Eukaryotic Replisome Components Cooperate to Process Histones During Chromosome Replication

Foltman, Magdalena; Evrin, Cécile; Piccoli, Giacomo De; Jones, Richard C.; Edmondson, Rick D.; Katou, Yuki; Nakato, Ryuichiro; Shirahige, Katsuhiko; Labib, Karim

doi:10.1016/j.celrep.2013.02.028

Cited by 177 publications

(246 citation statements)

References 67 publications

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“…We considered several possibilities to explain the apparent simultaneous DNA occupancy of Mcm2-7 and the flanking nucleosome (see the Results), but our data were most consistent with a nucleosome being pulled down together with the immunoprecipitated Mcm2-7 complex. Prior experiments have reported that certain Mcm2-7 subunits directly interact with histone H3 (Ishimi et al 1996), and the Mcm2-7 complex mediates histone contacts with FACT and Asf1 at replication forks (Groth et al 2007;Foltman et al 2013). We propose that the origin-flanking nucleosomes both positionally confine and engage with Mcm2-7 in vivo to facilitate subsequent unwinding of the origin DNA in S phase.…”

Section: Discussionmentioning

confidence: 96%

Genome-wide chromatin footprinting reveals changes in replication origin architecture induced by pre-RC assembly

et al. 2015

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Start sites of DNA replication are marked by the origin recognition complex (ORC), which coordinates Mcm2-7 helicase loading to form the prereplicative complex (pre-RC). Although pre-RC assembly is well characterized in vitro, the process is poorly understood within the local chromatin environment surrounding replication origins. To reveal how the chromatin architecture modulates origin selection and activation, we ''footprinted'' nucleosomes, transcription factors, and replication proteins at multiple points during the Saccharomyces cerevisiae cell cycle. Our nucleotide-resolution protein occupancy profiles resolved a precise ORC-dependent footprint at 269 origins in G2. A separate class of inefficient origins exhibited protein occupancy only in G1, suggesting that stable ORC chromatin association in G2 is a determinant of origin efficiency. G1 nucleosome remodeling concomitant with pre-RC assembly expanded the origin nucleosome-free region and enhanced activation efficiency. Finally, the local chromatin environment restricts the loading of the Mcm2-7 double hexamer either upstream of or downstream from the ARS consensus sequence (ACS).

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Section: Discussionmentioning

confidence: 96%

Genome-wide chromatin footprinting reveals changes in replication origin architecture induced by pre-RC assembly

et al. 2015

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“…Our complex structure may serve for understanding how FACT causes further disruption of nucleosome and histone replacements through cooperation with histone chaperones, such as Asf1, HIRA, and MCM2 (Tan et al 2006;Nakayama et al 2007;Takahata et al 2009;Foltman et al 2013). For instance, hMid-AID and one MCM2 histone-binding domain could simultaneously bind to (H3-H4) 2 without the steric hindrance in the superimposed model (Supplemental Fig.…”

Section: General Implications For Nucleosome Reorganization By Hfactmentioning

confidence: 99%

Integrated molecular mechanism directing nucleosome reorganization by human FACT

et al. 2016

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Facilitates chromatin transcription (FACT) plays essential roles in chromatin remodeling during DNA transcription, replication, and repair. Our structural and biochemical studies of human FACT-histone interactions present precise views of nucleosome reorganization, conducted by the FACT-SPT16 (suppressor of Ty 16) Mid domain and its adjacent acidic AID segment. AID accesses the H2B N-terminal basic region exposed by partial unwrapping of the nucleosomal DNA, thereby triggering the invasion of FACT into the nucleosome. The crystal structure of the Mid domain complexed with an H3-H4 tetramer exhibits two separate contact sites; the Mid domain forms a novel intermolecular β structure with H4. At the other site, the Mid-H2A steric collision on the H2A-docking surface of the H3-H4 tetramer within the nucleosome induces H2A-H2B displacement. This integrated mechanism results in disrupting the H3 αN helix, which is essential for retaining the nucleosomal DNA ends, and hence facilitates DNA stripping from histone.

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“…One possibility is that the pre-RC recruits chromatin regulators to facilitate the removal of nucleosomes around origins. The histone chaperone facilitates chromatin transcription (FACT) was shown to bind histones together with Mcm2-7 and maintain proper levels of nucleosome occupancy at subtelomeric regions (Foltman et al 2013). The mcm2-2A mutation in the amino terminal tail prevents Mcm2-7 from binding histones with FACT, but is dispensable for DNA replication (Foltman et al 2013).…”

Section: Wwwgenomeorgmentioning

confidence: 99%

“…The histone chaperone facilitates chromatin transcription (FACT) was shown to bind histones together with Mcm2-7 and maintain proper levels of nucleosome occupancy at subtelomeric regions (Foltman et al 2013). The mcm2-2A mutation in the amino terminal tail prevents Mcm2-7 from binding histones with FACT, but is dispensable for DNA replication (Foltman et al 2013). We tested whether Mcm2-7 and FACT could regulate changes in nucleosome occupancy from G2/M to G1 by measuring nucleosome occupancy in the mcm2-2A mutant.…”

Section: Wwwgenomeorgmentioning

confidence: 99%

Nucleosome occupancy as a novel chromatin parameter for replication origin functions

et al. 2016

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Eukaryotic DNA replication initiates from multiple discrete sites in the genome, termed origins of replication (origins). Prior to S phase, multiple origins are poised to initiate replication by recruitment of the pre-replicative complex (pre-RC). For proper replication to occur, origin activation must be tightly regulated. At the population level, each origin has a distinct firing time and frequency of activation within S phase. Many studies have shown that chromatin can strongly influence initiation of DNA replication. However, the chromatin parameters that affect properties of origins have not been thoroughly established. We found that nucleosome occupancy in G1 varies greatly around origins across the S. cerevisiae genome, and nucleosome occupancy around origins significantly correlates with the activation time and efficiency of origins, as well as pre-RC formation. We further demonstrate that nucleosome occupancy around origins in G1 is established during transition from G2/M to G1 in a pre-RC-dependent manner. Importantly, the diminished cell-cycle changes in nucleosome occupancy around origins in the orc1-161 mutant are associated with an abnormal global origin usage profile, suggesting that proper establishment of nucleosome occupancy around origins is a critical step for regulation of global origin activities. Our work thus establishes nucleosome occupancy as a novel and key chromatin parameter for proper origin regulation.

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Eukaryotic Replisome Components Cooperate to Process Histones During Chromosome Replication

Cited by 177 publications

References 67 publications

Genome-wide chromatin footprinting reveals changes in replication origin architecture induced by pre-RC assembly

Genome-wide chromatin footprinting reveals changes in replication origin architecture induced by pre-RC assembly

Integrated molecular mechanism directing nucleosome reorganization by human FACT

Nucleosome occupancy as a novel chromatin parameter for replication origin functions

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