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J. Biol. Chem., Vol. 279, Issue 11, 10077-10084, March 12, 2004

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SC35 and Heterogeneous Nuclear Ribonucleoprotein A/B Proteins Bind to a Juxtaposed Exonic Splicing Enhancer/Exonic Splicing Silencer Element to Regulate HIV-1 tat Exon 2 Splicing^*

Alan M. Zahler, Christian K. Damgaard, Jorgen Kjems, and Massimo Caputi¶||

From the Department of Molecular, Cellular and Developmental Biology and Center for Molecular Biology of RNA, Sinsheimer Laboratories, University of California, Santa Cruz, California 95064, Department of Molecular Biology, University of Aarhus, DK-8000 Aarhus C, Denmark, and ^¶Biomedical Science Department, Florida Atlantic University, Boca Raton, Florida 33431

Splicing of the human immunodeficiency virus, type 1, primary transcript is highly regulated. Maintaining the proper equilibrium among spliced, unspliced, and partially spliced isoforms is essential for the replication of the virus. Here we characterize a complex cis-acting element located in tat exon 2 that is required for the splicing regulation of the upstream intron. An exonic splicing enhancer (ESE) and an exonic splicing silencer (ESS) are both located within the regulatory element. Heterogeneous nuclear ribonucleoprotein (hnRNP) A/B proteins bind the ESS to repress splicing, whereas the SR protein SC35 binds the ESE to activate it. We show that the SC35 and the hnRNP A1 binding sites overlap within the juxtaposed ESE/ESS. We propose that hnRNP A1 binding to the ESS inhibits splicing of the upstream intron by directly masking the SC35 binding site.

Received for publication, November 21, 2003 , and in revised form, December 22, 2003.

^* This work was supported by NIGMS, National Institutes of Health Grant 1R01GM61646 and a grant from the W. M. Keck Foundation to the University of California, Santa Cruz Center for Molecular Biology of RNA (to A. M. Z.), NIAID, National Institutes of Health grant 5R01AI052820-02 (to M. C.), and by grants from the Danish National Science and Medical Research Councils, the Carlsberg Foundation, and the Novo Nordic Foundation (to C. K. D. and J. K.). 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.: 561-297-0627; Fax: 561-297-2221; E-mail: mcaputi{at}fau.edu.

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