Erk5 Participates in Neuregulin Signal Transduction and Is Constitutively Active in Breast Cancer Cells Overexpressing ErbB2

REFERENCES

• Abe, J., M. Kusuhara, R. J. Ulevitch, B. C. Berk, and J. D. Lee. 1996. Big mitogen-activated protein kinase 1 (BMK1) is a redox-sensitive kinase. J. Biol. Chem. 271: 16586–16590.
   PubMed Web of Science ®Google Scholar
• Abe, J., M. Takahashi, M. Ishida, J. D. Lee, and B. C. Berk. 1997. c-Src is required for oxidative stress-mediated activation of big mitogen-activated protein kinase 1. J. Biol. Chem. 272: 20389–20394.
   PubMed Web of Science ®Google Scholar
• Alimandi, M., L.-M. Wang, D. Bottaro, C.-C. Lee, A. Kuo, M. Frankel, P. Fedi, C. Tang, M. Lippman, and J. H. Pierce. 1997. Epidermal growth factor and betacellulin mediate signal transduction through co-expressed ErbB2 and ErbB3 receptors. EMBO J. 16: 5608–5617.
   PubMed Web of Science ®Google Scholar
• Alroy, I., L. Soussan, R. Seger, and Y. Yarden. 1999. Neu differentiation factor stimulates phosphorylation and activation of the Sp1 transcription factor. Mol. Cell. Biol. 19: 1961–1972.
   PubMed Web of Science ®Google Scholar
• Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Ballinger, M. D., J. T. Jones, J. A. Lofgren, W. J. Fairbrother, R. W. Akita, M. X. Sliwkowski, and J. A. Wells. 1998. Selection of heregulin variants having higher affinity for the ErbB3 receptor by monovalent phage display. J. Biol. Chem. 273: 11675–11684.
   PubMedGoogle Scholar
• Besset, V., R. P. Scott, and C. F. Ibanez. 2000. Signaling complexes and protein-protein interactions involved in the activation of the Ras and phosphatidylinositol 3-kinase pathways by the c-Ret receptor tyrosine kinase. J. Biol. Chem. 275: 39159–39166.
   PubMedGoogle Scholar
• Britsch, S., L. Li, S. Kirchhoff, F. Theuring, V. Brinkmann, C. Birchmeier, and D. Riethmacher. 1998. The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12: 1825–1836.
   PubMed Web of Science ®Google Scholar
• Brunet, A., D. Roux, P. Lenormand, S. Dowd, S. Keyse, and J. Pouyssegur. 1999. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18: 664–674.
   PubMed Web of Science ®Google Scholar
• Buchdunger, E., U. Trinks, H. Mett, U. Regenass, M. Muller, T. Meyer, E. McGlynn, L. A. Pinna, P. Traxler, and N. B. Lydon. 1994. 4,5-Dianilinophthalimide: a protein-tyrosine kinase inhibitor with selectivity for the epidermal growth factor receptor signal transduction pathway and potent in vivo antitumor activity. Proc. Natl. Acad. Sci. USA 91: 2334–2338.
   PubMed Web of Science ®Google Scholar
• Burden, S., and Y. Yarden. 1997. Neuregulins and their receptors: a versatile signalling module in organogenesis and oncogenesis. Neuron 18: 847–855.
   PubMed Web of Science ®Google Scholar
• Cabrera, N., E. Díaz-Rodríguez, E. Becker, D. M. Zanca, and A. Pandiella. 1996. TrkA receptor ectodomain cleavage generates a tyrosine-phosphorylated cell-associated fragment. J. Cell Biol. 132: 427–436.
   PubMed Web of Science ®Google Scholar
• Chang, L., and M. Karin. 2001. Mammalian MAP kinase signalling cascades. Nature 410: 37–40.
   PubMed Web of Science ®Google Scholar
• Chao, T. H., M. Hayashi, R. I. Tapping, Y. Kato, and J. D. Lee. 1999. MEKK3 directly regulates MEK5 activity as part of the big mitogen-activated protein kinase 1 (BMK1) signaling pathway. J. Biol. Chem. 274: 36035–36038.
   PubMedGoogle Scholar
• Chiariello, M., M. J. Marinissen, and J. S. Gutkind. 2000. Multiple mitogen-activated protein kinase signaling pathways connect the Cot oncoprotein to the c-jun promoter and to cellular transformation. Mol. Cell. Biol. 20: 1747–1758.
   PubMed Web of Science ®Google Scholar
• Coso, O. A., S. Montaner, C. Fromm, J. C. Lacal, R. Prywes, H. Teramoto, and J. S. Gutkind. 1997. Signaling from G protein-coupled receptors to the c-jun promoter involves the MEF2 transcription factor. Evidence for a novel c-jun amino-terminal kinase-independent pathway. J. Biol. Chem. 272: 20691–20697.
   PubMedGoogle Scholar
• Daly, J. M., C. B. Jannot, R. R. Beerli, D. Graus-Porta, F. G. Maurer, and N. E. Hynes. 1997. Neu differentiation factor induces ErbB2 down-regulation and apoptosis of ErbB2-overexpressing breast tumor cells. Cancer Res. 57: 3804–3811.
   PubMed Web of Science ®Google Scholar
• Daly, J. M., M. A. Olayioye, A. M. Wong, R. Neve, H. A. Lane, F. G. Maurer, and N. E. Hynes. 1999. NDF/heregulin-induced cell cycle changes and apoptosis in breast tumour cells: role of PI3 kinase and p38 MAP kinase pathways. Oncogene 18: 3440–3451.
   PubMedGoogle Scholar
• Daly, R. J. 1999. Take your partners, please—signal diversification by the erbB family of receptor tyrosine kinases. Growth Factors 16: 255–263.
   PubMed Web of Science ®Google Scholar
• English, J. M., G. Pearson, R. Baer, and M. H. Cobb. 1998. Identification of substrates and regulators of the mitogen-activated protein kinase ERK5 using chimeric protein kinases. J. Biol. Chem. 273: 3854–3860.
   PubMed Web of Science ®Google Scholar
• English, J. M., G. Pearson, T. Hockenberry, L. Shivakumar, M. A. White, and M. H. Cobb. 1999. Contribution of the ERK5/MEK5 pathway to Ras/Raf signaling and growth control. J. Biol. Chem. 274: 31588–31592.
   PubMed Web of Science ®Google Scholar
• Esparís-Ogando, A., E. Díaz-Rodríguez, and A. Pandiella. 1999. Signalling-competent truncated forms of ErbB2 in breast cancer cells: differential regulation by protein kinase C and phosphatidylinositol 3-kinase. Biochem. J. 344: 339–348.
   PubMedGoogle Scholar
• Favata, M. F., K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, F. Hobbs, R. A. Copeland, R. L. Magolda, P. A. Scherle, and J. M. Trzaskos. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273: 18623–18632.
   PubMed Web of Science ®Google Scholar
• Fiddes, R. J., P. W. Janes, S. P. Sivertsen, R. L. Sutherland, E. A. Musgrove, and R. J. Daly. 1998. Inhibition of the MAP kinase cascade blocks heregulin-induced cell cycle progression in T-47D human breast cancer cells. Oncogene 16: 2803–2813.
   PubMedGoogle Scholar
• Fukuhara, S., M. J. Marinissen, M. Chiariello, and J. S. Gutkind. 2000. Signaling from G protein-coupled receptors to ERK5/Big MAPK 1 involves Gαq and Gα12/13 families of heterotrimeric G proteins. Evidence for the existence of a novel ras and rho-independent pathway. J. Biol. Chem. 275: 21730–21736.
   PubMedGoogle Scholar
• Garrington, T. P., and G. L. Johnson. 1999. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11: 211–218.
   PubMed Web of Science ®Google Scholar
• Gonzalez, F. A., A. Seth, D. L. Raden, D. S. Bowman, F. S. Fay, and R. J. Davis. 1993. Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus. J. Cell Biol. 122: 1089–1101.
   PubMedGoogle Scholar
• Grasso, A. W., D. Wen, C. M. Miller, J. S. Rhim, T. G. Pretlow, and H. J. Kung. 1997. ErbB kinases and NDF signaling in human prostate cancer cells. Oncogene 15: 2705–2716.
   PubMedGoogle Scholar
• Graus-Porta, D., R. R. Beerli, J. M. Daly, and N. E. Hynes. 1997. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16: 1647–1655.
   PubMed Web of Science ®Google Scholar
• Gullick, W. J., S. B. Love, C. Wright, D. M. Barnes, B. Gusterson, A. L. Harris, and D. G. Altman. 1991. c-erbB-2 protein overexpression in breast cancer is a risk factor in patients with involved and uninvolved lymph nodes. Br. J. Cancer 63: 434–438.
   PubMed Web of Science ®Google Scholar
• Gutkind, J. S. 1998. Cell growth control by G protein-coupled receptors: from signal transduction to signal integration. Oncogene 17: 1331–1342.
   PubMed Web of Science ®Google Scholar
• Guy, P. M., J. V. Platko, L. C. Cantley, R. A. Cerione, and K. L. Carraway III. 1994. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. USA 91: 8132–8136.
   PubMed Web of Science ®Google Scholar
• Han, T.-H., and R. Prywes. 1995. Regulatory role of MEF2D in serum induction of the c-jun promoter. Mol. Cell. Biol. 15: 2907–2915.
   PubMedGoogle Scholar
• Holmes, W. E., M. X. Sliwkowski, R. W. Akita, W. J. Henzel, J. Lee, J. W. Park, D. Yansura, N. Abadi, H. Raab, G. D. Lewis, H. M. Shepard, W. J. Kuang, W. I. Wood, D. V. Goeddel, and R. L. Vandlen. 1992. Identification of heregulin, a specific activator of p185erbB2. Science 256: 1205–1210.
   PubMed Web of Science ®Google Scholar
• Hou, X. S., T. B. Chou, M. B. Melnick, and N. Perrimon. 1995. The torso receptor tyrosine kinase can activate Raf in a Ras-independent pathway. Cell 81: 63–71.
   PubMedGoogle Scholar
• Hynes, N. E., and D. F. Stern. 1994. The biology of erbB-2/neu/HER2 and its role in cancer. Biochim. Biophys. Acta 1198: 165–184.
   PubMed Web of Science ®Google Scholar
• Ip, Y. T., and R. J. Davis. 1998. Signal transduction by the c-Jun N-terminal kinase (JNK)—from inflammation to development. Curr. Opin. Cell Biol. 10: 205–219.
   PubMed Web of Science ®Google Scholar
• Jones, J. T., M. D. Ballinger, P. I. Pisacane, J. A. Lofgren, V. D. Fitzpatrick, W. J. Fairbrother, J. A. Wells, and M. X. Sliwkowski. 1998. Binding interaction of the heregulinβ egf domain with ErbB3 and ErbB4 receptors assessed by alanine scanning mutagenesis. J. Biol. Chem. 273: 11667–11674.
   PubMedGoogle Scholar
• Kamakura, S., T. Moriguchi, and E. Nishida. 1999. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274: 26563–26571.
   PubMed Web of Science ®Google Scholar
• Kato, Y., V. V. Kravchenko, R. I. Tapping, J. Han, R. J. Ulevitch, and J. D. Lee. 1997. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16: 7054–7066.
   PubMed Web of Science ®Google Scholar
• Kato, Y., R. I. Tapping, S. Huang, M. H. Watson, R. J. Ulevitch, and J. D. Lee. 1998. Bmk1/Erk5 is required for cell proliferation induced by epidermal growth factor. Nature 395: 713–716.
   PubMed Web of Science ®Google Scholar
• Lange-Carter, C. A., and G. L. Johnson. 1994. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science 265: 1458–1461.
   PubMed Web of Science ®Google Scholar
• Lee, J. D., R. J. Ulevitch, and J. Han. 1995. Primary structure of BMK1: a new mammalian map kinase. Biochem. Biophys. Res. Commun. 213: 715–724.
   PubMed Web of Science ®Google Scholar
• Lenormand, P., C. Sardet, G. Pages, G. L’Allemain, A. Brunet, and J. Pouyssegur. 1993. Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts. J. Cell Biol. 122: 1079–1088.
   PubMed Web of Science ®Google Scholar
• Marinissen, M. J., M. Chiariello, M. Pallante, and J. S. Gutkind. 1999. A network of mitogen-activated protein kinases links G protein-coupled receptors to the c-jun promoter: a role for c-Jun NH2-terminal kinase, p38s, and extracellular signal-regulated kinase 5. Mol. Cell. Biol. 19: 4289–4301.
   PubMedGoogle Scholar
• Marshall, C. 1999. How do small GTPase signal transduction pathways regulate cell cycle entry? Curr. Opin. Cell Biol. 11: 732–736.
   PubMedGoogle Scholar
• Marshall, C. J. 1999. Small GTPases and cell cycle regulation. Biochem. Soc. Trans. 27: 363–370.
   PubMedGoogle Scholar
• Massagué, J., and A. Pandiella. 1993. Membrane-anchored growth factors. Annu. Rev. Biochem. 62: 515–541.
   PubMed Web of Science ®Google Scholar
• Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Derijard, R. J. Davis, G. L. Johnson, and M. Karin. 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266: 1719–1723.
   PubMed Web of Science ®Google Scholar
• Olayioye, M. A., D. Graus-Porta, R. R. Beerli, J. Rohrer, B. Gay, and N. E. Hynes. 1998. ErbB-1 and ErbB-2 acquire distinct signaling properties dependent upon their dimerization partner. Mol. Cell. Biol. 18: 5042–5051.
   PubMed Web of Science ®Google Scholar
• Peles, E., S. S. Bacus, R. A. Koski, H. S. Lu, D. Wen, S. G. Ogden, R. B. Levy, and Y. Yarden. 1992. Isolation of the Neu/HER-2 stimulatory ligand: a 44 kd glycoprotein that induces differentiation of mammary tumor cells. Cell 69: 205–216.
   PubMed Web of Science ®Google Scholar
• Pinkas-Kramarski, R., M. Shelly, S. Glathe, B. J. Ratzkin, and Y. Yarden. 1996. Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J. Biol. Chem. 271: 19029–19032.
   PubMed Web of Science ®Google Scholar
• Pinkas-Kramarski, R., M. Shelly, B. C. Guarino, L. M. Wang, L. Lyass, I. Alroy, M. Alimandi, A. Kuo, J. D. Moyer, S. Lavi, M. Eisenstein, B. J. Ratzkin, R. Seger, S. S. Bacus, J. H. Pierce, G. C. Andrews, Y. Yarden, and M. Alamandi. 1998. ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. Mol. Cell. Biol. 18: 6090–6101.
   PubMed Web of Science ®Google Scholar
• Riese, D. J., II, and D. F. Stern. 1998. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20: 41–48.
   PubMed Web of Science ®Google Scholar
• Riethmacher, D., E. Sonnenberg-Riethmacher, V. Brinkmann, T. Yamaai, G. R. Lewin, and C. Birchmeier. 1997. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389: 725–730.
   PubMed Web of Science ®Google Scholar
• Robinson, M. J., and M. H. Cobb. 1997. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9: 180–186.
   PubMed Web of Science ®Google Scholar
• Samanta, A., C. M. LeVea, W. C. Dougall, X. Quian, and M. I. Greene. 1994. Ligand and p185c-neu density govern receptor interactions and tyrosine kinase activation. Proc. Natl. Acad. Sci. USA 91: 1711–1715.
   PubMed Web of Science ®Google Scholar
• Schaeffer, H. J., and M. J. Weber. 1999. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 19: 2435–2444.
   PubMed Web of Science ®Google Scholar
• Schönwasser, D. C., R. M. Marais, C. J. Marshall, and P. J. Parker. 1998. Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel and atypical protein kinase C isotypes. Mol. Cell. Biol. 18: 790–798.
   PubMed Web of Science ®Google Scholar
• Shields, J. M., K. Pruitt, A. McFall, A. Shaub, and C. J. Der. 2000. Understanding Ras: ′it ain’t over ’til it’s over’. Trends Cell Biol. 10: 147–154.
   PubMed Web of Science ®Google Scholar
• Sibilia, M., J. P. Steinbach, L. Stingl, A. Aguzzi, and E. F. Wagner. 1998. A strain-independent postnatal neurodegeneration in mice lacking the EGF receptor. EMBO J. 17: 719–731.
   PubMedGoogle Scholar
• Siegel, P. M., E. D. Ryan, R. D. Cardiff, and W. J. Muller. 1999. Elevated expression of activated forms of Neu/ErbB-2 and ErbB-3 are involved in the induction of mammary tumors in transgenic mice: implications for human breast cancer. EMBO J. 18: 2149–2164.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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, et al. 1989. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244: 707–712.
   PubMed Web of Science ®Google Scholar
• Tzahar, E., R. Pinkas-Kramarski, J. D. Moyer, L. N. Klapper, I. Alroy, G. Levkowitz, M. Shelly, S. Henis, M. Eisenstein, B. J. Ratzkin, M. Sela, G. C. Andrews, and Y. Yarden. 1997. Bivalence of EGF-like ligands drives the ErbB signaling network. EMBO J. 16: 4938–4950.
   PubMed Web of Science ®Google Scholar
• Tzahar, E., and Y. Yarden. 1998. The ErbB-2/HER2 oncogenic receptor of adenocarcinomas: from orphanhood to multiple stromal ligands. Biochim. Biophys. Acta 1377: M25–M37.
   PubMed Web of Science ®Google Scholar
• Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212.
   PubMed Web of Science ®Google Scholar
• van der Geer, P., T. Hunter, and R. A. Lindberg. 1994. Receptor protein tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 10: 251–337.
   PubMedGoogle Scholar
• Wallasch, C., F. U. Weiss, G. Niederfellner, B. Jallal, W. Issing, and A. Ullrich. 1995. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO J. 14: 4267–4275.
   PubMed Web of Science ®Google Scholar
• Widmann, C., S. Gibson, M. B. Jarpe, and G. L. Johnson. 1999. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79: 143–180.
   PubMed Web of Science ®Google Scholar
• Wu, C. J., X. Qian, and D. M. O’Rourke. 1999. Sustained mitogen-activated protein kinase activation is induced by transforming erbB receptor complexes. DNA Cell Biol. 18: 731–741.
   PubMedGoogle Scholar
• Yan, C., H. Luo, J. D. Lee, J. Abe, and B. C. Berk. 2001. Molecular cloning of mouse ERK5/BMK1 splice variants and characterization of ERK5 functional domains. J. Biol. Chem. 276: 10870–10878.
   PubMedGoogle Scholar
• Yan, C., M. Takahashi, M. Okuda, J. D. Lee, and B. C. Berk. 1999. Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. Dependence on tyrosine kinases and intracellular calcium. J. Biol. Chem. 274: 143–150.
   PubMed Web of Science ®Google Scholar
• Yang, C. C., O. I. Ornatsky, J. C. McDermott, T. F. Cruz, and C. A. Prody. 1998. Interaction of myocyte enhancer factor 2 (MEF2) with a mitogen-activated protein kinase, ERK5/BMK1. Nucleic Acids Res. 26: 4771–4777.
   PubMedGoogle Scholar
• Zecevic, M., A. D. Catling, S. T. Eblen, L. Renzi, J. C. Hittle, T. J. Yen, G. J. Gorbsky, and M. J. Weber. 1998. Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J. Cell Biol. 142: 1547–1558.
   PubMed Web of Science ®Google Scholar
• Zhou, G., Z. Q. Bao, and J. E. Dixon. 1995. Components of a new human protein kinase signal transduction pathway. J. Biol. Chem. 270: 12665–12669.
   PubMed Web of Science ®Google Scholar
• Zwijsen, R. M., R. Klompmaker, E. B. Wientjens, P. M. Kristel, B. van der Burg, and R. J. Michalides. 1996. Cyclin D1 triggers autonomous growth of breast cancer cells by governing cell cycle exit. Mol. Cell. Biol. 16: 2554–2560.
   PubMed Web of Science ®Google Scholar