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Originally published In Press as doi:10.1074/jbc.M008847200 on April 23, 2001

J. Biol. Chem., Vol. 276, Issue 26, 23341-23348, June 29, 2001
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Membrane Proximal ERK Signaling Is Required for M-calpain Activation Downstream of Epidermal Growth Factor Receptor Signaling*

Angela GladingDagger , Florian Überall§, Stephen M. Keyse, Douglas A. Lauffenburger||, and Alan WellsDagger **

From the Dagger  Department of Pathology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, the § Institute of Medical Chemistry and Biochemistry, University of Innsbruck, A-6020 Innsbruck, Austria, the  Imperial Cancer Research Fund Molecular Pharmacology Unit, Biomedical Research Centre, Ninewells Hospital, Dundee, DD1 9SY, United Kingdom, and the || Division of Bioengineering and Environmental Health, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Localization of signaling is critical in directing cellular outcomes, especially in pleiotropic signaling pathways. The extracellular signal-regulated kinase (ERK)/microtubule-associated protein kinase, which promotes cell migration, proliferation, and differentiation is found in the nucleus and throughout the cytoplasm. Recently, it has been shown that nuclear translocation of ERK is required for transcriptional changes and cell proliferation. However, the cellular consequences, of cytoplasmic signaling have not been defined. We explored whether cytoplasmic, specifically membrane-proximal, ERK signaling is involved in growth factor-induced cell motility. We previously have demonstrated that increased M-calpain activity downstream of epidermal growth factor receptor (EGFR)-mediated ERK activation is necessary for epidermal growth factor (EGF)-induced motility. Calpain isoforms also have been found in nuclear, cytosolic, and plasma membrane-associated compartments in a variety of cell types. We now employ cell engineering approaches to control localization of the upstream EGFR and ERK activities to examine the spatial effect of upstream signal locale on downstream calpain activity. With differential ligand-induced internalization and trafficking-restricted receptor variants, we find that calpain activity is triggered only by plasma membrane-restricted activated EGFR, not by internalized (although still active) EGFR. Cells transfected with membrane-targeted ERK1 and ERK2, which sequester endogenous ERKs, exhibited normal EGF-induced calpain activity. Transfection of an inactive ERK phosphatase (MKP-3/Pyst1) that sequesters ERK in the cytoplasm prevented calpain activation as well as de-adhesion. These data strongly suggest that EGF-induced calpain activity can be enhanced near sites of membrane-proximal EGFR-mediated ERK signaling, providing insights about how calpain activity might be regulated and targeted to enhance its effects on adhesion-related substrates.

* This study was supported by NIGMS, National Institutes of Health (NIH), Grant GM54739, a grant from the Department of Defense/Veterans Affairs Initiative on Combat Casualty (to A. W.), and NCI, NIH, Grant CA69213 (to D. A. L.), and the Austrian Fond SFB, F208.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.

** To whom correspondence should be addressed: Dept. of Pathology, 713 Scaife Hall, University of Pittsburgh, Pittsburgh, PA 15261. Tel.: 412-647-7813; Fax: 412-647-8567; E-mail: wellsa@msx.upmc.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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