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J. Biol. Chem., Vol. 280, Issue 26, 24948-24956, July 1, 2005

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Identification of FEZ1 as a Protein That Interacts with JC Virus Agnoprotein and Microtubules

ROLE OF AGNOPROTEIN-INDUCED DISSOCIATION OF FEZ1 FROM MICROTUBULES IN VIRAL PROPAGATION^*

Tadaki Suzuki, Yuki Okada, Shingo Semba, Yasuko Orba, Satoko Yamanouchi, Shuichi Endo, Shinya Tanaka, Toshitsugu Fujita¶, Shun'ichi Kuroda¶, Kazuo Nagashima, and Hirofumi Sawa||**

From the Laboratory of Molecular and Cellular Pathology, School of Medicine, Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, the 21st Century Centers of Excellence Program for Zoonosis Control, and the ^||Department of Molecular Biology and Diagnosis, Research Center for Zoonosis Control, Hokkaido University, Sapporo 060-8638 and the ^¶Department of Structural Molecular Biology, Institute of Scientific and Industrial Research (Sanken), Osaka University, Osaka 567-0047, Japan

The human polyomavirus JC virus (JCV) is the causative agent of a fatal demyelinating disease, progressive multifocal leukoencephalopathy, and encodes six major proteins, including agnoprotein. Agnoprotein colocalizes with microtubules in JCV-infected cells, but its function is not fully understood. We have now identified fasciculation and elongation protein zeta 1 (FEZ1) as a protein that interacted with JCV agnoprotein in a yeast two-hybrid screen of a human brain cDNA library. An in vitro binding assay showed that agnoprotein interacted directly with FEZ1 and microtubules. A microtubule cosedimentation assay revealed that FEZ1 also associates with microtubules and that agnoprotein induces the dissociation of FEZ1 from microtubules. Agnoprotein inhibited the promotion by FEZ1 of neurite outgrowth in PC12 cells. Conversely, overexpression of FEZ1 suppressed JCV protein expression and intracellular trafficking in JCV-infected cells. These results suggest that FEZ1 promotes neurite extension through its interaction with microtubules, and that agnoprotein facilitates JCV propagation by inducing the dissociation of FEZ1 from microtubules.

Received for publication, October 8, 2004 , and in revised form, April 19, 2005.

^* This work was supported in part by grants from the Ministry of Education, Science, Technology, Sports, and Culture of Japan, the Ministry of Health, Labor, and Welfare of Japan, the Japan Human Science Foundation. 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.

Research fellows of the Japan Society for the Promotion of Science.

^** To whom correspondence should be addressed: Dept. of Molecular Biology and Diagnosis, Hokakido University Research Center for Zoonosis Control, N15, W7, Kita-ku, Sapporo 060-8638, Japan. Tel.: 81-11-706-5053; Fax: 81-11-706-7806; E-mail: h-sawa{at}patho2.med.hokudai.ac.jp.

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