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Originally published In Press as doi:10.1074/jbc.M206235200 on August 27, 2002

J. Biol. Chem., Vol. 277, Issue 46, 44485-44496, November 15, 2002
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Osteopontin Transcription in Aortic Vascular Smooth Muscle Cells Is Controlled by Glucose-regulated Upstream Stimulatory Factor and Activator Protein-1 Activities*

Miri BidderDagger §, Jian-Su ShaoDagger , Nichole Charlton-KachigianDagger , Arleen P. LoewyDagger , Clay F. Semenkovich§, and Dwight A. TowlerDagger §

From the Divisions of Dagger  Bone and Mineral Diseases and § Endocrinology, Diabetes, and Metabolism, Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri 63110

The expression of the matrix cytokine osteopontin (OPN) is up-regulated in aortic vascular smooth muscle cells (VSMCs) by diabetes. OPN expression in cultured VSMCs is reciprocally regulated by glucose and 2-deoxyglucose (2-DG; inhibitor of cellular glucose metabolism). Systematic analyses of OPN promoter-luciferase reporter constructs identify a CCTCATGAC motif at nucleotides -80 to -72 relative to the initiation site that supports OPN transcription in VSMCs. The region -83 to -45 encompassing this motif confers basal and glucose- and 2-DG-dependent transcription on an unresponsive promoter. Competition and gel mobility supershift assays identify upstream stimulatory factor (USF; USF1:USF2) and activator protein-1 (AP1; c-Fos:c-Jun) in complexes binding the composite CCTCATGAC element. Glucose up-regulates both AP1 and USF binding activities 2-fold in A7r5 cells and selectively up-regulates USF1 protein levels. By contrast, USF (but not AP1) binding activity is suppressed by 2-DG and restored by glucose treatment. Expression of either USF or AP1 activates the proximal OPN promoter in A7r5 VSMCs in part via the CCTCATGAC element. Moreover, glucose stimulates the transactivation functions of c-Fos and USF1, but not c-Jun, in one-hybrid assays. Mannitol does not regulate binding, transactivation functions, USF1 protein accumulation, or OPN transcription. Thus, OPN gene transcription is regulated by USF and AP1 in aortic VSMCs, entrained to changes in cellular glucose metabolism.

* This work was supported by Grants HL69229 and DK52446 (to D. A. T.) from the National Institutes of Health and by the Barnes-Jewish Hospital Research 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.

To whom correspondence should be addressed: Washington University Medical Center, Division of Bone and Mineral Diseases, Barnes-Jewish Hospital, North Campus, 216 South Kingshighway Blvd., St. Louis, MO 63110. Tel.: 314-454-7434; Fax: 314-454-5047; E-mail: dtowler@im.wustl.edu.

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