Table of Contents
Journal of Signal Transduction
Volume 2011 (2011), Article ID 804236, 8 pages
http://dx.doi.org/10.1155/2011/804236
Review Article

The Functional Crosstalk between HER2 Tyrosine Kinase and TGF-β Signaling in Breast Cancer Malignancy

Division of Tumor Cell Biology, Beckman Research Institute of City of Hope, KCRB-2007, 1500 East Duarte Road, Duarte, CA 91010, USA

Received 25 November 2010; Accepted 13 January 2011

Academic Editor: M. Gaestel

Copyright © 2011 Shizhen Emily Wang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Yarden and M. X. Sliwkowski, “Untangling the ErbB signalling network,” Nature Reviews Molecular Cell Biology, vol. 2, no. 2, pp. 127–137, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Graus-Porta, R. R. Beerli, J. M. Daly, and N. E. Hynes, “ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling,” EMBO Journal, vol. 16, no. 7, pp. 1647–1655, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Pinkas-Kramarski, L. Soussan, H. Waterman et al., “Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions,” EMBO Journal, vol. 15, no. 10, pp. 2452–2467, 1996. View at Google Scholar · View at Scopus
  4. L. M. Wang, A. Kuo, M. Alimandi et al., “ErbB2 expression increases the spectrum and potency of ligand-mediated signal transduction through ErbB4,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 12, pp. 6809–6814, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Worthylake, L. K. Opresko, and H. S. Wiley, “ErbB-2 amplification inhibits down-regulation and induces constitutive activation of both ErbB-2 and epidermal growth factor receptors,” Journal of Biological Chemistry, vol. 274, no. 13, pp. 8865–8874, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Carpenter, “Nuclear localization and possible functions of receptor tyrosine kinases,” Current Opinion in Cell Biology, vol. 15, no. 2, pp. 143–148, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. S. C. Wang, H. C. Lien, W. Xia et al., “Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2,” Cancer Cell, vol. 6, no. 3, pp. 251–261, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. D. J. Slamon, W. Godolphin, L. A. Jones et al., “Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer,” Science, vol. 244, no. 4905, pp. 707–712, 1989. View at Google Scholar · View at Scopus
  9. M. Alimandi, A. Romano, M. C. Curia et al., “Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas,” Oncogene, vol. 10, no. 9, pp. 1813–1821, 1995. View at Google Scholar · View at Scopus
  10. A. D. Thor, S. Liu, S. Edgerton et al., “Activation (tyrosine phosphorylation) of ErbB-2 (HER-2/neu): a study of incidence and correlation with outcome in breast cancer,” Journal of Clinical Oncology, vol. 18, no. 18, pp. 3230–3239, 2000. View at Google Scholar · View at Scopus
  11. S. K. Muthuswamy, D. Li, S. Lelievre, M. J. Bissell, and J. S. Brugge, “ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini,” Nature Cell Biology, vol. 3, no. 9, pp. 785–792, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. J. H. Pierce, P. Arnstein, E. DiMarco et al., “Oncogenic potential of erbB-2 in human mammary epithelial cells,” Oncogene, vol. 6, no. 7, pp. 1189–1194, 1991. View at Google Scholar · View at Scopus
  13. J. S. Ross and J. A. Fletcher, “The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy,” Oncologist, vol. 3, no. 4, pp. 237–252, 1998. View at Google Scholar · View at Scopus
  14. P. Carter, L. Presta, C. M. Gorman et al., “Humanization of an anti-p185(HER2) antibody for human cancer therapy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 10, pp. 4285–4289, 1992. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Roskoski, “The ErbB/HER receptor protein-tyrosine kinases and cancer,” Biochemical and Biophysical Research Communications, vol. 319, no. 1, pp. 1–11, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Baselga, D. Tripathy, J. Mendelsohn et al., “Phase II study of weekly intravenous trastuzumab (Herceptin) in patients with HER2/neu-overexpressing metastatic breast cancer,” Seminars in Oncology, vol. 26, no. 4, pp. 78–83, 1999. View at Google Scholar · View at Scopus
  17. M. A. Cobleigh, C. L. Vogel, D. Tripathy et al., “Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease,” Journal of Clinical Oncology, vol. 17, no. 9, pp. 2639–2648, 1999. View at Google Scholar
  18. C. L. Vogel, M. A. Cobleigh, D. Tripathy et al., “Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer,” Journal of Clinical Oncology, vol. 20, no. 3, pp. 719–726, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Lu, X. Zi, Y. Zhao, D. Mascarenhas, and M. Pollak, “Insulin-like growth factor-I receptor signaling and resistance to transtuzumab (Herceptin),” Journal of the National Cancer Institute, vol. 93, no. 24, pp. 1852–1857, 2001. View at Google Scholar · View at Scopus
  20. A. B. Motoyama, N. E. Hynes, and H. A. Lane, “The efficacy of ErbB receptor-targeted anticancer therapeutics is influenced by the availability of epidermal growth factor-related peptides,” Cancer Research, vol. 62, no. 11, pp. 3151–3158, 2002. View at Google Scholar · View at Scopus
  21. F. M. Yakes, W. Chinratanalab, C. A. Ritter, W. King, S. Seelig, and C. L. Arteaga, “Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, cyclin D1, and antitumor action,” Cancer Research, vol. 62, no. 14, pp. 4132–4141, 2002. View at Google Scholar · View at Scopus
  22. Y. Nagata, K. H. Lan, X. Zhou et al., “PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients,” Cancer Cell, vol. 6, no. 2, pp. 117–127, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Shigematsu, T. Takahashi, M. Nomura et al., “Somatic mutations of the HER2 kinase domain in lung adenocarcinomas,” Cancer Research, vol. 65, no. 5, pp. 1642–1646, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Stephens, C. Hunter, G. Bignell et al., “Lung cancer: intragenic ERBB2 kinase mutations in tumours,” Nature, vol. 431, pp. 525–526, 2004. View at Google Scholar
  25. J. W. Lee, Y. H. Soung, SI. H. Seo et al., “Somatic mutations of ERBB2 kinase domain in gastric, colorectal, and breast carcinomas,” Clinical Cancer Research, vol. 12, no. 1, pp. 57–61, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. S. E. Wang, A. Narasanna, M. Perez-Torres et al., “HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors,” Cancer Cell, vol. 10, no. 1, pp. 25–38, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. S. E. Wang, B. Xiang, M. Guix et al., “Transforming growth factor β engages TACE and ErbB3 to activate phosphatidylinositol-3 kinase/Akt in ErbB2-overexpressing breast cancer and desensitizes cells to trastuzumab,” Molecular and Cellular Biology, vol. 28, no. 18, pp. 5605–5620, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Y. Chang, D. S. A. Nuyten, J. B. Sneddon et al., “Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 10, pp. 3738–3743, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. M. J. Van De Vijver, Y. D. He, L. J. Van 'T Veer et al., “A gene-expression signature as a predictor of survival in breast cancer,” New England Journal of Medicine, vol. 347, no. 25, pp. 1999–2009, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. L. N. Harris, F. You, S. J. Schnitt et al., “Predictors of resistance to preoperative trastuzumab and vinorelbine for HER2-positive early breast cancer,” Clinical Cancer Research, vol. 13, no. 4, pp. 1198–1207, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Massagué, “TGFβ in cancer,” Cell, vol. 134, no. 2, pp. 215–230, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Wrana, L. Attisano, R. Wieser, F. Ventura, and J. Massague, “Mechanism of activation of the TGF-β receptor,” Nature, vol. 370, no. 6488, pp. 341–347, 1994. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Massagué, S. W. Blain, and R. S. Lo, “TGFβ signaling in growth control, cancer, and heritable disorders,” Cell, vol. 103, no. 2, pp. 295–309, 2000. View at Google Scholar · View at Scopus
  34. R. Derynck, R. J. Akhurst, and A. Balmain, “TGF-β signaling in tumor suppression and cancer progression,” Nature Genetics, vol. 29, no. 2, pp. 117–129, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. K. B. Ewan, G. Shyamala, S. A. Ravani et al., “Latent transforming growth factor-β activation in mammary gland: regulation by ovarian hormones affects ductal and alveolar proliferation,” American Journal of Pathology, vol. 160, no. 6, pp. 2081–2093, 2002. View at Google Scholar · View at Scopus
  36. H. L. Moses, E. L. Branum, J. A. Proper, and R. A. Robinson, “Transforming growth factor production by chemically transformed cells,” Cancer Research, vol. 41, no. 7, pp. 2842–2848, 1981. View at Google Scholar · View at Scopus
  37. A. B. Roberts, M. A. Anzano, and L. M. Wakefield, “Type β transforming growth factor: a bifunctional regulator of cellular growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 1, pp. 119–123, 1985. View at Google Scholar
  38. R. F. Tucker, G. D. Shipley, H. L. Moses, and R. W. Holley, “Growth inhibitor from BSC-1 cells closely related to platelet type β transforming growth factor,” Science, vol. 226, no. 4675, pp. 705–707, 1984. View at Google Scholar · View at Scopus
  39. H. Gobbi, W. D. Dupont, J. F. Simpson et al., “Transforming growth factor-β and breast cancer risk in women with mammary epithelial hyperplasia,” Journal of the National Cancer Institute, vol. 91, no. 24, pp. 2096–2101, 1999. View at Google Scholar · View at Scopus
  40. M. Goggins, M. Shekher, K. Turnacioglu, C. J. Yeo, R. H. Hruban, and S. E. Kern, “Genetic alterations of the transforming growth factor β receptor genes in pancreatic and biliary adenocarcinomas,” Cancer Research, vol. 58, no. 23, pp. 5329–5332, 1998. View at Google Scholar · View at Scopus
  41. S. A. Hahn, M. Schutte, A. T. M. Shamsul Hoque et al., “DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1,” Science, vol. 271, no. 5247, pp. 350–353, 1996. View at Google Scholar · View at Scopus
  42. S. Markowitz, J. Wang, L. Myeroff et al., “Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability,” Science, vol. 268, no. 5215, pp. 1336–1338, 1995. View at Google Scholar · View at Scopus
  43. D. Wang, T. Kanuma, H. Mizunuma et al., “Analysis of specific gene mutations in the transforming growth factor-β signal transduction pathway in human ovarian cancer,” Cancer Research, vol. 60, no. 16, pp. 4507–4512, 2000. View at Google Scholar · View at Scopus
  44. J. Wang, L. Sun, L. Myeroff et al., “Demonstration that mutation of the type II transforming growth factor β receptor inactivates its tumor suppressor activity in replication error- positive colon carcinoma cells,” Journal of Biological Chemistry, vol. 270, no. 37, pp. 22044–22049, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Dumont and C. L. Arteaga, “Targeting the TGFβ signaling network in human neoplasia,” Cancer Cell, vol. 3, no. 6, pp. 531–536, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. R. S. Muraoka-Cook, N. Dumont, C. L. Arteaga et al., “Dual role of transforming growth factor β in mammary tumorigenesis and metastatic progression,” Clinical Cancer Research, vol. 11, no. 2, pp. 937s–943s, 2005. View at Google Scholar · View at Scopus
  47. R. S. Muraoka, Y. Koh, L. R. Roebuck et al., “Increased malignancy of neu-induced mammary tumors overexpressing active transforming growth factor β1,” Molecular and Cellular Biology, vol. 23, no. 23, pp. 8691–8703, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. P. M. Siegel, W. Shu, R. D. Cardiff, W. J. Muller, and J. Massagué, “Transforming growth factor β signaling impairs neu-induced mammary tumorigenesis while promoting pulmonary metastasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8430–8435, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. R. S. Muraoka, N. Dumont, C. A. Ritter et al., “Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases,” Journal of Clinical Investigation, vol. 109, no. 12, pp. 1551–1559, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. R. S. Muraoka-Cook, H. Kurokawa, Y. Koh et al., “Conditional overexpression of active transforming growth factor β1 in vivo accelerates metastases of transgenic mammary tumors,” Cancer Research, vol. 64, no. 24, pp. 9002–9011, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bandyopadhyay, F. López-Casillas, S. N. Malik et al., “Antitumor activity of a recombinant soluble betaglycan in human breast cancer xenograft,” Cancer Research, vol. 62, no. 16, pp. 4690–4695, 2002. View at Google Scholar · View at Scopus
  52. S. E. Seton-Rogers, Y. Lu, L. M. Hines et al., “Cooperation of the ErbB2 receptor and transforming growth factor β in induction of migration and invasion in mammary epithelial cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 5, pp. 1257–1262, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Ueda, S. Wang, N. Dumont, J. Y. Yi, Y. Koh, and C. L. Arteaga, “Overexpression of HER2 (erbB2) in human breast epithelial cells unmasks transforming growth factor β-induced cell motility,” Journal of Biological Chemistry, vol. 279, no. 23, pp. 24505–24513, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. S. E. Wang, F. Y. Wu, I. Shin, S. Qu, and C. L. Arteaga, “Transforming growth factor β (TGF-β)-Smad target gene protein tyrosine phosphatase receptor type kappa is required for TGF-β function,” Molecular and Cellular Biology, vol. 25, no. 11, pp. 4703–4715, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Yu, Y. Wang, X. Ren et al., “Context-dependent bidirectional regulation of the muts homolog 2 by transforming growth factor β contributes to chemoresistance in breast cancer cells,” Molecular Cancer Research, vol. 8, no. 12, pp. 1633–1642, 2010. View at Publisher · View at Google Scholar
  56. S. E. Wang, I. Shin, F. Y. Wu, D. B. Friedman, and C. L. Arteaga, “HER2/Neu (ErbB2) signaling to Rac1-Pak1 is temporally and spatially modulated by transforming growth factor β,” Cancer Research, vol. 66, no. 19, pp. 9591–9600, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. S. E. Wang, B. Xiang, R. Zent, V. Quaranta, A. Pozzi, and C. L. Arteaga, “Transforming growth factor β induces clustering of HER2 and integrins by activating Src-focal adhesion kinase and receptor association to the cytoskeleton,” Cancer Research, vol. 69, no. 2, pp. 475–482, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. S. E. Wang, Y. Yu, T. L. Criswell et al., “Oncogenic mutations regulate tumor microenvironment through induction of growth factors and angiogenic mediators,” Oncogene, vol. 29, no. 23, pp. 3335–3348, 2010. View at Publisher · View at Google Scholar · View at Scopus