Activation of Stat3 by Heregulin/ErbB-2 through the Co-Option of Progesterone Receptor Signaling Drives Breast Cancer Growth

REFERENCES

• Balana, M. E., L. Labriola, M. Salatino, F. Movsichoff, G. Peters, E. H. Charreau, and P. V. Elizalde. 2001. Activation of ErbB-2 via a hierarchical interaction between ErbB-2 and type I insulin-like growth factor receptor in mammary tumor cells. Oncogene 20:34–47.
   PubMed Web of Science ®Google Scholar
• Balana, M. E., R. Lupu, L. Labriola, E. H. Charreau, and P. V. Elizalde. 1999. Interactions between progestins and heregulin (HRG) signaling pathways: HRG acts as mediator of progestins proliferative effects in mouse mammary adenocarcinomas. Oncogene 18:6370–6379.
   PubMedGoogle Scholar
• Boonyaratanakornkit, V., Y. Bi, M. Rudd, and D. P. Edwards. 2008. The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression. Steroids 73:922–928.
   PubMedGoogle Scholar
• Boonyaratanakornkit, V., E. McGowan, L. Sherman, M. A. Mancini, B. J. Cheskis, and D. P. Edwards. 2007. The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol. Endocrinol. 21:359–375.
   PubMed Web of Science ®Google Scholar
• Boonyaratanakornkit, V., M. P. Scott, V. Ribon, L. Sherman, S. M. Anderson, J. L. Maller, W. T. Miller, and D. P. Edwards. 2001. Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol. Cell 8:269–280.
   PubMed Web of Science ®Google Scholar
• Bromberg, J. F., C. M. Horvath, D. Besser, W. W. Lathem, and J. E. Darnell, Jr. 1998. Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18:2553–2558.
   PubMed Web of Science ®Google Scholar
• Bromberg, J. F., M. H. Wrzeszczynska, G. Devgan, Y. Zhao, R. G. Pestell, C. Albanese, and J. E. Darnell, Jr. 1999. Stat3 as an oncogene. Cell 98:295–303.
   PubMed Web of Science ®Google Scholar
• Burke, W. M., X. Jin, H. J. Lin, M. Huang, R. Liu, R. K. Reynolds, and J. Lin. 2001. Inhibition of constitutively active Stat3 suppresses growth of human ovarian and breast cancer cells. Oncogene 20:7925–7934.
   PubMed Web of Science ®Google Scholar
• Daniel, A. R., M. Qiu, E. J. Faivre, J. H. Ostrander, A. Skildum, and C. A. Lange. 2007. Linkage of progestin and epidermal growth factor signaling: phosphorylation of progesterone receptors mediates transcriptional hypersensitivity and increased ligand-independent breast cancer cell growth. Steroids 72:188–201.
   PubMedGoogle Scholar
• Dankort, D., N. Jeyabalan, N. Jones, D. J. Dumont, and W. J. Muller. 2001. Multiple ErbB-2/Neu phosphorylation sites mediate transformation through distinct effector proteins. J. Biol. Chem. 276:38921–38928.
   PubMedGoogle Scholar
• Dankort, D., B. Maslikowski, N. Warner, N. Kanno, H. Kim, Z. Wang, M. F. Moran, R. G. Oshima, R. D. Cardiff, and W. J. Muller. 2001. Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumorigenesis: implications for human breast cancer. Mol. Cell. Biol. 21:1540–1551.
   PubMed Web of Science ®Google Scholar
• Diaz, N., S. Minton, C. Cox, T. Bowman, T. Gritsko, R. Garcia, I. Eweis, M. Wloch, S. Livingston, E. Seijo, A. Cantor, J. H. Lee, C. A. Beam, D. Sullivan, R. Jove, and C. A. Muro-Cacho. 2006. Activation of stat3 in primary tumors from high-risk breast cancer patients is associated with elevated levels of activated SRC and survivin expression. Clin. Cancer Res. 12:20–28.
   PubMed Web of Science ®Google Scholar
• Dran, G., I. A. Luthy, A. A. Molinolo, F. Montecchia, E. H. Charreau, C. D. Pasqualini, and C. Lanari. 1995. Effect of medroxyprogesterone acetate (MPA) and serum factors on cell proliferation in primary cultures of an MPA-induced mammary adenocarcinoma. Breast Cancer Res. Treat. 35:173–186.
   PubMedGoogle Scholar
• Faivre, E. J., A. R. Daniel, C. J. Hillard, and C. A. Lange. 2008. Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol. Endocrinol. 22:823–837.
   PubMedGoogle Scholar
• Garcia, R., T. L. Bowman, G. Niu, H. Yu, S. Minton, C. A. Muro-Cacho, C. E. Cox, R. Falcone, R. Fairclough, S. Parsons, A. Laudano, A. Gazit, A. Levitzki, A. Kraker, and R. Jove. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20:2499–2513.
   PubMed Web of Science ®Google Scholar
• Gritsko, T., A. Williams, J. Turkson, S. Kaneko, T. Bowman, M. Huang, S. Nam, I. Eweis, N. Diaz, D. Sullivan, S. Yoder, S. Enkemann, S. Eschrich, J. H. Lee, C. A. Beam, J. Cheng, S. Minton, C. A. Muro-Cacho, and R. Jove. 2006. Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin. Cancer Res. 12:11–19.
   PubMed Web of Science ®Google Scholar
• Guo, W., Y. Pylayeva, A. Pepe, T. Yoshioka, W. J. Muller, G. Inghirami, and F. G. Giancotti. 2006. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 126:489–502.
   PubMed Web of Science ®Google Scholar
• Ishizawar, R. C., T. Miyake, and S. J. Parsons. 2007. c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 26:3503–3510.
   PubMed Web of Science ®Google Scholar
• Kim, H., R. Chan, D. L. Dankort, D. Zuo, M. Najoukas, M. Park, and W. J. Muller. 2005. The c-Src tyrosine kinase associates with the catalytic domain of ErbB-2: implications for ErbB-2 mediated signaling and transformation. Oncogene 24:7599–7607.
   PubMedGoogle Scholar
• Labriola, L., M. Salatino, C. J. Proietti, A. Pecci, O. A. Coso, A. R. Kornblihtt, E. H. Charreau, and P. V. Elizalde. 2003. Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells. Mol. Cell. Biol. 23:1095–1111.
   PubMedGoogle Scholar
• Lange, C. A., J. K. Richer, T. Shen, and K. B. Horwitz. 1998. Convergence of progesterone and epidermal growth factor signaling in breast cancer. Potentiation of mitogen-activated protein kinase pathways. J. Biol. Chem. 273:31308–31316.
   PubMed Web of Science ®Google Scholar
• Lange, C. A., T. Shen, and K. B. Horwitz. 2000. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc. Natl. Acad. Sci. USA 97:1032–1037.
   PubMed Web of Science ®Google Scholar
• Li, L., and P. E. Shaw. 2002. Autocrine-mediated activation of STAT3 correlates with cell proliferation in breast carcinoma lines. J. Biol. Chem. 277:17397–17405.
   PubMed Web of Science ®Google Scholar
• Lupu, R., R. B. Dickson, and M. E. Lippman. 1992. The role of erbB-2 and its ligands in growth control of malignant breast epithelium. J. Steroid Biochem. Mol. Biol. 43:229–236.
   PubMedGoogle Scholar
• Migliaccio, A., D. Piccolo, G. Castoria, M. Di Domenico, A. Bilancio, M. Lombardi, W. Gong, M. Beato, and F. Auricchio. 1998. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 17:2008–2018.
   PubMed Web of Science ®Google Scholar
• Olayioye, M. A., I. Beuvink, K. Horsch, J. M. Daly, and N. E. Hynes. 1999. ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J. Biol. Chem. 274:17209–17218.
   PubMedGoogle 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
• Proietti, C., M. Salatino, C. Rosemblit, R. Carnevale, A. Pecci, A. R. Kornblihtt, A. A. Molinolo, I. Frahm, E. H. Charreau, R. Schillaci, and P. V. Elizalde. 2005. Progestins induce transcriptional activation of signal transducer and activator of transcription 3 (Stat3) via a Jak- and Src-dependent mechanism in breast cancer cells. Mol. Cell. Biol. 25:4826–4840.
   PubMed Web of Science ®Google Scholar
• Real, P. J., A. Sierra, A. De Juan, J. C. Segovia, J. M. Lopez-Vega, and J. L. Fernandez-Luna. 2002. Resistance to chemotherapy via Stat3-dependent overexpression of Bcl-2 in metastatic breast cancer cells. Oncogene 21:7611–7618.
   PubMed Web of Science ®Google Scholar
• Ren, Z., and T. S. Schaefer. 2002. ErbB-2 activates Stat3 alpha in a Src- and JAK2-dependent manner. J. Biol. Chem. 277:38486–38493.
   PubMed Web of Science ®Google Scholar
• Sam, M. R., B. E. Elliott, and C. R. Mueller. 2007. A novel activating role of SRC and STAT3 on HGF transcription in human breast cancer cells. Mol. Cancer 6:69.
   PubMedGoogle Scholar
• Shen, T., K. B. Horwitz, and C. A. Lange. 2001. Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol. Cell. Biol. 21:6122–6131.
   PubMed Web of Science ®Google Scholar
• Simian, M., A. Molinolo, and C. Lanari. 2006. Involvement of matrix metalloproteinase activity in hormone-induced mammary tumor regression. Am. J. Pathol. 168:270–279.
   PubMedGoogle 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, and A. Ullrich. 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., 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.
   PubMed Web of Science ®Google Scholar
• Wang, S. C., H. C. Lien, W. Xia, I. F. Chen, H. W. Lo, Z. Wang, M. Ali-Seyed, D. F. Lee, G. Bartholomeusz, F. Ou-Yang, D. K. Giri, and M. C. Hung. 2004. Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 6:251–261.
   PubMed Web of Science ®Google Scholar
• Xu, W., X. Yuan, K. Beebe, Z. Xiang, and L. Neckers. 2007. Loss of Hsp90 association up-regulates Src-dependent ErbB2 activity. Mol. Cell. Biol. 27:220–228.
   PubMed Web of Science ®Google Scholar
• Yu, H., and R. Jove. 2004. The STATs of cancer—new molecular targets come of age. Nat. Rev. Cancer 4:97–105.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., W. Bai, V. E. Allgood, and N. L. Weigel. 1994. Multiple signaling pathways activate the chicken progesterone receptor. Mol. Endocrinol. 8:577–584.
   PubMedGoogle Scholar