Home LiteratureArticle Details
PMID: 16207817 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane.

Molecular biology of the cell ·Vol. 16 ·No. 12 ·2005-12-00 ·Pages 5832-42

Haslekås C, Breen K, Pedersen KW, Johannessen LE, Stang E, Madshus IH

Abstract

By constructing stably transfected cells harboring the same amount of epidermal growth factor (EGF) receptor (EGFR), but with increasing overexpression of ErbB2, we have demonstrated that ErbB2 efficiently inhibits internalization of ligand-bound EGFR. Apparently, ErbB2 inhibits internalization of EGF-bound EGFR by constitutively driving EGFR-ErbB2 hetero/oligomerization. We have demonstrated that ErbB2 does not inhibit phosphorylation or ubiquitination of the EGFR. Our data further indicate that the endocytosis deficiency of ErbB2 and of EGFR-ErbB2 heterodimers/oligomers cannot be explained by anchoring of ErbB2 to PDZ-containing proteins such as Erbin. Instead, we demonstrate that in contrast to EGFR homodimers, which are capable of inducing new clathrin-coated pits in serum-starved cells upon incubation with EGF, clathrin-coated pits are not induced upon activation of EGFR-ErbB2 heterodimers/oligomers.

MeSH Terms
Animals Aorta Cell Membrane/drug effects,physiology Clathrin-Coated Vesicles/drug effects,physiology,ultrastructure Endothelium, Vascular/cytology,drug effects,physiology Epidermal Growth Factor/antagonists & inhibitors,pharmacology ErbB Receptors/metabolism,physiology Humans Microscopy, Confocal Receptor, ErbB-2/physiology Swine
Chemicals
Epidermal Growth Factor ErbB Receptors Receptor, ErbB-2
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Haslekås Camilla
Institute of Pathology, University of Oslo, Rikshospitalet, 0027 Oslo, Norway.
Breen Kamilla
Pedersen Ketil W
Johannessen Lene E
Stang Espen
Madshus Inger Helene
References (41)
41 references, click to expand
  1. Immunoelectron microscopy using thin, frozen sections: application to studies of the intracellular transport of Semliki Forest virus spike glycoproteins.
    Methods Enzymol. 1983;96:466-85 PMID: 6656640
  2. ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases.
    J Cell Biol. 2000 Jan 24;148(2):385-97 PMID: 10648571
  3. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene.
    Science. 1987 Jan 9;235(4785):177-82 PMID: 3798106
  4. erbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells.
    Science. 1987 Jul 10;237(4811):178-82 PMID: 2885917
  5. Quantitative analysis of the endocytic system involved in hormone-induced receptor internalization.
    J Biol Chem. 1990 Sep 15;265(26):15713-23 PMID: 1975591
  6. Transformation mediated by the human HER-2 gene independent of the epidermal growth factor receptor.
    Oncogene. 1992 Sep;7(9):1859-66 PMID: 1354348
  7. The carboxyl terminus of epidermal growth factor receptor/erbB-2 chimerae is internalization impaired.
    Oncogene. 1993 Nov;8(11):3021-8 PMID: 8105439
  8. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin.
    J Biol Chem. 1994 May 20;269(20):14661-5 PMID: 7514177
  9. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3.
    EMBO J. 1995 Sep 1;14(17):4267-75 PMID: 7556068
  10. All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired.
    J Biol Chem. 1996 Mar 1;271(9):5251-7 PMID: 8617810
  11. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions.
    EMBO J. 1996 May 15;15(10):2452-67 PMID: 8665853
  12. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers.
    EMBO J. 1998 Jun 15;17(12):3385-97 PMID: 9628875
  13. Crystal structure of a truncated epidermal growth factor receptor extracellular domain bound to transforming growth factor alpha.
    Cell. 2002 Sep 20;110(6):763-73 PMID: 12297049
  14. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains.
    Cell. 2002 Sep 20;110(6):775-87 PMID: 12297050
  15. Novel mode of ligand recognition by the Erbin PDZ domain.
    J Biol Chem. 2003 Jan 17;278(3):1399-402 PMID: 12444095
  16. The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors.
    Mol Cell. 2003 Feb;11(2):495-505 PMID: 12620236
  17. Grb2 regulates internalization of EGF receptors through clathrin-coated pits.
    Mol Biol Cell. 2003 Mar;14(3):858-70 PMID: 12631709
  18. Polar expression of ErbB-2/HER2 in epithelia. Bimodal regulation by Lin-7.
    Dev Cell. 2003 Sep;5(3):475-86 PMID: 12967566
  19. HER2-mediated effects on EGFR endosomal sorting: analysis of biophysical mechanisms.
    Biophys J. 2003 Oct;85(4):2732-45 PMID: 14507736
  20. Association with membrane protrusions makes ErbB2 an internalization-resistant receptor.
    Mol Biol Cell. 2004 Apr;15(4):1557-67 PMID: 14742716
  21. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference.
    J Biol Chem. 2004 Apr 16;279(16):16657-61 PMID: 14985334
  22. Endocytosed epidermal growth factor (EGF) receptors contribute to the EGF-mediated growth arrest in A431 cells by inducing a sustained increase in p21/CIP1.
    Exp Cell Res. 1998 Aug 25;243(1):161-72 PMID: 9716460
  23. Removal of the membrane-anchoring domain of epidermal growth factor leads to intracrine signaling and disruption of mammary epithelial cell organization.
    J Cell Biol. 1998 Nov 30;143(5):1317-28 PMID: 9832559
  24. ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors.
    J Biol Chem. 1999 Mar 26;274(13):8865-74 PMID: 10085130
  25. Inhibition of clathrin-coated pit assembly by an Eps15 mutant.
    J Cell Sci. 1999 May;112 ( Pt 9):1303-11 PMID: 10194409
  26. Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation.
    Mol Biol Cell. 1999 May;10(5):1621-36 PMID: 10233167
  27. erbB-2 overexpression in human mammary epithelial cells confers growth factor independence.
    Endocrinology. 1999 Aug;140(8):3615-22 PMID: 10433219
  28. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin.
    Mol Biol Cell. 2004 Dec;15(12):5268-82 PMID: 15385631
  29. ERBIN: a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor.
    Nat Cell Biol. 2000 Jul;2(7):407-14 PMID: 10878805
  30. Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases.
    FEBS Lett. 2001 Feb 16;490(3):142-52 PMID: 11223029
  31. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking.
    Traffic. 2000 Mar;1(3):248-58 PMID: 11208108
  32. Untangling the ErbB signalling network.
    Nat Rev Mol Cell Biol. 2001 Feb;2(2):127-37 PMID: 11252954
  33. The ERBB2/HER2 receptor differentially interacts with ERBIN and PICK1 PSD-95/DLG/ZO-1 domain proteins.
    J Biol Chem. 2001 May 4;276(18):15256-63 PMID: 11278603
  34. The J chain is essential for polymeric Ig receptor-mediated epithelial transport of IgA.
    J Immunol. 2001 Nov 1;167(9):5185-92 PMID: 11673531
  35. Biology of HER2 and its importance in breast cancer.
    Oncology. 2001;61 Suppl 2:1-13 PMID: 11694782
  36. Signal transduction and endocytosis: close encounters of many kinds.
    Nat Rev Mol Cell Biol. 2002 Aug;3(8):600-14 PMID: 12154371
  37. Herceptin-induced inhibition of ErbB2 signaling involves reduced phosphorylation of Akt but not endocytic down-regulation of ErbB2.
    Int J Cancer. 2005 Sep 1;116(3):359-67 PMID: 15800944
  38. Ligand-induced, receptor-mediated dimerization and activation of EGF receptor.
    Cell. 2002 Sep 20;110(6):669-72 PMID: 12297041
  39. c-erbB-2/EGFR as dominant heterodimerization partners determine a motogenic phenotype in human breast cancer cells.
    FASEB J. 1999 Nov;13(14):1939-49 PMID: 10544177
  40. Biochemical and clinical implications of the ErbB/HER signaling network of growth factor receptors.
    Adv Cancer Res. 2000;77:25-79 PMID: 10549355
  41. On the preparation of cryosections for immunocytochemistry.
    J Ultrastruct Res. 1984 Oct;89(1):65-78 PMID: 6544882
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-12-00
Epub
2005-00-05
Pages
5832-42
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1289425
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