Abstract
SWI/SNF chromatin-remodeling complexes have crucial roles in transcription and other chromatin-related processes. The analysis of the two members of this class in Saccharomyces cerevisiae, SWI/SNF and RSC, has heavily contributed to our understanding of these complexes. To understand the in vivo functions of SWI/SNF and RSC in an evolutionarily distant organism, we have characterized these complexes in Schizosaccharomyces pombe. Although core components are conserved between the two yeasts, the compositions of S. pombe SWI/SNF and RSC differ from their S. cerevisiae counterparts and in some ways are more similar to metazoan complexes. Furthermore, several of the conserved proteins, including actin-like proteins, are markedly different between the two yeasts with respect to their requirement for viability. Finally, phenotypic and microarray analyses identified widespread requirements for SWI/SNF and RSC on transcription including strong evidence that SWI/SNF directly represses iron-transport genes.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
References
Cairns, B.R. Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol. 14, 989–996 (2007).
Mohrmann, L. & Verrijzer, C.P. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681, 59–73 (2005).
van Vugt, J.J., Ranes, M., Campsteijn, C. & Logie, C. The ins and outs of ATP-dependent chromatin remodeling in budding yeast: biophysical and proteomic perspectives. Biochim. Biophys. Acta 1769, 153–171 (2007).
Holstege, F.C. et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717–728 (1998).
Sudarsanam, P., Iyer, V.R., Brown, P.O. & Winston, F. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97, 3364–3369 (2000).
Dror, V. & Winston, F. The SWI/SNF chromatin remodeling complex is required for ribosomal DNA and telomeric silencing in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 8227–8235 (2004).
Chai, B., Huang, J., Cairns, B.R. & Laurent, B.C. Distinct roles for the RSC and SWI/SNF ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656–1661 (2005).
Cairns, B.R. et al. RSC, an essential, abundant chromatin-remodeling complex. Cell 87, 1249–1260 (1996).
Laurent, B.C., Yang, X. & Carlson, M. An essential Saccharomyces cerevisiae gene homologous to SNF2 encodes a helicase-related protein in a new family. Mol. Cell. Biol. 12, 1893–1902 (1992).
Angus-Hill, M.L. et al. A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control. Mol. Cell 7, 741–751 (2001).
Damelin, M. et al. The genome-wide localization of Rsc9, a component of the RSC chromatin-remodeling complex, changes in response to stress. Mol. Cell 9, 563–573 (2002).
Ng, H.H., Robert, F., Young, R.A. & Struhl, K. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev. 16, 806–819 (2002).
Kasten, M. et al. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23, 1348–1359 (2004).
Soutourina, J. et al. Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol. Cell. Biol. 26, 4920–4933 (2006).
Parnell, T.J., Huff, J.T. & Cairns, B.R. RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J. 27, 100–110 (2008).
Cao, Y., Cairns, B.R., Kornberg, R.D. & Laurent, B.C. Sfh1p, a component of a novel chromatin-remodeling complex, is required for cell cycle progression. Mol. Cell. Biol. 17, 3323–3334 (1997).
Hsu, J.M., Huang, J., Meluh, P.B. & Laurent, B.C. The yeast RSC chromatin-remodeling complex is required for kinetochore function in chromosome segregation. Mol. Cell. Biol. 23, 3202–3215 (2003).
Huang, J., Hsu, J.M. & Laurent, B.C. The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. Mol. Cell 13, 739–750 (2004).
Shim, E.Y. et al. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27, 1602–1613 (2007).
Cairns, B.R., Erdjument-Bromage, H., Tempst, P., Winston, F. & Kornberg, R.D. Two actin-related proteins are shared functional components of the chromatin-remodeling complexes RSC and SWI/SNF. Mol. Cell 2, 639–651 (1998).
Simone, C. SWI/SNF: the crossroads where extracellular signaling pathways meet chromatin. J. Cell. Physiol. 207, 309–314 (2006).
Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI/SNF complex. EMBO J. 15, 5370–5382 (1996).
Wang, W. et al. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117–2130 (1996).
Martens, J.A. & Winston, F. Recent advances in understanding chromatin remodeling by SWI/SNF complexes. Curr. Opin. Genet. Dev. 13, 136–142 (2003).
Sansam, C.G. & Roberts, C.W. Epigenetics and cancer: altered chromatin remodeling via Snf5 loss leads to aberrant cell cycle regulation. Cell Cycle 5, 621–624 (2006).
Grewal, S.I. & Jia, S. Heterochromatin revisited. Nat. Rev. Genet. 8, 35–46 (2007).
Yamada, T. et al. Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J. 23, 1792–1803 (2004).
Bernal, G. & Maldonado, E. Isolation of a novel complex of the SWI/SNF family from Schizosaccharomyces pombe and its effects on in vitro transcription in nucleosome arrays. Mol. Cell. Biochem. 303, 131–139 (2007).
Wilson, B., Erdjument-Bromage, H., Tempst, P. & Cairns, B.R. The RSC chromatin remodeling complex bears an essential fungal-specific protein module with broad functional roles. Genetics 172, 795–809 (2006).
Cairns, B.R. et al. Two functionally distinct forms of the RSC nucleosome-remodeling complex, containing essential AT hook, BAH, and bromodomains. Mol. Cell 4, 715–723 (1999).
Chen, M. & Shen, X. Nuclear actin and actin-related proteins in chromatin dynamics. Curr. Opin. Cell Biol. 19, 326–330 (2007).
Szerlong, H., Saha, A. & Cairns, B.R. The nuclear actin-related proteins Arp7 and Arp9: a dimeric module that cooperates with architectural proteins for chromatin remodeling. EMBO J. 22, 3175–3187 (2003).
Winston, F. & Carlson, M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 8, 387–391 (1992).
Aslett, M. & Wood, V. Gene Ontology annotation status of the fission yeast genome: preliminary coverage approaches 100%. Yeast 23, 913–919 (2006).
Tusher, V.G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116–5121 (2001).
Turi, T.G., Webster, P. & Rose, J.K. Brefeldin A sensitivity and resistance in Schizosaccharomyces pombe. Isolation of multiple genes conferring resistance. J. Biol. Chem. 269, 24229–24236 (1994).
Heiland, S., Radovanovic, N., Hofer, M., Winderickx, J. & Lichtenberg, H. Multiple hexose transporters of Schizosaccharomyces pombe. J. Bacteriol. 182, 2153–2162 (2000).
Fagerstrom-Billai, F., Durand-Dubief, M., Ekwall, K. & Wright, A.P. Individual subunits of the Ssn6-Tup11/12 corepressor are selectively required for repression of different target genes. Mol. Cell. Biol. 27, 1069–1082 (2007).
Mehta, S.V., Patil, V.B., Velmurugan, S., Lobo, Z. & Maitra, P.K. Std1, a gene involved in glucose transport in Schizosaccharomyces pombe. J. Bacteriol. 180, 674–679 (1998).
Labbe, S., Pelletier, B. & Mercier, A. Iron homeostasis in the fission yeast Schizosaccharomyces pombe. Biometals 20, 523–537 (2007).
Znaidi, S., Pelletier, B., Mukai, Y. & Labbe, S. The Schizosaccharomyces pombe corepressor Tup11 interacts with the iron-responsive transcription factor Fep1. J. Biol. Chem. 279, 9462–9474 (2004).
Minoda, A., Saitoh, S., Takahashi, K. & Toda, T. BAF53/Arp4 homolog Alp5 in fission yeast is required for histone H4 acetylation, kinetochore-spindle attachment, and gene silencing at centromere. Mol. Biol. Cell 16, 316–327 (2005).
Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201–215 (2007).
Wu, J.I. et al. Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94–108 (2007).
Shen, X., Ranallo, R., Choi, E. & Wu, C. Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12, 147–155 (2003).
Downs, J.A. et al. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16, 979–990 (2004).
Shivaswamy, S. & Iyer, V.R. Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response. Mol. Cell. Biol. 28, 2221–2234 (2008).
Martens, J.A. & Winston, F. Evidence that SWI/SNF directly represses transcription in S. cerevisiae. Genes Dev. 16, 2231–2236 (2002).
Martens, J.A., Wu, P.Y. & Winston, F. Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes Dev. 19, 2695–2704 (2005).
Borneman, A.R. et al. Divergence of transcription factor binding sites across related yeast species. Science 317, 815–819 (2007).
Forsburg, S.L. & Rhind, N. Basic methods for fission yeast. Yeast 23, 173–183 (2006).
Bahler, J. et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943–951 (1998).
Aves, S.J., Hindley, J., Phear, G.A. & Tongue, N. A fission yeast gene mapping close to suc1 encodes a protein containing two bromodomains. Mol. Gen. Genet. 248, 491–498 (1995).
Gould, K.L., Ren, L., Feoktistova, A.S., Jennings, J.L. & Link, A.J. Tandem affinity purification and identification of protein complex components. Methods 33, 239–244 (2004).
MacCoss, M.J., Wu, C.C. & Yates, J.R. III. Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal. Chem. 74, 5593–5599 (2002).
Elias, J.E. & Gygi, S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207–214 (2007).
Roberts, D.N., Stewart, A.J., Huff, J.T. & Cairns, B.R. The RNA polymerase III transcriptome revealed by genome-wide localization and activity-occupancy relationships. Proc. Natl. Acad. Sci. USA 100, 14695–14700 (2003).
Mata, J., Lyne, R., Burns, G. & Bahler, J. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32, 143–147 (2002).
Lyne, R. et al. Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4, 27 (2003).
Kippert, F. & Lloyd, D. The aniline blue fluorochrome specifically stains the septum of both live and fixed Schizosaccharomyces pombe cells. FEMS Microbiol. Lett. 132, 215–219 (1995).
Acknowledgements
We thank D. Helmlinger and M. Gelbart for helpful comments on the manuscript. We are grateful to C. Hoffman (Biology Department, Boston College) and S. Labbé (Department of Biochemistry, University of Sherbrooke) for providing S. pombe strains. We also thank D. Drubin and P. Silver for assistance with the microscopy analysis and use of their facilities. This work was supported by the US National Institutes of Health grant GM32967 to F.W., HG3456 to S.P.G., and a Cancer Research UK grant C9546/A6517 to J.B. B.J.M. was supported by a Post-Doctoral Research Fellowship from the New Zealand Foundation of Research Science and Technology, and S.M. was supported by a fellowship for Advanced Researchers from the Swiss National Science Foundation.
Author information
Authors and Affiliations
Contributions
B.J.M. designed and performed experiments. J.V. performed the MS analysis overseen by S.P.G. S.M. performed whole-genome microarray analysis overseen by J.B. F.W. assisted experimental design and supervised project. B.J.M. and F.W. wrote the manuscript.
Corresponding author
Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–4 and Supplementary Tables 1–6 (PDF 339 kb)
Excel File
Supplementary Table 7 (XLS 144 kb)
Rights and permissions
About this article
Cite this article
Monahan, B., Villén, J., Marguerat, S. et al. Fission yeast SWI/SNF and RSC complexes show compositional and functional differences from budding yeast. Nat Struct Mol Biol 15, 873–880 (2008). https://doi.org/10.1038/nsmb.1452
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nsmb.1452
This article is cited by
-
Emerging roles of SWI/SNF remodelers in fungal pathogens
Current Genetics (2022)
-
Long noncoding RNA SNHG14 promotes hepatocellular carcinoma progression by regulating miR-876-5p/SSR2 axis
Journal of Experimental & Clinical Cancer Research (2021)
-
A genome-wide analysis of carbon catabolite repression in Schizosaccharomyces pombe
BMC Genomics (2019)
-
Transcription factor Znf2 coordinates with the chromatin remodeling SWI/SNF complex to regulate cryptococcal cellular differentiation
Communications Biology (2019)
-
Actin-related proteins regulate the RSC chromatin remodeler by weakening intramolecular interactions of the Sth1 ATPase
Communications Biology (2018)