Association with Membrane Protrusions Makes ErbB2 an Internalization-resistant Receptor

Molecular Biology of the Cell

Volumn 15, Issue 4, 2004, Pages 1557-1567

  Hommelgaard, Anette M ^a   Lerdrup, Mads ^a   Van Deurs, Bo ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2;

ARTICLE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOGOLD LABELING; INTERNALIZATION; LIGAND BINDING; MEMBRANE BINDING; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR BINDING; RECEPTOR DOWN REGULATION;

ACTINS; ANTIBODIES, MONOCLONAL; BICYCLO COMPOUNDS, HETEROCYCLIC; BIOTIN; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MEMBRANE; CENTRIFUGATION, DENSITY GRADIENT; CHOLESTEROL; CLATHRIN; CROSS-LINKING REAGENTS; CYTOSKELETON; DETERGENTS; DOWN-REGULATION; ENDOSOMES; EPIDERMAL GROWTH FACTOR; HUMANS; IMMUNOHISTOCHEMISTRY; LIGANDS; MEMBRANE MICRODOMAINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; NEUREGULIN-1; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, ERBB-2; RECEPTORS, TRANSFERRIN; SIGNAL TRANSDUCTION; SUCROSE; THIAZOLES; THIAZOLIDINES;

EID: 1642422374     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-08-0596     Document Type: Article

References (49)

1. Adam, L., Vadlamudi, R., Kondapaka, S.B., Chernoff, J., Mendelsohn, J., and Kumar, R. (1998). Heregulin regulates cytoskeletal reorganization and cell migration through the p21-activated kinase-1 via phosphatidylinositol-3 kinase. J. Biol. Chem. 273, 28238-28246.
2. Baulida, J., and Carpenter, G. (1997). Heregulin degradation in the absence of rapid receptor-mediated internalization Exp. Cell Res. 232, 167-172.
3. Baulida, J., Kraus, M.H., Alimandi, M., Di Fiore, P.P., and Carpenter, G. (1996). All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 271, 5251-5257.
4. Braccia, A., Villani, M., Immerdal, L., Niels-Christiansen, L.L., Nystrom, B.T., Hansen, G.H., and Danielsen, E.M. (2003). Microvillar membrane microdomains exist at physiological temperature: galectin-4's role as lipid raft stabilizer revealed by 'superrafts'. J. Biol. Chem. 19, 19.
5. Brandt, B.H., et al. (1999). c-erbB-2/EGFR as dominant heterodimerization partners determine a motogenic phenotype in human breast cancer cells. FASEB J. 13, 1939-1949.
6. Brown, D.A., and London, E. (2000). Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
7. Brown, D.A., and Rose, J.K. (1992). Sorting of GP1-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
8. Burgess, A.W., et al. (2003). An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12, 541-552.
9. Cao, H., Orth, J.D., Chen, J., Weller, S.G., Heuser, J.E., and McNiven, M.A. (2003). Cortactin is a component of clathrin-coated pits and participate in receptor-mediated endocytosis. Mol. Cell. Biol. 23, 2162-2170.
10. Chausovsky, A., Waterman, H., Elbaum, M., Yarden, Y., Geiger, B., and Bershadsky, A.D. (2000). Molecular requirements for the effect of neuregulin on cell spreading, motility and colony organization. Oncogene 19, 878-888.
11. Citri, A., Skaria, K.B., and Yarden, Y. (2003). The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp Cell Res. 284, 54-65.
12. da Costa, S. R., et al. (2003). Impairing actin filament or syndapin functions promotes accumulation of clathrin-coated vesicles at the apical plasma membrane of acinar epithelial cells. Mol. Biol. Cell 14, 4397-4413.
13. Drevot, P., Langlet, C., Guo, X.J., Bernard, A.M., Colard, O., Chauvin, J.P., Lasserre, R., and He, H.T. (2002). TCR signal initiation machinery is preassembled and activated in a subset of membrane rafts. EMBO J. 21, 1899-1908.
14. Eccles, S.A. (2001). The role of c-erbB-2/HER2/neu in breast cancer progression and metastasis. J. Mammary Gland Biol. Neoplasia 6, 393-406.
15. Feldner, J.C., and Brandt, B.H. (2002). Cancer cell motility-on the road from c-erbB-2 receptor steered signaling to actin reorganization. Exp. Cell Res. 272, 93-108.
16. Gaidarov, I., Santini, F., Warren, R.A., and Keen, J.H. (1999). Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1, 1-7.
17. Gilboa, L., Ben-Levy, R., Yarden, Y., and Henis, Y.I. (1995). Roles for a cytoplasmic tyrosine and tyrosine kinase activity in the interactions of Neu receptors with coated pits. J. Biol. Chem. 270, 7061-7067.
18. Hansen, S.H., Sandvig, K., and van Deurs, B. (1992). Internalization efficiency of the transferrin receptor. Exp. Cell Res. 199, 19-28.
19. Heerklotz, H. (2002). Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83, 2693-2701.
20. Hendriks, B.S., Opresko, L.K., Wiley, H.S., and Lauffenburger, D. (2003a). Coregulation of epidermal growth factor receptor/human epidermal growth factor receptor 2 (HER2) levels and locations: quantitative analysis of HER2 overepression effects. Cancer Res. 63, 1130-1137.
21. Hendriks, B.S., Opresko, L.K., Wiley, H.S., and Lauffenburger, D.A. (2003b). Quantitative analysis of HER2-mediated effects on HER2 and EGFR endocytosis: distribution of homo- and heterodimers depends on relative HER2 levels. J. Biol. Chem. 278, 243343-243351.
22. Hinrichsen, L., Harborth, J., Andrees, L., Weber, K., and Ungewickell, E.J. (2003). Effect of clathrin heavy chain- and alpha-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J. Biol. Chem. 278, 45160-45170.
23. Hurwitz, E., Stancovski, I., Sela, M., and Yarden, Y. (1995). Suppression and promotion of tumor growth by monoclonal antibodies to ErbB-2 differentially correlate with cellular uptake. Proc. Natl. Acad. Sci. USA 92, 3353-3357.
24. Klapper, L.N., Vaisman, N., Hurwitz, E., Pinkas-Kramarski, R., Yarden, Y., and Sela, M. (1997). A subclass of tumor-inhibitory monoclonal antibodies to ErbB-2/HER2 blocks crosstalk with growth factor receptors. Oncogene 14, 2099-2109.
25. Klapper, L.N., Waterman, H., Sela, M., and Yarden, Y. (2000). Tumor-inhibitory antibodies to HER-2/ErbB-2 may act by recruiting c-Cbl and enhancing ubiquitination of HER-2. Cancer Res. 60, 3384-3388:
26. Lenferink, A.E.G., et al. (1998). Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 17, 3385-3397.
27. Li, Y., Hua, F., Carraway, K.L., and Carraway, C.A. (1999). The p185(neu)-containing glycoprotein complex of a microfilament-associated signal transduction particle. Purification, reconstitution, and molecular associations with p58(gag) and actin. J. Biol. Chem. 274, 25651-25658.
28. Maier, L.A., Xu, F.J., Hester, S., Boyer, C.M., McKenzie, S., Bruskin, A.M., Argon, Y., and Bast, R.C., Jr. (1991). Requirements for the internalization of a murine monoclonal antibody directed against the HER-2/neu gene product c-erbB-2. Cancer Res. 51, 5361-5369.
29. Menard, S., Pupa, S.M., Campiglio, M., and Tagliabue, E. (2003). Biologic and therapeutic role of HER2 in cancer. Oncogene. 22, 6570-6578.
30. Miljan, E.A., and Bremer, E.G. (2002). Regulation of growth factor receptors by gangliosides. Science' STKE 2002. Available online at www.stke.org/cgi/content/full/sigtrans;2002/160/rel5.
31. Mineo, C., Gill, G.N., and Anderson, R.G.W. (1999). Regulated Migration of Epidermal Growth Factor Receptor from Caveolae. J. Biol. Chem. 274, 30636-30643.
32. Molina, M.A., Codony-Servat, J., Albanell, J., Rojo, F., Arribas, J., and Baselga, J. (2001). trastuzumab (herceptin), a humanized anti-Her2 receptor monoclonal antibody, inhibits basal and activated Her2 ectodomain cleavage in breast cancer cells. Cancer Res. 61, 4744-4749.
33. Muller, G. (2002). Dynamics of plasma membrane microdomains and crosstalk to the insulin signalling cascade. FEBS Lett. 531, 81-87.
34. Nagy, P., Vereb, G., Sebestyen, Z., Horvath, G., Lockett, S.J., Damjanovich, S., Park, J.W., Jovin, T.M., and Szollosi, J. (2002). Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2. J. Cell Sci. 115, 4251-4262.
35. Reese, D.M., and Slamon, D.J. (1997). HER-2/neu signal transduction in human breast and ovarian cancer stem cells. 15, 1-8.
36. Roepstorff, K., Thomsen, P., Sandvig, K., and van Deurs, B. (2002). Sequestration of EGF receptors in non-caveolar lipid rafts inhibits ligand binding. J. Biol. Chem. 277, 18954-18960.
37. Rubin, I., and Yarden, Y. (2001). The basic biology of HER2. Ann. Oncol. 12, S3-S8.
38. Sandvig, K., and van Deurs, B. (2002). Membrane traffic exploited by protein toxins. Annu. Rev. Cell Dev. Biol. 18, 1-24.
39. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
40. Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1, 31-39.
41. Slamon, D.J., et al. (1989). Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer Science 244, 707-712.
42. Sliwkowski, M.X., et al. (1994). Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269, 14661-14665.
43. Sorkin, A., Di Fiore, P.P., and Carpenter, G. (1993). The carboxyl terminus of epidermal growth factor receptor/erbB-2 chimerae is internalization impaired. Oncogene 8, 3021-3028.
44. Sorkin, A., and Von Zastrow, M. (2002). Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell. Biol. 3, 600-614.
45. Wang, Z., Zhang, L., Yeung, T.K., and Chen, X. (1999). Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell 10, 1621-1636.
46. Waterman, H., Sabanai, I., Geiger, B., and Yarden, Y. (1998). Alternative intracellular routing of ErbB receptors may determine signaling potency. J. Biol. Chem. 273, 13819-13827.
47. Yarden, Y. (2001). Biology of HER2 and its importance in breast cancer. Oncology. 61, 1-13.
48. Yarden, Y., and Sliwkowski, M.X. (2001). Untangling the ErbB signalling network. Nat. Rev. Mol. Cell. Biol. 2, 127-137.
49. Zhou, W., and Carpenter, G. (2001). Heregulin-dependent translocation and hyperphosphorylation of ErbB-2. Oncogene. 20, 3918-3920.