Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis (original) (raw)

• Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE et al. (1999). Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1: 260–266.
  Article CAS Google Scholar
• Bruna A, Darken RS, Rojo F, Ocana A, Penuelas S, Arias A et al. (2007). High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 11: 147–160.
  Article CAS Google Scholar
• Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, ten Dijke P, van der Pluijm G . (2007b). TGF-β and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis 24: 609–617.
  Article CAS Google Scholar
• Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, Que I, Schwaninger R et al. (2007a). Bone morphogenetic protein 7 in the development and treatment of bone metastases from breast cancer. Cancer Res 67: 8742–8751.
  Article CAS Google Scholar
• Buijs JT, van der Pluijm G . (2009). Osteotropic cancers: from primary tumor to bone. Cancer Lett 273: 177–193.
  Article CAS Google Scholar
• Burdette JE, Jeruss JS, Kurley SJ, Lee EJ, Woodruff TK . (2005). Activin A mediates growth inhibition and cell cycle arrest through Smads in human breast cancer cells. Cancer Res 65: 7968–7975.
  Article CAS Google Scholar
• Deckers M, van Dinther M, Buijs J, Que I, Lowik C, van der Pluijm G et al. (2006). The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res 66: 2202–2209.
  Article CAS Google Scholar
• Dennler S, Huet S, Gauthier JM . (1999). A short amino-acid sequence in MH1 domain is responsible for functional differences between Smad2 and Smad3. Oncogene 18: 1643–1648.
  Article CAS Google Scholar
• Desruisseau S, Palmari J, Giusti C, Romain S, Martin PM, Berthois Y . (2006). Determination of TGFbeta1 protein level in human primary breast cancers and its relationship with survival. Br J Cancer 94: 239–246.
  Article CAS Google Scholar
• Donovan D, Harmey JH, Toomey D, Osborne DH, Redmond HP, Bouchier-Hayes DJ . (1997). TGF beta-1 regulation of VEGF production by breast cancer cells. Ann Surg Oncol 4: 621–627.
  Article CAS Google Scholar
• Dzwonek J, Preobrazhenska O, Cazzola S, Conidi A, Schellens A, van Dinther M et al. (2009). Smad3 is a key nonredundant mediator of transforming growth factor beta signaling in Nme mouse mammary epithelial cells. Mol Cancer Res 7: 1342–1353.
  Article CAS Google Scholar
• Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS . (2009). Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15: 232–239.
  Article CAS Google Scholar
• Ehata S, Hanyu A, Fujime M, Katsuno Y, Fukunaga E, Goto K et al. (2007). Ki26894, a novel transforming growth factor-β type I receptor kinase inhibitor, inhibits in vitro invasion and in vivo bone metastasis of a human breast cancer cell line. Cancer Sci 98: 127–133.
  Article CAS Google Scholar
• Ge R, Rajeev V, Ray P, Lattime E, Rittling S, Medicherla S et al. (2006). Inhibition of growth and metastasis of mouse mammary carcinoma by selective inhibitor of transforming growth factor-β type I receptor kinase in vivo. Clin Cancer Res 12: 4315–4330.
  Article CAS Google Scholar
• Ghellal A, Li C, Hayes M, Byrne G, Bundred N, Kumar S . (2000). Prognostic significance of TGF beta 1 and TGF beta 3 in human breast carcinoma. Anticancer Res 20: 4413–4418.
  CAS PubMed Google Scholar
• Heffelfinger SC, Miller MA, Yassin R, Gear R . (1999). Angiogenic growth factors in preinvasive breast disease. Clin Cancer Res 5: 2867–2876.
  CAS PubMed Google Scholar
• Hoot KE, Lighthall J, Han G, Lu SL, Li A, Ju W et al. (2008). Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J Clin Invest 118: 2722–2732.
  CAS PubMed PubMed Central Google Scholar
• Isogai C, Laug WE, Shimada H, Declerck PJ, Stins MF, Durden DL et al. (2001). Plasminogen activator inhibitor-1 promotes angiogenesis by stimulating endothelial cell migration toward fibronectin. Cancer Res 61: 5587–5594.
  CAS PubMed Google Scholar
• Ivanovic V, Todorovic-Rakovic N, Demajo M, Neskovic-Konstantinovic Z, Subota V, Ivanisevic-Milovanovic O et al. (2003). Elevated plasma levels of transforming growth factor-β 1 (TGF-β1) in patients with advanced breast cancer: association with disease progression. Eur J Cancer 39: 454–461.
  Article CAS Google Scholar
• Kang Y, He W, Tulley S, Gupta GP, Serganova I, Chen CR et al. (2005). Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc Natl Acad Sci USA 102: 13909–13914.
  Article CAS Google Scholar
• Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C et al. (2003). A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537–549.
  Article CAS Google Scholar
• Kingsley LA, Fournier PG, Chirgwin JM, Guise TA . (2007). Molecular biology of bone metastasis. Mol Cancer Ther 6: 2609–2617.
  Article CAS Google Scholar
• Kirkbride KC, Blobe GC . (2003). Inhibiting the TGF-β signalling pathway as a means of cancer immunotherapy. Expert Opin Biol Ther 3: 251–261.
  CAS PubMed Google Scholar
• Kobayashi T, Liu X, Wen FQ, Fang Q, Abe S, Wang XQ et al. (2005). Smad3 mediates TGF-β1 induction of VEGF production in lung fibroblasts. Biochem Biophys Res Commun 327: 393–398.
  Article CAS Google Scholar
• Kretschmer A, Moepert K, Dames S, Sternberger M, Kaufmann J, Klippel A . (2003). Differential regulation of TGF-β signaling through Smad2, Smad3 and Smad4. Oncogene 22: 6748–6763.
  Article CAS Google Scholar
• LaGamba D, Nawshad A, Hay ED . (2005). Microarray analysis of gene expression during epithelial-mesenchymal transformation. Dev Dyn 234: 132–142.
  Article CAS Google Scholar
• Leivonen SK, Kahari VM . (2007). Transforming growth factor-beta signaling in cancer invasion and metastasis. Int J Cancer 121: 2119–2124.
  Article CAS Google Scholar
• Massague J . (2008). TGFbeta in Cancer. Cell 134: 215–230.
  Article CAS Google Scholar
• Massague J, Seoane J, Wotton D . (2005). Smad transcription factors. Genes Dev 19: 2783–2810.
  Article CAS Google Scholar
• Matsui J, Funahashi Y, Uenaka T, Watanabe T, Tsuruoka A, Asada M . (2008). Multi-kinase inhibitor E7080 suppresses lymph node and lung metastases of human mammary breast tumor MDA-MB-231 via inhibition of vascular endothelial growth factor-receptor (VEGF-R) 2 and VEGF-R3 kinase. Clin Cancer Res 14: 5459–5465.
  Article CAS Google Scholar
• McEarchern JA, Kobie JJ, Mack V, Wu RS, Meade-Tollin L, Arteaga CL et al. (2001). Invasion and metastasis of a mammary tumor involves TGF-β signaling. Int J Cancer 91: 76–82.
  Article CAS Google Scholar
• Moustakas A, Heldin CH . (2007). Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98: 1512–1520.
  Article CAS Google Scholar
• Muraoka RS, Dumont N, Ritter CA, Dugger TC, Brantley DM, Chen J et al. (2002). Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 109: 1551–1559.
  Article CAS Google Scholar
• Nakagawa T, Li JH, Garcia G, Mu W, Piek E, Bottinger EP et al. (2004). TGF-β induces proangiogenic and antiangiogenic factors via parallel but distinct Smad pathways. Kidney Int 66: 605–613.
  Article CAS Google Scholar
• Nam JS, Terabe M, Mamura M, Kang MJ, Chae H, Stuelten C et al. (2008). An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 68: 3835–3843.
  Article CAS Google Scholar
• Nawshad A, LaGamba D, Polad A, Hay ED . (2005). Transforming growth factor-β signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs 179: 11–23.
  Article CAS Google Scholar
• Oft M, Akhurst RJ, Balmain A . (2002). Metastasis is driven by sequential elevation of H-ras and Smad2 levels. Nat Cell Biol 4: 487–494.
  Article CAS Google Scholar
• Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F et al. (2009). Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15: 220–231.
  Article CAS Google Scholar
• Petersen M, Thorikay M, Deckers M, van Dinther M, Grygielko ET, Gellibert F et al. (2008). Oral administration of GW788388, an inhibitor of TGF-β type I and II receptor kinases, decreases renal fibrosis. Kidney Int 73: 705–715.
  Article CAS Google Scholar
• Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C . (2001). Synergistic cooperation between hypoxia and transforming growth factor-β pathways on human vascular endothelial growth factor gene expression. J Biol Chem 276: 38527–38535.
  Article CAS Google Scholar
• Schmierer B, Hill CS . (2007). TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8: 970–982.
  Article CAS Google Scholar
• Sheen-Chen SM, Chen HS, Sheen CW, Eng HL, Chen WJ . (2001). Serum levels of transforming growth factor beta1 in patients with breast cancer. Arch Surg 136: 937–940.
  Article CAS Google Scholar
• Tannehill-Gregg SH, Kusewitt DF, Rosol TJ, Weinstein M . (2004). The roles of Smad2 and Smad3 in the development of chemically induced skin tumors in mice. Vet Pathol 41: 278–282.
  Article CAS Google Scholar
• ten Dijke P, Hill CS . (2004). New insights into TGF-β-Smad signalling. Trends Biochem Sci 29: 265–273.
  Article CAS Google Scholar
• Tian F, Byfield SD, Parks WT, Stuelten CH, Nemani D, Zhang YE et al. (2004). Smad-binding defective mutant of transforming growth factor beta type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res 64: 4523–4530.
  Article CAS Google Scholar
• Tian F, DaCosta BS, Parks WT, Yoo S, Felici A, Tang B et al. (2003). Reduction in Smad2/3 signaling enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res 63: 8284–8292.
  CAS Google Scholar
• van der Pluijm G, Sijmons B, Vloedgraven H, Deckers M, Papapoulos S, Lowik C . (2001). Monitoring metastatic behavior of human tumor cells in mice with species-specific polymerase chain reaction: elevated expression of angiogenesis and bone resorption stimulators by breast cancer in bone metastases. J Bone Miner Res 16: 1077–1091.
  Article CAS Google Scholar
• Weinstein M, Yang X, Li C, Xu X, Gotay J, Deng CX . (1998). Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor Smad2. Proc Natl Acad Sci USA 95: 9378–9383.
  Article CAS Google Scholar
• Xie W, Mertens JC, Reiss DJ, Rimm DL, Camp RL, Haffty BG et al. (2002). Alterations of Smad signaling in human breast carcinoma are associated with poor outcome: a tissue microarray study. Cancer Res 62: 497–505.
  CAS PubMed Google Scholar
• Yang X, Letterio JJ, Lechleider RJ, Chen L, Hayman R, Gu H et al. (1999). Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J 18: 1280–1291.
  Article CAS Google Scholar
• Yin JJ, Selander K, Chirgwin JM, Dallas M, Grubbs BG, Wieser R et al. (1999). TGF-β signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J Clin Invest 103: 197–206.
  Article CAS Google Scholar