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Journal of Virology, September 2004, p. 9890-9903, Vol. 78, No. 18
0022-538X/04/$08.00+0     DOI: 10.1128/JVI.78.18.9890-9903.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Major and Minor Capsid Proteins of Human Polyomavirus JC Cooperatively Accumulate to Nuclear Domain 10 for Assembly into Virions{dagger}

Yukiko Shishido-Hara,1,2,3,4* Shizuko Ichinose,5 Kayoko Higuchi,6 Yoshinobu Hara,4 and Kotaro Yasui1

Department of Microbiology, Tokyo Metropolitan Institute for Neuroscience,1 Japan Society for the Promotion of Science,2 Japan Science and Technology Corporation,3 Laboratory of Molecular Neurobiology, Human Gene Sciences Center,4 Instrument Analysis Center, Tokyo Medical and Dental University Tokyo,5 Section of Surgical Pathology, Aizawa Hospital, Matsumoto Tokyo, Japan6

Received 21 February 2004/ Accepted 12 May 2004

The human polyomavirus JC (JCV) replicates in the nuclei of infected cells. Here we report that JCV virions are efficiently assembled at nuclear domain 10 (ND10), which is also known as promyelocytic leukemia (PML) nuclear bodies. The major capsid protein VP1, the minor capsid proteins VP2 and VP3, and a regulatory protein called agnoprotein were coexpressed from a polycistronic expression vector in COS-7 cells. We found that VP1 accumulated to distinct subnuclear domains in the presence of VP2/VP3 and agnoprotein, while VP1 expressed alone was distributed both in the cytoplasm and in the nucleus. Mutation analysis revealed that discrete intranuclear accumulation of VP1 requires the presence of either VP2 or VP3. However, VP2 or VP3 expressed in the absence of VP1 showed diffuse, not discrete, nuclear localization. The C-terminal sequence of VP2/VP3 contains two basic regions, GPNKKKRRK (cluster 1) and KRRSRSSRS (cluster 2). The deletion of cluster 2 abolished the accumulation of VP1 to distinct subnuclear domains. Deletion of the C-terminal 34 residues of VP2/VP3, including both cluster 1 and cluster 2, caused VP1 to localize both in the cytoplasm and in the nucleus. Using immunoelectron microscopy of cells that coexpressed VP1, VP2/VP3, and agnoprotein, we detected the assembly of virus-like particles in discrete locations along the inner nuclear periphery. Both in oligodendrocytes of the human brain and in transfected cells, discrete nuclear domains for VP1 accumulation were identified as ND10, which contains the PML protein. These results indicate that major and minor capsid proteins cooperatively accumulate in ND10, where they are efficiently assembled into virions.

* Corresponding author. Present address: Department of Pathology, Kyorin University School of Medicine, 6-20-2, Shinkawa, Mitaka, Tokyo 181-8611, Japan. Phone: 81-422-47-5511, ext. 3420. Fax: 81-422-40-7093. E-mail: shishido-hara{at}par.odn.ne.jp.

{dagger} This paper is in memory of Gerald L. Stoner for his great support and encouragement of this project.

Journal of Virology, September 2004, p. 9890-9903, Vol. 78, No. 18
0022-538X/04/$08.00+0     DOI: 10.1128/JVI.78.18.9890-9903.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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