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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

b-gumbiner{at}ski.mskcc.org

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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   Abstract »    Full Text »    PDF »
An Alternatively Spliced Cadherin-11 Enhances Human Breast Cancer Cell Invasion.
C. M. Feltes, A. Kudo, O. Blaschuk, and S. W. Byers (2002)
Cancer Res. 62, 6688-6697
   Abstract »    Full Text »    PDF »
A yeast model system for functional analysis of {beta}-catenin signaling.
M. S. Lee, K. A. D'Amour, and J. Papkoff (2002)
J. Cell Biol. 158, 1067-1078
   Abstract »    Full Text »    PDF »
Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and beta -catenin.
K. Venkiteswaran, K. Xiao, S. Summers, C. C. Calkins, P. A. Vincent, K. Pumiglia, and A. P. Kowalczyk (2002)
Am J Physiol Cell Physiol 283, C811-C821
   Abstract »    Full Text »    PDF »
Regulation of leukemic cell adhesion, proliferation, and survival by beta -catenin.
E. J. Chung, S.-G. Hwang, P. Nguyen, S. Lee, J.-S. Kim, J. W. Kim, P. A. Henkart, D. P. Bottaro, L. Soon, P. Bonvini, et al. (2002)
Blood 100, 982-990
   Abstract »    Full Text »    PDF »
The Role of Cadherin, beta -Catenin, and AP-1 in Retinoid-regulated Carcinoma Cell Differentiation and Proliferation.
S. Shah, M. J. Pishvaian, V. Easwaran, P. H. Brown, and S. W. Byers (2002)
J. Biol. Chem. 277, 25313-25322
   Abstract »    Full Text »    PDF »
Cell adhesion differentially regulates the nucleocytoplasmic distribution of active MAP kinases.
A. E. Aplin, B. P. Hogan, J. Tomeu, and R. L. Juliano (2002)
J. Cell Sci. 115, 2781-2790
   Abstract »    Full Text »    PDF »
Galpha 12 and Galpha 13 Negatively Regulate the Adhesive Functions of Cadherin.
T. E. Meigs, M. Fedor-Chaiken, D. D. Kaplan, R. Brackenbury, and P. J. Casey (2002)
J. Biol. Chem. 277, 24594-24600
   Abstract »    Full Text »    PDF »

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