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Originally published In Press as doi:10.1074/jbc.M107611200 on October 31, 2001

J. Biol. Chem., Vol. 277, Issue 3, 2065-2072, January 18, 2002
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Matrix Metalloproteinase Gelatinase B (MMP-9) Coordinates and Effects Epithelial Regeneration*

Royce MohanDagger §, Shravan K. ChintalaDagger , Jae Chang JungDagger , Winston V. L. Villar, Frank McCabe, Laoti A. Russo, Yunhee Lee, Brendan E. McCarthy, Kurt R. Wollenberg, James V. Jester||, Min Wang**, Howard G. Welgus**Dagger Dagger , J. Michael Shipley§§, Robert M. Senior§§, and M. Elizabeth Fini¶¶

From the New England Eye Center, Tufts University School of Medicine, and the Tufts Center for Vision Research, Boston, Massachusetts 02111, the || Department of Ophthalmology, University of Texas Southwestern Medical Center, Dallas, Texas 75390, and the ** Division of Dermatology and §§ Department of Medicine, Washington University School of Medicine at Barnes-Jewish Hospital, St. Louis, Missouri 63110

We studied the role of the matrix metalloproteinase gelatinase B (gelB; MMP-9) in epithelial regeneration using the gelB-deficient mouse. We report the novel finding that, in contrast to other MMPs expressed at the front of the advancing epithelial sheet in wounds of cornea, skin, or trachea, gelB acts to inhibit the rate of wound closure. We determined this to be due to control of cell replication, a novel capacity for MMPs not previously described. We also found that gelB delays the inflammatory response. Acceleration of these processes in gelB-deficient mice is correlated with a delay in signal transduction through Smad2, a transcription factor that inhibits cell proliferation, and in accumulation of epithelial-associated interleukin-1alpha , a cytokine that inhibits Smad2 signaling and promotes the inflammatory response. GelB-deficient mice also reveal defects in remodeling of extracellular matrix at the epithelial basement membrane zone, in particular, failure to effectively remove the fibrin(ogen) provisional matrix. We conclude that gelB coordinates and effects multiple events involved in the process of epithelial regeneration.

* This work was supported by project grants AR42981 and EY12651 (to M. E. F.), EY07348 (to J. V. J.), and HL47328 (to R. M. S.), National Eye Institute Center Grant EY13078 (to M. E. F.), the Massachusetts Lions Eye Research Fund, Inc. (to M. E. F.), by an unrestricted grant from Research to Prevent Blindness (to M. E. F., and J. V. J.), the Alan A. and Edith L. Wolff Charitable Trust (to R. M. S.), and the New England Medical Center Hospitals Research Fund (to M. E. F.).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.

Dagger These authors contributed equally to the results of this work.

§ Present address: EntreMed, Inc., Rockville, MD 20850.

Present address: Eye Research Institute, Oakland University, Rochester, MI 48309.

Dagger Dagger Present address: Parke-Davis Pharmaceutical Research, Ann Arbor, MI 48103.

¶¶ Jules and Doris Stein Research to Prevent Blindness Professor. To whom correspondence should be addressed: New England Eye Center, Tufts University School of Medicine, 750 Washington St., Box 450, Boston, MA 02111. Tel.: 617-636-9027; Fax: 617-636-4594; E-mail: efini@lifespan.org.

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