The Saccharomyces cerevisiae Histone Chaperone Rtt106 Mediates the Cell Cycle Recruitment of SWI/SNF and RSC to the HIR-Dependent Histone Genes
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BACKGROUND: In Saccharomyces cerevisiae, three out of the four histone gene pairs (HTA1-HTB1, HHT1-HHF1, and HHT2-HHF2) are regulated by the HIR co-repressor complex. The histone chaperone Rtt106 has recently been shown to be present at these histone gene loci throughout the cell cycle in a HIR- and Asf1-dependent manner and involved in their transcriptional repression. The SWI/SNF and RSC chromatin remodeling complexes are both recruited to the HIR-dependent histone genes; SWI/SNF is required for their activation in S phase, whereas RSC is implicated in their repression outside of S phase. Even though their presence at the histone genes is dependent on the HIR complex, their specific recruitment has not been well characterized. In this study we focused on characterizing the role played by the histone chaperone Rtt106 in the cell cycle-dependent recruitment of SWI/SNF and RSC complexes to the histone genes. METHODOLOGY/PRINCIPAL FINDINGS: Using GST pull-down and co-immunoprecipitation assays, we showed that Rtt106 physically interacts with both the SWI/SNF and RSC complexes in vitro and in vivo. We then investigated the function of this interaction with respect to the recruitment of these complexes to HIR-dependent histone genes. Using chromatin immunoprecipitation assays (ChIP), we found that Rtt106 is important for the recruitment of both SWI/SNF and RSC complexes to the HIR-dependent histone genes. Furthermore, using synchronized cell cultures, we showed by ChIP assays that the Rtt106-dependent SWI/SNF recruitment to these histone gene loci is cell cycle regulated and restricted to late G1 phase just before the peak of histone gene expression in S phase. CONCLUSIONS/SIGNIFICANCE: Overall, these data strongly suggest that the interaction between the histone chaperone Rtt106 and both the SWI/SNF and RSC chromatin remodeling complexes is important for the cell cycle regulated recruitment of these two complexes to the HIR-dependent histone genes.
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Outside S phase, Rtt106 forms a repressive complex together with other histone chaperones HIR and Asf1 to recruit RSC to the histone promoters.
“Outside S phase, Rtt106 forms a repressive complex together with other histone chaperones HIR and Asf1 to recruit RSC (Remodel the Structure of Chromatin), an essential ATP-dependent chromatin-remodelling complex, to the histone promoters31–33.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [33]
In the late G1 and early S phase, Rtt106 recruits SWI/SNF, which activates transcription of the histone genes by releasing HIR- and RSC-mediated repression.
“In contrast, in the late G1 and early S phase Rtt106 recruits SWI/SNF, another ATP-dependent chromatin-remodelling complex, which activates transcription of the histone genes by releasing HIR- and RSC-mediated repression33,34.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [33]
At the histone promoters, SWI/SNF is recruited by Rtt106, probably through direct physical interactions.
“However, at the histone promoters, SWI/SNF is recruited by Rtt106, probably through direct physical interactions33.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [33]
Rtt106 and SWI/SNF physically interact.
“The possibility that Rtt106 and SWI/SNF cooperate is further supported by their physical interaction (Fig. 6d)33.”
From SWI/SNF and the histone chaperone Rtt106 drive expression of the Pleiotropic Drug Resistance network genes (2022) · cites this paper as [33]
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Cites
Crystal structure of the nucleosome core particle at 2.8 Å resolution
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., & Richmond, T. J. (1997) · Nature · doi:10.1038/38444 · Cited by 9,466 · see citing works
Spellman, P. T., Sherlock, G. J., Zhang, M. Q., Iyer, V. R., Anders, K. R., Eisen, M. B., Brown, P. O., Botstein, D., & Futcher, B. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.12.3273 · Cited by 4,724 · see citing works
The biology of chromatin remodeling complexes.
Clapier, C. R., & Cairns, B. (2009) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.062706.153223 · Cited by 2,384 · see citing works
Tagami, H., Ray-Gallet, D., Almouzni, G., & Nakatani, Y. (2004) · Cell · doi:10.1016/s0092-8674(03)01064-x · Cited by 1,297 · see citing works
The Histone Variant H3.3 Marks Active Chromatin by Replication-Independent Nucleosome Assembly
Ahmad, K., & Henikoff, S. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00542-7 · Cited by 1,117 · see citing works
THE REGULATION OF HISTONE SYNTHESIS IN THE CELL CYCLE
Osley, M. A. (1991) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.60.070191.004143 · Cited by 497 · see citing works
Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly
Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A., & Zhang, Z. (2008) · Cell · doi:10.1016/j.cell.2008.06.018 · Cited by 447 · see citing works
Elevated histone expression promotes life span extension
Feser, J., Truong, D., Das, C., Carson, J. J., Kieft, J., Harkness, T., & Tyler, J. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.08.015 · Cited by 435 · see citing works
Acetylation in Histone H3 Globular Domain Regulates Gene Expression in Yeast
Xu, F., Zhang, K., & Grunstein, M. R. (2005) · Cell · doi:10.1016/j.cell.2005.03.011 · Cited by 394 · see citing works
Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complexPreprint
Ng, H., Robert, F., Young, R. A., & Struhl, K. (2002) · Genes & Development · doi:10.1101/gad.978902 · Cited by 275 · see citing works
Replication-Independent Histone Deposition by the HIR Complex and Asf1
Green, E. M., Antczak, A. J., Bailey, A. O., Franco, A. A., Wu, K. J., Yates, J. R., & Kaufman, P. D. (2005) · Current Biology · doi:10.1016/j.cub.2005.10.053 · Cited by 219 · see citing works
Identification of sequences in a yeast histone promoter involved in periodic transcription
Osley, M. A., Gould, J. H., Kim, S., Kane, M., & Hereford, L. M. (1986) · Cell · doi:10.1016/0092-8674(86)90285-0 · Cited by 197 · see citing works
Angus-Hill, M. L., Schlichter, A., Roberts, D. N., Erdjument‐Bromage, H., Tempst, P., & Cairns, B. R. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00219-2 · Cited by 187 · see citing works
Transcription Activator Interactions with Multiple SWI/SNF Subunits
Neely, K. E., Hassan, A. H., Brown, C. E., Howe, L., & Workman, J. L. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.6.1615-1625.2002 · Cited by 183 · see citing works
Yeast ASF1 Protein Is Required for Cell Cycle Regulation of Histone Gene Transcription
Sutton, A., Bucaria, J., Osley, M. A., & Sternglanz, R. (2001) · Genetics · doi:10.1093/genetics/158.2.587 · Cited by 150 · see citing works
Gowrishankar, B., Somaiah, N., Zhang, R., Tang, Y., Hoffmann, J., Andrake, M., Ceulemans, H., Schultz, D., Marmorstein, R., & Adams, P. D. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01047-08 · Cited by 141 · see citing works
Applicability of Tandem Affinity Purification MudPIT to Pathway Proteomics in Yeast
Graumann, J., Dunipace, L., Seol, J. H., McDonald, W. H., Yates, J. R., Wold, B. J., & Deshaies, R. J. (2003) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m300099-mcp200 · Cited by 139 · see citing works
Spector, M. S., Raff, A. C., DeSilva, H., Lee, K. M. L., & Osley, M. A. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.2.545 · Cited by 135 · see citing works
Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing
Huang, S., Zhou, H., Katzmann, D., Hochstrasser, M., Atanasova, E., & Zhang, Z. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506176102 · Cited by 130 · see citing works
Lamour, V., Lécluse, Y., Desmaze, C., Spector, M. E., Bodescot, M., Aurias, A., Osley, M. A., & Lipinski, M. (1995) · Human Molecular Genetics · doi:10.1093/hmg/4.5.791 · Cited by 125 · see citing works
Osley, M. A., & Lycan, D. E. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.12.4204 · Cited by 124 · see citing works
Regulation of histone synthesis and nucleosome assembly
Gunjan, A., Paik, J., & Verreault, A. (2005) · Biochimie · doi:10.1016/j.biochi.2005.02.008 · Cited by 119 · see citing works
Fillingham, J., Kainth, P., Lambert, J.-P., van Bakel, H., Tsui, K., Peña-Castillo, L., Nislow, C., Figeys, D., Hughes, T. R., Greenblatt, J., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.06.023 · Cited by 108 · see citing works
A Role for Transcriptional Repressors in Targeting the Yeast Swi/Snf Complex
Dimova, D., Nackerdien, Z., Furgeson, S., Eguchi, S., & Osley, M. A. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80189-6 · Cited by 105 · see citing works
Simultaneous Recruitment of Coactivators by Gcn4p Stimulates Multiple Steps of Transcription In Vivo
Govind, C. K., Yoon, S., Qiu, H., Govind, S., & Hinnebusch, A. G. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.13.5626-5638.2005 · Cited by 104 · see citing works
Prochasson, P., Florens, L. A., Swanson, S. K., Washburn, M. P., & Workman, J. L. (2005) · Genes & Development · doi:10.1101/gad.1341105 · Cited by 104 · see citing works
Self-citationProchasson, P., Neely, K. E., Hassan, A. H., Li, B., & Workman, J. L. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00366-6 · Cited by 97 · see citing works
Self-citationXu, H., Kim, U. J., Schuster, T., & Grunstein, M. R. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.11.5249 · Cited by 83 · see citing works
SWI/SNF-dependent chromatin remodeling ofRNR3requires TAFIIs and the general transcription machineryPreprint
Sharma, V. M., Li, B., & Reese, J. C. (2003) · Genes & Development · doi:10.1101/gad.1039503 · Cited by 78 · see citing works
HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes
Balaji, S., Iyer, L. M., & Aravind, L. (2009) · Molecular BioSystems · doi:10.1039/b816424j · Cited by 72 · see citing works
Imbeault, D., Gamar, L., Rufiange, A., Paquet, E., & Nourani, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.c800147200 · Cited by 66 · see citing works
Freeman, K. B., Karns, L. R., Lutz, K. A., & Smith, M. M. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.12.5455-5463.1992 · Cited by 39 · see citing works
Lee, K. K., Prochasson, P., Florens, L. A., Swanson, S. K., Washburn, M. P., & Workman, J. L. (2004) · Biochemical Society Transactions · doi:10.1042/bst0320899 · Cited by 39 · see citing works
Self-citationAnderson, H., Kagansky, A., Wardle, J., Rappsilber, J., Allshire, R., & Whitehall, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013488 · Cited by 33 · see citing works
Spt10 and Swi4 Control the Timing of Histone H2A/H2B Gene Activation in Budding Yeast
Eriksson, P. R., Ganguli, D., & Clark, D. J. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00909-10 · Cited by 32 · see citing works
Ferreira, M. E., Prochasson, P., Berndt, K. D., Workman, J. L., & Wright, A. P. H. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.06979.x · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Regulation of Histone Gene Expression in Budding Yeast
Eriksson, P. R., Ganguli, D., Nagarajavel, V, & Clark, D. J. (2012) · Genetics · doi:10.1534/genetics.112.140145 · Cited by 114 · see citing works
Regulation of histone gene transcription in yeast
Kurat, C. F., Recht, J., Radovani, E., Durbic, T., Andrews, B., & Fillingham, J. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1443-9 · Cited by 68 · see citing works
Regulation of DNA replication-coupled histone gene expression
Mei, Q., Huang, J., Chen, W., Tang, J., Xu, C., Yu, Q., Cheng, Y., Ma, L., Yu, X., & Li, S. (2017) · Oncotarget · doi:10.18632/oncotarget.21887 · Cited by 69 · see citing works
Cattaneo, M., Morozumi, Y., Perazza, D., Boussouar, F., Jamshidikia, M., Rousseaux, S., Verdel, A., & Khochbin, S. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.0258 · Cited by 55 · see citing works
A global requirement for the HIR complex in the assembly of chromatin
Amin, A. D., Vishnoi, N., & Prochasson, P. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.07.008 · Cited by 52 · see citing works
Self-citationKurat, C. F., Lambert, J.-P., van Dyk, D., Tsui, K., van Bakel, H., Kaluarachchi, S., Friesen, H., Kainth, P., Nislow, C., Figeys, D., et al. (2011) · Genes & Development · doi:10.1101/gad.173427.111 · Cited by 41 · see citing works
Mei, Q., Xu, C., Gogol, M., Tang, J., Chen, W., Yu, X., Workman, J. L., & Li, S. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz101 · Cited by 35 · see citing works
Jenull, S., Tscherner, M., Gulati, M., Nobile, C. J., Chauhan, N., & Kuchler, K. (2017) · Scientific Reports · doi:10.1038/s41598-017-08239-9 · Cited by 28 · see citing works
Ciftci-Yilmaz, S., Au, W.-C., Mishra, P. K., Eisenstatt, J. R., Chang, J. W., Dawson, A. R., Zhu, I., Rahman, M., Bilke, S., Costanzo, M., et al. (2018) · Genetics · doi:10.1534/genetics.118.301305 · Cited by 28 · see citing works
Zunder, R. M., & Rine, J. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00871-12 · Cited by 22 · see citing works
Identification of Elg1 interaction partners and effects on post-replication chromatin re-formation
Gali, V. K., Dickerson, D. R., Katou, Y., Fujiki, K., Shirahige, K., Owen‐Hughes, T., Kubota, T., & Donaldson, A. D. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007783 · Cited by 21 · see citing works
Jenull, S., Mair, T., Tscherner, M., Penninger, P., Zwolanek, F., Silao, F. G. S., Vicente, K. M. D. S., Riedelberger, M., Bandari, N. C., Shivarathri, R., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109406 · Cited by 19 · see citing works
Nikolov, V. N., Malavia, D., & Kubota, T. (2022) · Nature Communications · doi:10.1038/s41467-022-29591-z · Cited by 16 · see citing works
Maintenance of Nucleosomal Balance in<i>cis</i>by Conserved AAA-ATPase Yta7
Lombardi, L. M., Davis, M. D., & Rine, J. (2015) · Genetics · doi:10.1534/genetics.114.168039 · Cited by 16 · see citing works
Amin, A. D., Dimova, D. K., Ferreira, M. E., Vishnoi, N., Hancock, L. C., Osley, M. A., & Prochasson, P. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.09.003 · Cited by 7 · see citing works
Self-citationBragantini, B., Charron, C., Bourguet, M., Paul, A., Tiotiu, D., Rothé, B., Marty, H., Terral, G., Hessmann, S., Decourty, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22077-4 · Cited by 4 · see citing works
Sacharowski, S., Kubala, S., Cwiek, P., Steciuk, J., Gratkowska, D. M., Oksinska, P., Bucior, E., Rolicka, A. T., Ciesla, M., Nowicka, K., et al. (2025) · New Phytologist · doi:10.1111/nph.70182 · Cited by 2 · see citing works
Regulation of telomere silencing by the core histones–autophagy–Sir2 axis
Mei, Q., Yu, Q., Li, X., Chen, J., & Yu, X. (2022) · Life Science Alliance · doi:10.26508/lsa.202201614 · Cited by 2 · see citing works
Checkpoint Kinase Mediated Regulation of Histone Gene Expression in Response to Genotoxic Stress
Gajjalaiahvari, U. R. (2012)
A Global Mapping of Protein Complexes in S. cerevisiae
Vlasblom, J. (2013) · TSpace (University of Toronto)
Sanayhie, S. A., Pra, V. A. D., Khodabshakian, N., Karam, E., Chhipa, M. A., Kang, S., Ahmed, A., Fillingham, J., & Sabatinos, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.01.686071
- Authors
- Ferreira, M. E., Flaherty, K., & Prochasson, P.
- Affiliations
- University of Kansas Medical Center (US)
- Corresponding author
- Prochasson, Philippe
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-06-15
- Volume
- 6
- Issue
- 6
- Pages
- e21113
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3115976
- OpenAlex
- W2056036222
- Cited by
- 21
- References
- 36
- Citations by year
- 2025: 2 · 2022: 2 · 2021: 2 · 2019: 1 · 2018: 2 · 2017: 2 · 2014: 2 · 2013: 2 · 2012: 3
- FWCI
- 1.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Leukemia and Lymphoma Society
- Kansas Bioscience Authority
- Pennsylvania State University
- Kansas IDeA Network of Biomedical Research Excellence (RR016475)
- National Center for Research Resources (P20RR016475)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- histone chaperone, SWI/SNF complex, RSC complex, histone gene transcription, cell cycle regulation, chromatin remodeling, Asf1, G1 phase, Saccharomyces cerevisiae
- MeSH terms
- Cell Cycle, Chromosomal Proteins, Non-Histone, Protein Binding, Saccharomyces cerevisiae, Molecular Chaperones, Saccharomyces cerevisiae Proteins, Immunoprecipitation
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