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Journal of Virology, October 2009, p. 10582-10595, Vol. 83, No. 20
0022-538X/09/$08.00+0     doi:10.1128/JVI.00497-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Open Reading Frame 33 of a Gammaherpesvirus Encodes a Tegument Protein Essential for Virion Morphogenesis and Egress {triangledown}

Haitao Guo,1,2 Lili Wang,1,2,{dagger} Li Peng,3,{dagger} Z. Hong Zhou,3,4 and Hongyu Deng1,5*

Center for Infection and Immunity, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, People's Republic of China,1 Graduate School of the Chinese Academy of Sciences, Beijing 100080, People's Republic of China,2 Department of Microbiology, Immunology, and Molecular Genetics,3 California NanoSystems Institute,4 School of Dentistry, University of California Los Angeles, California, California 900955

Received 10 March 2009/ Accepted 26 July 2009

Tegument is a unique structure of herpesvirus, which surrounds the capsid and interacts with the envelope. Morphogenesis of gammaherpesvirus is poorly understood due to lack of efficient lytic replication for Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8, which are etiologically associated with several types of human malignancies. Murine gammaherpesvirus 68 (MHV-68) is genetically related to the human gammaherpesviruses and presents an excellent model for studying de novo lytic replication of gammaherpesviruses. MHV-68 open reading frame 33 (ORF33) is conserved among Alpha-, Beta-, and Gammaherpesvirinae subfamilies. However, the specific role of ORF33 in gammaherpesvirus replication has not yet been characterized. We describe here that ORF33 is a true late gene and encodes a tegument protein. By constructing an ORF33-null MHV-68 mutant, we demonstrated that ORF33 is not required for viral DNA replication, early and late gene expression, viral DNA packaging or capsid assembly but is required for virion morphogenesis and egress. Although the ORF33-null virus was deficient in release of infectious virions, partially tegumented capsids produced by the ORF33-null mutant accumulated in the cytoplasm, containing conserved capsid proteins, ORF52 tegument protein, but virtually no ORF45 tegument protein and the 65-kDa glycoprotein B. Finally, we found that the defect of ORF33-null MHV-68 could be rescued by providing ORF33 in trans or in an ORF33-null revertant virus. Taken together, our results indicate that ORF33 is a tegument protein required for viral lytic replication and functions in virion morphogenesis and egress.

* Corresponding author. Mailing address: Center for Infection and Immunity and National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, People's Republic of China. Phone and fax: 86-10-64888407. E-mail: rrain6{at}yahoo.com

{triangledown} Published ahead of print on 5 August 2009.

{dagger} L.W. and L.P. contributed equally to this study.

Journal of Virology, October 2009, p. 10582-10595, Vol. 83, No. 20
0022-538X/09/$08.00+0     doi:10.1128/JVI.00497-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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