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© The Rockefeller University Press, 0021-9525/1997//225 $5.00
The Journal of Cell Biology, Volume 138, Number 2, , 1997 225-238

Role of the Modular Domains of SR Proteins in Subnuclear Localization and Alternative Splicing Specificity

Javier F. Cáceres^*, Tom Misteli^*, Gavin R. Screaton, David L. Spector^*, and Adrian R. Krainer^*

^* Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724-2208; and Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK

SR proteins are required for constitutive pre-mRNA splicing and also regulate alternative splice site selection in a concentration-dependent manner. They have a modular structure that consists of one or two RNA-recognition motifs (RRMs) and a COOH-terminal arginine/serine-rich domain (RS domain). We have analyzed the role of the individual domains of these closely related proteins in cellular distribution, subnuclear localization, and regulation of alternative splicing in vivo. We observed striking differences in the localization signals present in several human SR proteins. In contrast to earlier studies of RS domains in the Drosophila suppressor-of-white-apricot (SWAP) and Transformer (Tra) alternative splicing factors, we found that the RS domain of SF2/ASF is neither necessary nor sufficient for targeting to the nuclear speckles. Although this RS domain is a nuclear localization signal, subnuclear targeting to the speckles requires at least two of the three constituent domains of SF2/ASF, which contain additive and redundant signals. In contrast, in two SR proteins that have a single RRM (SC35 and SRp20), the RS domain is both necessary and sufficient as a targeting signal to the speckles. We also show that RRM2 of SF2/ASF plays an important role in alternative splicing specificity: deletion of this domain results in a protein that, although active in alternative splicing, has altered specificity in 5' splice site selection. These results demonstrate the modularity of SR proteins and the importance of individual domains for their cellular localization and alternative splicing function in vivo.

Abbreviations used in this paper: G-domain, glycine-rich domain; RRM, RNA-recognition motif; RS domain, arginine/serine-rich domain; RT-PCR, reverse transcriptase PCR; snRNP, small nuclear ribonucleoprotein particle; SWAP, suppressor-of-white-apricot; Tra, Transformer.

Please address all correspondence to Adrian R. Krainer, Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724-2208. Tel.: (516) 367-8417. Fax: (516) 367-8453. E-mail: krainer{at}cshl.org

J.F. Cáceres' present address is MRC Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh EH4 2XU, United Kingdom.

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• Blencowe, B. J., Issner, R., Nickerson, J. A., Sharp, P. A. (1998). A coactivator of pre-mRNA splicing. Genes Dev. 12: 996-1009 [Abstract] [Full Text]  
• Tate, P, Lee, M, Tweedie, S, Skarnes, W., Bickmore, W. (1998). Capturing novel mouse genes encoding chromosomal and other nuclear proteins. J. Cell Sci. 111: 2575-2585 [Abstract]  
• Iborra, F., Jackson, D., Cook, P. (1998). The path of transcripts from extra-nucleolar synthetic sites to nuclear pores: transcripts in transit are concentrated in discrete structures containing SR proteins. J. Cell Sci. 111: 2269-2282 [Abstract]  
• Cáceres, J. F., Screaton, G. R., Krainer, A. R. (1998). A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12: 55-66 [Abstract] [Full Text]  
• Gama-Carvalho, M., Carvalho, M. P., Kehlenbach, A., Valcarcel, J., Carmo-Fonseca, M. (2001). Nucleocytoplasmic Shuttling of Heterodimeric Splicing Factor U2AF. J. Biol. Chem. 276: 13104-13112 [Abstract] [Full Text]  
• Cowper, A. E., Caceres, J. F., Mayeda, A., Screaton, G. R. (2001). Serine-Arginine (SR) Protein-like Factors That Antagonize Authentic SR Proteins and Regulate Alternative Splicing. J. Biol. Chem. 276: 48908-48914 [Abstract] [Full Text]  

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