TGF-β signaling in breast cancer cell invasion and bone metastasis

Journal of Mammary Gland Biology and Neoplasia

Volumn 16, Issue 2, 2011, Pages 97-108

  Drabsch, Yvette ^a   Ten Dijke, Peter ^a,b  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

EMT; Invasion; Metastasis; Microenvironment; Stroma; TGF

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHEMOKINE RECEPTOR CXCR4; CONNECTIVE TISSUE GROWTH FACTOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; CRE RECOMBINASE; CYCLIN DEPENDENT KINASE; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; FIBRONECTIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 11; LIPOCORTIN 1; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE RELATED PROTEIN; PLECKSTRIN; PROTEIN MDM2; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; UROKINASE RECEPTOR; UVOMORULIN; VASCULOTROPIN; VIMENTIN;

ANGIOGENESIS; BONE METASTASIS; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER INVASION; CYTOSKELETON; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; LUNG METASTASIS; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PLASTICITY; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; BONE NEOPLASMS; BREAST NEOPLASMS; FEMALE; HUMANS; NEOPLASM INVASIVENESS; TRANSFORMING GROWTH FACTOR BETA;

EID: 79959526395     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-011-9217-1     Document Type: Review

References (125)

1. PL Porter 2009 Global trends in breast cancer incidence and mortality Salud Pública Méx 51 Suppl 2 s141 s146 19967268
2. Sanchez-Zamorano LM, Flores-Luna L, Angeles-Llerenas A, et al. Healthy lifestyle on the risk of breast cancer. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2011.
3. RC Travis GK Reeves J Green, et al. 2010 Gene-environment interactions in 7610 women with breast cancer: prospective evidence from the Million Women Study Lancet 375 9732 2143 2151 20605201 1:CAS:528:DC%2BC3cXnvVelt78%3D
4. MB Buck C Knabbe 2006 TGF-β signaling in breast cancer Ann NY Acad Sci 1089 119 126 17261761 1:CAS:528:DC%2BD2sXhsFertL0%3D
5. P ten Dijke CS Hill 2004 New insights into TGF-β-Smad signalling Trends Biochem Sci 29 5 265 273 15130563
6. A Moustakas CH Heldin 2005 Non-Smad TGF-β signals J Cell Sci 118 Pt 16 3573 3584 16105881 1:CAS:528:DC%2BD2MXhtVaktrvK
7. YE Zhang 2009 Non-Smad pathways in TGF-β signaling Cell Res 19 1 128 139 19114990 1:CAS:528:DC%2BD1MXht1GhsQ%3D%3D
8. MK Lee C Pardoux MC Hall, et al. 2007 TGF-β activates Erk MAP kinase signalling through direct phosphorylation of ShcA EMBO J 26 17 3957 3967 17673906 1:CAS:528:DC%2BD2sXpvFWhsL0%3D (Pubitemid 47367487)
9. NA Bhowmick R Zent M Ghiassi, et al. 2001 Integrin β 1 signaling is necessary for transforming growth factor-β activation of p38MAPK and epithelial plasticity J Biol Chem 276 50 46707 46713 11590169 1:CAS:528:DC%2BD3MXpt1Gns7g%3D
10. S Edlund M Landstrom CH Heldin, et al. 2002 Transforming growth factor-β-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA Mol Biol Cell 13 3 902 914 11907271 1:CAS:528:DC%2BD38XivVequrc%3D (Pubitemid 34250354)
11. MC Wilkes SJ Murphy N Garamszegi, et al. 2003 Cell-type-specific activation of PAK2 by transforming growth factor β independent of Smad2 and Smad3 Mol Cell Biol 23 23 8878 8889 14612425 1:CAS:528:DC%2BD3sXptFait7w%3D (Pubitemid 37433386)
12. MH Barcellos-Hoff RJ Akhurst 2009 Transforming growth factor-β in breast cancer: too much, too late Breast Cancer Res 11 1 202 19291273
13. B Kleuser D Malek R Gust, et al. 2008 17-β-estradiol inhibits transforming growth factor-β signaling and function in breast cancer cells via activation of extracellular signal-regulated kinase through the G protein-coupled receptor 30 Mol Pharmacol 74 6 1533 1543 18768737 1:CAS:528:DC%2BD1cXhsVGls73N
14. RA Hinshelwood LI Huschtscha J Melki, et al. 2007 Concordant epigenetic silencing of transforming growth factor-β signaling pathway genes occurs early in breast carcinogenesis Cancer Res 67 24 11517 11527 18089780 1:CAS:528:DC%2BD2sXhsVCjs73I
15. RJ Akhurst R Derynck 2001 TGF-β signaling in cancer-a double-edged sword Trends Cell Biol 11 11 S44 S51 11684442 1:CAS:528:DC%2BD3MXnvFGrsb8%3D
16. G Turashvili J Bouchal K Baumforth, et al. 2007 Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis BMC Cancer 7 55 17389037
17. JD Figueroa KC Flanders M Garcia-Closas, et al. 2010 Expression of TGF-β signaling factors in invasive breast cancers: relationships with age at diagnosis and tumor characteristics Breast Cancer Res Treat 121 3 727 735 19937272 1:CAS:528:DC%2BC3cXmtVyrsb8%3D
18. Zhang S, Royer R, Li S, et al. Frequencies of BRCA1 and BRCA2 mutations among 1,342 unselected patients with invasive ovarian cancer. Gynecol Oncol. 2011.
19. Li J, Zhu H, Chen T, et al. TGF-β1 and BRCA2 expression are associated with clinical factors in breast cancer. Cell Biochem Biophys. 2011.
20. J Xu S Lamouille R Derynck 2009 TGF-β-induced epithelial to mesenchymal transition Cell Res 19 2 156 172 19153598 1:CAS:528: DC%2BD1MXht1amsL4%3D
21. K Miyazono 2009 Transforming growth factor-β signaling in epithelial-mesenchymal transition and progression of cancer Proc Jpn Acad B Phys Biol Sci 85 8 314 323 1:CAS:528:DC%2BD1MXhsFejsrnE
22. J Massagué 2008 TGFβ in cancer Cell 134 2 215 230 18662538
23. P ten Dijke MJ Goumans E Pardali 2008 Endoglin in angiogenesis and vascular diseases Angiogenesis 11 1 79 89 18283546 1:CAS:528: DC%2BD1cXjsFWksbc%3D
24. RA Flavell S Sanjabi SH Wrzesinski, et al. 2010 The polarization of immune cells in the tumour environment by TGF-β. Nature reviews Immunology 10 8 554 567 20616810 1:CAS:528:DC%2BC3cXosFeltbo%3D
25. JT Buijs NV Henriquez PG van Overveld, et al. 2007 Bone morphogenetic protein 7 in the development and treatment of bone metastases from breast cancer Cancer Res 67 18 8742 8751 17875715 1:CAS:528:DC%2BD2sXhtVCit7vK (Pubitemid 47437450)
26. PD Bos DX Nguyen J Massagué 2010 Modeling metastasis in the mouse Curr Opin Pharmacol 10 5 571 577 20598638 1:CAS:528:DC%2BC3cXhtFygurfO
27. T Tsuji S Ibaragi GF Hu 2009 Epithelial-mesenchymal transition and cell cooperativity in metastasis Cancer Res 69 18 7135 7139 19738043 1:CAS:528:DC%2BD1MXhtFaku7zM
28. S Grunert M Jechlinger H Beug 2003 Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nature reviews Molec Cell Biol 4 8 657 665 (Pubitemid 36934968)
29. D Padua XH Zhang Q Wang, et al. 2008 TGF-β primes breast tumors for lung metastasis seeding through angiopoietin-like 4 Cell 133 1 66 77 18394990 1:CAS:528:DC%2BD1cXkslOlu7Y%3D (Pubitemid 351442989)
30. NJ Godde RC Galea IA Elsum, et al. 2010 Cell polarity in motion: redefining mammary tissue organization through EMT and cell polarity transitions J Mammary Gland Biol Neoplasia 15 2 149 168 20461450
31. J Zavadil EP Bottinger 2005 TGF-β and epithelial-to-mesenchymal transitions Oncogene 24 37 5764 5774 16123809 1:CAS:528:DC%2BD2MXptVertbw%3D
32. PJ Miettinen R Ebner AR Lopez, et al. 1994 TGF-β induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors J Cell Biol 127 6 Pt 2 2021 2036 7806579 1:CAS:528:DyaK2MXitlWgsrw%3D
33. E Piek A Moustakas A Kurisaki, et al. 1999 TGF-(β) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells J Cell Sci 112 Pt 24 4557 4568 10574705 1:CAS:528:DC%2BD3cXntlGisQ%3D%3D (Pubitemid 30034805)
34. LE Lindley KJ Briegel 2010 Molecular characterization of TGFβ-induced epithelial-mesenchymal transition in normal finite lifespan human mammary epithelial cells Biochem Biophys Res Commun 399 4 659 664 20691661 1:CAS:528:DC%2BC3cXhtFamsLfP
35. M Jo RD Lester V Montel, et al. 2009 Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling J Biol Chem 284 34 22825 22833 19546228 1:CAS:528:DC%2BD1MXpvFKitLk%3D
36. AJ Trimboli K Fukino A de Bruin, et al. 2008 Direct evidence for epithelial-mesenchymal transitions in breast cancer Cancer Res 68 3 937 945 18245497 1:CAS:528:DC%2BD1cXhtlygur4%3D (Pubitemid 351206773)
37. G Turashvili J Bouchal J Ehrmann, et al. 2007 Novel immunohistochemical markers for the differentiation of lobular and ductal invasive breast carcinomas Biomedical papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia 151 1 59 64 17690741 1:CAS:528:DC%2BD2sXhtFejt7vP
38. DS Micalizzi SM Farabaugh HL Ford 2010 Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression J Mammary Gland Biol Neoplasia 15 2 117 134 20490631
39. G Christofori 2006 New signals from the invasive front Nature 441 7092 444 450 16724056 1:CAS:528:DC%2BD28XkvVyrsro%3D (Pubitemid 44050139)
40. T Vincent EP Neve JR Johnson, et al. 2009 A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-β mediated epithelial-mesenchymal transition Nat Cell Biol 11 8 943 950 19597490 1:CAS:528:DC%2BD1MXpsVaktbk%3D
41. S Thuault U Valcourt M Petersen, et al. 2006 Transforming growth factor-β employs HMGA2 to elicit epithelial-mesenchymal transition J Cell Biol 174 2 175 183 16831886 1:CAS:528:DC%2BD28XntFaqsbo%3D (Pubitemid 44079853)
42. AM Viloria-Petit L David JY Jia, et al. 2009 A role for the TGFβ-Par6 polarity pathway in breast cancer progression Proc Natl Acad Sci USA 106 33 14028 14033 19667198 1:CAS:528:DC%2BD1MXhtFWksL%2FP
43. T Shirakihara K Horiguchi K Miyazawa, et al. 2011 TGF-β regulates isoform switching of FGF receptors and epithelial-mesenchymal transition EMBO J 30 4 783 795 21224849 1:CAS:528:DC%2BC3MXjslWqsA%3D%3D
44. MK Wendt JA Smith WP Schiemann 2010 Transforming growth factor-β-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression Oncogene 29 49 6485 6498 20802523 1:CAS:528:DC%2BC3cXhtVyqsL7O
45. DS Micalizzi KL Christensen P Jedlicka, et al. 2009 The Six1 homeoprotein induces human mammary carcinoma cells to undergo epithelial-mesenchymal transition and metastasis in mice through increasing TGF-β signaling J Clin Invest 119 9 2678 2690 19726885 1:CAS:528:DC%2BD1MXhtFWgs77I
46. DS Micalizzi CA Wang SM Farabaugh, et al. 2010 Homeoprotein Six1 increases TGF-β Type I receptor and converts TGF-β signaling from suppressive to supportive for tumor growth Cancer Res 70 24 10371 10380 21056993 1:CAS:528:DC%2BC3cXhsFGrtL%2FJ
47. M Deckers M van Dinther J Buijs, et al. 2006 The tumor suppressor Smad4 is required for transforming growth factor β-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells Cancer Res 66 4 2202 2209 16489022 1:CAS:528:DC%2BD28XhsFals78%3D
48. S Thuault EJ Tan H Peinado, et al. 2008 HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition J Biol Chem 283 48 33437 33446 18832382 1:CAS:528:DC%2BD1cXhsVSgt73P
49. PA Gregory AG Bert EL Paterson, et al. 2008 The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1 Nat Cell Biol 10 5 593 601 18376396 1:CAS:528:DC%2BD1cXltl2is7c%3D (Pubitemid 351627379)
50. AV Bakin AK Tomlinson NA Bhowmick, et al. 2000 Phosphatidylinositol 3-kinase function is required for transforming growth factor β-mediated epithelial to mesenchymal transition and cell migration J Biol Chem 275 47 36803 36810 10969078 1:CAS:528:DC%2BD3cXoslWlsrY%3D (Pubitemid 32002090)
51. M de Graauw MH van Miltenburg MK Schmidt, et al. 2010 Annexin A1 regulates TGF-β signaling and promotes metastasis formation of basal-like breast cancer cells Proc Natl Acad Sci USA 107 14 6340 6345 20308542
52. S Araki JA Eitel CN Batuello, et al. 2010 TGF-β1-induced expression of human Mdm2 correlates with late-stage metastatic breast cancer J Clin Investig 120 1 290 302 19955655 1:CAS:528:DC%2BC3cXislWmuw%3D%3D
53. Sabbah M, Prunier C, Ferrand N, et al. CCN5, a novel transcriptional repressor of transforming growth factor-β signaling pathway. Mol Cell Biol. 2011.
54. M Mareel MJ Oliveira I Madani 2009 Cancer invasion and metastasis: interacting ecosystems Virchows Archiv: An International Journal of Pathology 454 6 599 622 1:CAS:528:DC%2BD1MXmvFGhsbs%3D
55. M Mareel A Leroy 2003 Clinical, cellular, and molecular aspects of cancer invasion Physiol Rev 83 2 337 376 12663862 1:CAS:528:DC%2BD3sXjtVagtr8%3D (Pubitemid 36382891)
56. M Hu J Yao DK Carroll, et al. 2008 Regulation of in situ to invasive breast carcinoma transition Cancer Cell 13 5 394 406 18455123 1:CAS:528:DC%2BD1cXlvFemu7s%3D (Pubitemid 351609443)
57. YP Luo H Zhou J Krueger, et al. 2010 The role of proto-oncogene Fra-1 in remodeling the tumor microenvironment in support of breast tumor cell invasion and progression Oncogene 29 5 662 673 19966854 1:CAS:528:DC%2BD1MXhsFWrsbbK
58. S Mandal KR Johnson MJ Wheelock 2008 TGF-β induces formation of F-actin cores and matrix degradation in human breast cancer cells via distinct signaling pathways Exp Cell Res 314 19 3478 3493 18848540 1:CAS:528: DC%2BD1cXhtlGht7fJ
59. Wiercinska E, Naber HP, Pardali E, et al. The TGF-β/Smad pathway induces breast cancer cell invasion through the up-regulation of matrix metalloproteinase 2 and 9 in a spheroid invasion model system. Breast Cancer Res Treat. 2010.
60. S Giampieri C Manning S Hooper, et al. 2009 Localized and reversible TGF-β signalling switches breast cancer cells from cohesive to single cell motility Nat Cell Biol 11 11 1287 1296 19838175 1:CAS:528:DC%2BD1MXhtlCnu7rN
61. SS McAllister RA Weinberg 2010 Tumor-host interactions: a far-reaching relationship J Clin Oncol: Official Journal of the American Society of Clinical Oncology 28 26 4022 4028
62. CC Park MJ Bissell MH Barcellos-Hoff 2000 The influence of the microenvironment on the malignant phenotype Mol Med Today 6 8 324 329 10904250 1:CAS:528:DC%2BD3cXls1ansrc%3D (Pubitemid 30619340)
63. MM Mueller NE Fusenig 2004 Friends or foes - bipolar effects of the tumour stroma in cancer Nat Rev Cancer 4 11 839 849 15516957 1:CAS:528:DC%2BD2cXptFegt78%3D (Pubitemid 39472951)
64. MH Sieweke MJ Bissell 1994 The tumor-promoting effect of wounding: a possible role for TGF-β-induced stromal alterations Crit Rev Oncog 5 2-3 297 311 7849089 1:STN:280:DyaK2M7ltFygsw%3D%3D
65. MP Shekhar R Pauley G Heppner 2003 Host microenvironment in breast cancer development: extracellular matrix-stromal cell contribution to neoplastic phenotype of epithelial cells in the breast Breast Cancer Res 5 3 130 135 12793893 1:CAS:528:DC%2BD3sXjt12ju74%3D (Pubitemid 36519405)
66. CJ Olsen J Moreira EM Lukanidin, et al. 2010 Human mammary fibroblasts stimulate invasion of breast cancer cells in a three-dimensional culture and increase stroma development in mouse xenografts BMC Cancer 10 444 20723242
67. CH Stuelten JI Busch B Tang, et al. 2010 Transient tumor-fibroblast interactions increase tumor cell malignancy by a TGF-β mediated mechanism in a mouse xenograft model of breast cancer PLoS ONE 5 3 e9832 20352126
68. AE Karnoub AB Dash AP Vo, et al. 2007 Mesenchymal stem cells within tumour stroma promote breast cancer metastasis Nature 449 7162 557 563 17914389 1:CAS:528:DC%2BD2sXhtFagt7fI (Pubitemid 47525152)
69. I Haviv K Polyak W Qiu, et al. 2009 Origin of carcinoma associated fibroblasts Cell Cycle 8 4 589 595 19182519 1:CAS:528:DC%2BD1MXlvFWjtLg%3D
70. Y Kojima A Acar EN Eaton, et al. 2010 Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts Proc Natl Acad Sci USA 107 46 20009 20014 21041659 1:CAS:528:DC%2BC3cXhsVyitL3K
71. NA Bhowmick A Chytil D Plieth, et al. 2004 TGF-β signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia Science 303 5659 848 851 14764882 1:CAS:528:DC%2BD2cXovVKmtQ%3D%3D (Pubitemid 38174665)
72. N Cheng NA Bhowmick A Chytil, et al. 2005 Loss of TGF-β type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-α-, MSP- and HGF-mediated signaling networks Oncogene 24 32 5053 5068 15856015 1:CAS:528:DC%2BD2MXmsFKrur4%3D (Pubitemid 41129083)
73. N Cheng A Chytil Y Shyr, et al. 2008 Transforming growth factor-β signaling-deficient fibroblasts enhance hepatocyte growth factor signaling in mammary carcinoma cells to promote scattering and invasion Molec Cancer Res 6 10 1521 1533 1:CAS:528:DC%2BD1cXht1Cmsb7O
74. MH Barcellos-Hoff SA Ravani 2000 Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells Cancer Res 60 5 1254 1260 10728684 1:CAS:528:DC%2BD3cXhvFWrtr0%3D (Pubitemid 30151992)
75. MH Barcellos-Hoff 1993 Radiation-induced transforming growth factor β and subsequent extracellular matrix reorganization in murine mammary gland Cancer Res 53 17 3880 3886 8358713 1:CAS:528:DyaK3sXms1Gnt7w%3D (Pubitemid 23267682)
76. TM Casey J Eneman A Crocker, et al. 2008 Cancer associated fibroblasts stimulated by transforming growth factor β1 (TGF-β1) increase invasion rate of tumor cells: a population study Breast Cancer Res Treat 110 1 39 49 17674196 1:CAS:528:DC%2BD1cXmslOqu7c%3D (Pubitemid 351793849)
77. A Mantovani F Marchesi C Porta, et al. 2007 Inflammation and cancer: breast cancer as a prototype Breast 16 Suppl 2 S27 S33 17764938
78. B Bierie HL Moses 2006 TGF-β and cancer Cytokine Growth Factor Rev 17 1-2 29 40 16289860 1:CAS:528:DC%2BD28Xos1CrsA%3D%3D
79. I Marigo L Dolcetti P Serafini, et al. 2008 Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells Immunol Rev 222 162 179 18364001 1:CAS:528:DC%2BD1cXlsFejt74%3D (Pubitemid 351430364)
80. G Gallina L Dolcetti P Serafini, et al. 2006 Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells J Clin Investig 116 10 2777 2790 17016559 1:CAS:528:DC%2BD28XhtVKgu7vF (Pubitemid 44511641)
81. L Yang J Huang X Ren, et al. 2008 Abrogation of TGF-β signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis Cancer Cell 13 1 23 35 18167337 1:CAS:528:DC%2BD1cXnsVKnuw%3D%3D (Pubitemid 350309741)
82. MJ Oliveira J Van Damme T Lauwaet, et al. 2003 β-casein-derived peptides, produced by bacteria, stimulate cancer cell invasion and motility EMBO J 22 22 6161 6173 14609961 1:CAS:528:DC%2BD3sXptVeqtLg%3D (Pubitemid 37463258)
83. A Leask DJ Abraham 2004 TGF-β signaling and the fibrotic response FASEB J: Official Publication of the Federation of American Societies for Experimental Biology 18 7 816 827 1:CAS:528:DC%2BD2cXjvVOnt70%3D
84. Y Kang W He S Tulley, et al. 2005 Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway Proc Natl Acad Sci USA 102 39 13909 13914 16172383 1:CAS:528:DC%2BD2MXhtVOqsbjM (Pubitemid 41377677)
85. EL Alarmo J Parssinen JM Ketolainen, et al. 2009 BMP7 influences proliferation, migration, and invasion of breast cancer cells Cancer Lett 275 1 35 43 18980801 1:CAS:528:DC%2BD1MXhtVeiurg%3D
86. JM Ketolainen EL Alarmo VJ Tuominen, et al. 2010 Parallel inhibition of cell growth and induction of cell migration and invasion in breast cancer cells by bone morphogenetic protein 4 Breast Cancer Res Treat 124 2 377 386 20182795 1:CAS:528:DC%2BC3cXht12qur3L
87. EL Alarmo T Korhonen T Kuukasjarvi, et al. 2008 Bone morphogenetic protein 7 expression associates with bone metastasis in breast carcinomas Ann Oncol: Official Journal of the European Society for Medical Oncology/ESMO 19 2 308 314 (Pubitemid 351201712)
88. HC Blair NA Athanasou 2004 Recent advances in osteoclast biology and pathological bone resorption Histol Histopathol 19 1 189 199 14702187 1:CAS:528:DC%2BD2cXjtFyrtb8%3D (Pubitemid 38111263)
89. MA Henderson JA Danks JL Slavin, et al. 2006 Parathyroid hormone-related protein localization in breast cancers predict improved prognosis Cancer Res 66 4 2250 2256 16489028 1:CAS:528:DC%2BD28XhsFals7k%3D
90. GJ Powell J Southby JA Danks, et al. 1991 Localization of parathyroid hormone-related protein in breast cancer metastases: increased incidence in bone compared with other sites Cancer Res 51 11 3059 3061 2032246 1:STN:280:DyaK3M3jsFaiuw%3D%3D
91. TA Guise JJ Yin SD Taylor, et al. 1996 Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis J Clin Investig 98 7 1544 1549 8833902 1:CAS:528:DyaK28XmtVCmu70%3D (Pubitemid 26327863)
92. JJ Yin K Selander JM Chirgwin, et al. 1999 TGF-β signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development J Clin Invest 103 2 197 206 9916131 1:CAS:528:DyaK1MXltFeqsQ%3D%3D (Pubitemid 29053137)
93. SM Kakonen KS Selander JM Chirgwin, et al. 2002 Transforming growth factor-β stimulates parathyroid hormone-related protein and osteolytic metastases via Smad and mitogen-activated protein kinase signaling pathways J Biol Chem 277 27 24571 24578 11964407 1:CAS:528:DC%2BD38XltlOht7s%3D (Pubitemid 34951984)
94. V Evtimova M Schwirzke N Tarbe, et al. 2001 Identification of breast cancer metastasis-associated genes by chip technology Anticancer Res 21 6A 3799 3806 11911250 1:CAS:528:DC%2BD38Xis1arsb8%3D (Pubitemid 34229244)
95. MA Watson LR Ylagan KM Trinkaus, et al. 2007 Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients Clin Cancer Res: An Official Journal of the American Association for Cancer Research 13 17 5001 5009 1:CAS:528:DC%2BD2sXpvFGrurc%3D (Pubitemid 47502064)
96. Juarez P, Guise TA. TGF-β in cancer and bone: implications for treatment of bone metastases. Bone 2010.
97. X Lu Q Wang G Hu, et al. 2009 ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis Genes Dev 23 16 1882 1894 19608765 1:CAS:528:DC%2BD1MXhtVegurbN
98. Y Kang J Massagué 2004 Epithelial-mesenchymal transitions: twist in development and metastasis Cell 118 3 277 279 15294153 1:CAS:528: DC%2BD2cXmslKrs7w%3D (Pubitemid 39061108)
99. LK Dunn KS Mohammad PG Fournier, et al. 2009 Hypoxia and TGF-β drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment PLoS ONE 4 9 e6896 19727403
100. M Katoh 2010 Integrative genomic analyses of CXCR4: transcriptional regulation of CXCR4 based on TGFβ, Nodal, Activin signaling and POU5F1, FOXA2, FOXC2, FOXH1, SOX17, and GFI1 transcription factors Int J Oncol 36 2 415 420 20043076 1:CAS:528:DC%2BC3cXitF2gt7s%3D
101. T Shimo S Kubota N Yoshioka, et al. 2006 Pathogenic role of connective tissue growth factor (CTGF/CCN2) in osteolytic metastasis of breast cancer J Bone Miner Res: The Official Journal of the American Society for Bone and Mineral Research 21 7 1045 1059 1:CAS:528:DC%2BD28XntlWqur0%3D (Pubitemid 43962833)
102. EL Alarmo A Kallioniemi 2010 Bone morphogenetic proteins in breast cancer: dual role in tumourigenesis? Endocr-Relat Cancer 17 2 R123 R139 20335308 1:CAS:528:DC%2BC3cXptV2mu7g%3D
103. RW Johnson MP Nguyen SS Padalecki, et al. 2011 TGF-β promotion of Gli2-induced expression of parathyroid hormone-related protein, an important osteolytic factor in bone metastasis, is independent of canonical hedgehog signaling Cancer Res 71 3 822 831 21189326 1:CAS:528:DC%2BC3MXhsVCisbg%3D
104. M Futakuchi KC Nannuru ML Varney, et al. 2009 Transforming growth factor-β signaling at the tumor-bone interface promotes mammary tumor growth and osteoclast activation Cancer Sci 100 1 71 81 19038005 1:CAS:528:DC%2BD1MXhtlGnsrg%3D
105. B Bierie DG Stover TW Abel, et al. 2008 Transforming growth factor-β regulates mammary carcinoma cell survival and interaction with the adjacent microenvironment Cancer Res 68 6 1809 1819 18339861 1:CAS:528: DC%2BD1cXjtFOhsLY%3D (Pubitemid 351416566)
106. M Korpal J Yan X Lu, et al. 2009 Imaging transforming growth factor-β signaling dynamics and therapeutic response in breast cancer bone metastasis Nat Med 15 8 960 966 19597504 1:CAS:528:DC%2BD1MXosFWhtr0%3D
107. M Petersen E Pardali G van der Horst, et al. 2010 Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis Oncogene 29 9 1351 1361 20010874 1:CAS:528:DC%2BD1MXhsFGmsLvF
108. JT Buijs I Que CW Lowik, et al. 2009 Inhibition of bone resorption and growth of breast cancer in the bone microenvironment Bone 44 2 380 386 19041433 1:CAS:528:DC%2BD1MXhtFSmur4%3D
109. JT Buijs NV Henriquez PG van Overveld, et al. 2007 TGF-β and BMP7 interactions in tumour progression and bone metastasis Clin Exp Metastasis 24 8 609 617 18008174 1:CAS:528:DC%2BD1cXhvFGgtr8%3D (Pubitemid 50003597)
110. JT Buijs CC Kuijpers G van der Pluijm 2010 Targeted therapy options for treatment of bone metastases; beyond bisphosphonates Curr Pharm Des 16 27 3015 3027 20722621 1:CAS:528:DC%2BC3cXhsVKlur3K
111. JT Buijs M Petersen G van der Horst, et al. 2010 Bone morphogenetic proteins and its receptors; therapeutic targets in cancer progression and bone metastasis? Curr Pharm Des 16 11 1291 1300 20166979 1:CAS:528: DC%2BC3cXlvFymurs%3D
112. LA Kingsley PG Fournier JM Chirgwin, et al. 2007 Molecular biology of bone metastasis Mol Cancer Ther 6 10 2609 2617 17938257 1:CAS:528: DC%2BD2sXhtFKltbnE (Pubitemid 350058141)
113. S McMahon M Charbonneau S Grandmont, et al. 2006 Transforming growth factor β1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression J Biol Chem 281 34 24171 24181 16815840 1:CAS:528:DC%2BD28Xot1eqsrY%3D (Pubitemid 44274191)
114. G van der Pluijm B Sijmons H Vloedgraven, et al. 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: The Official Journal of the American Society for Bone and Mineral Research 16 6 1077 1091 (Pubitemid 32467152)
115. S Davies WG Jiang 2010 ALCAM, activated leukocyte cell adhesion molecule, influences the aggressive nature of breast cancer cells, a potential connection to bone metastasis Anticancer Res 30 4 1163 1168 20530423 1:CAS:528: DC%2BC3cXovV2gsrk%3D
116. A Galaup A Cazes S Le Jan, et al. 2006 Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness Proc Natl Acad Sci USA 103 49 18721 18726 17130448 1:CAS:528:DC%2BD28Xhtlaht7vF (Pubitemid 44913477)
117. GP Gupta J Perk S Acharyya, et al. 2007 ID genes mediate tumor reinitiation during breast cancer lung metastasis Proc Natl Acad Sci USA 104 49 19506 19511 18048329 1:CAS:528:DC%2BD1cXisVOgsw%3D%3D
118. R Sadej H Romanska D Kavanagh, et al. 2010 Tetraspanin CD151 regulates transforming growth factor β signaling: implication in tumor metastasis Cancer Res 70 14 6059 6070 20570898 1:CAS:528:DC%2BC3cXovVamsrY%3D
119. Henry LA, Johnson DA, Sarrio D, et al. Endoglin expression in breast tumor cells suppresses invasion and metastasis and correlates with improved clinical outcome. Oncogene. 2010.
120. E Perez-Gomez G Del Castillo S Juan Francisco, et al. 2010 The role of the TGF-β coreceptor endoglin in cancer Scientific World Journal 10 2367 2384 21170488 1:CAS:528:DC%2BC3MXksVGksLw%3D
121. GY Lee PA Kenny EH Lee, et al. 2007 Three-dimensional culture models of normal and malignant breast epithelial cells Nat Meth 4 4 359 365 1:CAS:528:DC%2BD2sXkt1eqsLk%3D (Pubitemid 46766981)
122. EA Kohn Z Du M Sato, et al. 2010 A novel approach for the generation of genetically modified mammary epithelial cell cultures yields new insights into TGF-β signaling in the mammary gland Breast Cancer Res 12 5 R83 20942910
123. LM Wakefield AB Roberts 2002 TGF-β signaling: positive and negative effects on tumorigenesis Curr Opin Genet Dev 12 1 22 29 11790550 1:CAS:528:DC%2BD38XktFGmtw%3D%3D (Pubitemid 34094985)
124. V Ganapathy R Ge A Grazioli, et al. 2010 Targeting the transforming growth factor-β pathway inhibits human basal-like breast cancer metastasis Mol Cancer 9 122 20504320
125. EF Saunier RJ Akhurst 2006 TGF-β inhibition for cancer therapy Curr Cancer Drug Targets 6 7 565 578 17100564 1:CAS:528:DC%2BD28XhtFSju7%2FK