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Vol. 20, Issue 3, 1102-1117, February 1, 2009

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Zona Occludens-2 Inhibits Cyclin D1 Expression and Cell Proliferation and Exhibits Changes in Localization along the Cell Cycle

Rocio Tapia^*, Miriam Huerta, Socorro Islas^*, Antonia Avila-Flores, Esther Lopez-Bayghen, Jörg Weiske, Otmar Huber^,||, and Lorenza González-Mariscal^*

*Department of Physiology, Biophysics, and Neuroscience, and Department of Genetics and Molecular Biology, Center for Research and Advanced Studies (CINVESTAV), Mexico, D.F., 07360, Mexico; Department of Immunology and Oncology, National Center for Biotechnology, Consejo Superior de Investigaciones Cientificas, Campus Cantoblanco, E-28049 Madrid, Spain; Department of Laboratory Medicine and Pathobiochemistry, Charité-Universitätsmedizin Berlin, 12200 Berlin, Germany; and ^||Department of Biochemistry II, Friedrich-Schiller-University Jena, 07743 Jena, Germany

Submitted March 14, 2008; Revised October 28, 2008; Accepted November 21, 2008
Monitoring Editor: Keith E. Mostov

Here, we have studied the effect of the tight junction protein zona occludens (ZO)-2 on cyclin D1 (CD1) protein expression. CD1 is essential for cell progression through the G1 phase of the cell cycle. We have found that in cultures of synchronized Madin-Darby canine kidney cells, ZO-2 inhibits cell proliferation at G0/G1 and decreases CD1 protein level. These effects occur in response to a diminished CD1 translation and an augmented CD1 degradation at the proteosome triggered by ZO-2. ZO-2 overexpression decreases the amount of Glycogen synthase kinase-3β phosphorylated at Ser9 and represses β-catenin target gene expression. We have also explored the expression of ZO-2 through the cell cycle and demonstrate that ZO-2 enters the nucleus at the late G1 phase and leaves the nucleus when the cell is in mitosis. These results thus explain why in confluent quiescent epithelia ZO-2 is absent from the nucleus and localizes at the cellular borders, whereas in sparse proliferating cultures ZO-2 is conspicuously present at the nucleus.

Address correspondence to: Lorenza Gonzalez-Mariscal (lorenza{at}fisio.cinvestav.mx)

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