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J. Biol. Chem., Vol. 282, Issue 46, 33459-33465, November 16, 2007

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Wobble Inosine tRNA Modification Is Essential to Cell Cycle Progression in G₁/S and G₂/M Transitions in Fission Yeast^*

Satoshi Tsutsumi, Reiko Sugiura, Yan Ma, Hideki Tokuoka, Kazuki Ohta, Rieko Ohte, Akiko Noma^¶, Tsutomu Suzuki^¶, and Takayoshi Kuno¹

From the Division of Molecular Pharmacology and Pharmacogenomics, Department of Biochemistry and Molecular Biology, Graduate School of Medicine, Kobe University, 7-5-1 Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan, Laboratory of Molecular Pharmacogenomics, School of Pharmaceutical Sciences, Kinki University, Kowakae 3-4-1, Higashi-Osaka, 577-8502, Japan, and the ^¶Department of Chemistry and Biotechnology, Graduate School of Engineering, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8656, Japan

Inosine (I) at position 34 (wobble position) of tRNA is formed by the hydrolytic deamination of a genomically encoded adenosine (A). The enzyme catalyzing this reaction, termed tRNA A:34 deaminase, is the heterodimeric Tad2p/ADAT2·Tad3p/ADAT3 complex in eukaryotes. In budding yeast, deletion of each subunit is lethal, indicating that the wobble inosine tRNA modification is essential for viability; however, most of its physiological roles remain unknown. To identify novel cell cycle mutants in fission yeast, we isolated the tad3-1 mutant that is allelic to the tad3⁺ gene encoding a homolog of budding yeast Tad3p. Interestingly, the tad3-1 mutant cells principally exhibited cell cycle-specific phenotype, namely temperature-sensitive and irreversible cell cycle arrest both in G₁ and G₂. Further analyses revealed that in the tad3-1 mutant cells, the S257N mutation that occurred in the catalytically inactive Tad3 subunit affected its association with catalytically active Tad2 subunit, leading to an impairment in the A to I conversion at position 34 of tRNA. In tad3-1 mutant cells, the overexpression of the tad3⁺ gene completely suppressed the decreased tRNA inosine content. Notably, the overexpression of the tad2⁺ gene partially suppressed the temperature-sensitive phenotype and the decreased tRNA inosine content, indicating that the tad3-1 mutant phenotype is because of the insufficient I₃₄ formation of tRNA. These results suggest that the wobble inosine tRNA modification is essential for cell cycle progression in the G₁/S and G₂/M transitions in fission yeast.

Received for publication, August 17, 2007 , and in revised form, September 17, 2007.

^* This work was supported by the 21st Century Center of Excellence Program and research grants from the Ministry of Education, Culture, Sports, 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. Tel.: 81-78-382-5440; Fax: 81-78-382-5459; E-mail: tkuno{at}med.kobe-u.ac.jp.

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