A novel role for p120 catenin in E-cadherin function (original) (raw)

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Article| November 11 2002

Reneé C. Ireton,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Michael A. Davis,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Jolanda van Hengel,

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

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Deborah J. Mariner,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Kirk Barnes,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Molly A. Thoreson,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Panos Z. Anastasiadis,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Linsey Matrisian,

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Linda M. Bundy,

2Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232

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Linda Sealy,

2Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232

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Barbara Gilbert,

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

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Frans van Roy,

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

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Albert B. Reynolds

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

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Reneé C. Ireton

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Michael A. Davis

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Jolanda van Hengel

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

Deborah J. Mariner

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Kirk Barnes

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Molly A. Thoreson

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Panos Z. Anastasiadis

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Linsey Matrisian

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Linda M. Bundy

2Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232

Linda Sealy

2Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232

Barbara Gilbert

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

Frans van Roy

3Molecular Cell Biology Unit, Department of Molecular Biology, Flanders Interuniversity Institute for Biotechnology, University of Gent, B-9000 Gent, Belgium

Albert B. Reynolds

1Department of Cancer Biology, Vanderbilt University School of Medicine, Nashville, TN 37232

Address correspondence to Albert B. Reynolds, Dept. Cancer Biology, Vanderbilt University, 771 PRB, Nashville, TN 37232-6840. Tel.: (615) 343-9532. Fax: (615) 936-6399. E-mail: [email protected]

*

Abbreviations used in this paper: ARM, armadillo; IRES, internal ribosomal entry site; JMD, juxtamembrane domain; neo, neomycin resistance gene; p120, p120-catenin; PS, presenilin.

Received: May 23 2002

Revision Received: September 30 2002

Accepted: September 30 2002

Online ISSN: 1540-8140

Print ISSN: 0021-9525

The Rockefeller University Press

2002

J Cell Biol (2002) 159 (3): 465–476.

Article history

Revision Received:

September 30 2002

Accepted:

September 30 2002

Citation

Reneé C. Ireton, Michael A. Davis, Jolanda van Hengel, Deborah J. Mariner, Kirk Barnes, Molly A. Thoreson, Panos Z. Anastasiadis, Linsey Matrisian, Linda M. Bundy, Linda Sealy, Barbara Gilbert, Frans van Roy, Albert B. Reynolds; A novel role for p120 catenin in E-cadherin function . _J Cell Biol 11 November 2002; 159 (3): 465–476. doi: https://doi.org/10.1083/jcb.200205115

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Îndirect evidence suggests that p120-catenin (p120) can both positively and negatively affect cadherin adhesiveness. Here we show that the p120 gene is mutated in SW48 cells, and that the cadherin adhesion system is impaired as a direct consequence of p120 insufficiency. Restoring normal levels of p120 caused a striking reversion from poorly differentiated to cobblestone-like epithelial morphology, indicating a crucial role for p120 in reactivation of E-cadherin function. The rescue efficiency was enhanced by increased levels of p120, and reduced by the presence of the phosphorylation domain, a region previously postulated to confer negative regulation. Surprisingly, the rescue was associated with substantially increased levels of E-cadherin. E-cadherin mRNA levels were unaffected by p120 expression, but E-cadherin half-life was more than doubled. Direct p120–E-cadherin interaction was crucial, as p120 deletion analysis revealed a perfect correlation between E-cadherin binding and rescue of epithelial morphology. Interestingly, the epithelial morphology could also be rescued by forced expression of either WT E-cadherin or a p120-uncoupled mutant. Thus, the effects of uncoupling p120 from E-cadherin can be at least partially overcome by artificially maintaining high levels of cadherin expression. These data reveal a cooperative interaction between p120 and E-cadherin and a novel role for p120 that is likely indispensable in normal cells.

The Rockefeller University Press

2002

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