The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo

In budding yeast, a single cenH3 (Cse4) nucleosome occupies the ∼120-bp functional centromere, however conflicting structural models for the particle have been proposed. To resolve this controversy, we have applied H4S47C-anchored cleavage mapping, which reveals the precise position of histone H4 in every nucleosome in the genome. We find that cleavage patterns at centromeres are unique within the genome and are incompatible with symmetrical structures, including octameric nucleosomes and (Cse4/H4)2 tetrasomes. Centromere cleavage patterns are compatible with a precisely positioned core structure, one in which each of the 16 yeast centromeres is occupied by oppositely oriented Cse4/H4/H2A/H2B hemisomes in two rotational phases within the population. Centromere-specific hemisomes are also inferred from distances observed between closely-spaced H4 cleavages, as predicted from structural modeling. Our results indicate that the orientation and rotational position of the stable hemisome at each yeast centromere is not specified by the functional centromere sequence. DOI: http://dx.doi.org/10.7554/eLife.01861.001

• Publication year

  2014

• Venue

  eLife

• Publication date

  2014-04-15

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.7554/eLife.01861PMID 24737863PMCID 3983907
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• CENP-A octamers do not confer a reduction in nucleosome height by AFM

  2014cited by this paper
• Author response: The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo

  2014cited by this paper
• The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo

  2014cited by this paper
• CENP-A octamers do not confer a reduction in nucleosome height by AFM

  2014cited by this paper
• ISWI and CHD chromatin remodelers bind to promoters but act in gene bodies

  2013cited by this paper
• Reconstitution of hemisomes on budding yeast centromeric DNA

  2013cited by this paper
• The octamer is the major form of CENP-A nucleosomes at human centromeres

  2013cited by this paper
• The budding yeast point centromere associates with two Cse4 molecules during mitosis.

  2013influential reference
• CENP-A confers a reduction in height on octameric nucleosomes

  2013cited by this paper
• ISWI and CHD Chromatin Remodelers Bind Promoters but Act in Gene Bodies

  2013cited by this paper
• ochore Reveals the Presence of Core and Accessory Centromere-Specific Histone

  2013cited by this paper
• Solo or doppio: how many CENP-As make a centromeric nucleosome?

  2013influential reference
• ‘Point’ Centromeres of Saccharomyces harbor single CenH3 nucleosomes

  2012cited by this paper
• Cell-cycle-dependent structural transitions in the human CENP-A nucleosome in vivo.

  2012cited by this paper
• Histone H3 Localizes to the Centromeric DNA in Budding Yeast

  2012influential reference
• Avogadro: an advanced semantic chemical editor, visualization, and analysis platform

  2012cited by this paper
• The unconventional structure of centromeric nucleosomes

  2012cited by this paper
• Cell-cycle-coupled structural oscillation of centromeric nucleosomes in yeast.

  2012influential reference
• “Point” Centromeres of Saccharomyces Harbor Single Centromere-Specific Nucleosomes

  2012cited by this paper
• The CENP-A nucleosome: a dynamic structure and role at the centromere

  2012cited by this paper
• A base pair resolution map of nucleosome positions in yeast

  2012cited by this paper
• Genome-wide analysis of longevity in nutrient-deprived Saccharomyces cerevisiae reveals importance of recycling in maintaining cell viability.

  2012cited by this paper
• A chemical approach to mapping nucleosomes at base pair resolution in yeast.

  2012cited by this paper
• Effect of PCR extension temperature on high-throughput sequencing.

  2011cited by this paper
• Optimal enzymes for amplifying sequencing libraries

  2011cited by this paper
• The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere

  2011cited by this paper
• Centromere-specific histone Cse4 by the chaperone Scm3

  2011cited by this paper
• CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast

  2011cited by this paper
• Nonhistone Scm3 binds to AT-rich DNA to organize atypical centromeric nucleosome of budding yeast.

  2011influential reference
• Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes

  2011cited by this paper
• Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome

  2011cited by this paper
• Epigenome characterization at single base-pair resolution

  2011cited by this paper
• Automated minimization of steric clashes in protein structures

  2011cited by this paper
• Scm3 Is a Centromeric Nucleosome Assembly Factor*

  2011influential reference
• Epigenetic centromere propagation and the nature of CENP-a nucleosomes.

  2011cited by this paper
• Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

  2011cited by this paper
• Crystal structure of the human centromeric nucleosome containing CENP-A

  2011influential reference
• Nucleosome fragility reveals novel functional states of chromatin and poises genes for activation.

  2011cited by this paper
• Tripartite organization of centromeric chromatin in budding yeast

  2011cited by this paper
• H2A.Z Demarcates Intergenic Regions of the Plasmodium falciparum Epigenome That Are Dynamically Marked by H3K9ac and H3K4me3

  2010influential reference
• The Effect of Micrococcal Nuclease Digestion on Nucleosome Positioning Data

  2010cited by this paper
• Elevated histone expression promotes life span extension.

  2010cited by this paper
• A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding.

  2010cited by this paper
• A genetic system to assess in vivo the functions of histones and histone modifications in higher eukaryotes

  2010cited by this paper
• Centromeric nucleosomes induce positive DNA supercoils.

  2009cited by this paper
• Cse4 is part of an octameric nucleosome in budding yeast.

  2009cited by this paper
• Tetrameric Structure of Centromeric Nucleosomes in Interphase Drosophila Cells

  2007cited by this paper
• Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes.

  2007cited by this paper
• Centromere identity is specified by a single centromeric nucleosome in budding yeast

  2007cited by this paper
• Genetic and Genomic Analysis of the AT-Rich Centromere DNA Element II of Saccharomyces cerevisiae

  2005influential reference
• Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution.

  2002cited by this paper
• Molecular Cloning: A Laboratory Manual

  2001cited by this paper
• Preparation of nucleosome core particle from recombinant histones.

  1999cited by this paper
• Transforming the Escherichia coli Trp repressor into a site-specific nuclease.

  1993cited by this paper
• A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere.

  1992cited by this paper
• Molecular cloning : a laboratory manual. Cold Spring Harbor, NY

  1989cited by this paper
• A new method of sequencing DNA.

  1988cited by this paper
• A genetic analysis of dicentric minichromosomes in Saccharomyces cerevisiae.

  1987cited by this paper
• Analysis of chromatin structure and DNA sequence organization: use of the 1,10-phenanthroline-cuprous complex.

  1982cited by this paper
• A new method for sequencing DNA.

  1977cited by this paper
• Report Octameric Cenp-a Nucleosomes Are Present at Human Centromeres throughout the Cell Cycle the Majority of Cenp-a-containing Complexes in Cells Contain Two Cenp-a Molecules

  year unknowncited by this paper

• Locations of consecutive G•C base-pairs direct genomic nucleosome positioning

  2025cites this paper
• The dynamic centromere

  2025cites this paper
• Genome-Wide Nucleosome Mapping by H3Q85C-Directed Chemical Cleavage in Saccharomyces cerevisiae.

  2025cites this paper
• High-resolution analysis of human centromeric chromatin

  2025cites this paper
• Structure and evolution of metapolycentromeres

  2024cites this paper
• Resolution of transcription-induced hexasome-nucleosome complexes by Chd1 and FACT.

  2024influential citation
• Molecular dynamics simulations of nucleosomes are coming of age

  2024cites this paper
• Finish the unfinished: Chd1 resolving hexasome-nucleosome complex with FACT.

  2024cites this paper
• ISW1a modulates cohesin distribution in centromeric and pericentromeric regions

  2023cites this paper
• Asymmetric patterns of nucleosome positioning sequences in protein-coding regions

  2023cites this paper
• Humanized nucleosomes reshape replication initiation and rDNA/nucleolar integrity in yeast

  2023cites this paper
• Synthetic yeast chromosome XI design provides a testbed for the study of extrachromosomal circular DNA dynamics

  2023cites this paper
• The CENP-A nucleosome: where and when it happens during the inner kinetochore's assembly.

  2023cites this paper
• Structure of the human inner kinetochore CCAN complex and its significance for human centromere organization

  2022influential citation
• The chromatin remodeler RSC prevents ectopic CENP-A propagation into pericentromeric heterochromatin at the chromatin boundary

  2022cites this paper
• In Vitro Mapping of Nucleosome Positions at Base‐Pair Resolution Using Ortho‐Phenanthroline

  2022cites this paper
• Structural and dynamic mechanisms of CBF3-guided centromeric nucleosome formation

  2021cites this paper
• Reb1, Cbf1, and Pho4 Bias Histone Sliding and Deposition Away from Their Binding Sites

  2021cites this paper
• CUT&RUN Identifies Centromeric DNA Regions of Rhodotorula toruloides IFO0880.

  2021cites this paper
• A high-resolution protein architecture of the budding yeast genome

  2021cites this paper
• Nucleosomes and Epigenetics from a Chemical Perspective

  2020cites this paper
• What makes a centromere?

  2020cites this paper
• Thermosensitive Nucleosome Editing Reveals the Role of DNA Sequence in Targeted Histone Variant Deposition.

  2020cites this paper
• Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function

  2020cites this paper
• Seeing is believing: our evolving view of kinetochore structure, composition, and assembly.

  2019cites this paper
• RSC-Associated Subnucleosomes Define MNase-Sensitive Promoters in Yeast.

  2019cites this paper
• The Yeast Minichromosome System Consisting of Highly Positioned Nucleosomes in Vivo.

  2019cites this paper
• Chemical map-based prediction of nucleosome positioning using the Bioconductor package nuCpos

  2019cites this paper
• Computational Infrastructures for biomolecular research

  2019cites this paper
• Synergistic Coordination of Chromatin Torsional Mechanics and Topoisomerase Activity.

  2019cites this paper
• Nucleosome Dynamics: a new tool for the dynamic analysis of nucleosome positioning

  2019cites this paper
• The ratio between centromeric proteins CENP-A and CENP-C maintains homeostasis of human centromeres

  2019cites this paper
• Centromeric and ectopic assembly of CENP-A chromatin in health and cancer: old marks and new tracks

  2018influential citation
• Precise genome-wide mapping of single nucleosomes and linkers in vivo

  2018influential citation
• Non-B-Form DNA Is Enriched at Centromeres

  2018influential citation
• NDF, a nucleosome-destabilizing factor that facilitates transcription through nucleosomes

  2018cites this paper
• Bioinformatic Analysis of Nucleosome and Histone Variant Positioning.

  2018cites this paper
• An asymmetric centromeric nucleosome

  2018cites this paper
• Novel genetic tools for probing individual H3 molecules in each nucleosome

  2018cites this paper
• Architecture of the CBF3-Centromere Complex of the Budding Yeast Kinetochore

  2018cites this paper
• A strong structural correlation between short inverted repeat sequences and the polyadenylation signal in yeast and nucleosome exclusion by these inverted repeats

  2018cites this paper
• Characterization and analysis of repetitive centromeres

  2018cites this paper
• Cryo-EM structure of the CBF3-core-Ndc10-DBD complex of the budding yeast kinetochore

  2018cites this paper
• Long-range single-molecule mapping of chromatin accessibility in eukaryotes

  2018cites this paper
• MNase-Sensitive Complexes in Yeast: Nucleosomes and Non-histone Barriers.

  2017cites this paper
• is at all cell cycle points.

  2017influential citation
• Evolving Centromeres and Kinetochores.

  2017cites this paper
• JCB_201608083 607..622

  2017cites this paper
• Human centromeric CENP-A chromatin is a homotypic, octameric nucleosome at all cell cycle points

  2017cites this paper
• Establishing nucleosome architecture and stability at promoters: Roles of pioneer transcription factors and the RSC chromatin remodeler.

  2017cites this paper
• Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives

  2017cites this paper
• Non-B-form DNA structures mark centromeres

  2017cites this paper
• Chromatin dynamics during the cell cycle at centromeres

  2017cites this paper
• Regulation of Centromeric Chromatin

  2017cites this paper
• Genome-wide Mapping of the Nucleosome Landscape by Micrococcal Nuclease and Chemical Mapping.

  2017cites this paper
• Partially Assembled Nucleosome Structures at Atomic Detail.

  2017cites this paper
• Centromere Structure and Function.

  2017cites this paper
• DMS-Seq for In Vivo Genome-wide Mapping of Protein-DNA Interactions and Nucleosome Centers.

  2017cites this paper
• Structural basis for assembly of the CBF3 kinetochore complex

  2017cites this paper
• Remarkable Evolutionary Plasticity of Centromeric Chromatin.

  2017influential citation
• Understanding nucleosome dynamics and their links to gene expression and DNA replication

  2017cites this paper
• Parallel mapping with site-directed hydroxyl radicals and micrococcal nuclease reveals structural features of positioned nucleosomes in vivo

  2017cites this paper
• An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites

  2016cites this paper
• Centromere identity and the nature of the CENP-A-containing nucleosome

  2016cites this paper
• Exploring the roles of chromatin remodelers in regulating chromatin organisation and transcription in Dictyostelium discoideum

  2016cites this paper
• Histone chaperones FACT and Spt6 prevent histone variants from turning into histone deviants.

  2016cites this paper
• Strong nucleosomes of yeasts

  2016influential citation
• Nucleosome dynamics during chromatin remodeling in vivo

  2016cites this paper
• Promiscuous Histone Mis-Assembly Is Actively Prevented by Chaperones.

  2016cites this paper
• Chromatin assembly: Journey to the CENter of the chromosome

  2016cites this paper
• Molecular dynamic simulations of nucleosomes and histone tails: The effects of histone variance and post-translational modification

  2015cites this paper
• Genome-wide profiling of nucleosome sensitivity and chromatin accessibility in Drosophila melanogaster

  2015cites this paper
• Development of haploid inducers in bananas (musa spp.) by modification of centromere specific histone 3 protein

  2015influential citation
• A unique chromatin complex occupies young α-satellite arrays of human centromeres

  2015cites this paper
• Transcription dynamically patterns the meiotic chromosome-axis interface

  2015cites this paper
• Diversity in the organization of centromeric chromatin.

  2015cites this paper
• Asymmetric nucleosomes flank promoters in the budding yeast genome

  2015cites this paper
• The Structural Determinants behind the Epigenetic Role of Histone Variants

  2015cites this paper
• Shearing of the CENP-A dimerization interface mediates plasticity in the octameric centromeric nucleosome

  2015cites this paper
• Chromatin Dynamics in Vivo: A Game of Musical Chairs

  2015cites this paper
• The right place at the right time: chaperoning core histone variants

  2015cites this paper
• CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere

  2015cites this paper
• DNA Topology and Global Architecture of Point Centromeres.

  2015cites this paper
• The Genetic Map Enters Its Second Century

  2015influential citation
• The prenucleosome, a stable conformational isomer of the nucleosome

  2015influential citation
• Inner Kinetochore Protein Interactions with Regional Centromeres of Fission Yeast

  2015influential citation
• CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells

  2015cites this paper
• The budding yeast Centromere DNA Element II wraps a stable Cse4 hemisome in either orientation in vivo

  2014cites this paper
• An integrated overview of spatiotemporal organization and regulation in mitosis in terms of the proteins in the functional supercomplexes

  2014cites this paper
• High-resolution digital profiling of the epigenome

  2014cites this paper
• The centromere: epigenetic control of chromosome segregation during mitosis.

  2014cites this paper