This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bryk, M. Articles by Curcio, M. J. Search for Related Content PubMed PubMed Citation Articles by Bryk, M. Articles by Curcio, M. J.

Molecular and Cellular Biology, August 2001, p. 5374-5388, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5374-5388.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

The Sgs1 Helicase of Saccharomyces cerevisiae Inhibits Retrotransposition of Ty1 Multimeric Arrays

Mary Bryk,^1,2 Mukti Banerjee,¹ Darryl Conte Jr.,^1, and M. Joan Curcio^1,*

Molecular Genetics Program, Wadsworth Center and School of Public Health, State University of New York at Albany, Albany, New York 12208,¹ and Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115²

Received 24 April 2001/Returned for modification 9 May 2001/Accepted 17 May 2001

Ty1 retrotransposons in the yeast Saccharomyces cerevisiae are maintained in a genetically competent but transpositionally dormant state. When located in the ribosomal DNA (rDNA) locus, Ty1 elements are transcriptionally silenced by the specialized heterochromatin that inhibits rDNA repeat recombination. In addition, transposition of all Ty1 elements is repressed at multiple posttranscriptional levels. Here, we demonstrate that Sgs1, a RecQ helicase required for genome stability, inhibits the mobility of Ty1 elements by a posttranslational mechanism. Using an assay for the mobility of Ty1 cDNA via integration or homologous recombination, we found that the mobility of both euchromatic and rDNA-Ty1 elements was increased 32- to 79-fold in sgs1 mutants. Increased Ty1 mobility was not due to derepression of silent rDNA-Ty1 elements, since deletion of SGS1 reduced the mitotic stability of rDNA-Ty1 elements but did not stimulate their transcription. Furthermore, deletion of SGS1 did not significantly increase the levels of total Ty1 RNA, protein, or cDNA and did not alter the level or specificity of Ty1 integration. Instead, Ty1 cDNA molecules recombined at a high frequency in sgs1 mutants, resulting in transposition of heterogeneous Ty1 multimers. Formation of Ty1 multimers required the homologous recombination protein Rad52 but did not involve recombination between Ty1 cDNA and genomic Ty1 elements. Therefore, Ty1 multimers that transpose at a high frequency in sgs1 mutants are formed by intermolecular recombination between extrachromosomal Ty1 cDNA molecules before or during integration. Our data provide the first evidence that the host cell promotes retrotransposition of monomeric Ty1 elements by repressing cDNA recombination.

---

^* Corresponding author. Mailing address: Wadsworth Center, P.O. Box 22002, Albany, NY 12201-2002. Phone: (518) 473-6078. Fax: (518) 474-3181. E-mail: joan.curcio{at}wadsworth.org.

Present address: Program in Molecular Medicine, University of Massachusetts Cancer Center, Worcester, MA 01605.

---

Molecular and Cellular Biology, August 2001, p. 5374-5388, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5374-5388.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

• Nyswaner, K. M., Checkley, M. A., Yi, M., Stephens, R. M., Garfinkel, D. J. (2008). Chromatin-Associated Genes Protect the Yeast Genome From Ty1 Insertional Mutagenesis. Genetics 178: 197-214 [Abstract] [Full Text]  
• Curcio, M. J., Kenny, A. E., Moore, S., Garfinkel, D. J., Weintraub, M., Gamache, E. R., Scholes, D. T. (2007). S-Phase Checkpoint Pathways Stimulate the Mobility of the Retrovirus-Like Transposon Ty1. Mol. Cell. Biol. 27: 8874-8885 [Abstract] [Full Text]  
• Maxwell, P. H., Curcio, M. J. (2007). Host Factors That Control Long Terminal Repeat Retrotransposons in Saccharomyces cerevisiae: Implications for Regulation of Mammalian Retroviruses. Eukaryot Cell 6: 1069-1080 [Full Text]  
• Garfinkel, D. J., Stefanisko, K. M., Nyswaner, K. M., Moore, S. P., Oh, J., Hughes, S. H. (2006). Retrotransposon Suicide: Formation of Ty1 Circles and Autointegration via a Central DNA Flap. J. Virol. 80: 11920-11934 [Abstract] [Full Text]  
• Irwin, B., Aye, M., Baldi, P., Beliakova-Bethell, N., Cheng, H., Dou, Y., Liou, W., Sandmeyer, S. (2005). Retroviruses and yeast retrotransposons use overlapping sets of host genes. Genome Res. 15: 641-654 [Abstract] [Full Text]  
• Maxwell, P. H., Coombes, C., Kenny, A. E., Lawler, J. F., Boeke, J. D., Curcio, M. J. (2004). Ty1 Mobilizes Subtelomeric Y' Elements in Telomerase-Negative Saccharomyces cerevisiae Survivors. Mol. Cell. Biol. 24: 9887-9898 [Abstract] [Full Text]  
• Buck, S. W., Gallo, C. M., Smith, J. S. (2004). Diversity in the Sir2 family of protein deacetylases. J. Leukoc. Biol. 75: 939-950 [Abstract] [Full Text]  
• Gallo, C. M., Smith, D. L. Jr., Smith, J. S. (2004). Nicotinamide Clearance by Pnc1 Directly Regulates Sir2-Mediated Silencing and Longevity. Mol. Cell. Biol. 24: 1301-1312 [Abstract] [Full Text]  
• Bowen, N. J., Jordan, I. K., Epstein, J. A., Wood, V., Levin, H. L. (2003). Retrotransposons and Their Recognition of pol II Promoters: A Comprehensive Survey of the Transposable Elements From the Complete Genome Sequence of Schizosaccharomyces pombe. Genome Res. 13: 1984-1997 [Abstract] [Full Text]  
• Sundararajan, A., Lee, B.-S., Garfinkel, D. J. (2003). The Rad27 (Fen-1) Nuclease Inhibits Ty1 Mobility in Saccharomyces cerevisiae. Genetics 163: 55-67 [Abstract] [Full Text]  
• Scholes, D. T., Banerjee, M., Bowen, B., Curcio, M. J. (2001). Multiple Regulators of Ty1 Transposition in Saccharomyces cerevisiae Have Conserved Roles in Genome Maintenance. Genetics 159: 1449-1465 [Abstract] [Full Text]