In Vivo Evidence That the Stromelysin-3 Metalloproteinase Contributes in a Paracrine Manner to Epithelial Cell Malignancy

doi:10.1083/jcb.140.6.1535

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© The Rockefeller University Press, 0021-9525/1998//1535 $5.00
The Journal of Cell Biology, Volume 140, Number 6, , 1998 1535-1541

Article

In Vivo Evidence That the Stromelysin-3 Metalloproteinase Contributes in a Paracrine Manner to Epithelial Cell Malignancy

Régis Masson^*, Olivier Lefebvre^*, Agnès Noël, Mostapha El Fahime^*, Marie-Pierre Chenard^||, Corinne Wendling^*, Florence Kebers, Marianne LeMeur^*, Andrée Dierich^*, Jean-Michel Foidart, Paul Basset^*, and Marie-Christine Rio^*

^* Institut de Génétique et de Biologie Moléculaire et Cellulaire, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Université Louis Pasteur, BP 163, 67404 Illkirch Cedex, C.U. de Strasbourg, France; Laboratoire de Biologie des Tumeurs et du Développement, University of Liège, 4000 Sart-Tilman, Liège, Belgium; and ^|| Service d'Anatomie Pathologique Générale, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, 67098 Strasbourg Cedex, France

Stromelysin-3 (ST3; Basset, P., J.P. Bellocq, C. Wolf, I. Stoll,P. Hutin, J.M. Limacher, O.L. Podhajcer, M.P. Chenard, M.C.Rio, P. Chambon. 1990. Nature. 348:699–704) is a matrixmetalloproteinase (MMP) expressed in mesenchymal cells locatedclose to epithelial cells, during physiological and pathological tissue remodeling processes. In human carcinomas, high ST3levels are associated with a poor clinical outcome, suggestingthat ST3 plays a role during malignant processes. In this studywe report the ST3 gene inactivation by homologous recombination.Although ST3 null mice (ST3^–/–) were fertile anddid not exhibit obvious alterations in appearance and behavior,the lack of ST3 altered malignant processes. Thus, the suppression of ST3 results in a decreased 7,12-dimethylbenzanthracene-inducedtumorigenesis in ST3^–/– mice. Moreover, ST3^–/–fibroblasts have lost the capacity to promote implantation ofMCF7 human malignant epithelial cells in nude mice (P <0.008). Finally, we show that this ST3 paracrine function requiresextracellular matrix (ECM)-associated growth factors. Altogether,these findings give evidence that ST3 promotes, in a paracrinemanner, homing of malignant epithelial cells, a key processfor both primary tumors and metastases. Therefore, ST3 representsan appropriate target for specific MMP inhibitor(s) in futuretherapeutical approaches directed against the stromal compartmentof human carcinomas.

Abbreviations used in this paper: DMBA, 7,12-dimethylbenzanthracene; ECM, extracellular matrix; ES, embryonic stem; Gel A, gelatinase A; MMP, matrix metalloproteinase; ST3, stromelysin-3; TPA, 12-O-tetradecanoylphorbol 13-acetate.

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