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Originally published In Press as doi:10.1074/jbc.M010133200 on March 16, 2001

J. Biol. Chem., Vol. 276, Issue 24, 20839-20848, June 15, 2001
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Fli-1 Inhibits Collagen Type I Production in Dermal Fibroblasts via an Sp1-dependent Pathway*

Joanna Czuwara-LadykowskaDagger §, Fumiaki ShirasakiDagger §||, Pascale Jackers**, Dennis K. Watson**, and Maria TrojanowskaDagger Dagger Dagger

From the Dagger  Department of Medicine, Division of Rheumatology and Immunology, and the ** Laboratory of Cancer Genomics, Hollings Cancer Center, Medical University of South Carolina, Charleston, South Carolina 29401 and the || Department of Dermatology, Kanazawa University, Kanazawa, 920-0947 Japan

Fibrosis is characterized by the excessive deposition of extracellular matrix (ECM), especially collagen. Because Ets factors are implicated in physiological and pathological ECM remodeling, the aim of this study was to investigate the role of Ets factors in collagen production. We demonstrate that the expression of collagenous proteins and collagen alpha 2(I) (COL1A2) mRNA was inhibited following stable transfection of Fli-1 in dermal fibroblasts. Subsequent analysis of the COL1A2 promoter identified a critical Ets binding site that mediates Fli-1 inhibition. In contrast, Ets-1 stimulates COL1A2 promoter activity. In vitro binding assays demonstrate that both Fli-1 and Ets-1 form DNA-protein complexes with sequences present in COL1A2 promoter. Furthermore, Fli-1 binding to the COL1A2 is enhanced via Sp1-dependent interaction. Studies using Fli-1 dominant interference and DNA binding mutants indicate that Fli-1 inhibition is mediated by both direct (DNA binding) and indirect (via protein-protein interaction) mechanisms and that Sp1 is an important mediator of the Fli-1 function. Furthermore, experiments using the Gal4 system in the context of different cell types as well as experiments with the COL1A2 promoter in different cell lines demonstrate that the direction and magnitude of the effect of Fli-1 is promoter- and cell context-specific. We propose that Fli-1 inhibits COL1A2 promoter activity by competition with Ets-1. In addition, we postulate that another factor (co-repressor) may be required for maximal inhibition after recruitment to the Fli-1-Sp1 complex. We conclude that the ratio of Fli-1 to Ets-1 and the presence of co-regulatory proteins ultimately control ECM production in fibroblasts.

* This work was supported by National Institutes of Health Grant AR 42334, NCI National Institutes of Health Grant PO1 CA78582, and the R. G. Kozmetsky Foundation.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.

Recipient of a grant from the Zarkin Fund of Boston.

Dagger Dagger Division of Rheumatology and Immunology, Medical University of South Carolina, 96 Jonathan Lucas St., Ste. 912, Charleston, SC 29401. Tel.: 843-792-7921; Fax: 843-792-7121; E-mail: trojanme@musc.edu.

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