Essential Role for Rac in Heregulin β1 Mitogenic Signaling: a Mechanism That Involves Epidermal Growth Factor Receptor and Is Independent of ErbB4

REFERENCES

• Adam, L., R. K. Vadlamudi, P. McCrea, and R. Kumar. 2001. Tiam1 overexpression potentiates heregulin-induced lymphoid enhancer factor-1/beta-catenin nuclear signaling in breast cancer cells by modulating the intercellular stability. J. Biol. Chem. 276:28443–28450.
   PubMed Web of Science ®Google Scholar
• Adam, L., R. Vadlamudi, S. B. Kondapaka, J. Chernoff, J. Mendelsohn, and R. Kumar. 1998. Heregulin regulates cytoskeletal reorganization and cell migration through the p21-activated kinase-1 via phosphatidylinositol-3 kinase. J. Biol. Chem. 273:28238–28246.
   PubMed Web of Science ®Google Scholar
• Atlas, E., M. Cardillo, I. Mehmi, H. Zahedkargaran, C. Tang, and R. Lupu. 2003. Heregulin is sufficient for the promotion of tumorigenicity and metastasis of breast cancer cells in vivo. Mol. Cancer Res. 1:165–175.
   PubMedGoogle Scholar
• Baulida, J., M. H. Kraus, M. Alimandi, P. P. Di Fiore, and G. Carpenter. 1996. All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired. J. Biol. Chem. 271:5251–5257.
   PubMed Web of Science ®Google Scholar
• Burgess, A. W., H. S. Cho, C. Eigenbrot, K. M. Ferguson, T. P. Garrett, D. J. Leahy, M. A. Lemmon, M. X. Sliwkowski, C. W. Ward, and S. Yokoyama. 2003. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12:541–552.
   PubMed Web of Science ®Google Scholar
• Caloca, M. J., H. Wang, A. Delemos, S. Wang, and M. G. Kazanietz. 2001. Phorbol esters and related analogs regulate the subcellular localization of beta 2-chimaerin, a non-protein kinase C phorbol ester receptor. J. Biol. Chem. 276:18303–18312.
   PubMedGoogle Scholar
• Canagarajah, B., F. Coluccio Leskow, J. Y. Ho, H. Mischak, L. F. Saidi, M. G. Kazanietz, and J. H. Hurley. 2004. Structural mechanism for lipid activation of the Rac-specific GAP, beta2-chimaerin. Cell 119:407–418.
   PubMed Web of Science ®Google Scholar
• Carpenter, G. 2003. ErbB-4: mechanism of action and biology. Exp. Cell Res. 10:66–77.
   Google Scholar
• Citri, A., K. B. Skaria, and Y. Yarden. 2003. The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp. Cell Res. 10:54–65.
   Google Scholar
• Cohen, B. D., J. M. Green, L. Foy, and H. P. Fell. 1996. HER4-mediated biological and biochemical properties in NIH 3T3 cells. Evidence for HER1-HER4 heterodimers. J. Biol. Chem. 271:4813–4818.
   PubMedGoogle Scholar
• Dunn, M., P. Sinha, R. Campbell, E. Blackburn, N. Levinson, R. Rampaul, T. Bates, S. Humphreys, and W. J. Gullick. 2004. Co-expression of neuregulins 1, 2, 3 and 4 in human breast cancer. J. Pathol. 203:672–680.
   PubMed Web of Science ®Google Scholar
• Eblen, S. T., J. K. Slack, M. J. Weber, and A. D. Catling. 2002. Rac-PAK signaling stimulates extracellular signal-regulated kinase (ERK) activation by regulating formation of MEK1-ERK complexes. Mol. Cell. Biol. 22:6023–6033.
   PubMed Web of Science ®Google Scholar
• Falls, D. L. 2003. Neuregulins: functions, forms, and signaling strategies. Exp. Cell Res. 284:14–30.
   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
• Fleming, I. N., I. H. Batty, A. R. Prescott, A. Gray, G. S. Kular, H. Stewart, and C. P. Downes. 2004. Inositol phospholipids regulate the guanine-nucleotide-exchange factor Tiam1 by facilitating its binding to the plasma membrane and regulating GDP/GTP exchange on Rac1. Biochem. J. 382:857–865.
   PubMed Web of Science ®Google Scholar
• Fritz, G., I. Just, and B. Kaina. 1999. Rho GTPases are over-expressed in human tumors. Int. J. Cancer 81:682–687.
   PubMed Web of Science ®Google Scholar
• Gamett, D. C., G. Pearson, R. A. Cerione, and I. Friedberg. 1997. Secondary dimerization between members of the epidermal growth factor receptor family. J. Biol. Chem. 272:12052–12056.
   PubMed Web of Science ®Google 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
• Han, J., K. Luby-Phelps, B. Das, X. Shu, Y. Xia, R. D. Mosteller, U. M. Krishna, J. R. Falck, M. A. White, and D. Broek. 1998. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279:558–560.
   PubMedGoogle Scholar
• Hellyer, N. J., M. S. Kim, and J. G. Koland. 2001. Heregulin-dependent activation of phosphoinositide 3-kinase and Akt via the ErbB2/ErbB3 co-receptor. J. Biol. Chem. 276:42153–42161.
   PubMedGoogle Scholar
• Huang, G. C., X. Ouyang, and R. J. Epstein. 1998. Proxy activation of protein ErbB2 by heterologous ligands implies a heterotetrameric mode of receptor tyrosine kinase interaction. Biochem. J. 331:113–119.
   PubMed Web of Science ®Google Scholar
• Hynes, N. E., and H. A. Lane. 2005. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 5:341–354.
   PubMed Web of Science ®Google Scholar
• Jackson, J. G., P. St Clair, M. X. Sliwkowski, and M. G. Brattain. 2004. Blockade of epidermal growth factor- or heregulin-dependent ErbB2 activation with the anti-ErbB2 monoclonal antibody 2C4 has divergent downstream signaling and growth effects. Cancer Res. 64:2601–2609.
   PubMed Web of Science ®Google Scholar
• Joyce, D., B. Bouzahzah, M. Fu, C. Albanese, M. D'Amico, J. Steer, J. U. Klein, R. J. Lee, J. E. Segall, J. K. Westwick, C. J. Der, and R. G. Pestell. 1999. Integration of Rac-dependent regulation of cyclin D1 transcription through a nuclear factor-kappaB-dependent pathway. J. Biol. Chem. 274:25245–25249.
   PubMed Web of Science ®Google Scholar
• Kawakatsu, T., H. Ogita, T. Fukuhara, T. Fukuyama, Y. Minami, K. Shimizu, and Y. Takai. 2005. Vav2 as a Rac-GDP/GTP exchange factor responsible for the nectin-induced, c-Src- and Cdc42-mediated activation of Rac. J. Biol. Chem. 280:4940–4947.
   PubMed Web of Science ®Google Scholar
• Lamarche, N., N. Tapon, L. Stowers, P. D. Burbelo, P. Aspenstrom, T. Bridges, J. Chant, and A. Hall. 1996. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87:519–529.
   PubMed Web of Science ®Google Scholar
• Lambert, J. M., Q. T. Lambert, G. W. Reuther, A. Malliri, D. P. Siderovski, J. Sondek, J. G. Collard, and C. J. Der. 2002. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat. Cell Biol. 4:621–625.
   PubMed Web of Science ®Google Scholar
• Lenferink, A. E., R. Pinkas-Kramarski, M. L. van de Poll, M. J. van Vugt, L. N. Klapper, E. Tzahar, H. Waterman, M. Sela, E. J. van Zoelen, and Y. Yarden. 1998. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. EMBO J. 17:3385–3397.
   PubMed Web of Science ®Google Scholar
• Li, S., K. R. Schmitz, P. D. Jeffrey, J. J. Wiltzius, P. Kussie, and K. M. Ferguson. 2005. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7:301–311.
   PubMed Web of Science ®Google Scholar
• Lorenzano-Menna, P., G. Skilton, F. Coluccio Leskow, D. F. Alonso, D. E. Gomez, and M. G. Kazanietz. 2003. Inhibition of aggressiveness of metastatic mouse mammary carcinoma cells by the beta2-chimaerin GAP domain. Cancer Res. 63:2284–2291.
   PubMedGoogle Scholar
• Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4:82–89.
   PubMed Web of Science ®Google Scholar
• Mattoon, D. R., B. Lamothe, I. Lax, and J. Schlessinger. 2004. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol. 2:24.
   PubMedGoogle Scholar
• Moulder, S. L., F. M. Yakes, S. K. Muthuswamy, R. Bianco, J. F. Simpson, and C. L. Arteaga. 2001. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res. 61:8887–8895.
   PubMed Web of Science ®Google Scholar
• Neve, R. M., T. Holbro, and N. E. Hynes. 2002. Distinct roles for phosphoinositide 3-kinase, mitogen-activated protein kinase and p38 MAPK in mediating cell cycle progression of breast cancer cells. Oncogene 21:4567–4576.
   PubMed Web of Science ®Google Scholar
• Nicholson, R. I., J. M. Gee, and M. E. Harper. 2001. EGFR and cancer prognosis. Eur. J. Cancer 37:S9>-S15.
   PubMed Web of Science ®Google Scholar
• Olayioye, M. A., R. M. Neve, H. A. Lane, and N. E. Hynes. 2000. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19:3159–3167.
   PubMed Web of Science ®Google Scholar
• Olson, M. F., A. Ashworth, and A. Hall. 1995. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269:1270–1272.
   PubMed Web of Science ®Google Scholar
• Page, K., J. Li, J. A. Hodge, P. T. Liu, T. L. Vanden Hoek, L. B. Becker, R. G. Pestell, M. R. Rosner, and M. B. Hershenson. 1999. Characterization of a Rac1 signaling pathway to cyclin D(1) expression in airway smooth muscle cells. J. Biol. Chem. 274:22065–22071.
   PubMed Web of Science ®Google Scholar
• Qiu, R. G., J. Chen, D. Kirn, F. McCormick, and M. Symons. 1995. An essential role for Rac in Ras transformation. Nature 374:457–459.
   PubMed Web of Science ®Google Scholar
• Ren, X. D., and M. A. Schwartz. 2000. Determination of GTP loading on Rho. Methods Enzymol. 325:264–272.
   PubMed Web of Science ®Google Scholar
• Riese, D. J., II, T. M. van Raaij, G. D. Plowman, G. C. Andrews, and D. F. Stern. 1995. The cellular response to neuregulins is governed by complex interactions of the erbB receptor family. Mol. Cell. Biol. 15:5770–5776.
   PubMed Web of Science ®Google Scholar
• Sartor, C. I., H. Zhou, E. Kozlowska, K. Guttridge, E. Kawata, L. Caskey, J. Harrelson, N. E. Hynes, S. Ethier, B. Calvo, and H. S. Earp III. 2001. Her4 mediates ligand-dependent antiproliferative and differentiation responses in human breast cancer cells. Mol. Cell. Biol. 21:4265–4275.
   PubMed Web of Science ®Google Scholar
• Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211–225.
   PubMed Web of Science ®Google Scholar
• Schnelzer, A., D. Prechtel, U. Knaus, K. Dehne, M. Gerhard, H. Graeff, N. Harbeck, M. Schmitt, and E. Lengyel. 2000. Rac1 in human breast cancer: overexpression, mutation analysis, and characterization of a new isoform, Rac1b. Oncogene 19:3013–3020.
   PubMed Web of Science ®Google Scholar
• Seger, R., and E. G. Krebs. 1995. The MAPK signaling cascade. FASEB J. 9:726–735.
   PubMed Web of Science ®Google Scholar
• Servitja, J. M., M. J. Marinissen, A. Sodhi, X. R. Bustelo, and J. S. Gutkind. 2003. Rac1 function is required for Src-induced transformation. Evidence of a role for Tiam1 and Vav2 in Rac activation by Src. J. Biol. Chem. 278:34339–34346.
   PubMedGoogle Scholar
• Sundberg-Smith, L. J., J. T. Doherty, C. P. Mack, and J. M. Taylor. 2005. Adhesion stimulates direct PAK1/ERK2 association and leads to ERK-dependent PAK1 Thr212 phosphorylation. J. Biol. Chem. 280:2055–2064.
   PubMed Web of Science ®Google Scholar
• Tamas, P., Z. Solti, P. Bauer, A. Illes, S. Sipeki, A. Bauer, A. Farago, J. Downward, and L. Buday. 2003. Mechanism of epidermal growth factor regulation of Vav2, a guanine nucleotide exchange factor for Rac. J. Biol. Chem. 278:5163–5171.
   PubMedGoogle Scholar
• Tsai, M. S., L. A. Shamon-Taylor, I. Mehmi, C. K. Tang, and R. Lupu. 2003. Blockage of heregulin expression inhibits tumorigenicity and metastasis of breast cancer. Oncogene 22:761–768.
   PubMed Web of Science ®Google Scholar
• Vijapurkar, U., M. S. Kim, and J. G. Koland. 2003. Roles of mitogen-activated protein kinase and phosphoinositide 3′-kinase in ErbB2/ErbB3 coreceptor-mediated heregulin signaling. Exp. Cell Res. 284:291–302.
   PubMedGoogle Scholar
• Witton, C. J., J. R. Reeves, J. J. Going, T. G. Cooke, and J. M. Bartlett. 2003. Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J. Pathol. 200:290–297.
   PubMed Web of Science ®Google Scholar
• Yamauchi, T., K. Ueki, K. Tobe, H. Tamemoto, N. Sekine, M. Wada, M. Honjo, M. Takahashi, T. Takahashi, H. Hirai, T. Tushima, Y. Akanuma, T. Fujita, I. Komuro, Y. Yazaki, and T. Kadowaki. 1997. Tyrosine phosphorylation of the EGF receptor by the kinase Jak2 is induced by growth hormone. Nature 390:91–96.
   PubMed Web of Science ®Google Scholar
• Yang, C., Y. Liu, F. Coluccio Leskow, V. M. Weaver, and M. G. Kazanietz. 2005. Rac-GAP-dependent inhibition of breast cancer cell proliferation by beta2-chimaerin. J. Biol. Chem. 280:24363–24370.
   PubMed Web of Science ®Google Scholar
• Yarden, Y. 2001. Biology of HER2 and its importance in breast cancer. Oncology 61:1–13.
   PubMed Web of Science ®Google Scholar
• Yarden, Y., and M. X. Sliwkowski. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell. Biol. 2:127–137.
   PubMed Web of Science ®Google Scholar
• Zhang, K., J. Sun, N. Liu, D. Wen, D. Chang, A. Thomason, and S. K. Yoshinaga. 1996. Transformation of NIH 3T3 cells by HER3 or HER4 receptors requires the presence of HER1 or HER2. J. Biol. Chem. 271:3884–3890.
   PubMed Web of Science ®Google Scholar