The DOI matches its Crossref record; 58 of the 58 references it cites were found in a registry or an index.
Cell Cycle–Specified Fluctuation of Nucleosome Occupancy at Gene Promoters
Open accessAbstract
The packaging of DNA into nucleosomes influences the accessibility of underlying regulatory information. Nucleosome occupancy and positioning are best characterized in the budding yeast Saccharomyces cerevisiae, albeit in asynchronous cell populations or on individual promoters such as PHO5 and GAL1-10. Using FAIRE (formaldehyde-assisted isolation of regulatory elements) and whole-genome microarrays, we examined changes in nucleosome occupancy throughout the mitotic cell cycle in synchronized populations of S. cerevisiae. Perhaps surprisingly, nucleosome occupancy did not exhibit large, global variation between cell cycle phases. However, nucleosome occupancy at the promoters of cell cycle-regulated genes was reduced specifically at the cell cycle phase in which that gene exhibited peak expression, with the notable exception of S-phase genes. We present data that establish FAIRE as a high-throughput method for assaying nucleosome occupancy. For the first time in any system, nucleosome occupancy was mapped genome-wide throughout the cell cycle. Fluctuation of nucleosome occupancy at promoters of most cell cycle-regulated genes provides independent evidence that periodic expression of these genes is controlled mainly at the level of transcription. The promoters of G2/M genes are distinguished from other cell cycle promoters by an unusually low baseline nucleosome occupancy throughout the cell cycle. This observation, coupled with the maintenance throughout the cell cycle of the stereotypic nucleosome occupancy states between coding and non-coding loci, suggests that the largest component of variation in nucleosome occupancy is "hard wired," perhaps at the level of DNA sequence.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“These data, taken together with our expression analyses, indicate that tissue-specific gene expression can be dictated by tissue-specific transcription factor binding and by the tissue-specific recruitment of nucleosome-remodeling complexes (e.g., SWI/SNF) (Hogan et al. 2006;Schwabish and Struhl 2007) to transcription factor occupied loci.”
From Locus co-occupancy, nucleosome positioning, and H3K4me1 regulate the functionality of FOXA2-, HNF4A-, and PDX1-bound loci in islets and liver (2010) · cites this paper as Hogan et al. 2006
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Cluster analysis and display of genome-wide expression patterns
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14863 · Cited by 16,184
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
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
Hoffman, C. S., & Winston, F. (1987) · Gene · doi:10.1016/0378-1119(87)90131-4 · Cited by 2,492
Transcriptional regulatory code of a eukaryotic genome
Harbison, C. T., Gordon, D. B., Lee, T. I., Rinaldi, N. J., MacIsaac, K. D., Danford, T., Hannett, N. M., Tagne, J., Reynolds, D. B., Yoo, J. Y., et al. (2004) · Nature · doi:10.1038/nature02800 · Cited by 2,135
A Genome-Wide Transcriptional Analysis of the Mitotic Cell Cycle
Cho, R. J., Campbell, M. J., Winzeler, E. A., Steinmetz, L. M., Conway, A. R., Wodicka, L. M., Wolfsberg, T. G., Gabrielian, A. E., Landsman, D., Lockhart, D. J., et al. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80114-8 · Cited by 2,024
A genomic code for nucleosome positioning
Segal, E., Fondufe‐Mittendorf, Y. N., Chen, L., Thåström, A., Field, Y., Moore, I. K., Wang, J.-P. Z., & Widom, J. (2006) · Nature · doi:10.1038/nature04979 · Cited by 1,492
Genome-wide Map of Nucleosome Acetylation and Methylation in Yeast
Pokholok, D., Harbison, C. T., Levine, S. S., Cole, M. F., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, A., Herbolsheimer, E., et al. (2005) · Cell · doi:10.1016/j.cell.2005.06.026 · Cited by 1,477
Genome-Scale Identification of Nucleosome Positions in S. cerevisiae
Yuan, G., Liu, Y.-J., Dion, M. F., Slack, M. D., Wu, L. F., Altschuler, S. J., & Rando, O. J. (2005) · Science · doi:10.1126/science.1112178 · Cited by 1,139
Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF
Iyer, V. R., Horak, C. E., Scafe, C., Botstein, D., Snyder, M. P., & Brown, P. O. (2001) · Nature · doi:10.1038/35054095 · Cited by 1,084
Evidence for nucleosome depletion at active regulatory regions genome-wide
Lee, C.-K., Shibata, Y., Rao, B., Strahl, B. D., & Lieb, J. D. (2004) · Nature Genetics · doi:10.1038/ng1400 · Cited by 738
Self-citationPromoter-specific binding of Rap1 revealed by genome-wide maps of protein–DNA association
Lieb, J. D., Liu, X., Botstein, D., & Brown, P. O. (2001) · Nature Genetics · doi:10.1038/ng569 · Cited by 707
Self-citationCosma, M. P., Tanaka, T. U., & Nasmyth, K. (1999) · Cell · doi:10.1016/s0092-8674(00)80740-0 · Cited by 693
Histone Variant H2A.Z Marks the 5′ Ends of Both Active and Inactive Genes in Euchromatin
Raisner, R. M., Hartley, P. D., Meneghini, M. D., Bao, M. Z., Liu, C. L., Schreiber, S. L., Rando, O. J., & Madhani, H. D. (2005) · Cell · doi:10.1016/j.cell.2005.10.002 · Cited by 676
Polach, K. J., & Widom, J. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0606 · Cited by 657
Serial Regulation of Transcriptional Regulators in the Yeast Cell Cycle
Simon, I., Barnett, J., Hannett, N. M., Harbison, C. T., Rinaldi, N. J., Volkert, T. L., Wyrick, J. J., Zeitlinger, J., Gifford, D. K., Jaakkola, T., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00494-9 · Cited by 654
Lawrence, J., Villnave, C. A., & Singer, R. (1988) · Cell · doi:10.1016/0092-8674(88)90530-2 · Cited by 552
Formaldehyde-mediated DNA-protein crosslinking: a probe for in vivo chromatin structures.
Solomon, M. J., & Varshavsky, A. J. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.19.6470 · Cited by 462
Nucleosome loss activates yeast downstream promoters in vivo
Han, M., & GRUNSTEIN, M. M. (1988) · Cell · doi:10.1016/0092-8674(88)90258-9 · Cited by 462
Almer, A., Rudolph, H. K., Hinnen, A., & Hörz, W. (1986) · The EMBO Journal · doi:10.1002/j.1460-2075.1986.tb04552.x · Cited by 455
Nucleosomes Unfold Completely at a Transcriptionally Active Promoter
Boeger, H., Griesenbeck, J., Strattan, J. S., & Kornberg, R. D. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00231-4 · Cited by 402
Histones Are First Hyperacetylated and Then Lose Contact with the Activated PHO5 Promoter
Reinke, H., & Hörz, W. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00186-2 · Cited by 394
Global nucleosome occupancy in yeast
Bernstein, B., Liu, C. L., Humphrey, E. L., Perlstein, E. O., & Schreiber, S. L. (2004) · Genome biology · doi:10.1186/gb-2004-5-9-r62 · Cited by 366
Sekinger, E. A., Moqtaderi, Z., & Struhl, K. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.05.003 · Cited by 334
Reactions of Nucleic Acids and NucleoDroteins with Formaldehyde
Feldman, M. Y. (1973) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)60099-9 · Cited by 331
Chromosome condensation and sister chromatid pairing in budding yeast.
Guacci, V., Hogan, E., & Koshland, D. E. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.3.517 · Cited by 323
Adkins, M. W., Howar, S. R., & Tyler, J. K. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.05.016 · Cited by 294
Cell cycle-regulated histone acetylation required for expression of the yeast HO gene
Krebs, J. E., Kuo, M.-H., Allis, C. D., & Peterson, C. L. (1999) · Genes & Development · doi:10.1101/gad.13.11.1412 · Cited by 275
Ahn, S.-H., Cheung, W. L., Hsu, J.-Y., Diaz, R. L., Smith, M. M., & Allis, C. D. (2005) · Cell · doi:10.1016/j.cell.2004.11.016 · Cited by 259
Removal of Promoter Nucleosomes by Disassembly Rather Than Sliding In Vivo
Boeger, H., Griesenbeck, J., Strattan, J. S., & Kornberg, R. D. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.05.013 · Cited by 258
Global Role for Chromatin Remodeling Enzymes in Mitotic Gene Expression
Krebs, J. E., Fry, C. J., Samuels, M. L., & Peterson, C. L. (2000) · Cell · doi:10.1016/s0092-8674(00)00081-7 · Cited by 237
Zeitlinger, J., Simon, I., Harbison, C. T., Hannett, N. M., Volkert, T. L., Fink, G. R., & Young, R. A. (2003) · Cell · doi:10.1016/s0092-8674(03)00301-5 · Cited by 224
The Dynamics of Chromatin Remodeling at Promoters
Mellor, J. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.023 · Cited by 221
Depletion of histone H4 and nucleosomes activates the PHO5 gene in Saccharomyces cerevisiae.
Han, M., Kim, U. J., Kayne, P. S., & Grunstein, M. R. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03061.x · Cited by 221
Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters
Koranda, M., Schleiffer, A., Endler, L., & Ammerer, G. (2000) · Nature · doi:10.1038/35017589 · Cited by 202
Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes
Wittenberg, C., & Reed, S. I. (2005) · Oncogene · doi:10.1038/sj.onc.1208606 · Cited by 201
Properties of formaldehyde-treated nucleohistone
Brutlag, D. L., Schlehuber, C., & Bonner, J. (1969) · Biochemistry · doi:10.1021/bi00836a013 · Cited by 197
Pheromone-regulated Genes Required for Yeast Mating Differentiation
Erdman, S. E., Li, L., Malczynski, M., & Snyder, M. P. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.3.461 · Cited by 193
A method for the rapid sequence-independent amplification of microdissected chromosomal material
Bohlander, S. K., Espinosa, R., Beau, M. M. L., Rowley, J. D., & Dı́az, M. O. (1992) · Genomics · doi:10.1016/0888-7543(92)90057-y · Cited by 182
Transcription factors vs nucleosomes: regulation of the PH05 promoter in yeast
Svaren, J. P. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01001-3 · Cited by 171
Nasmyth, K. (1987) · Cell · doi:10.1016/0092-8674(87)90236-4 · Cited by 161
A functional role for nucleosomes in the repression of a yeast promoter.
Straka, C., & Hörz, W. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07957.x · Cited by 155
Schmid, A., Fascher, K.-D., & Hörz, W. (1992) · Cell · doi:10.1016/0092-8674(92)90560-y · Cited by 153
Venter, U., Svaren, J. P., Schmitz, J., Schmid, A., & Hörz, W. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06811.x · Cited by 132
Liu, X., Lee, C., Granek, J. A., Clarke, N. D., & Lieb, J. D. (2006) · Genome Research · doi:10.1101/gr.5655606 · Cited by 132
Self-citationDevelopment and validation of a T7 based linear amplification for genomic DNA
Liu, C. L., Schreiber, S. L., & Bernstein, B. (2003) · BMC Genomics · doi:10.1186/1471-2164-4-19 · Cited by 119
Nagy, P. L., Cleary, M. L., Brown, P. O., & Lieb, J. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1131966100 · Cited by 114
Self-citationKorber, P., Barbaric, S., Luckenbach, T., Schmid, A., Schermer, U. J., Blaschke, D., & Hörz, W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513340200 · Cited by 106
Loy, C. J., Lydall, D. A., & Surana, U. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3312 · Cited by 97
Evidence for Histone Eviction in trans upon Induction of the Yeast PHO5 Promoter
Korber, P., Luckenbach, T., Blaschke, D., & Hörz, W. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.24.10965-10974.2004 · Cited by 96
Histones Are Incorporated in trans during Reassembly of the Yeast PHO5 Promoter
Schermer, U. J., Korber, P., & Hörz, W. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.05.028 · Cited by 88
Fedor, M. J., & Kornberg, R. D. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.4.1721-1732.1989 · Cited by 75
Control of Transcription through Intragenic Patterns of Nucleosome Composition
Lieb, J. D., & Clarke, N. D. (2005) · Cell · doi:10.1016/j.cell.2005.12.010 · Cited by 68
Self-citationNucleosome Transactions on the Promoters of the YeastGAL and PHO Genes
Lohr, D. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.43.26795 · Cited by 60
Hertel, C. B., Längst, G., Hörz, W., & Korber, P. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.24.10755-10767.2005 · Cited by 33
Interplay between nucleosomes and transcription factors at the yeastPHO5promoter
Svaren, J. P., & Hörz, W. (1995) · Seminars in Cell Biology · doi:10.1006/scel.1995.0025 · Cited by 27
Ercan, S., & Simpson, R. T. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.22.10026-10035.2004 · Cited by 27
Regulation of nucleosome stability as a mediator of chromatin function
Giresi, P. G., Gupta, M., & Lieb, J. D. (2006) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2006.02.003 · Cited by 23
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The ENCODE Project Consortium (2007) · Nature · doi:10.1038/nature05874 · Cited by 5,223
Nucleosome positioning and gene regulation: advances through genomics
Jiang, C., & Pugh, B. F. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2522 · Cited by 1,059
G-quadruplex structures mark human regulatory chromatin
Hänsel-Hertsch, R., Beraldi, D., Lensing, S. V., Marsico, G., Zyner, K., Parry, A., Di Antonio, M., Pike, J., Kimura, H., Narita, M., et al. (2016) · Nature Genetics · doi:10.1038/ng.3662 · Cited by 964
Giresi, P. G., Kim, J., McDaniell, R. M., Iyer, V. R., & Lieb, J. D. (2006) · Genome Research · doi:10.17615/8cez-3e87 · Cited by 993
Self-citationA high-resolution atlas of nucleosome occupancy in yeast
Lee, W., Tillo, D., Bray, N., Morse, R. H., Davis, R. W., Hughes, T. R., & Nislow, C. (2007) · Nature Genetics · doi:10.1038/ng2117 · Cited by 829
Metadata
- Authors
- Hogan, G. J., Lee, C.-K., & Lieb, J. D.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Lieb, Jason D
- ORCID
- Lee, Cheol-Koo
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2006-09-22
- Volume
- 2
- Issue
- 9
- Pages
- e158
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC1570381
- OpenAlex
- W1983386103
- Cited by
- 109
- References
- 58
- Citations by year
- 2025: 2 · 2022: 2 · 2020: 3 · 2019: 3 · 2018: 4 · 2017: 4 · 2016: 8 · 2015: 3 · 2014: 10 · 2013: 7 · 2012: 7
- FWCI
- 4.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Frances C. and William P. Smallwood Foundation
- National Institutes of Health
- National Institute of General Medical Sciences (GM 072518, R01GM072518)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- nucleosome occupancy, cell cycle, promoter, Saccharomyces cerevisiae, FAIRE, mitotic cycle, cell cycle-regulated genes, transcriptional regulation, DNA accessibility, nucleosome positioning, genome-wide mapping
- MeSH terms
- Cell Cycle, Genes, Fungal, Histones, Lipoproteins, Mitosis, Molecular Sequence Data, Mutation, Nucleosomes, Pheromones, Promoter Regions, Genetic, Saccharomyces cerevisiae, Cell Adhesion Molecules, G1 Phase, G2 Phase, S Phase, Cyclins, Cyclin B, Saccharomyces cerevisiae Proteins, Microarray Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
