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J. Biol. Chem., Vol. 281, Issue 19, 13817-13827, May 12, 2006

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Asf1 Is Required for Viability and Chromatin Assembly during DNA Replication in Vertebrate Cells^*

Fumiyuki Sanematsu, Yasunari Takami, Hirak Kumar Barman, Tatsuo Fukagawa, Tatsuya Ono^¶, Kei-ichi Shibahara^¶, and Tatsuo Nakayama^||1

From the Section of Biochemistry and Molecular Biology, Department of Medical Sciences, Miyazaki Medical College, University of Miyazaki, 5200 Kihara, Kiyotake, Miyazaki 889-1692, Japan, the ^¶Department of Integrated Genetics, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan, the Department of Molecular Genetics, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan, and the ^||Department of Life Science, Frontier Science Research Center, University of Miyazaki, 5200, Kihara, Kiyotake, Miyazaki 889-1692, Japan

Asf1 (anti-silencing function 1), a well conserved protein from yeast to humans, acts as a histone chaperone and is predicted to participate in a variety of chromatin-mediated cellular processes. To investigate the physiological role of vertebrate Asf1 in vivo, we generated a conditional Asf1-deficient mutant from chicken DT40 cells. Induction of Asf1 depletion resulted in the accumulation of cells in S phase with decreased DNA replication and increased mitotic aberrancy forming multipolar spindles, leading to cell death. In addition, nascent chromatin in Asf1-depleted cells showed increased nuclease sensitivity, indicating impaired nucleosome assembly during DNA replication. Complementation analyses revealed that the functional domain of Asf1 for cell viability was confined to the N-terminal core domain (amino acids 1-155) that is a binding platform for histones H3/H4, CAF-1p60, and HIRA, whereas Asf1 mutant proteins, abolishing binding abilities with both p60 and HIRA, exhibit no effect on viability. These results together indicate that the vertebrate Asf1 plays a crucial role in replication-coupled chromatin assembly, cell cycle progression, and cellular viability and provide a clue of a possible role in a CAF-1- and HIRA-independent chromatin-modulating process for cell proliferation.

Received for publication, October 26, 2005 , and in revised form, March 14, 2006.

^* This work was supported in part by the 21st Century Center of Excellence Program (Life Science); a grant-in-aid for scientific research from the Ministry of Education, Culture, Sports, Science, and Technology; and grants from the Japan Society for the Promotion of Science and CREST from Japan Science and Technology 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.

¹ To whom correspondence should be addressed: Section of Biochemistry and Molecular Biology, Dept. of Medical Sciences, Miyazaki Medical College, University of Miyazaki, 5200, Kihara, Kiyotake, Miyazaki 889-1692, Japan. Tel.: 81-985-85-3127; Fax: 81-985-85-6503; E-mail: tnakayam{at}med.miyazaki-u.ac.jp.

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