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J. Biol. Chem., Vol. 280, Issue 14, 13272-13278, April 8, 2005

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Importin / Mediates Nuclear Transport of a Mammalian Circadian Clock Component, mCRY2, Together with mPER2, through a Bipartite Nuclear Localization Signal^*

Yoko Sakakida, Yoichi Miyamoto¶, Emi Nagoshi, Makoto Akashi||, Takahiro J. Nakamura, Takayoshi Mamine**, Megumi Kasahara, Yasuhiro Minami, Yoshihiro Yoneda¶, and Toru Takumi¶¶

From the Osaka Bioscience Institute, Suita, Osaka 565-0874, Japan, Department of Cell Biology and Neuroscience, Graduate School of Medicine, ^¶Department of Frontier Biosciences, Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan, ^**Life Science Laboratory, Materials Laboratories, Sony Corporation, Shinagawa, Tokyo 144-0001, Japan, Department of Natural Sciences, Hyogo University of Teacher Education, Yashiro, Hyogo 673-1494, Japan, and Department of Genome Science, Faculty of Medical Sciences, Graduate School of Medicine, Kobe University, Kobe, Hyogo 650-0017, Japan

Circadian rhythms, which period is approximately one day, are generated by endogenous biological clocks. These clocks are found throughout the animal kingdom, as well as in plants and even in prokaryotes. Molecular mechanisms for circadian rhythms are based on transcriptional oscillation of clock component genes, consisting of interwoven autoregulatory feedback loops. Among the loops, the nuclear transport of clock proteins is a crucial step for transcriptional regulation. In the present study, we showed that the nuclear entry of mCRY2, a mammalian clock component, is mediated by the importin / system through a bipartite nuclear localization signal in its carboxyl end. In vitro transport assay using digitonin-permeabilized cells demonstrated that all three importin s, 1 (Rch1), 3 (Qip-1), and 7 (NPI-2), can mediate mCRY2 import. mCRY2 with the mutant nuclear localization signal failed to transport mPER2 into the nucleus of mammalian cultured cells, indicating that the nuclear localization signal identified in mCRY2 is physiologically significant. These results suggest that the importin / system is involved in nuclear entry of mammalian clock components, which is indispensable to transcriptional oscillation of clock genes.

Received for publication, November 23, 2004 , and in revised form, January 31, 2005.

^* This work was supported in part by research grants from Ministry of Education, Culture, Sports, Science, and Technology (to Y. Y. and T. T.). 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.

^|| Supported by fellowships from the Japan Society for the Promotion of Science.

^¶¶ To whom correspondence should be addressed: Osaka Bioscience Institute, 6-2-4 Furuedai, Suita, Osaka 565-0874, Japan. Tel.: 81-6-6872-4816; Fax: 81-6-6872-0240; E-mail: takumi{at}obi.or.jp.

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