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Originally published In Press as doi:10.1074/jbc.M311131200 on March 5, 2004 Originally published In Press as doi:10.1074/jbc.M311131200 on March 1, 2004 Originally published In Press as doi:10.1074/jbc.M311131200 on February 27, 2004

J. Biol. Chem., Vol. 279, Issue 20, 20794-20806, May 14, 2004
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Ets Gene PEA3 Cooperates with {beta}-Catenin-Lef-1 and c-Jun in Regulation of Osteopontin Transcription*

Mohamed El-Tanani{ddagger}§, Angela Platt-Higgins¶, Philip S. Rudland¶, and Frederick Charles Campbell{ddagger}

From the {ddagger}Department of Surgery, Cancer Research Centre, Queen's University of Belfast, Grosvenor Road, Belfast BT12 6BJ and the Cancer and Polio Research Laboratories, School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, United Kingdom

Osteopontin (OPN) is a multifunctional protein implicated in mammary development, neoplastic change, and metastasis. OPN is a target gene for {beta}-catenin-T cell factor signaling, which is commonly disturbed during mammary oncogenesis, but the understanding of OPN regulation is incomplete. Data base-assisted bioinformatic analysis of the OPN promoter region has revealed the presence of T cell factor-, Ets-, and AP-1-binding motifs. Here we report that {beta}-catenin, Lef-1, Ets transcription factors, and the AP-1 protein c-Jun each weakly enhanced luciferase expression from a OPN promoter-luciferase reporter construct, transiently transfected into a rat mammary cell line. OPN promoter responsiveness to {beta}-catenin and Lef-1, however, was considerably enhanced by Ets transcription factors including Ets-1, Ets-2, ERM, and particularly PEA3. PEA3 also enhanced promoter responsiveness to the AP-1 protein c-Jun. Co-transfection of cells with {beta}-catenin, Lef-1, PEA3, and c-Jun in combination increased luciferase expression by up to 280-fold and induced expression of endogenous rat OPN. In six human breast cell lines, those that highly expressed OPN also expressed PEA3 and Ets-1. Moreover, there was a significant association of immunocytochemical staining for OPN and one of {beta}-catenin, Ets-1, Ets-2, PEA3, or c-Jun, in the 29 human breast carcinomas tested. This study shows that {beta}-catenin/Lef-1, Ets, and AP-1 transcription factors can cooperate in a rat mammary cell line in stimulating transcription of OPN and that their independent presence is associated with that of OPN in a group of human breast cancers. These results suggest that the presence of these transcription factors in human breast cancer is responsible in part for the overexpression of OPN that, in turn, is implicated in mammary neoplastic progression and metastasis.

Received for publication, October 9, 2003 , and in revised form, February 15, 2004.

* This work was supported by grants from Action Cancer (Northern Ireland), the Royal Victoria Hospital Research Fund (Belfast), the North West Research Fund, and the Cancer and Polio Research Fund Ltd. The costs of publication of this article were defrayed in part by the payment of page charges. This 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. Tel.: 44-28-90-632528; Fax: 44-28-321811; E-mail: m.el-tanani{at}qub.ac.uk.


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