438
  29. An essential role for a protein and lipid kinase complex in secretory protein sorting.
    Trends Cell Biol. 1992 Dec;2(12):363-8 PMID: 14731957
  30. Receptor-mediated endocytosis in semiintact cells.
    Methods Enzymol. 1992;219:223-34 PMID: 1487996
  31. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis.
    J Cell Biol. 1993 Jan;120(1):37-45 PMID: 8416994
  32. Activation of the purified protein tyrosine kinase domain of the epidermal growth factor receptor.
    J Biol Chem. 1989 Jul 5;264(19):11346-53 PMID: 2661557
  33. Analysis of deletions of the carboxyl terminus of the epidermal growth factor receptor reveals self-phosphorylation at tyrosine 992 and enhanced in vivo tyrosine phosphorylation of cell substrates.
    J Biol Chem. 1990 Jan 25;265(3):1750-4 PMID: 1688559
  34. Stage-specific assays for coated pit formation and coated vesicle budding in vitro.
    J Cell Biol. 1991 Sep;114(5):869-80 PMID: 1908470
  35. Anomalous binding of epidermal growth factor to A431 cells is due to the effect of high receptor densities and a saturable endocytic system.
    J Cell Biol. 1988 Aug;107(2):801-10 PMID: 3262110
  36. Interaction of activated EGF receptors with coated pit adaptins.
    Science. 1993 Jul 30;261(5121):612-5 PMID: 8342026
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1995-04-00
Pages
47-54
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120379
Subset
IM
Grants
NCI NIH HHS · CA27489 · United States
NCI NIH HHS · CA58689 · United States
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