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Vol. 20, Issue 5, 1289-1301, March 1, 2009

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Cohesin Associates with Spindle Poles in a Mitosis-specific Manner and Functions in Spindle Assembly in Vertebrate Cells

Xiangduo Kong^*, Alexander R. Ball, Jr.^*, Eiichiro Sonoda, Jie Feng, Shunichi Takeda, Tatsuo Fukagawa, Tim J. Yen, and Kyoko Yokomori^*

*Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697-1700; CREST Research Project, Japan Science and Technology, Radiation Genetics, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan; Fox Chase Cancer Center, Philadelphia, PA 19111; and Department of Molecular Genetics, National Institute of Genetics and SOKENDAI, Mishima, Shizuoka 411-8540, Japan

Submitted April 24, 2008; Revised December 11, 2008; Accepted December 19, 2008
Monitoring Editor: Stephen Doxsey

Cohesin is an essential protein complex required for sister chromatid cohesion. Cohesin associates with chromosomes and establishes sister chromatid cohesion during interphase. During metaphase, a small amount of cohesin remains at the chromosome-pairing domain, mainly at the centromeres, whereas the majority of cohesin resides in the cytoplasm, where its functions remain unclear. We describe the mitosis-specific recruitment of cohesin to the spindle poles through its association with centrosomes and interaction with nuclear mitotic apparatus protein (NuMA). Overexpression of NuMA enhances cohesin accumulation at spindle poles. Although transient cohesin depletion does not lead to visible impairment of normal spindle formation, recovery from nocodazole-induced spindle disruption was significantly impaired. Importantly, selective blocking of cohesin localization to centromeres, which disrupts centromeric sister chromatid cohesion, had no effect on this spindle reassembly process, clearly separating the roles of cohesin at kinetochores and spindle poles. In vitro, chromosome-independent spindle assembly using mitotic extracts was compromised by cohesin depletion, and it was rescued by addition of cohesin that was isolated from mitotic, but not S phase, cells. The combined results identify a novel spindle-associated role for human cohesin during mitosis, in addition to its function at the centromere/kinetochore regions.

Address correspondence to: Kyoko Yokomori (kyokomor{at}uci.edu)

Abbreviations used: H3K9me, histone H3 lysine 9 methylation; HMTase, histone methyltransferase; MTs, microtubules; NuMA, nuclear mitotic apparatus protein; plk1, polo-like kinase 1; SMC, structural maintenance of chromosomes.

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