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J. Biol. Chem., Vol. 279, Issue 37, 38803-38812, September 10, 2004

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Post-translational Modification of Rta of Epstein-Barr Virus by SUMO-1^*

Li-Kwan Chang, Yu-Hsiu Lee, Tai-Shan Cheng, Yi-Ren Hong, Pei-Jung Lu¶, Janng J. Wang||, Wen-Hung Wang, Chung-Wen Kuo, Steven S.-L. Li**, and Shih-Tung Liu

From the Faculty of Biological Medicine and Environmental Biology and Graduate Institute of Biochemistry, Kaohsiung Medical University, 100, Shih-Chuan 1st Road, Kaohsiung 807, the Molecular Genetics Laboratory, Department of Microbiology and Immunology, Chang Gung University, 259, Wen-Hua 1st Road, Kwei-Shan, Taoyuan 333, the ^¶Department of Medical Education and Research, Veterans General Hospital, Kaohsiung, 386 Ta-Chung 1st Road, Kaohsiung 813, the ^||Institute of Biology and Anatomy, National Defense Medical School, 161, Section 6, Min-Chuang E. Road, Taipei 114, and the ^**Institute of Biomedical Sciences, National Sun Yat-Sen University, Kaohsiung 804, Taiwan

Epstein-Barr virus (EBV) expresses an immediate-early protein, Rta, to activate the transcription of EBV lytic genes and the lytic cycle. This work identifies Ubc9 and PIAS1 as binding partners of Rta in a yeast two-hybrid screen. These bindings are verified by glutathione S-transferase pull-down assay, coimmunoprecipitation, and confocal microscopy. The interactions appear to cause Rta sumoylation, because not only can Rta be sumoylated in vitro but also sumoylated Rta can be detected in P3HR1 cells following lytic induction and in 293T cells after transfecting plasmids that express Rta and SUMO-1. Moreover, PIAS1 stimulates conjugation of SUMO-1 to Rta, thus acting as an E3 ligase. Furthermore, transfecting plasmids that express Ubc9, PIAS1, and SUMO-1 increases the capacity of Rta to transactivate the promoter that includes an Rta response element, indicating that the modification by SUMO-1 increases the transactivation activity of Rta. This study reveals that Rta is sumoylated at the Lys-19, Lys-213, and Lys-517 residues and that SUMO-1 conjugation at the Lys-19 residue is crucial for enhancing the transactivation activity of Rta. These results indicate that sumoylation of Rta may be important in EBV lytic activation.

Received for publication, May 17, 2004 , and in revised form, June 29, 2004.

^* This work was supported by Medical Research Grant CMRP720-VI from Chang-Gung Memorial Hospital, National Health Research Institute Grant NHRI-EX91-8901SL, and National Council Grants NSC-91-2320-B-182-048, NSC-92-2311-B-037-002, and NSC-91-3112-B-110-001. 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.

To whom correspondence should be addressed. Tel./Fax: 886-3-211-8292; E-mail: cgliu{at}mail.cgu.edu.tw.

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