51
Views
48
CrossRef citations to date
0
Altmetric
Original Article

Take Your Partners, Please — Signal Diversification by the erbB Family of Receptor Tyrosine Kinases

Pages 255-263 | Received 25 Jan 1999, Accepted 10 Feb 1999, Published online: 11 Jul 2009

References

  • Alimandi M., Wang L.-M., Bottaro D., Lee C. C., Kuo A., Frankel M., Fedi P., Tang C., Lippman M., Pierce J. Epidermal growth factor and betacellulin mediate signal transduction through co-expressed ErbB2 and ErbB3 receptors. EMBO J. 1997; 16: 5608–5617
  • Barbacci E., Guarino B., Stroh J., Singleton D., Rosnack K., Moyer J., Andrews G. The structural basis for the specificity of epidermal growth factor and heregulin binding. J. Biol. Chem. 1995; 270: 9585–9589
  • Batzer A. G., Blaikie P., Nelson K., Schlessinger J., Margolis B. The phosphotyrosine interaction domain of She binds an LXNPXY motif on the epidermal growth factor receptor. Mol. Cell. Biol. 1995; 15: 4403–4409
  • Batzer A. G., Rotin D., Urena J. M., Skolnik E. Y., Schlessinger J. Hierarchy of binding sites for Grb2 and She on the epidermal growth factor receptor. Mol. Cell. Biol. 1994; 14: 5192–5201
  • Baulida J., Kraus M., Alimandi M., Di Fiore P., Carpenter G. All erbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 1996; 271: 5251–5257
  • Beerli R., Hynes N. Epidermal growth factor-related peptides activate distinct subsets of ErbB receptors and differ in their biological activities. J. Biol. Chem. 1996; 271: 6071–6076
  • Busfield S., Michnick D., Chickering T., Revett T., Ma J., Woolf E., Comrack C., Dussault B., Woolf J., Goodearl A., Gearing D. Characterization of a neuregulin-related gene, Don-1, that is highly expressed in restricted regions of the cerebellum and hippocampus. Mol. Cell. Biol. 1997; 17: 4007–4014
  • Carraway K., Weber J., Unger M., Ledesma J., Yu N., Gassman M., Lai C. Neuregulin-2, a new ligand of ErbB3. ErbB4-receptor tyrosine kinases. Nature 1997; 387: 512–516
  • Carraway K. L., III, Sliwkowski M. X., Akita R., Platko J. V., Guy P. M., Nuijens A., Diamonti A. J., Vandlen R. L., Cantley L. C., Cerione R. A. The erbB3 gene product is a receptor for heregulin. J. Biol. Chem. 1994; 269: 14303–14306
  • Chang H., Riese I I, Gilbert W. D., Stern D., McMahan U. Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature 1997; 387: 509–512
  • Cohen B., Green J., Foy L., Fell H. HER4-mediated biological and biochemical properties in NIH-3T3 cells. J. Biol. Chem. 1996; 271: 4813–4818
  • Crovello C., Lai C., Cantley L., Carraway K., III. Differential signaling by the epidermal growth factor-like growth factors neuregulin-1 and neuregulin-2. J. Biol. Chem. 1998; 273: 26954–26961
  • Di Fiore P. P., Pierce J. H., Kraus M. H., Segatto O., King C. R., Aaronson S. A. erbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science 1987; 237: 178–182
  • Elenius K., Paul S., Allison G., Sun J., Klagsbrun M. Activation of HER4 by heparin-binding EGF-like growth factor stimulates chemotaxis but not proliferation. EMBO J. 1997; 16: 1268–1278
  • Fazioli F., Kim U., Rhee S., Molloy C., Segatto O., Di Fiore P. The erbB-2 mitogenic signalling pathway: tyrosine phosphorylation of phospholipase C-γ and GTPase-activating protein does not correlate with erbB-2 mitogenic potency. Mol. Cell. Biol. 1991; 11: 2040–2048
  • Fcdi P., Pierce J. H., DiFiore P. P., Kraus M. H. Efficient coupling with phosphatidylinositol 3-kinase, but not phospholipase Cγ or GTPase activating protein, distinguishes erbB-3 signaling from that of other erbB: EGFR family members. Mol. Cell. Biol. 1994; 14: 492–500
  • Fiddes R. J., Campbell D. H., Janes P. W., Sivertsen S. P., Sasaki H., Wallasch C., Daly R. J. Analysis of Grb7 recruitment by heregulin-activated erbB receptors reveals a novel target selectivity for erbB3. J. Biol. Chem. 1998; 273: 7717–7724
  • Fiddes R. J., Janes P. W., Sanderson G. M., Sivertsen S. P., Sutherland R. L., Daly R. J. Heregulin (HRG)-induced mitogenic signaling and cytotoxic activity of a HRG PE40 ligand toxin in human breast cancer cells. Cell Growth Differ. 1995; 6: 1567–1577
  • Gassman M., Casagranda F., Orioli D., Simon H., Lai C., Klein R., Lemke G. Aberrant neural and cardiac development in mice lacking the erbB4 neuregulin receptor. Nature 1995; 378: 390–394
  • Graus-Porta D., Beerli R. R., Daly J. M., Hynes N. E. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 1997; 16: 1647–1655
  • Guy P. M., Platko J. V., Cantley L. C., Cerione R. A., Carraway K. L. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. USA 1994; 91: 8132–8136
  • Holgado-Madruga M., Emlet D., Moscatello D., Godwin A., Wong A. A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature 1996; 379: 560–564
  • Holmes W. E., Sliwkowski M. X., Akita R. W., Hcnzel W. J., Lee J., Park J. W., Yansura D., Abadi N., Raab H., Lewis C. D., Shepard H. M., Kuang W. J., Wood W. I., Goeddel D. V., Vandlen R. L. Identification of heregulin, a specific activator of p185erbB-2. Science 1992; 256: 1205–1210
  • Hu P., Margolis B., Skolnik E. Y., Lammers R., Ullrich A., Schlessinger J. Interaction of phosphatidylinositol 3-kinase-associated p85 with epidermal growth factor and platelet-derived growth factor receptors. Mol. Cell. Biol. 1992; 12: 981–990
  • Jacobsen N., Abadi N., Sliwkowski M., Reilly D., Skelton N., Fairbrother W. High-resolution solution structure of the EGF-like domain of heregulin-alpha. Biochemistry 1996; 35: 3402–3417
  • Janes P. W., Daly R. J., deFazio A., Sutherland R. L. Activation of the Ras signalling pathway in human breast cancer cell lines overexpressing erbB-2. Oncogene 1994; 9: 3601–3608
  • Karunagaran D., Tzahar E., Beerli R., Chen X., Graus-Porta D., Ratzkin B., Seger R., Hynes N., Yarden Y. ErbB2 is a common auxiliary subunit of NDF and EGF receptors: implications for breast cancer. EMBO J. 1996; 15: 254–264
  • Kim H. H., Sierke S. L., Koland J. G. Epidermal growth factor-dependent association of phosphatidyl 3-kinase with the erbH3 gene product. J. Biol. Chem. 1994; 269: 24747–24755
  • King C. R., Borrello I., Bellot F., Comoglio P., Schlessinger J. EGF binding to its receptor triggers a rapid tyrosine phosphorylation of the erbB-2 protein in the mammary tumor cell line SK-BR-3. EMBO J. 1988; 7: 1647–1651
  • Komurasaki T., Toyoda H., Uchida D., Morimoto S. Epiregulin binds to epidermal growth factor receptor and ErbB4 and induces tyrosine phosphorylation of epidermal growth factor receptor. ErbB2, ErbB3 and ErbB4. Oncogene 1997; 15: 2841–2848
  • Lee K. F., Simon H., Chen H., Bates B., Hung M. C., Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 1995; 378: 394–398
  • Lenferink A., Pinkas-Kramarski R., van de Poll M., van Vugt M., Klapper L., Tzahar E., Waterman H., Sela M., van Zoelen E., Yarden Y. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 1998; 17: 3385–3397
  • Levkowitz G., Klapper L. N., Tzahar E., Freywald A., Sela M., Yarden Y. Coupling of the c-Cbl proto-oncogene to erbB-1/EGF-receptor but not to other erbB proteins. Oncogene 1996; 12: 1117–1125
  • Lonardo F., Di Marco E., King C. R., Pierce J. H., Segatto O., Aaronson S. A., Di Fiore P. P. The normal erbB-2 product is an atypical receptor-like tyrosine kinase with constitutive activity in the absence of ligand. New Biol. 1990; 2: 992–1003
  • Lowenstein E. J., Daly R. J., Batzer A. G., Li W., Margolis B., Lammers R., Ullrich A., Skolnik E. Y., Bar-Sagi D., Schlessinger J. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signalling. Cell 1992; 70: 431–442
  • Luttrell D. K., Lee A., Lansing T. J., Crosby R. M., Jung K. D., Willard D., Luther M., Rodriguez M., Berman J., Gilmer T. M. Involvement of pp60c-src with two major signalling pathways in human breast cancer. Proc. Natl. Acad. Sci. USA 1994; 91: 83–87
  • Margolis B., Rhee S. G., Felder S., Mervic M., Lyall R., Levitzki A., Ullrich A., Zilberstein A., Schlessinger J. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling. Cell 1989; 57: 1101–1107
  • Margolis B., Silvennoinen O., Comoglio F., Roonprapunt C., Skolnik E., Ullrich A., Schlessinger J. High-efficiency expression/cloning of epidermal growth factor receptor-binding proteins with src homology 2 domains. Proc. Natl. Acad. Sci. USA 1992; 89: 8894–8898
  • Massague J. Transforming growth factor-α, a model for membrane-anchored growth factors. J. Biol. Chem. 1990; 265: 21393–21396
  • Mc Innes C., Sykes B. Growth factor receptors: structure, mechanism and drug discovery. Biopolymers 1998; 43: 339–366
  • Muthuswamy S., Muller W. Direct and specific interaction of c-Src with Neu is involved in signaling by the epidermal growth factor receptor. Oncogene 1995; 11: 271–279
  • Nagata K., Kohda D., Hatanaka H., Ichikawa S., Matsuda S., Yamamoto T., Suzuki A., Inagaki F. Solution structure of the epidermal growth factor-like domain of heregulin-alpha, a ligand for p180erbB-4. EMBO J. 1994; 13: 3517–3523
  • Olayioye M., Graus-Porta D., Beerli R., Rohrer J., Gay B., Hynes N. EerbB-1 and ErbB-2 acquire distinct signaling properties dependent upon their dimerization partner. Mol. Cell. Biol. 1998; 18: 5042–5051
  • Peles E., Levy R., Or E., Ullrich A., Yarden Y. Oncogenic forms of the neu/HER2 tyrosine kinase are permanently coupled to phospholipase Cγ. EMBO J. 1991; 10: 2077–2086
  • Pinkas-Kramarski R., Alroy I., Yarden Y. ErbB receptors and EGF-like ligands: cell lineage determination and oncogenesis through combinatorial signaling. J. Mammary Gland Biol. Neoplasia 1997; 2: 97–107
  • Pinkas-Kramarski R., Lenferink A., Bacus S., Lyass L., van de Poll M., Klapper L., Tzahar E., Sela M., van Zoelen E., Yarden Y. The oncogenic ErbB-2/ErbB-3 heterodimer is a surrogate receptor of the epidermal growth factor and betacellulin. Oncogene 1998a; 16: 1249–1258
  • Pinkas-Kramarski R., Shelly M., Glathe S., Ratzkin B., Yarden Y. Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J. Biol. Chem. 1996; 271: 19029–19032
  • Pinkas-Kramarski R., Shelly M., Guarino B., Wang L., Lyass L., Alroy I., Alamandi M., Kuo A., Moyer J., Lavi S., Eisenstein M., Ratzkin B., Seger R., Bacus S., Pierce J., Andrews G., Yarden Y. ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. Mol. Cell. Biol. 1998b; 18: 6090–6101
  • Plowman G. D., Green J. M., Culouscou J. M., Carlton G. W., Rothwell V. M., Buckley S. Heregulin induces tyrosine phosphorylation of HER4/p180erbB4. Nature 1993; 366: 473–475
  • Prigent S. A., Gullick W. J. Identification of c-erbB-3 binding sites for phosphatidylinositol 3-kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J. 1994; 13: 2831–2841
  • Ricci A., Lanfrancone L., Chiari R., Belardo G., Pertica C., Natali P. G., Pelicci P. G., Segatto O. Analysis of protein-protein interactions involved in the activation of the Shc/Grb2 pathway by the erbB-2 kinase. Oncogene 1995; 11: 1519–1529
  • Riese D., II, van Raaij T., Plowman G., Andrews G., Stern D. The cellular response to neuregulins is governed by complex interactions of the erbB receptor family. Mol. Cell. Biol. 1995; 15: 5770–5776
  • Riese D. J., II, Bermingham Y., van Raaij T. M., Buckley S., Plowman G. D., Stern D. F. Betacellulin activates the epidermal growth factor receptor and erbB-4, and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-ß. Oncogene 1996; 12: 345–353
  • Riethmacher D., Sonnenberg-Riethmacher E., Brinkmann V., Yamaai T., Lewin G., Birchmeier C. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 1997; 389: 725–729
  • Sepp-Lorenzino L., Eberhard I., Ma Z., Cho C., Serve H., Liu F., Rosen N., Lupu R. Signal transduction pathways induced by heregulin in MDA-MB-453 breast cancer cells. Oncogene 1996; 12: 1679–1687
  • Sibilia M., Wagner E. Strain-dependent epithelial defects in mice lacking EGF receptor. Science 1995; 269: 234–238
  • Slamon D. J., Godolphin W., Jones L. A., Holt J. A., Wong S. G., Keith D. E., Levin W. J., Stuart S. G., Udove J., Ullrich A., Press M. F. Studies of the HER2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244: 707–712
  • Sliwkowski M. X., Schaefer G., Akita R. W., Lofgren J. A., Fitzpatrick V. D., Nuijens A., Fendly B. M., Cerione R. A., Vandlen R. L., Carraway K. L. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 1994; 269: 14661–14665
  • Soltoff S. P., Carraway K. L., Prigent S. A., Gullick W. G., Cantley L. C. ErbB3 is involved in activation of phosphatidyl 3-kinase by epidermal growth factor. Mol. Cell. Biol. 1994; 14: 3550–3558
  • Stover D., Becker M., Liebetanz J., Lydon N. Src phosphorylation of the epidermal growth factor receptor at novel sites mediates receptor interaction with Src and p85α. J. Biol. Chem. 1995; 270: 15591–15597
  • Threadgill D., Dlugosz A., Hansen L., Tennenbaum T., Lichti U., Yee D., La-Mantia C., Mourton T., Herrup K., Harris R., Barnard J., Yuspa S., Coffey R., Magnuson T. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 1995; 269: 230–234
  • Tzahar E., Levkowitz G., Karunagaran D., Yi L., Peles E., Lavi S., Chang D., Liu N., Yayon A., Wen D., Yarden Y. ErbB-3 and ErbB-4 function as the respective low and high affinity receptors of all neu differentiation factor/heregulin isoforms. J. Biol. Chem. 1994; 269: 25226–25233
  • Tzahar E., Pinkas-Kramarski R., Moyer J., Klapper L., Alroy I., Levkowitz G., Shelly M., Henis S., Eisenstein S., Ratzkin B., Sela M., Andrews G., Yarden Y. Bivalence of EGF-like ligands drives the ErbB signaling network. EMBO J. 1997; 16: 4938–4950
  • Tzahar E., Waterman H., Chen X., Levkowitz G., Karunagaran D., Lavi S., Ratzkin B., Yarden Y. A hierarchical network of interreceptor interactions determines signal transduction by neu differentiation factor neuregulin and epidermal growth factor. Mol. Cell. Biol. 1996; 16: 5276–5287
  • Wada T., Qian X., Greene M. I. Intermolecular association of p185neu protein and EGF receptor modulates EGF receptor function. Cell 1990; 61: 1339–1347
  • Wallasch C., Weiss F., Niederfellner G., Jallal B., Issing W., Ullrich A. Heregulin-dependent regulation of HER2 neu oncogenic signaling by heterodimerization with HER3. EMBO J. 1995; 14: 4267–4275
  • Wen D., Peles E., Cupples R., Suggs S. V., Bacus S. S., Luo Y., Trail G., Hu S., Silbiger S. M., Levy R. B., BenLevy R., Koski R. A., Lu H. S., Yarden Y. Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 1992; 69: 559–572
  • Wong A., Ruppert J., Bigner S., Grzeschik C., Humphrey P., Bigner D., Vogelstein B. Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc. Natl. Acad. Sci (USA) 1992; 89: 2965–2969
  • Zhang D., Sliwkowski M., Mark M., Frantz G., Akita R., Sun Y., Hillan K., Crowley C., Brush J., Godowski P. Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Natl. Acad. Sci (USA) 1997; 94: 9562–9567
  • Zhang K., Sun J., Liu N., Wen D., Chang D., Thomason A., Yoshinaga S. Transformation of NIH 3T3 cells by HER3 or HER4 receptors requires the presence of HER1 or HER2. J. Biol. Chem. 1996; 271: 3884–3890

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.