Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2

Journal of Cell Science

Volumn 115, Issue 22, 2002, Pages 4251-4262

  Nagy, Peter ^a,b,c   Vereb, György ^a   Sebestyén, Zsolt ^a   Horváth, Gábor ^a   Lockett, Stephen J ^d,f   Damjanovich, Sándor ^a,b   Park, John W ^e   Jovin, Thomas M ^c   Szöllosi, János ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Breast cancer; ErbB proteins; Fluorescence resonance energy transfer; Lipid rafts

Indexed keywords

BINDING PROTEIN; CHOLERA TOXIN; EPIDERMAL GROWTH FACTOR; GANGLIOSIDE GM1; LIPID; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 4D5; NEU DIFFERENTIATION FACTOR; ONCOPROTEIN; PROTEIN SHC; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; TRASTUZUMAB; TYROSINE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CELL SURFACE RECEPTOR; CYTOSKELETON PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SRC HOMOLOGY 2 DOMAIN CONTAINING, TRANSFORMING PROTEIN 1; SRC HOMOLOGY 2 DOMAIN-CONTAINING, TRANSFORMING PROTEIN 1; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANTIBODY LABELING; BETA CHAIN; BREAST CANCER; CANCER CELL CULTURE; CANCER IMMUNOTHERAPY; CELL PROLIFERATION; CYTOSKELETON; DENSITY; DIMERIZATION; ENERGY TRANSFER; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTERNALIZATION; MALIGNANT NEOPLASTIC DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION; ARTICLE; BREAST TUMOR; CARCINOMA; CELL CULTURE; CELL DIVISION; CELL MEMBRANE; CELL TRANSFORMATION; DRUG EFFECT; EUKARYOTIC CELL; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; MACROMOLECULE; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; ULTRASTRUCTURE;

MURINAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CARCINOMA; CELL DIVISION; CELL MEMBRANE; CELL TRANSFORMATION, NEOPLASTIC; CHOLERA TOXIN; CYTOSKELETAL PROTEINS; DIMERIZATION; EUKARYOTIC CELLS; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MACROMOLECULAR SUBSTANCES; MEMBRANE MICRODOMAINS; ONCOGENE PROTEINS V-ERBB; PROTEIN BINDING; PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 0037112996     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00118     Document Type: Review

References (55)

1. Alroy, I. and Yarden, Y. (1997). The ErbB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett. 410, 83-86.
2. Anderson, R. G. and Jacobson, K. (2002). A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821-1825.
3. Baeckstrom, D., Alford, D. and Taylor, P. J. (2000). Morphogenetic and proliferative responses to heregulin of mammary epithelial cells in vitro are dependent on HER2 and HER3 and differ from the responses to HER2 homodimerisation or hepatocyte growth factor. Int. J. Oncol. 16, 1081-1090.
4. Baulida, J. and Carpenter, G. (1997). Heregulin degradation in the absence of rapid receptor-mediated internalization. Exp. Cell Res. 232, 167-172.
5. 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.
6. Bodnár, A., Jenei, A., Bene, L., Damjanovich, S. and Matkó, J. (1996). Modification of membrane cholesterol level affects expression and clustering of class I HLA molecules at the surface of JY human lymphoblasts. Immunol. Lett. 54, 221-226.
7. Brock, R. and Jovin, T. M. (2001). Heterogeneity of signal transduction at the subcellular level: microsphere-based focal EGF receptor activation and stimulation of Shc translocation. J. Cell Sci. 114, 2437-2447.
8. Chamberlin, S. G. and Davies, D. E. (1998). A unified model of c-erbB receptor homo- and heterodimerisation. Biochim. Biophys. Acta 1384, 223-232.
9. Cobleigh, M. A., Vogel, C. L., Tripathy, D., Robert, N. J., Scholl, S., Fehrenbacher, L., Wolter, J. M., Paton, V., Shak, S., Lieberman, G. et al. (1999). Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol. 17, 2639-2648.
10. Demandolx, D. and Davoust, J. (1997). Multiparameter image cytometry: from confocal micrographs to subcellular fluorograms. Bioimaging 5, 159-169.
11. Edidin, M. (2001). Shrinking patches and slippery rafts: scales of domains in the plasma membrane. Trends Cell Biol. 11, 492-496.
12. Furuchi, T. and Anderson, R. G. (1998). Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J. Biol. Chem. 273, 21099-21104.
13. Germain, R. N. (2001). The T cell receptor for antigen: signaling and ligand discrimination. J. Biol. Chem. 276, 35223-35226.
14. Glasbey, C. A. and Horgan, G. W. (1995). Mathematical morphology. In Image Analysis for the Biological Sciences (ed. C. A. Glasbey and G. W. Horgan), pp. 125-152. John Wiley & Sons.
15. Graus Porta, D., Beerli, R. R., Daly, J. M. and Hynes, N. E. (1997). ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16, 1647-1655.
16. Harder, T. and Simons, K. (1997). Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9, 534-542.
17. Harder, T., Scheiffele, P., Verkade, P. and Simons, K. (1998). Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942.
18. Harris, R. A., Eichholtz, T. J., Hiles, I. D., Page, M. J. and O'Hare, M. J. (1999). New model of ErbB-2 over-expression in human mammary luminal epithelial cells. Int. J. Cancer 80, 477-484.
19. Hwang, J., Gheber, L. A., Margolis, L. and Edidin, M. (1998). Domains in cell plasma membranes investigated by near-field scanning optical microscopy. Biophys. J. 74, 2184-2190.
20. Ilangumaran, S., Arni, S., van Echten-Deckert, G., Borisch, B. and Hoessli, D. C. (1999). Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol. Biol. Cell 10, 891-905.
21. Jacobson, K. and Dietrich, C. (1999). Looking at lipid rafts? Trends. Cell Biol. 9, 87-91.
22. Janes, P. W., Ley, S. C. and Magee, A. I. (1999). Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461.
23. Jovin, T. M. and Arndt Jovin, D. J. (1989). FRET microscopy: Digital imaging of fluorescence resonance energy transfer. Application in cell biology. In Cell Structure and Function by Microspectrofluorometry (ed. E. Kohen and J. G. Hirschberg), pp. 99-117. San Diego, CA: Academic Press.
24. Karunagaran, D., Tzahar, E., Beerli, R. R., Chen, X., Graus Porta, D., Ratzkin, B. J., Seger, R., Hynes, N. E. and Yarden, Y. (1996). ErbB-2 is a common auxiliary subunit of NDF and EGF receptors: implications for breast cancer. EMBO J. 15, 254-264.
25. Kenworthy, A. K., Petranova, N. and Edidin, M. (2000). High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol. Biol. Cell 11, 1645-1655.
26. 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.
27. Kurzchalia, T. V. and Parton, R. G. (1999). Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11, 424-431.
28. Le, X. F., Vadlamudi, R., McWatters, A., Bae, D. S., Mills, G. B., Kumar, R. and Bast, R. C., Jr (2000). Differential signaling by an anti-p185(HER2) antibody and heregulin. Cancer Res. 60, 3522-3531.
29. Levkowitz, G., Klapper, L. N., Tzahar, E., Freywald, A., Sela, M. and Yarden, Y. (1996). Coupling of the c-Cbl protooncogene product to ErbB-1/EGF- receptor but not to other ErbB proteins. Oncogene 12, 1117-1125.
30. Levkowitz, G., Oved, S., Klapper, L. N., Harari, D., Lavi, S., Sela, M. and Yarden, Y. (2000). c-Cbl is a suppressor of the neu oncogene. J. Biol. Chem. 275, 35532-35539.
31. Matkó, J., Bodnár, A., Vereb, G., Bene, L., Vámosi, G., Szentesi, G., Szöllosi, J., Gáspár, R., Jr, Horejsi, V., Waldmann, T. A. et al. (2002). GPI-microdomains (membrane rafts) and signaling of the multi-chain interleukin-2 receptor in human lymphoma/leukemia T cell lines. Eur. J. Biochem. 269, 1199-1208.
32. Mineo, C., Gill, G. N. and Anderson, R. G. (1999). Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem. 274, 30636-30643.
33. Nagy, P., Bene, L., Balázs, M., Hyun, W. C., Lockett, S. J., Chiang, N. Y., Waldman, F. M., Feuerstein, B. G., Damjanovich, S. and Szöllosi, J. (1998). EGF-induced redistribution of erbB2 on breast tumor cells: Flow and image cytometric energy transfer measurements. Cytometry 32, 120-131.
34. Nagy, P., Jenei, A., Damjanovich, S., Jovin, T. M. and Szöllosi, J. (1999a). Complexity of signal transduction mediated by erbB2: clues to the potential of receptor-targeted cancer therapy. Pathol. Oncol. Res. 5, 255-271.
35. Nagy, P., Jenei, A., Kirsch, A. K., Szöllosi, J., Damjanovich, S. and Jovin, T. M. (1999b). Activation-dependent clustering of the erbB2 receptor tyrosine kinase detected by scanning near-field optical microscopy. J. Cell Sci. 112, 1733-1741.
36. Neve, R. M., Nielsen, U. B., Kirpotin, D., Poul, M. A., Marks, J. D. and Benz, C. C. (2001). Biological effects of anti-ErbB2 single chain antibodies selected for internalizing function. Biochem. Biophys. Res. Commun. 280, 274-279.
37. Nichols, B. J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4, 374-378.
38. Orlandi, P. A. and Fishman, P. H. (1998). Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141, 905-915.
39. Park, J. W., Tripathy, D., Campbell, M. J. and Esserman, L. J. (2000). Biological therapy of breast cancer. Biodrugs 14, 221-245.
40. Pinkas Kramarski, R., Shelly, M., Glathe, S., Ratzkin, B. J. and Yarden, Y. (1996). Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J. Biol. Chem. 271, 19029-19032.
41. Plyte, S., Majolini, M. B., Pacini, S., Scarpini, F., Bianchini, C., Lanfrancone, L., Pelicci, P. and Baldari, C. T. (2000). Constitutive activation of the Ras/MAP kinase pathway and enhanced TCR signaling by targeting the Shc adaptor to membrane rafts. Oncogene 19, 1529-1537.
42. Pralle, A., Keller, P., Florin, E. L., Simons,.K. and Horber, J. K. (2000). Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148, 997-1008.
43. Sarup, J. C., Johnson, R. M., King, K. L., Fendly, B. M., Lipari, M. T., Napier, M. A., Ullrich, A. and Shepard, H. M. (1991). Characterization of an anti-p185HER2 monoclonal antibody that stimulates receptor function and inhibits tumor cell growth. Growth Regul. 1, 72-82.
44. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
45. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A. and McGuire, W. L. (1987). Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182.
46. Slamon, D. J., Leyland-Jones, B., Shak, S., Fuchs, H., Paton, V., Bajamonde, A., Fleming, T., Eiermann, W., Wolter, J., Pegram, M. et al. (2001). Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. New Engl. J. Med. 344, 783-792.
47. Sliwkowski, M. X., Lofgren, J. A., Lewis, G. D., Hotaling, T. E., Fendly, B. M. and Fox, J. A. (1999). Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin. Oncol. 26, 60-70.
48. Spencer, K. S. R., Graus, P., Leng, J., Hynes, N. E. and Klemke, R. L. (2000). ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases. J. Cell Biol. 148, 385-397.
49. Szöllosi, J., Trón, L., Damjanovich, S., Helliwell, S. H., Arndt Jovin, D. and Jovin, T. M. (1984). Fluorescence energy transfer measurements on cell surfaces: a critical comparison of steady-state fluorimetric and flow cytometric methods. Cytometry 5, 210-216.
50. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J. and Yarden, Y. (1996). A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16, 5276-5287.
51. Vereb, G., Matkó, J., Vamosi, G., Ibrahim, S. M., Magyar, E., Varga, S., Szöllosi, J., Jenei, A., Gáspár, R., Jr, Waldmann, T. A. et al. (2000). Cholesterol-dependent clustering of IL-2Ralpha and its colocalization with HLA and CD48 on T lymphoma cells suggest their functional association with lipid rafts. Proc. Natl. Acad. Sci. USA 97, 6013-6018.
52. Vyas, K. A., Patel, H. V., Vyas, A. A. and Schnaar, R. L. (2001). Segregation of gangliosides GM1 and GD3 on cell membranes, isolated membrane rafts, and defined supported lipid monolayers. Biol. Chem. 382, 241-250.
53. Worthylake, R., Opresko, L. K. and Wiley, H. S. (1999). ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both erbB-2 and epidermal growth factor receptors. J. Biol. Chem. 274, 8865-8874.
54. Wouters, F. S., Bastiaens, P. I., Wirtz, K. W. and Jovin, T. M. (1998). FRET microscopy demonstrates molecular association of non-specific lipid transfer protein (nsL-TP) with fatty acid oxidation enzymes in peroxisomes. EMBO J. 17, 7179-7189.
55. Yarden, Y. and Sliwkowski, M. X. (2001). Untangling the ErbB signalling work. Nat. Rev. Mol. Cell. Biol. 2, 127-137.