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J. Biol. Chem., Vol. 280, Issue 50, 41609-41618, December 16, 2005

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Human Centromere Protein B Induces Translational Positioning of Nucleosomes on -Satellite Sequences^*

Yoshinori Tanaka1, Hiroaki Tachiwana¶, Kinya Yoda||, Hiroshi Masumoto**, Tsuneko Okazaki, Hitoshi Kurumizaka¶2, and Shigeyuki Yokoyama3

From the Protein Research Group, RIKEN Genomic Sciences Center, 1-7-22 Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan, the Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan, ^¶Graduate School of Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan, ^||Bioscience Center, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan, ^**Laboratory of Biosystems and Cancer, NCI, National Institutes of Health, Bethesda, Maryland 20892, Fujita Health University Institute for Comprehensive Medical Science, Kutsukake-cho, Toyoake, Aichi 470-1192, Japan, and RIKEN Harima Institute at SPring-8, 1-1-1 Kohto, Mikazuki-cho, Sayo, Hyogo 679-5148, Japan

The human centromere proteins A (CENP-A) and B (CENP-B) are the fundamental centromere components of chromosomes. CENP-A is the centromere-specific histone H3 variant, and CENP-B specifically binds a 17-base pair sequence (the CENP-B box), which appears within every other -satellite DNA repeat. In the present study, we demonstrated centromere-specific nucleosome formation in vitro with recombinant proteins, including histones H2A, H2B, H4, CENP-A, and the DNA-binding domain of CENP-B. The CENP-A nucleosome wraps 147 base pairs of the -satellite sequence within its nucleosome core particle, like the canonical H3 nucleosome. Surprisingly, CENP-B binds to nucleosomal DNA when the CENP-B box is wrapped within the nucleosome core particle and induces translational positioning of the nucleosome without affecting its rotational setting. This CENP-B-induced translational positioning only occurs when the CENP-B box sequence is settled in the proper rotational setting with respect to the histone octamer surface. Therefore, CENP-B may be a determinant for translational positioning of the centromere-specific nucleosomes through its binding to the nucleosomal CENP-B box.

Received for publication, September 1, 2005 , and in revised form, September 23, 2005.

^* This work was supported by 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.

¹ Present address: Toray Industries, Inc. New Frontiers Research Laboratories, 1111 Tebiro, Kamakura, Kanagawa 248-8555, Japan.

² To whom correspondence may be addressed: Dept. of Electrical Engineering and Bioscience, Graduate School of Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan. Tel.: 81-3-5286-8189; Fax: 81-3-5292-9211; E-mail: kurumizaka{at}waseda.jp.

³ To whom correspondence may be addressed. Tel.: 81-45-503-9196; Fax: 81-45-503-9201; E-mail: yokoyama{at}biochem.s.u-tokyo.ac.jp.

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