Transforming growth factor-β1 inhibits trophoblast cell invasion by inducing snail-mediated down-regulation of vascular endothelial-cadherin protein

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 33181-33192

  Cheng, Jung Chien ^a   Chang, Hsun Ming ^a   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION ANALYSIS; DIRECT BINDINGS; INHIBITORY EFFECT; MOLECULAR MECHANISM; OVER-EXPRESSION; PRIMARY CULTURE; SIGNALING PATHWAYS; TRANSFORMING GROWTH FACTORS;

ANIMALS; CYTOLOGY; ENDOTHELIAL CELLS; MOLLUSCS;

GLYCOPROTEINS;

MESSENGER RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR ENDOTHELIAL CADHERIN;

ARTICLE; CELL INVASION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; PRIMARY CULTURE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TROPHOBLAST; UPREGULATION; VASCULAR ENDOTHELIAL CADHERIN GENE;

CADHERINS; INVASION; SMAD TRANSCRIPTION FACTOR; SNAIL; TRANSFORMING GROWTH FACTOR-Β (TGFΒ); TROPHOBLAST; VE-CADHERIN;

ANTIGENS, CD; CADHERINS; CELL LINE, TRANSFORMED; DOWN-REGULATION; HUMANS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TROPHOBLASTS;

EID: 84887834889     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.488866     Document Type: Article

References (53)

1. Chaddha, V., Viero, S., Huppertz, B., and Kingdom, J. (2004) Developmental biology of the placenta and the origins of placental insufficiency. Semin. Fetal Neonatal Med. 9, 357-369
2. Lim, K. H., Zhou, Y., Janatpour, M., McMaster, M., Bass, K., Chun, S. H., and Fisher, S. J. (1997) Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am. J. Pathol. 151, 1809-1818
3. Brosens, I., Pijnenborg, R., Vercruysse, L., and Romero, R. (2011) The "Great Obstetrical Syndromes" are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 204, 193-201
4. Böttner, M., Krieglstein, K., and Unsicker, K. (2000) The transforming growth factor-βs. Structure, signaling, and roles in nervous system development and functions. J. Neurochem, 75, 2227-2240
5. Blobe, G. C., Schiemann, W. P., and Lodish, H. F. (2000) Role of transforming growth factor β in human disease. N. Engl. J. Med. 342, 1350-1358
6. Krieglstein, K., Rufer, M., Suter-Crazzolara, C., and Unsicker, K. (1995) Neural functions of the transforming growth factors β. Int. J. Dev. Neurosci. 13, 301-315
7. Shi, Y., and Massagué, J. (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700
8. Heldin, C. H., Miyazono, K., and ten Dijke, P. (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471
9. Vestweber, D. (2008) VE-cadherin. The major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28, 223-232
10. Le Guelte, A., Dwyer, J., and Gavard, J. (2011) Jumping the barrier. VEcadherin, VEGF and other angiogenic modifiers in cancer. Biol. Cell 103, 593-605
11. Kobielak, A., and Fuchs, E. (2004) α-Catenin. At the junction of intercellular adhesion and actin dynamics. Nat. Rev. Mol. Cell Biol. 5, 614-625
12. Zhou, Y., Fisher, S. J., Janatpour, M., Genbacev, O., Dejana, E., Wheelock, M., and Damsky, C. H. (1997) Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 99, 2139-2151
13. Kokkinos, M. I., Murthi, P., Wafai, R., Thompson, E. W., and Newgreen, D. F. (2010) Cadherins in the human placenta-epithelial-mesenchymal transition (EMT) and placental development. Placenta 31, 747-755
14. Zhou, Y., Damsky, C. H., and Fisher, S. J. (1997) Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J. Clin. Invest. 99, 2152-2164
15. Jones, R. L., Stoikos, C., Findlay, J. K., and Salamonsen, L. A. (2006) TGF-β superfamily expression and actions in the endometrium and placenta. Reproduction 132, 217-232
16. Lash, G. E., Otun, H. A., Innes, B. A., Bulmer, J. N., Searle, R. F., and Robson, S. C. (2005) Inhibition of trophoblast cell invasion by TGFB1, -2, and -3 is associated with a decrease in active proteases. Biol. Reprod. 73, 374-381
17. Graham, C. H., Hawley, T. S., Hawley, R. G., MacDougall, J. R., Kerbel, R. S., Khoo, N., and Lala, P. K. (1993) Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp. Cell Res. 206, 204-211
18. Graham, C. H., Lysiak, J. J., McCrae, K. R., and Lala, P. K. (1992) Localization of transforming growth factor-β at the human fetal-maternal interface. Role in trophoblast growth and differentiation. Biol. Reprod. 46, 561-572
19. Woo, M. M., Salamanca, C. M., Minor, A., and Auersperg, N. (2007) An improved assay to quantitate the invasiveness of cells in modified Boyden chambers. In Vitro Cell Dev. Biol. Anim 43, 7-9
20. Gleeson, L. M., Chakraborty, C., McKinnon, T., and Lala, P. K. (2001) Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through α5β1 integrin via mitogen-activated protein kinase pathway. J. Clin. Endocrinol. Metab. 86, 2484-2493
21. Lala, P. K., and Graham, C. G. (2001) TGFB-responsive human trophoblast- derived cell lines. Placenta 22, 889-890
22. Inman, G. J., Nicolás, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J., and Hill, C. S. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74
23. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890
24. Brown, K. A., Pietenpol, J. A., and Moses, H. L. (2007) A tale of two proteins. Differential roles and regulation of Smad2 and Smad3 in TGF-β signaling. J. Cell. Biochem. 101, 9-33
25. Saitoh, M., and Miyazawa, K. (2012) Transcriptional and post-transcriptional regulation in TGF-β-mediated epithelial-mesenchymal transition. J. Biochem. 151, 563-571
26. Lopez, D., Niu, G., Huber, P., and Carter, W. B. (2009) Tumor-induced upregulation of Twist, Snail, and Slug represses the activity of the human VE-cadherin promoter. Arch. Biochem. Biophys. 482, 77-82
27. Xu, G., Chakraborty, C., and Lala, P. K. (2001) Expression of TGF-β signaling genes in the normal, premalignant, and malignant human trophoblast. Loss of smad3 in choriocarcinoma cells. Biochem. Biophys. Res. Commun. 287, 47-55
28. Benian, A., Madazli, R., Aksu, F., Uzun, H., and Aydin, S. (2002) Plasma and placental levels of interleukin-10, transforming growth factor-β1, and epithelial-cadherin in preeclampsia. Obstet. Gynecol. 100, 327-331
29. Muy-Rivera, M., Sanchez, S. E., Vadachkoria, S., Qiu, C., Bazul, V., and Williams, M. A. (2004) Transforming growth factor-β1 (TGF-β1) in plasma is associated with preeclampsia risk in Peruvian women with systemic inflammation. Am. J. Hypertens. 17, 334-338
30. Xuan, Y. H., Choi, Y. L., Shin, Y. K., Ahn, G. H., Kim, K. H., Kim, W. J., Lee, H. C., and Kim, S. H. (2007) Expression of TGF-β signaling proteins in normal placenta and gestational trophoblastic disease. Histol. Histopathol. 22, 227-234
31. Meisser, A., Chardonnens, D., Campana, A., and Bischof, P. (1999) Effects of tumour necrosis factor-α, interleukin-1α, macrophage colony stimulating factor and transforming growth factor β on trophoblastic matrix metalloproteinases. Mol. Hum. Reprod. 5, 252-260
32. Graham, C. H. (1997) Effect of transforming growth factor-beta on the plasminogen activator system in cultured first trimester human cytotrophoblasts. Placenta 18, 137-143
33. Karmakar, S., and Das, C. (2002) Regulation of trophoblast invasion by IL-1β and TGF-β1. Am. J. Reprod. Immunol. 48, 210-219
34. Lim, J., and Thiery, J. P. (2012) Epithelial-mesenchymal transitions. Insights from development. Development 139, 3471-3486
35. Voulgari, A., and Pintzas, A. (2009) Epithelial-mesenchymal transition in cancer metastasis. Mechanisms, markers, and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta 1796, 75-90
36. Li, H. W., Cheung, A. N., Tsao, S. W., Cheung, A. L., and O, W. S. (2003) Expression of E-cadherin and -catenin in trophoblastic tissue in normal and pathological pregnancies. Int. J. Gynecol. Pathol. 22, 63-70
37. Katsuno, Y., Lamouille, S., and Derynck, R. (2013) TGF-β signaling and epithelial-mesenchymal transition in cancer progression. Curr. Opin. Oncol. 25, 76-84
38. Fritzmann, J., Morkel, M., Besser, D., Budczies, J., Kosel, F., Brembeck, F. H., Stein, U., Fichtner, I., Schlag, P. M., and Birchmeier, W. (2009) A colorectal cancer expression profile that includes transforming growth factor β inhibitor BAMBI predicts metastatic potential. Gastroenterology 137, 165-175
39. Humbert, L., and Lebrun, J. J. (2013) TGF-β inhibits human cutaneous melanoma cell migration and invasion through regulation of the plasminogen activator system. Cell Signal. 25, 490-500
40. Hölting, T., Zielke, A., Siperstein, A. E., Clark, O. H., and Duh, Q. Y. (1994) Transforming growth factor-β1 is a negative regulator for differentiated thyroid cancer. Studies of growth, migration, invasion, and adhesion of cultured follicular and papillary thyroid cancer cell lines. J. Clin. Endocrinol. Metab. 79, 806-813
41. Wang, X., Sun, W., Zhang, C., Ji, G., Ge, Y., Xu, Y., and Zhao, Y. (2011) TGF-β1 inhibits the growth and metastasis of tongue squamous carcinoma cells through Smad4. Gene 485, 160-166
42. Zhao, M. R., Qiu, W., Li, Y. X., Zhang, Z. B., Li, D., and Wang, Y. L. (2006) Dual effect of transforming growth factorß1 on cell adhesion and invasion in human placenta trophoblast cells. Reproduction 132, 333-341
43. Chen, Y., Wang, K., and Leach, R. (2013) 5-Aza-dC treatment induces mesenchymal-to-epithelial transition in 1st trimester trophoblast cell line HTR8/SVneo. Biochem. Biophys. Res. Commun. 432, 116-122
44. Ng, Y. H., Zhu, H., and Leung, P. C. (2012) Twist modulates human trophoblastic cell invasion via regulation of N-cadherin. Endocrinology 153, 925-936
45. Lala, N., Girish, G. V., Cloutier-Bosworth, A., and Lala, P. K. (2012) Mechanisms in decorin regulation of vascular endothelial growth factor-induced human trophoblast migration and acquisition of endothelial phenotype. Biol. Reprod. 87, 59
46. Li, Z., and Jimenez, S. A. (2011) Protein kinase Cδ and c-Abl kinase are required for transforming growth factor-β induction of endothelial-mesenchymal transition in vitro. Arthritis Rheum. 63, 2473-2483
47. Yang, H., Zhang, L., Weakley, S. M., Lin, P. H., Yao, Q., and Chen, C. (2011) Transforming growth factor-β increases the expression of vascular smooth muscle cell markers in human multi-lineage progenitor cells. Med. Sci. Monit. 17, BR55-61
48. Maroni, D., and Davis, J. S. (2011) TGFB1 disrupts the angiogenic potential of microvascular endothelial cells of the corpus luteum. J. Cell Sci. 124, 2501-2510
49. Birdsey, G. M., Dryden, N. H., Amsellem, V., Gebhardt, F., Sahnan, K., Haskard, D. O., Dejana, E., Mason, J. C., and Randi, A. M. (2008) Transcription factor Erg regulates angiogenesis and endothelial apoptosis through VE-cadherin. Blood 111, 3498-3506
50. Deleuze, V., Chalhoub, E., El-Hajj, R., Dohet, C., Le Clech, M., Couraud, P. O., Huber, P., and Mathieu, D. (2007) TAL-1/SCL and its partners E47 and LMO2 up-regulate VE-cadherin expression in endothelial cells. Mol. Cell. Biol. 27, 2687-2697
51. Gory, S., Dalmon, J., Prandini, M. H., Kortulewski, T., de Launoit, Y., and Huber, P. (1998) Requirement of a GT box (Sp1 site) and two Ets binding sites for vascular endothelial cadherin gene transcription. J. Biol. Chem. 273, 6750-6755
52. Becker, K. F., Rosivatz, E., Blechschmidt, K., Kremmer, E., Sarbia, M., and Höfler, H. (2007) Analysis of the E-cadherin repressor Snail in primary human cancers. Cells Tissues Organs 185, 204-212
53. Ward, S. T., Dangi-Garimella, S., Shields, M. A., Collander, B. A., Siddiqui, M. A., Krantz, S. B., and Munshi, H. G. (2011) Ethanol differentially regulates snail family of transcription factors and invasion of premalignant and malignant pancreatic ductal cells. J. Cell. Biochem. 112, 2966-2973