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J. Biol. Chem., Vol. 281, Issue 19, 13374-13381, May 12, 2006

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The Sox2 Regulatory Region 2 Functions as a Neural Stem Cell-specific Enhancer in the Telencephalon^*

Satoru Miyagi, Masazumi Nishimoto¹, Tetsuichiro Saito^¶, Mikiko Ninomiya^||**, Kazunobu Sawamoto^||**, Hideyuki Okano^||, Masami Muramatsu, Hideyuki Oguro, Atsushi Iwama, and Akihiko Okuda²

From the Division of Developmental Biology, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, Hidaka, Saitama 350-1241, the Department of Cellular and Molecular Medicine and the ^¶Department of Developmental Biology, Graduate School of Medicine, Chiba University, Chiba 260-8670, the ^||Department of Physiology and ^**Bridgestone Laboratory of Developmental and Regenerative Neurobiology, Keio University School of Medicine, Shinjyuku-ku, Tokyo 160-8582, and REDS Group, Saitama Small Enterprise Promotion Corp., Skip City, Kawaguchi, Saitama 333-0844, Japan

Sox2 is expressed at high levels in neuroepithelial stem cells and persists in neural stem/progenitor cells throughout adulthood. We showed previously that the Sox2 regulatory region 2 (SRR2) drives strong expression in these cells. Here we generated transgenic mouse strains with the -geo reporter gene under the control of the SRR2 in order to examine the spatiotemporal function of this regulatory region. We show that the SRR2 functions specifically in neural stem/progenitor cells. However, unlike Nestin 2nd intronic enhancer, the SRR2 shows strong regional specificity functioning only in restricted areas of the telencephalon but not in any other portions of the central nervous system such as the spinal cord. We also show by in vitro clonogenic assay that at least some of these SRR2-functioning cells possess the hallmark properties of neural stem cells. In adult brains, we could detect strong -geo expression in the subventricular zone of the lateral ventricle and along the rostral migrating stream where actively dividing cells reside. Chromatin immunoprecipitation assays reveal interactions of POU and Sox factors with SRR2 in neural stem/progenitor cells. Our data also suggest that the specific recruitment of these proteins to the SRR2 in the telencephalon defines the spatiotemporal activity of the enhancer in the developing nervous system.

Received for publication, November 28, 2005 , and in revised form, March 16, 2006.

^* This work was supported in part by the Ministry of Education, Science, Sports, and Culture. This work was performed as part of the Rational Evolutionary Design of Advanced Biomolecules Project, the Saitama Prefecture Collaboration of Regional Entities for the Advancement of Technological Excellence, supported by the Japan Science and Technology Agency. 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.

¹ Present address: Radioisotope Experimental Laboratory, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, Hidaka, Saitama 350-1241, Japan.

² To whom correspondence should be addressed: Division of Developmental Biology, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, Hidaka, Saitama 350-1241, Japan. Tel.: 81-42-985-7268; Fax: 81-42-985-7264; E-mail: akiokuda{at}saitama-med.ac.jp.

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