GDF5 Regulates TGFß-Dependent Angiogenesis in Breast Carcinoma MCF-7 Cells: In Vitro and In Vivo Control by Anti-TGFß Peptides

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Margheri, Francesca ^a,b   Schiavone, Nicola ^a,b   Papucci, Laura ^a,b   Magnelli, Lucia ^a,b   Serratì, Simona ^a,c   Chillà, Anastasia ^a,b   Laurenzana, Anna ^a,b   Bianchini, Francesca ^a,b   Calorini, Lido ^a,b   Torre, Eugenio ^a   Dotor, Javier ^d   Feijoo, Esperanza ^d   Fibbi, Gabriella ^a,b   Del Rosso, Mario ^a,b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b ISTITUTO TOSCANO TUMORI   (Italy)

^c NATIONAL CANCER INSTITUTE GIOVANNI PAOLO II   (Italy)

^d Digna Biotech   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; GROWTH DIFFERENTIATION FACTOR 5; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; UROKINASE RECEPTOR;

ANGIOGENESIS; ARTICLE; BREAST CARCINOMA; CANCER CELL; CELL ACTIVATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE ACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; ONCOGENE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TGFBETA GENE; UPREGULATION;

AMINO ACID SEQUENCE; ANTIBODIES; BREAST NEOPLASMS; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GROWTH DIFFERENTIATION FACTOR 5; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; PEPTIDES; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84870593890     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050342     Document Type: Article

References (53)

1. Roberts AB, Sporn MB, (1985) Transforming growth factors. Cancer Surv 4 (4):: 683-705.
2. de Caestecker MP, Piek E, Roberts AB, (2000) Role of transforming growth factor-beta signaling in cancer. J Natl Cancer Inst 92 (17):: 1388-1402.
3. Wakefield LM, Sporn MB, (1990) Suppression of carcinogenesis: a role for TGF-beta and related molecules in prevention of cancer. Immunol Ser 51: 217-243.
4. Akhurst RJ, Derynck R, (2001) TGF-beta signaling in cancer-a double-edged sword. Trends Cell Biol 11 (11):: S44-51.
5. Roberts AB, Wakefield LM, (2003) The two faces of transforming growth factor beta in carcinogenesis. Proc Natl Acad Sci U S A 100 (15):: 8621-8623.
6. Taylor MA, Lee YH, Schiemann WP, (2011) Role of TGF-beta and the tumor microenvironment during mammary tumorigenesis. Gene Expr 15 (3):: 117-132.
7. Zu X, Zhang Q, Cao R, Liu J, Zhong J, et al. (2012) Transforming growth factor-beta signaling in tumor initiation, progression and therapy in breast cancer: an update. Cell Tissue Res 347 (1):: 73-84.
8. Tian M, Neil JR, Schiemann WP, (2011) Transforming growth factor-beta and the hallmarks of cancer. Cell Signal 23 (6):: 951-962.
9. Seoane J, (2006) Escaping from the TGFbeta anti-proliferative control. Carcinogenesis 27 (11):: 2148-2156.
10. Buijs JT, Stayrook KR, Guise TA, (2011) TGF-beta in the Bone Microenvironment: Role in Breast Cancer Metastases. Cancer Microenviron 4 (3):: 261-281.
11. Vicent S, Luis-Ravelo D, Anton I, Garcia-Tunon I, Borras-Cuesta F, et al. (2008) A novel lung cancer signature mediates metastatic bone colonization by a dual mechanism. Cancer Res 68 (7):: 2275-2285.
12. Derynck R, Akhurst RJ, Balmain A, (2011) TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 29 (2):: 117-129.
13. Drabsch Y, ten Dijke P, (2011) TGF-beta signaling in breast cancer cell invasion and bone metastasis. J Mammary Gland Biol Neoplasia 16 (2):: 97-108.
14. Goumans MJ, Lebrin F, Valdimarsdottir G, (2003) Controlling the angiogenic switch: a balance between two distinct TGF-b receptor signaling pathways. Trends Cardiovasc Med 13 (7):: 301-307.
15. Pardali E, ten Dijke P, (2009) Transforming growth factor-beta signaling and tumor angiogenesis. Front Biosci 14: 4848-4861.
16. Pepper MS, (1997) Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 8 (1):: 21-43.
17. Serrati S, Margheri F, Pucci M, Cantelmo AR, Cammarota R, et al. (2009) TGFbeta1 antagonistic peptides inhibit TGFbeta1-dependent angiogenesis. Biochem Pharmacol 2009 77 (5):: 813-825.
18. Ferrari G, Pintucci G, Seghezzi G, Hyman K, Galloway AC, et al. (2006) VEGF, a prosurvival factor, acts in concert with TGF-beta1 to induce endothelial cell apoptosis. Proc Natl Acad Sci U S A 103 (46):: 17260-17265.
19. Ferrari G, Cook BD, Terushkin V, Pintucci G, Mignatti P, (2009) Transforming growth factor-beta 1 (TGF-beta1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J Cell Physiol 219 (2):: 449-458.
20. Enholm B, Paavonen K, Ristimaki A, Kumar V, Gunji Y, et al. (1997) Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14 (20):: 2475-2483.
21. Benckert C, Jonas S, Cramer T, Von Marschall Z, Schafer G, et al. (2003) Transforming growth factor beta 1 stimulates vascular endothelial growth factor gene transcription in human cholangiocellular carcinoma cells. Cancer Res 63 (5):: 1083-1092.
22. Oshima M, Oshima H, Taketo MM, (1996) TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 179 (1):: 297-302.
23. Pardali E, Goumans MJ, ten Dijke P, (2010) Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol 20 (9):: 556-567.
24. Ota T, Fujii M, Sugizaki T, Ishii M, Miyazawa K, et al. (2002) Aburatani H, Miyazono K: Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-beta in human umbilical vein endothelial cells. J Cell Physiol 193 (3):: 299-318.
25. Stefansson S, Lawrence DA, (1996) The serpin PAI-1 inhibits cell migration by blocking integrin alpha V beta 3 binding to vitronectin. Nature 383 (6599):: 441-443.
26. Stefansson S, Petitclerc E, Wong MK, McMahon GA, Brooks PC, et al. (2001) Inhibition of angiogenesis in vivo by plasminogen activator inhibitor-1. J Biol Chem 276 (11):: 8135-8141.
27. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, et al. (2002) Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J 21 (7):: 1743-1753.
28. Lamouille S, Mallet C, Feige JJ, Bailly S, (2002) Activin receptor-like kinase 1 is implicated in the maturation phase of angiogenesis. Blood 100 (13):: 4495-4501.
29. Cunha SI, Pietras K, (2011) ALK1 as an emerging target for antiangiogenic therapy of cancer. Blood 117 (26):: 6999-7006.
30. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S, (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109 (5):: 1953-1961.
31. Suzuki Y, Ohga N, Morishita Y, Hida K, Miyazono K, et al. (2010) BMP-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J Cell Sci 123 (Pt 10):: 1684-1692.
32. Cunha SI, Pardali E, Thorikay M, Anderberg C, Hawinkels L, (2010) Genetic and pharmacological targeting of activin receptor-like kinase 1 impairs tumor growth and angiogenesis. J Exp Med 207 (1):: 85-100.
33. Ueki N, Nakazato M, Ohkawa T, Ikeda T, Amuro Y, et al. (1992) Excessive production of transforming growth-factor beta 1 can play an important role in the development of tumorigenesis by its action for angiogenesis: validity of neutralizing antibodies to block tumor growth. Biochim Biophys Acta 1137 (2):: 189-196.
34. Pertovaara L, Kaipainen A, Mustonen T, Orpana A, Ferrara N, et al. (1994) Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells. J Biol Chem 269 (9):: 6271-6274.
35. D'Alessio S, Fibbi G, Cinelli M, Guiducci S, Del Rosso A, et al. (2004) Matrix metalloproteinase 12-dependent cleavage of urokinase receptor in systemic sclerosis microvascular endothelial cells results in impaired angiogenesis. Arthritis Rheum 50 (10):: 3275-3285.
36. Giusti B, Fibbi G, Margheri F, Serrati S, Rossi L, et al. (2006) A model of anti-angiogenesis: differential transcriptosome profiling of microvascular endothelial cells from diffuse systemic sclerosis patients. Arthritis Res Ther 8 (4):: R115.
37. Ezquerro IJ, Lasarte JJ, Dotor J, Castilla-Cortazar I, Bustos M, et al. (2003) A synthetic peptide from transforming growth factor beta type III receptor inhibits liver fibrogenesis in rats with carbon tetrachloride liver injury. Cytokine 22 (1-2):: 12-20.
38. Dotor J, Lopez-Vazquez AB, Lasarte JJ, Sarobe P, Garcia-Granero M, et al. (2007) Identification of peptide inhibitors of transforming growth factor beta 1 using a phage-displayed peptide library. Cytokine 39 (2):: 106-115.
39. Margheri F, Chilla A, Laurenzana A, Serrati S, Mazzanti B, et al. (2011) Endothelial progenitor cell-dependent angiogenesis requires localization of the full-length form of uPAR in caveolae. Blood 118 (13):: 3743-3755.
40. Akilesh S, Shaffer DJ, Roopenian D, (2003) Customized molecular phenotyping by quantitative gene expression and pattern recognition analysis. Genome Res 13 (7):: 1719-1727.
41. Fibbi G, Pucci M, Grappone C, Pellegrini G, Salzano R, et al. (1999) Functions of the fibrinolytic system in human Ito cells and its control by basic fibroblast and platelet-derived growth factor. Hepatology 29 (3):: 868-878.
42. Luo W, Fang W, Li S, Yao K, (2012) Aberrant expression of nuclear vimentin and related epithelial-mesenchymal transition markers in nasopharyngeal carcinoma. Int J Cancer.
43. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, et al. (2008) Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis 25 (6):: 629-642.
44. Upton PD, Long L, Trembath RC, Morrell NW, (2008) Functional characterization of bone morphogenetic protein binding sites and Smad1/5 activation in human vascular cells. Mol Pharmacol 73 (2):: 539-552.
45. Yamashita H, Shimizu A, Kato M, Nishitoh H, Ichijo H, et al. (1997) Growth/differentiation factor-5 induces angiogenesis in vivo. Exp Cell Res 235 (1):: 218-226.
46. Ramoshebi LN, Ripamonti U, (2000) Osteogenic protein-1, a bone morphogenetic protein, induces angiogenesis in the chick chorioallantoic membrane and synergizes with basic fibroblast growth factor and transforming growth factor-beta1. Anat Rec 259 (1):: 97-107.
47. Lebrin F, Deckers M, Bertolino P, Ten Dijke P, (2005) TGF-beta receptor function in the endothelium. Cardiovasc Res 65 (3):: 599-608.
48. Lin SJ, Lerch TF, Cook RW, Jardetzky TS, Woodruff TK, (2006) The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding. Reproduction 132 (2):: 179-190.
49. Gelbart WM, (1989) The decapentaplegic gene: a TGF-beta homologue controlling pattern formation in Drosophila. Development 107 Suppl: 65-74.
50. Kingsley DM, (1994) The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8 (2):: 133-146.
51. Wall NA, Hogan BL, (1994) TGF-beta related genes in development. Curr Opin Genet Dev 4 (4):: 517-522.
52. David L, Feige JJ, Bailly S, (2009) Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev 20 (3):: 203-212.
53. Hu-Lowe DD, Chen E, Zhang L, Watson KD, Mancuso P, et al. (2011) Targeting activin receptor-like kinase 1 inhibits angiogenesis and tumorigenesis through a mechanism of action complementary to anti-VEGF therapies. Cancer Res 71 (4):: 1362-1373.