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J. Cell Biol. 153 (5): 1049-1060

Copyright © 2001 by the Rockefeller University Press.

Original Article

E-Cadherin Suppresses Cellular Transformation by Inhibiting β-Catenin Signaling in an Adhesion-Independent Manner

Cara J. Gottardia, Ellen Wonga, , and Barry M. Gumbinera

a Cellular Biochemistry and Biophysics Program, Memorial Sloan-Kettering Cancer Center, New York, New York 10021
1275 York Ave., Box 564, New York, NY 10021.(212) 717-3047(212) 639-6147


Abstract: E-cadherin is a tumor suppressor protein with a well-established role in cell–cell adhesion. Adhesion could contribute to tumor suppression either by physically joining cells or by facilitating other juxtacrine signaling events. Alternatively, E-cadherin tumor suppressor activity could result from binding and antagonizing the nuclear signaling function of β-catenin, a known proto-oncogene. To distinguish between an adhesion- versus a β-catenin signaling–dependent mechanism, chimeric cadherin constructs were expressed in the SW480 colorectal tumor cell line. Expression of wild-type E-cadherin significantly inhibits the growth of this cell line. Growth inhibitory activity is retained by all constructs that have the β-catenin binding region of the cytoplasmic domain but not by E-cadherin constructs that exhibit adhesive activity, but lack the β-catenin binding region. This growth suppression correlates with a reduction in β-catenin/T cell factor (TCF) reporter gene activity. Importantly, direct inhibition of β-catenin/TCF signaling inhibits the growth of SW480 cells, and the growth inhibitory activity of E-cadherin is rescued by constitutively activated forms of TCF. Thus, the growth suppressor activity of E-cadherin is adhesion independent and results from an inhibition of the β-catenin/TCF signaling pathway, suggesting that loss of E-cadherin expression can contribute to upregulation of this pathway in human cancers. E-cadherin–mediated growth suppression was not accompanied by overall depletion of β-catenin from the cytosol and nucleus. This appears to be due to the existence of a large pool of cytosolic β-catenin in SW480 cells that is refractory to both cadherin binding and TCF binding. Thus, a small pool of β-catenin that can bind TCF (i.e., the transcriptionally active pool) can be selectively depleted by E-cadherin expression. The existence of functionally distinct pools of cytosolic β-catenin suggests that there are mechanisms to regulate β-catenin signaling in addition to controlling its level of accumulation.

Key Words: E-cadherin • tumor suppressor • adhesion • β-catenin • T cell factor

Abbreviations used in this paper: ConA, concanavalin A; GST, glutathione S-transferase; LEF, lymphocyte enhancer factor; TCF, T cell factor.

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M. G. Lampugnani, A. Zanetti, M. Corada, T. Takahashi, G. Balconi, F. Breviario, F. Orsenigo, A. Cattelino, R. Kemler, T. O. Daniel, et al. (2003)
J. Cell Biol. 161, 793-804
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Hepatocyte Growth Factor Receptor Tyrosine Kinase Met Is a Substrate of the Receptor Protein-tyrosine Phosphatase DEP-1.
H. L. Palka, M. Park, and N. K. Tonks (2003)
J. Biol. Chem. 278, 5728-5735
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The LIM Protein Ajuba Is Recruited to Cadherin-dependent Cell Junctions through an Association with alpha -Catenin.
H. Marie, S. J. Pratt, M. Betson, H. Epple, J. T. Kittler, L. Meek, S. J. Moss, S. Troyanovsky, D. Attwell, G. D. Longmore, et al. (2003)
J. Biol. Chem. 278, 1220-1228
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Intermediate filament-membrane attachments function synergistically with actin-dependent contacts to regulate intercellular adhesive strength.
A. C. Huen, J. K. Park, L. M. Godsel, X. Chen, L. J. Bannon, E. V. Amargo, T. Y. Hudson, A. K. Mongiu, I. M. Leigh, D. P. Kelsell, et al. (2002)
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