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J. Biol. Chem., Vol. 281, Issue 9, 5445-5452, March 3, 2006

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CREB-AP1 Protein Complexes Regulate Transcription of the Collagen XXIV Gene (Col24a1) in Osteoblasts^*

Noritaka Matsuo, Shizuko Tanaka, Marion K. Gordon^¶, Manuel Koch^||, Hidekatsu Yoshioka, and Francesco Ramirez^**1

From the Laboratory of Genetics and Organogenesis, Research Division of the Hospital for Special Surgery, and Department of Physiology and Biophysics, Weill Medical College, Cornell University, New York, New York 10021, the Department of Anatomy, Biology, and Medicine, Oita University, 1-1 Hasama-machi, Oita 879-5593, Japan, the ^¶Enviromental and Occupational Health Sciences Institute and the Department of Pharmacology and Toxicology, Ernest Mario School of Pharmacy, Rutgers University, Piscataway, New Jersey 00854, the ^||Institute for Biochemistry II, University of Cologne, 50931 Cologne, Germany, and ^**CEINGE-Biotecnologie Avanzate, 80131 Naples, Italy

Collagen XXIV is a newly discovered and poorly characterized member of the fibril-forming family of collagen molecules, which displays unique structural features of invertebrate fibrillar collagens and is expressed predominantly in bone tissue. Here we report the characterization of the proximal promoter of the mouse gene (Col24a1) and its regulation in osteoblastic cells. Using well characterized murine models of osteoblast differentiation, we found that the Col24a1 gene is activated sometime before onset of the late differentiation marker osteocalcin. Additional analyses revealed that Col24a1 produces equal amounts of two alternatively spliced products with different 5'-untranslated sequences that originate from distinct transcriptional start sites. Cell transfection experiments in combination with DNA binding assays demonstrated that Col24a1 promoter activity in ROS17/2.8 osteosarcoma cells is under the control of an upstream cis-acting element, which is shared by both transcripts and is recognized by specific combinations of c-Jun, CREB1, ATF1, and ATF2 dimers. Consistent with these results, overexpression of c-Jun, ATF1, ATF2, or CREB1 in transiently transfected osteoblastic cells stimulated transcription from reporter gene constructs driven by the Col24a1 promoter to different degrees. Moreover, chromatin immunoprecipitation experiments showed that these nuclear factors bind the same upstream sequence of the endogenous Col24a1 gene. Collectively these data provide new information about transcriptional control of collagen fibrillogenesis, in addition to implicating for the first time CREB-AP1 protein complexes in the regulation of collagen gene expression in osteoblasts.

Received for publication, September 8, 2005 , and in revised form, December 13, 2005.

^* This work was supported by National Institutes of Health Grants AR-38648 and EY-09056, the St. Giles Foundation, and Deutsche Forschungsgemeinschaft Grant SFB 589. 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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) DQ157748 [GenBank] .

¹ To whom correspondence should be addressed: Child Health Institute of New Jersey, UMDNJ-Robert Wood Johnson Medical School, 89 French St., New Brunswick, NJ 08901. Tel.: 732-235-9534; Fax: 732-235-9333; E-mail: ramirefr{at}umdnj.edu.

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