ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases

Journal of Cell Biology

Volumn 148, Issue 2, 2000, Pages 385-397

  Spencer, Kathryn S R ^a   Graus Porta, Diana ^b   Leng, Jie ^a   Hynes, Nancy E ^b   Klemke, Richard L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Adaptor proteins; Cell migration; Epidermal growth factor; ERK; Signal transduction

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR; PHOSPHOTRANSFERASE; TYROSINE KINASE RECEPTOR;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; BREAST NEOPLASMS; CELL MOVEMENT; CRK-ASSOCIATED SUBSTRATE PROTEIN; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; PEPTIDE FRAGMENTS; PHOSPHOPROTEINS; PROTEIN KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CRK; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, ERBB-2; RECEPTORS, GROWTH FACTOR; RECOMBINANT PROTEINS; RETINOBLASTOMA-LIKE PROTEIN P130; SIGNAL TRANSDUCTION;

EID: 0034707581     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.148.2.385     Document Type: Article

References (62)

1. Alroy, I., and Y. Yarden. 1997. The ErhB signaling network in embryogenesis and oncogenesis: signal diversification through combinatorial ligand-receptor interactions. FEBS Lett. 410:83-86.
2. Bacus, S.S., A. Gudkov, C.R. Zelnick, D. Chin, R. Stern, L. Stancovski, E. Peles, N. Ben-Baruch, H. Farhstein, R. Lupu, et al. 1993. Neu differentiation factor (Heregulin) induces expression of intracellular adhesion molecule I: implications for mammary tumors. Cancer Res. 53:5251-5261.
3. Beerli, R.R., and N.E. Hynes. 1996. Epidermal growth factor-related peptides activate distinct subsets of ErhB receptors and differ in their biological activities. J. Biol. Chem. 271:6071-6076.
4. Beerli, R.R., W. Wels, and N.E. Hynes. 1994. Intracellular expression of single-chain antibodies reverts ErbB-2 transformation. J. Biol. Chem. 269:23931-23936.
5. Ben-Levy, R.H., F. Paterson, C.J. Marshall, and Y. Yarden. 1994. A single autophosphorylation site confers oncogenicity to the Neu/ErbB-2 receptor and enables coupling to the MAP kinase pathway. EMBO (Eur. Mol. Biol. Organ.) J. 13:3302-3311.
6. Britsch, S., L. Li, S. Kirchoff, F. Theuring, V. Brinkman, C. Birchmeier, and D. Riethmacher. 1998. The erbB2 and erbB3 receptors and their ligand, neuregulin-1 are essential for development of the symathetic nervous system. Gen. Dev. 12:1825-1836.
7. Casamassima, A., and E. Rozengurt. 1998. Insulin-like growth factor I stimulates lyrosine phosphorylation of p130CAS focal adhesion kinase, and paxillin. J. Biol. Chem. 273:26149-26156.
8. Chausovsky, A., I. Tsarfaty, Z. Kam, Y. Yarden, B. Geiger, and A. Bershadsky. 1998. Morphogenetic effects of neuregulin (neu differentiation factor) in cultured epithelial cells. Mol. Biol. Cell. 9:3195-3209.
9. Chen, P., K. Gupta, and A. Wells. 1994. Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from milogenesis. J. Cell Biol. 124:547-555.
10. De Potter, C.R., and J. Ouatacker. 1993. The p185ErbB2 protein is localized on cell organelles involved in cell molility. Clin. Exp. Metastasis. 11:462-472.
11. Di Fiore, P.P., J.H. Pierce, T.P. Fleming R. Hazan, A. Ullrich, C. King, J. Schlessinger, and S. Aaronson. 1987a. Overexpression of the human EGF receptor confers and EGF-dependent transformed phenotype to NIH 3T3 cells. Cell. 51:1063-1070.
12. Di Fiore, P.P., J.H. Pierce, M.H. Kraus, O. Segatto, C.R. King, and S.A. Aaronson. 1987b. ErbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science, 237:178-182.
13. Dougall, W.C., X. Qian, N.C. Peterson, M.J. Miller, A. Samanta, and M.I. Greene. 1994. The neu-oncogene: signal transduction pathways, transformation mechanisms and evolving therapies. Oncogene. 9:2109-2123.
14. Dudley, D., L. Pang, S. Decker, A. Bridges, and A. Saltiel. 1995. A synthetic inhibitor of the milogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA. 92:7686-7689.
15. Elenius, K., S. Paul, G. Allison, J. Sun, and M. Klagsbrun. 1997. Activation of HER4 by heparin-binding EGF-like growth factor stimulates chemotaxis but not proliferation. EMBO (Eur. Mol. Biol. Organ.) J. 16:1268-1278.
16. Falcioni, R., A. Antonini, P. Nistica, S. Di Stefano, M. Crescendi, P. Natali, and A. Sacchi. 1997. A6b4 and a6b1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp. Cell Res. 236:76-85.
17. Feller, S., R. Ren, H. Hanafusa, and D. Baltimore. 1994. SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Abl. TIBS. 19:453-458.
18. Friess, H., Y. Yammanaka, M.S. Kobrin, D. Da, M. Buchler, and M. Korc. 1995. Enhanced ErhB-3 expression in human pancreatic cancer correlates with tumor progression. Clin. Cancer Res. 1:1413-1420.
19. Gassmann, M., F. Casagranda, D. Orioli, H. Simon, C. Lai, R. Klein, G. Lemke. 1995. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature. 378:390-394.
20. Gilbertson, R.J., S.C. Clifford, W. MacMeckin, C. Wright, R.H. Perry, P. Kelly, A. Pearson, and J. Lunec. 1998. Expression of the ErhB-neuregulin signaling network during human cerebellar development: implications for the biology of medulloblastoma. Cancer Res. 58:3932-3941.
21. Graus-Porta, D., R.R. Beerli, and N.E. Hynes. 1995. Single-chain antibody-mediated intracellular retention of ErbB-2 impairs neu differentiation factor and epidermal growth factor signaling. Mol. Cell. Biol. 15:1182-1191.
22. Graus-Porta, D., R.R. Beerli, J.M. Daly, and N.E. Hynes. 1997. ErbB-2, the preferred heterodimerization partner of alt ErhB receptors, is a mediator of lateral signaling. EMBO (Eur. Mol. Biol. Organ.) J. 16:1647-1655.
23. Hynes, N.B., and D.F. Stern. 1994. The biology of ErhB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta. 1198:165-184.
24. Jones, F.E., D.J. Jerry, B.C. Guarino, G.C. Andrews, and D.F. Stern. 1996. Heregulin induces in vivo proliferation and differentiation of mammary epithelium into secretory lobuloalveoli. Cell Growth Differ. 7:1031-1038.
25. Karunagaran, D., E. Tzahar, R.R. Beerli, X. Chen, D. Graus-Porta, B.J. Ratzkin, R. Seger, N.E. Hynes, and Y. Yarden. 1996. ErhB-2 is a common auxiliary subunit of NDF and EGF receptors: implications for breast cancer. EMBO (Eur. Mol. Biol. Organ.) J. 15:254-264.
26. Keely, P.J., J.K. Westwick, I.P. Whitehead, C.J. Der, and L. Parise. 1997. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature. 390:632-636.
27. Kiyokawa, E., Y. Hasimoto, S. Kobayashi, H. Sugimura, T. Kurata, and M. Matsuda. 1998. Activalion of Rac1 by Crk SH3-binding protein, DOCKI80. Genes Dev. 12:3331-3336.
28. Klemke, R., S. Cai, A. Giannini, P. Gallagher, P. de Lanerolle, D. Cheresh. 1997. Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137:481-492.
29. Klemke, R.L., J. Leng, R. Molander, P.C. Brooks, K. Vuori, and D.A. Chcresh. 1998. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140:961-972.
30. Leavesley, D.I., G.D. Fergusion, E.A. Wayner, and D.A. Cheresh. 1992. Requirement of the integrin β3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen. J. Cell Biol. 117:1101-1107.
31. Lee, K., H. Simon, H. Chen, B. Bates, M. Hung, and C. Hauser. 1995. Requirement for neuregulin receptor ErbB2 in neural and cardiac development. Nature. 378:394-398.
32. Levkowitz, G.L., L.N. Klapper, E. Tzahar, A. Freywald, M. Sela, and Y. Yarden. 1996. Coupling of the c-CbI protooncogene to ErbB-1/EGF-receptor but not to other ErbB proteins. Oncogene. 12:1117-1125.
33. Li, J., M. Lin, J. Wiepz, A.G. Guadarrama, and P.J. Bertics. 1999. Integrin-medialed migration of murine B82L fibroblasts is dependent on the expression of an intact epidermal growth factor receptor. J. Biol. Chem. 274:11209-11219.
34. c-sfc with two major signaling pathways in human breast cancer. Proc. Natl. Acad. Sci. USA. 91:83-87.
35. Matsuda, M., and T. Kurata. 1996. Emerging components of the Crk oncogene product: the first identified adaptor protein. Cell. Signal. 8:335-340.
36. Matsuda, M., S. Nagata, S. Tanaka, K. Nagashima, T. Kurata. 1993. Structural requirement of Crk SH2 region for binding to phosphotyrosinc-containing proteins. J. Biol. Chem. 268:4441-4446.
37. Mayer. B.J., H. Hirai, and R. Sakai. 1995. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol. 5:296-305.
38. Meyer, D., and C. Birchmeier. 1995. Multiple essential functions of neuregulin in development. Nature. 378:386-390.
39. Moro, L., M. Venturino, C. Bozzu, L. Silengo, F. Altruda, L. Beguinot, G. Tarone, and P. Defilippi. 1998. Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO (Eur. Mol. Biol. Organ.) J. 17:6622-6632.
40. Muthuswamy, S.K., P.M. Siegel, D.L. Dankort, M.A. Webster, and W.J. Muller. 1994. Mammary tumors expressing the neu proto-oncogene possess elevated c-src tyrosine kinase activity. Mol. Cell. Biol. 14:735-743.
41. Nguyen, D., A.D. Catling, D.J. Webb, M. Sankovic, L.A. Walker, A.V. Somlyo, M.J. Weber, and S.L. Gonias. 1999. Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-mediated manner. J. Cell Biol. 146:149-164.
42. Niemann, C., V. Brinkman, E. Spitzer, G. Hartmann, M. Sachs, H. Naundorf, and W. Birchmeier. 1998. Reconstitution of mammary gland development in vitro: requirement of c-met and c-erbB2 signaling for branching and alveolar morphogenesis. J. Cell Biol. 143:533-545.
43. Ojaniemi, M., and K. Vuori. 1997. Epidermal growth factor modulates tyrosine phosphorylation of p130CAS. J. Biol. Chem. 272:25993-25998.
44. Olayioye, M.A., D. Graus-Porta, R.R. Beerli, J. Rohrer, B. Gay, and N.E. Hynes. 1998. ErbB-1 and ErhB-2 acquire distinct signaling properties dependent upon their dimerization partner. Mol. Cell. Biol. 18:5042-5051.
45. Ottenhoff-Kalff, A.E., G. Rijksen, E. van Beurden, A. Hennipman, A.A. Michels, and G.E. Staal. 1992. Characterization of protein tyrosine kinases from breast cancer: involvement of the c-src oncogene product. Cancer Res. 52:4773-4778.
46. Pantel, K., G. Schlimok, and S. Braun. 1993. Differential expression of proliferation-associated molecules in individual micrometastatic carcinoma cells. J. Natl. Cancer Inst. 85:1419-1424.
47. Pinkas-Kramarski, R., M. Shelly, B.C. Guarino, L.M. Wang, L. Lyass, I. Alroy, M. Alamandi, A. Kuo, J.D. Mover, S. Lavi, et al. 1998. ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. Mol. Cell. Biol. 18:6090-6101.
48. Polte, T.R., and S.K. Hanks. 1997. Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130CAS) are elevated in cytoskelelon-associated fractions following adhesion and src transformation. J. Biol. Chem. 272:5501-5509.
49. Riese, D.J., and D.F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bio Essays 20:41-18.
50. Ricthmacher, D., E. Sonnenherg-Riethmacher, V. Brinkman, T. Yamaai, G.R. Lewin, and C. Birchmeier. 1997. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature. 389:725-730.
51. Rio, C., H.I. Rieff, P. Qi, G. Corfas. 1997. Neuregulin and ErhB receptors play a critical role in neuronal migration. Neuron. 19:39-50.
52. Sivaraman, V.S., H. Wang, G.J. Nuovo, and C.C. Malbon. 1997. Hyperexpression of mitogen-activated protein kinase in human breast cancer. J. Clin. Invest. 99:1478-1483.
53. Slamon, D.J., G.M Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire. 1987. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 235:177-182.
54. Slamon, D.J., W. Godolphin, L.A. Jones, J.A. Holt, S.G. Wong, D.E. Keith, W.J. Levin, S.G. Stuart, J. Udove, A. Ullrich, and M.F. Press. 1989. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science. 244:707-712.
55. Stern, D.F., M.P. Kamps, and H. Cao. 1988. Oncogenic activation of p185neu stimulates tyrosine phosphorylation in vivo. Mol. Cell Biol. 8:3969-3973.
56. Tzahar, E., H. Waterman, X. Chen, G. Levkowitz, D. Karunagaran, S. Lavi, B.J. Ratzkin, and Y. Yarden. 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.
57. Verbeek, B.S., S.S. Adriaansen-Slot, T. Vroom, T. Beckers, and G. Rijksen. 1998. Overexpression of EGFR and c-erbB2 causes enhanced cell migration in human breast cancer cells and NIH3T3 fibroblasts. FEBS Lett. 425:145-150.
58. Vuori, K., H. Hirai, S. Aizawa, and E. Ruoslahti. 1996. Induction of p130Cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16:2606-2613.
59. Wang, Z., L. Zhang, T.K. Yeung, and X. Chen. 1999. Endocytosis deficiency of epidermal growth factor (EGF) receptor-erbB2 heterodimers in response to EGF stimulation. Mol. Biol. Cell. 10:1621-1636.
60. Wong, L., T. Deb, S. Thompson, A. Wells, and G. Johnson. 1999. A differential requirement for the COOH-terminal region of the epidermal growth factor (EGF) receptor in amphiregulin and EGF mitogenic signaling. J. Biol. Chem. 274:8900-8909.
61. Yang, Y., E. Spitzer, D. Meyer, M. Sachs, C. Niemann, G. Hartmann, K.M. Weidner, C. Birchmeier, and W. Birchmeier. 1995. Sequential requirement of HGF and neuregulin in the morphogenesis and differentiation of the mammary gland. J. Cell Biol. 131:215-226.
62. Zrihan-Licht, S., J. Lim, I. Keydar, M. Sliwkowski, J. Groopman, and H. Avraham. 1997. Association of CSK-homologous kinase (CHK) (formerly MATK) with HER-2/ErbB-2 in breast cancer cells. J. Biol. Chem. 272:1856-1863.