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J. Biol. Chem., Vol. 282, Issue 29, 21415-21424, July 20, 2007

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Human NUF2 Interacts with Centromere-associated Protein E and Is Essential for a Stable Spindle Microtubule-Kinetochore Attachment^*

Dan Liu, Xia Ding^¶, Jian Du, Xin Cai, Yuejia Huang, Tarsha Ward, Andrew Shaw, Yong Yang, Renming Hu^||, Changjiang Jin¹, and Xuebiao Yao, Georgia Cancer Coalition Eminent Cancer Research Scholar²

From the Laboratory of Cellular Dynamics, University of Science and Technology of China and the National Laboratory for Physical Sciences, Hefei 230027, China, Department of Physiology and the Cancer Biology Program, Morehouse School of Medicine, Atlanta, Georgia 30310, ^¶Department of Medicine, Beijing University of Chinese Medicine, Beijing 100029, China, and ^||Department of Endocrinology and Metabolism, Fudan University, Shanghai 200040, China

Chromosome segregation in mitosis is orchestrated by dynamic interaction between spindle microtubules and the kinetochore, a multiprotein complex assembled onto centromeric DNA of the chromosome. Here, we show that Homo sapiens (Hs) NUF2 is required for stable kinetochore localization of centromere-associated protein E (CENP-E) in HeLa cells. HsNUF2 specifies the kinetochore association of CENP-E by interacting with its C-terminal domain. The region of HsNUF2 binding to CENP-E was mapped to its C-terminal domain by glutathione S-transferase pulldown and yeast two-hybrid assays. Suppression of synthesis of HsNUF2 by small interfering RNA abrogated the localization of CENP-E to the kinetochore, demonstrating the requirement of HsNUF2 for CENP-E kinetochore localization. In addition, depletion of HsNUF2 caused aberrant chromosome segregation. These HsNUF2-suppressed cells displayed reduced tension at kinetochores of bi-orientated chromosomes. Double knockdown of CENP-E and HsNUF2 further abolished the tension at the kinetochores. Our results indicate that HsNUF2 and CENP-E are required for organization of stable microtubule-kinetochore attachment that is essential for faithful chromosome segregation in mitosis.

Received for publication, September 22, 2006 , and in revised form, May 21, 2007.

^* This work was supported by Chinese 973 Project Grant 2002CB713700; Chinese Academy of Science Grants KSCX1-YW-R65 and KSCX2-YW-H-10; Chinese Natural Science Foundation Grants 39925018, 30270293, 30500183 (to X. D.), and 90508002; Chinese 863 Project Grant 2001AA215331; Chinese Ministry of Education Grant 20020358051; and a Georgia Cancer Coalition grant and National Institutes of Health Grants DK56292, CA89019, and CA92080 (to X. Y.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1-3.

¹ To whom correspondence may be addressed: Laboratory of Cellular Dynamics, University of Science and Technology of China, Hefei 230027, China. Tel.: 86-551-3607141; Fax: 86-551-3606304; E-mail: jincj{at}ustc.edu.cn. ² To whom correspondence may be addressed: Lab. of Cellular Dynamics, University of Science and Technology of China, Hefei 230027, China. E-mail: yaoxb{at}ustc.edu.cn.

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