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JCS ePress online publication date 11 Dec 2002
doi: 10.1242/jcs.00224

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Research Article

The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors


Victoria Bolós, Hector Peinado, Mirna A. Pérez-Moreno, Mario F. Fraga, Manel Esteller, and Amparo Cano*
* Author for correspondence (e-mail: acano{at}iib.uam.es)

Transcriptional repression mechanisms have emerged as one of the crucial processes for the downregulation of E-cadherin expression during development and tumour progression. Recently, several E-cadherin transcriptional repressors have been characterized (Snail, E12/E47, ZEB-1 and SIP-1) and shown to act through an interaction with proximal E-boxes of the E-cadherin promoter. We have analyzed the participation of another member of the Snail family, Slug, and observed that it also behaves as a repressor of E-cadherin expression. Stable expression of Slug in MDCK cells leads to the full repression of E-cadherin at transcriptional level and triggers a complete epithelial to mesenchymal transition. Slug-induced repression of E-cadherin is mediated by its binding to proximal E-boxes, particularly to the E-pal element of the mouse promoter. Detailed analysis of the binding affinity of different repressors to the E-pal element indicates that Slug binds with lower affinity than Snail and E47 proteins. These results, together with the known expression patterns of these factors in embryonic development and carcinoma cell lines, support the idea that the in vivo action of the different factors in E-cadherin repression can be modulated by their relative concentrations as well as by specific cellular or tumour contexts.


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 Am. J. Physiol. Cell Physiol.Home page
F. Carrozzino, P. Soulie, D. Huber, N. Mensi, L. Orci, A. Cano, E. Feraille, and R. Montesano
Inducible expression of Snail selectively increases paracellular ion permeability and differentially modulates tight junction proteins
Am J Physiol Cell Physiol, October 1, 2005; 289(4): C1002 - C1014.
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C. Huan, D. Sashital, T. Hailemariam, M. L. Kelly, and C. A. J. Roman
Renal Carcinoma-associated Transcription Factors TFE3 and TFEB Are Leukemia Inhibitory Factor-responsive Transcription Activators of E-cadherin
J. Biol. Chem., August 26, 2005; 280(34): 30225 - 30235.
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M. Jorda, D. Olmeda, A. Vinyals, E. Valero, E. Cubillo, A. Llorens, A. Cano, and A. Fabra
Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor
J. Cell Sci., August 1, 2005; 118(15): 3371 - 3385.
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 J. Am. Soc. Nephrol.Home page
K. Surendran, S. Schiavi, and K. A. Hruska
Wnt-Dependent {beta}-Catenin Signaling Is Activated after Unilateral Ureteral Obstruction, and Recombinant Secreted Frizzled-Related Protein 4 Alters the Progression of Renal Fibrosis
J. Am. Soc. Nephrol., August 1, 2005; 16(8): 2373 - 2384.
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 DevelopmentHome page
A. Barrallo-Gimeno and M. A. Nieto
The Snail genes as inducers of cell movement and survival: implications in development and cancer
Development, July 15, 2005; 132(14): 3151 - 3161.
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M. Maeda, K. R. Johnson, and M. J. Wheelock
Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition
J. Cell Sci., March 1, 2005; 118(5): 873 - 887.
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 J. Am. Soc. Nephrol.Home page
P. J. Margetts, P. Bonniaud, L. Liu, C. M. Hoff, C. J. Holmes, J. A. West-Mays, and M. M. Kelly
Transient Overexpression of TGF-{beta}1 Induces Epithelial Mesenchymal Transition in the Rodent Peritoneum
J. Am. Soc. Nephrol., February 1, 2005; 16(2): 425 - 436.
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 Mol. Cell. Biol.Home page
F. Palacios, J. S. Tushir, Y. Fujita, and C. D'Souza-Schorey
Lysosomal Targeting of E-Cadherin: a Unique Mechanism for the Down-Regulation of Cell-Cell Adhesion during Epithelial to Mesenchymal Transitions
Mol. Cell. Biol., January 1, 2005; 25(1): 389 - 402.
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M. J. Morgan, J. M. Woltering, P. M. J. In der Rieden, A. J. Durston, and J. P. Thiery
YY1 Regulates the Neural Crest-associated slug Gene in Xenopus laevis
J. Biol. Chem., November 5, 2004; 279(45): 46826 - 46834.
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 Mol. Cell. Biol.Home page
M. Kajita, K. N. McClinic, and P. A. Wade
Aberrant Expression of the Transcription Factors Snail and Slug Alters the Response to Genotoxic Stress
Mol. Cell. Biol., September 1, 2004; 24(17): 7559 - 7566.
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H. Peinado, F. Marin, E. Cubillo, H.-J. Stark, N. Fusenig, M. A. Nieto, and A. Cano
Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo
J. Cell Sci., June 1, 2004; 117(13): 2827 - 2839.
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 Am. J. Physiol. Cell Physiol.Home page
E. E. Schneeberger and R. D. Lynch
The tight junction: a multifunctional complex
Am J Physiol Cell Physiol, June 1, 2004; 286(6): C1213 - C1228.
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 BloodHome page
G. Prindull and D. Zipori
Environmental guidance of normal and tumor cell plasticity: epithelial mesenchymal transitions as a paradigm
Blood, April 15, 2004; 103(8): 2892 - 2899.
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 Mol. Cell. Biol.Home page
H. Peinado, E. Ballestar, M. Esteller, and A. Cano
Snail Mediates E-Cadherin Repression by the Recruitment of the Sin3A/Histone Deacetylase 1 (HDAC1)/HDAC2 Complex
Mol. Cell. Biol., January 1, 2004; 24(1): 306 - 319.
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 Cancer Res.Home page
M. A. Ginos, G. P. Page, B. S. Michalowicz, K. J. Patel, S. E. Volker, S. E. Pambuccian, F. G. Ondrey, G. L. Adams, and P. M. Gaffney
Identification of a Gene Expression Signature Associated with Recurrent Disease in Squamous Cell Carcinoma of the Head and Neck
Cancer Res., January 1, 2004; 64(1): 55 - 63.
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 JCBHome page
M. Conacci-Sorrell, I. Simcha, T. Ben-Yedidia, J. Blechman, P. Savagner, and A. Ben-Ze'ev
Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of {beta}-catenin signaling, Slug, and MAPK
J. Cell Biol., November 24, 2003; 163(4): 847 - 857.
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 JCBHome page
F. Zhang, C. C. Tom, M. C. Kugler, T.-T. Ching, J. A. Kreidberg, Y. Wei, and H. A. Chapman
Distinct ligand binding sites in integrin {alpha}3{beta}1 regulate matrix adhesion and cell-cell contact
J. Cell Biol., October 13, 2003; 163(1): 177 - 188.
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 J. Biol. Chem.Home page
H. Peinado, M. Quintanilla, and A. Cano
Transforming Growth Factor {beta}-1 Induces Snail Transcription Factor in Epithelial Cell Lines: MECHANISMS FOR EPITHELIAL MESENCHYMAL TRANSITIONS
J. Biol. Chem., May 30, 2003; 278(23): 21113 - 21123.
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J. Ikenouchi, M. Matsuda, M. Furuse, and S. Tsukita
Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail
J. Cell Sci., May 15, 2003; 116(10): 1959 - 1967.
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