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J. Biol. Chem., Vol. 281, Issue 22, 15073-15081, June 2, 2006

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Transcription Factors, cAMP-responsive Element Modulator (CREM) and Tisp40, Act in Concert in Postmeiotic Transcriptional Regulation^*

Ippei Nagamori, Kentaro Yomogida, Peter D. Adams^¶, Paolo Sassone-Corsi^||, and Hiroshi Nojima¹

From the Department of Molecular Genetics, Research Institute for Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita City, Osaka 565-0871, Japan the School of Human Environmental Sciences, Mukogawa Women's University, 6-46 Ikekaichou, Nishinomiya, Hyogo 663-8558, Japan, the ^¶Fox Chase Cancer Center, Philadelphia, Pennsylvania 19111, and the ^||Institut de Génétique et de Biologie Moléculaire et Cellulaire, 1 Rue Laurent Fries, 67404 Illkirch-Strasbourg, France

We previously isolated 80 TISP (transcript induced in spermiogenesis) genes whose transcription is dramatically induced during spermiogenesis. Our analysis here of the expression of these genes in the testis of the cAMP-responsive element modulator (CREM)-null mouse revealed that 54 TISP genes are under the transcriptional regulation of CREM. One CREM-regulated gene is TISP40, which encodes a basic leucine zipper (bZip)-type transcription factor bearing a transmembrane domain that generates the two proteins Tisp40 and Tisp40. Both of these proteins function by binding to UPRE (unfolded protein-response element) but do not recognize CRE motifs. We show here that Tisp40 mRNA is generated under the direct transcriptional regulation of CREM. CREM and Tisp40 form a heterodimer, which functions through CRE but not through UPRE. Furthermore, binding ability of CREM to CRE is dramatically up-regulated by forming a heterodimer with Tisp40TM, a truncated form of Tisp40 that lacks the transmembrane domain. We confirmed that Tisp40 and CREM actually bind to the Tisp40 promoter in vivo by chromatin immunoprecipitation assay. Finally, we demonstrate that the Tisp40TM-CREM heterodimer acts as a recruiter of HIRA, a histone chaperone, to CRE. Taken together, we propose that Tisp40 is an important transcriptional regulator during spermiogenesis.

Received for publication, March 3, 2006 , and in revised form, March 28, 2006.

^* This work was supported by grants-in-aid for Scientific Research on Priority Areas, Scientific Research (S), Exploratory Research and Science, and Technology Incubation Program in Advanced Regions, from the Ministry of Education, Science, Sports and Culture of Japan. 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 on-line version of this article (available at http://www.jbc.org) contains supplemental Tables.

¹ To whom correspondence should be addressed: Dept. of Molecular Genetics, Research Institute for Microbial Disease, Osaka University, Yamadaoka 3-1, Suita City, Osaka 565-0871, Japan. Tel.: 81-6-6875-3980; Fax: 81-6-6875-5192; E-mail: snj-0212{at}biken.osaka-u.ac.jp.

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