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Originally published In Press as doi:10.1074/jbc.M202959200 on July 8, 2002

J. Biol. Chem., Vol. 277, Issue 38, 35766-35775, September 20, 2002
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Interferons Inhibit Tumor Necrosis Factor-alpha -mediated Matrix Metalloproteinase-9 Activation via Interferon Regulatory Factor-1 Binding Competition with NF-kappa B*

Josiane SancéauDagger , Douglas D. Boyd§, Motoharu Seiki, and Brigitte BauvoisDagger ||

From the Dagger  Unité 365 INSERM, Section de Recherche, Institut Curie, 75248 Paris Cedex 05, France, § Department of Cancer Biology, MD Anderson Cancer Center, Houston, Texas 77030, and  Department of Cancer Cell Research, Institute of Medical Science, the University of Tokyo 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan

Enhanced expression of matrix metalloproteinase-9 (MMP-9) correlates with invasion during tumor progression. Interferons (IFNs) inhibit MMP-9 activation in response to tumor necrosis factor-alpha (TNF-alpha ), and the latter activates the MMP-9 gene through NF-kappa B. Understanding the molecular basis for MMP-9 inhibition may provide tools to control cell invasion. The data reported here show the critical role of interferon regulatory factor-1 (IRF1) in the inhibition of MMP-9. (i) IFN treatment suppresses TNF-alpha -induced MMP-9 reporter activity in STAT1(+/+) cells but not in STAT1(-/-) cells. (ii) IRF1 transfection blocks TNF-alpha -mediated MMP-9 activation. (iii) IFNs phosphorylate STAT1 and induce IRF1 but do not affect Ikappa -B degradation nor NF-kappa B nuclear translocation. (iv) Nuclear NF-kappa B (p50/p65) and IRF1, but not STAT1, bind to the MMP-9 promoter region containing an IFN-responsive-like element overlapping the NF-kappa B-binding site. (v) Recombinant IRF1, although unable to bind to an NF-kappa B consensus sequence, competes with NF-kappa B proteins for binding to the MMP-9 promoter. (vi) Conversely recombinant p50/p65 proteins reduce IRF1-DNA binding. (vii) In cells cotransfected with IRF1 and/or p65 expression vectors, an excess of IRF1 reduces MMP-9 reporter activity, whereas an excess of p65 blocks the inhibitory effect of IFN-gamma . Thus, in contrast to the known synergism between IRF1 and NF-kappa B, our data identify a novel role for IRF1 as a competitive inhibitor of NF-kappa B binding to the particular MMP-9 promoter context.

* This work was supported by grants from INSERM and Grant 5424 from the Association pour la Recherche sur le Cancer.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: Unité 365 INSERM, Institut Curie, Pavillon Pasteur, 26 Rue d'Ulm, 75248 Paris Cedex 05, France. Tel.: 01-42-34-67-11; Fax: 01-44-07-07-85; E-mail: Brigitte.Bauvois@curie.fr.

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