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Differential nucleosome organization in human interphase and metaphase chromosomes [Chemical Mapping]

ABSTRACT: Mitosis induces profound changes in chromosome structure, impacting nucleosome organization. Here, we employed chemical mapping to achieve single-base-pair resolution of nucleosome positioning in human interphase and metaphase chromosomes, unveiling distinct organizing principles between the two states. During interphase, we observe greater variability in internucleosome spacing, with a higher abundance of shorter linkers compared to metaphase, reflecting the genome's adaptability in accommodating nucleosome arrays for gene expression. Local analyses further uncover differential nucleosome landscapes at key euchromatin landmarks, including promoters, enhancers, and insulators, in each state. Moreover, we analyzed the relationship between DNA cyclizability and dyad positioning during mitosis. Our results indicate that in metaphase, nucleosomes exhibit significantly higher cyclizability around the dyad, whereas during interphase, nucleosomes more frequently position DNA with higher cyclizability in the nucleosome shoulder near regulatory genomic regions. Together, this study offers novel insights into the intricate interplay between DNA mechanics and nucleosome dynamics during mitosis.

ORGANISM(S): Homo sapiens

PROVIDER: GSE264401 | GEO | 2025/12/17

REPOSITORIES: GEO

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Project description:Javasky E, Shamir I, Gandhi S, Egri S, Sandler O, Rothbart SB, Kaplan N, Jaffe JD, Goren A, and Simon I. Genome Research 2018. Mitosis encompasses key molecular changes including chromatin condensation, nuclear envelope breakdown and reduced transcription levels. Immediately after mitosis, the interphase chromatin structure is reestablished and transcription resumes. The reestablishment of the interphase chromatin requires bookmarking, i.e., the retention of at least partial information during mitosis. Yet, while recent studies demonstrate that chromatin accessibility is generally preserved during mitosis and is only locally modulated, the exact details of the bookmarking process and its components are still unclear. To gain a deeper understanding of the mitotic bookmarking process, we merged proteomics, immunofluorescence, and ChIP-seq approaches to study the mitotic and interphase organization in human cells. We focused on key histone modifications, and employed the HeLa-S3 cells as a model system. Generally, we observed a global concordance between the genomic organization of histone modifications in interphase and mitosis, yet the abundance of the two types of modifications we investigated was different. Whereas histone methylation patterns remain highly similar, histone acetylation patterns show a general reduction while maintaining their genomic organization. In line with a recent study demonstrating that minimal transcription is retained during mitosis, we show that RNA polymerase II does not fully disassociate from the genome, but rather maintains its genomic localization at reduced levels. Next, we followed up on previous studies demonstrating that nucleosome depleted regions (NDRs) become occupied by a nucleosome during mitosis. Surprisingly, we observed that the nucleosome introduced into the NDR during mitosis encompasses a distinctive set of histone modifications, differentiating it from the surrounding nucleosomes. We show that the nucleosomes in the vicinity of the NDR appear to both shift into the NDR during mitosis and undergo deacetylation. HDAC inhibition by the small molecule TSA reverts the deacetylation pattern of the shifted nucleosome. Taken together, our results demonstrate that the epigenomic landscape can serve as a major component of the mitotic bookmarking process, and provide evidence for a mitotic deposition and deacetylation of the nucleosomes surrounding the NDR.

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Differential nucleosome organization in human interphase and metaphase chromosomes [Chemical Mapping]

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