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Published online February 11, 2008
doi:10.1083/jcb.200708003
The Journal of Cell Biology, Vol. 180, No. 3, 493-506
The Rockefeller University Press, 0021-9525 $30.00
© 2008 Tahara et al.
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Article

Importin-β and the small guanosine triphosphatase Ran mediate chromosome loading of the human chromokinesin Kid



Kiyoshi Tahara1, Masatoshi Takagi1, Miho Ohsugi2, Takefumi Sone3, Fumiko Nishiumi3, Kazuhiro Maeshima1, Yasuomi Horiuchi2, Noriko Tokai-Nishizumi2, Fumio Imamoto3, Tadashi Yamamoto2, Shingo Kose1, and Naoko Imamoto1

1 Cellular Dynamics Laboratory, Discovery Research Institute, Institute of Physical and Chemical Research, Wako, Saitama, 351-0198, Japan
2 Division of Oncology, Department of Cancer Biology, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan
3 Laboratory of Molecular Biology, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan

Correspondence to Naoko Imamoto: nimamoto{at}riken.jp

Nucleocytoplasmic transport factors mediate various cellular processes, including nuclear transport, spindle assembly, and nuclear envelope/pore formation. In this paper, we identify the chromokinesin human kinesin-like DNA binding protein (hKid) as an import cargo of the importin-{alpha}/β transport pathway and determine its nuclear localization signals (NLSs). Upon the loss of its functional NLSs, hKid exhibited reduced interactions with the mitotic chromosomes of living cells. In digitonin-permeabilized mitotic cells, hKid was bound only to the spindle and not to the chromosomes themselves. Surprisingly, hKid bound to importin-{alpha}/β was efficiently targeted to mitotic chromosomes. The addition of Ran–guanosine diphosphate and an energy source, which generates Ran–guanosine triphosphate (GTP) locally at mitotic chromosomes, enhanced the importin-β–mediated chromosome loading of hKid. Our results indicate that the association of importin-β and -{alpha} with hKid triggers the initial targeting of hKid to mitotic chromosomes and that local Ran-GTP–mediated cargo release promotes the accumulation of hKid on chromosomes. Thus, this study demonstrates a novel nucleocytoplasmic transport factor–mediated mechanism for targeting proteins to mitotic chromosomes.

Abbreviations used in this paper: CAS, cellular apoptosis susceptibility; FLIP, fluorescence loss in photobleaching; GAP, GTPase-activating protein; hKid, human kinesin-like DNA binding protein; RCC1, regulator of chromosome condensation 1; SAF, spindle assembly factor; wt, wild type.


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