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J. Biol. Chem., Vol. 279, Issue 34, 35263-35272, August 20, 2004

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Positive Role of the Mammalian TBPIP/HOP2 Protein in DMC1-mediated Homologous Pairing^*

Rima Enomoto, Takashi Kinebuchi, Makoto Sato¶, Hideshi Yagi, Takehiko Shibata||, Hitoshi Kurumizaka**, and Shigeyuki Yokoyama¶¶||||

From the RIKEN Genomic Sciences Center, 1-7-22 Suehiro-cho, Tsurumi, Yokohama 230-0045, the Division of Cell Biology and Neuroscience, Department of Morphological and Physiological Sciences, Faculty of Medical Sciences, University of Fukui, 23 Shimoaizuki, Matsuoka, Fukui 910-1193, ^¶Solution Oriented Research for Science and Technology, Japan Science and Technology Agency (JST), Kawaguchi, Saitama 332-0012, the ^||Cellular and Molecular Biology Laboratory, RIKEN Discovery Research Institute, 2-1 Hirosawa, Wako, Saitama 351–0198, ^**Waseda University School of Science and Engineering, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, the Cellular Signaling Laboratory and Structurome Research Group, RIKEN Harima Institute at SPring-8, 1-1-1 Kohto, Mikazuki-cho, Sayo, Hyogo 679-5148, the ^¶¶Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyoku, Tokyo 113-0033, Japan

In meiosis, homologous recombination preferentially occurs between homologous chromosomes rather than between sister chromatids, which is opposite to the bias of mitotic recombinational repair. The TBPIP/HOP2 protein is a factor that ensures the proper pairing of homologous chromosomes during meiosis. In the present study, we found that the purified mouse TBPIP/HOP2 protein stimulated homologous pairing catalyzed by the meiotic DMC1 recombinase in vitro. In contrast, TBPIP/HOP2 did not stimulate homologous pairing by RAD51, which is another homologous pairing protein acting in both meiotic and mitotic recombination. The positive effect of TBPIP/HOP2 in the DMC1-mediated homologous pairing was only observed when TBPIP/HOP2 first binds to double-stranded DNA, not to single-stranded DNA, before the initiation of the homologous pairing reaction. Deletion analyses revealed that the C-terminal basic region of TBPIP/HOP2 is required for efficient DNA binding and is also essential for its homologous pairing stimulation activity. Therefore, these results suggest that TBPIP/HOP2 directly binds to DNA and functions as an activator for DMC1 during the homologous pairing step in meiosis.

Received for publication, March 4, 2004 , and in revised form, May 7, 2004.

^* This work was supported by the Bioarchitect Research Program (RIKEN), Core Research for Evolutional Science and Technology of JST, the RIKEN Structural Genomics/Proteomics Initiative, the National Project on Protein Structural and Functional Analyses, and grants-in-aid from the Japanese Society for the Promotion of Science and the Ministry of Education, Sports, Culture, Science, and Technology, 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.

To whom correspondence may be addressed. E-mail: kurumizaka{at}waseda.jp. |||| To whom correspondence may be addressed. E-mail: yokoyama{at}biochem.s.u-tokyo.ac.jp.

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