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Originally published In Press as doi:10.1074/jbc.M202384200 on July 23, 2002

J. Biol. Chem., Vol. 277, Issue 41, 38159-38167, October 11, 2002
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Proteinase Suppression by E-cadherin-mediated Cell-Cell Attachment in Premalignant Oral Keratinocytes*

Hidayatullah G. MunshiDagger §||, Supurna Ghosh**, Subhendu Mukhopadhyay**, Yi I. Wu**, Ratna Sen**, Kathleen J. Green§§§, and M. Sharon Stack§**Dagger Dagger ¶¶

From the Dagger  Division of Hematology/Oncology, Department of Medicine, Departments of ** Cell and Molecular Biology, Dagger Dagger  Obstetrics and Gynecology, §§ Pathology and Dermatology, Feinberg School of Medicine, Northwestern University and the § Robert H. Lurie Comprehensive Cancer Center of Northwestern University, Chicago, Illinois 60611

The expression and activity of epithelial proteinases is under stringent control to prevent aberrant hydrolysis of structural proteins and disruption of tissue architecture. E-cadherin-dependent cell-cell adhesion is also important for maintenance of epithelial structural integrity, and loss of E-cadherin expression has been correlated with enhanced invasive potential in multiple tumor models. To address the hypothesis that there is a functional link between E-cadherin and proteinase expression, we have examined the role of E-cadherin in proteinase regulation. By using a calcium switch protocol to manipulate junction assembly, our data demonstrate that initiation of de novo E-cadherin-mediated adhesive contacts suppresses expression of both relative matrix metalloproteinase-9 levels and net urinary-type plasminogen activator activity. E-cadherin-mediated cell-cell adhesion increases both phosphatidylinositol 3'-kinase (PI3-kinase)-dependent AKT phosphorylation and epidermal growth factor receptor-dependent MAPK/ERK activation. Pharmacologic inhibition of the PI3-kinase pathway, but not the epidermal growth factor receptor/MAPK pathway, prevents E-cadherin-mediated suppression of proteinases and delays junction assembly. Moreover, inhibition of junction assembly with a function-blocking anti-E-cadherin antibody stimulates proteinase-dependent Matrigel invasion. As matrix metalloproteinase-9 and urinary-type plasminogen activator potentiate the invasive activity of oral squamous cell carcinoma, these data suggest E-cadherin-mediated signaling through PI3-kinase can regulate the invasive behavior of cells by modulating proteinase secretion.

* This work was supported in part by NIDCR Research Grant PO1 DE12328 from the National Institutes of Health (to M. S. S. and K. J. G.) and National Institutes of Health Grant RO1 CA 85870 (to M. S. S.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Both authors contributed equally to this work.

|| Supported by NCI Clinical Oncology Research Training Program Grant T32 CA79447 from the National Institutes of Health.

¶¶ To whom correspondence should be addressed: Dept. of Cell and Molecular Biology, Northwestern University Medical School, 303 E. Chicago Ave., Tarry 8-715, Chicago IL 60611. Tel.: 312-908-8216; Fax: 312-503-7912; E-mail: mss130@northwestern.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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