Oligomer formation and G-quadruplex binding by purified murine Rif1 protein, a key organizer of higher-order chromatin architecture

Moriyama, Kenji; Yoshizawa-Sugata, Naoko; Masai, Hisao

doi:10.1074/jbc.ra117.000446

Cited by 41 publications

(60 citation statements)

References 74 publications

(46 reference statements)

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“…We noticed that peptides corresponding to RIF1 were also isolated with nascent DNA but not after the chase, suggesting that RIF1 localizes in proximity of active replisomes ( Figure 1A), consistent with a recent work performed in Drosophila melanogaster (Munden, Rong et al, 2018). Interestingly, it has been proposed that the capacity of RIF1 to associate with G-quadruplexes may underlie its role in the organization of high-order chromatin domains and in the establishment of a replication timing program (Moriyama, Yoshizawa-Sugata et al, 2018). To confirm that RIF1 associates with newly synthesized DNA, we performed iPOND and probed RIF1 by immunoblotting.…”

Section: Rif1 Localizes Near Replisomessupporting

confidence: 90%

“…Since the suppression of RIF1 does not impair DNA synthesis at the level of individual replication forks (Figure 2A and SupFig 1A), we surmised that RIF1 could play a role in the organization of replication factories that is important to limit the accumulation of replication-associated DNA lesions. This is based on several observations demonstrating that RIF1 is involved in nuclear organization (Foti et al, 2016, Moriyama et al, 2018, Yamazaki et al, 2012. Interestingly, in the Foti et al study the authors used conformation capture sequencing (4C-seq) to show the impact of RIF1 impairment on nuclear architecture.…”

Section: Rif1 Depletion Reduces Ipond Pull Down Efficiency Without Afmentioning

confidence: 99%

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The organizer of chromatin topology RIF1 ensures cellular resilience to DNA replication stress

Ribeyre

Lebdy

Patouillard

et al. 2019

Preprint

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Eukaryotic genomes are duplicated from thousands of replication origins that fire sequentially forming a defined spatiotemporal pattern of replication clusters. The importance of the organization of replisomes into functional clusters, also called replication factories, is still poorly understood. Here we identified the multifunctional protein RIF1 as a structural component of replication factories. RIF1 depletion did not impair the velocity of replication forks, neither in basic conditions nor in presence of a molecule that interferes with replication fork progression but increased the frequency of DNA lesions induced in S phase. Isolation of replication-associated proteins from RIF1-depleted cells revealed a major defect in the clustering of replication factors on nascent DNA, without any noticeable impact on DNA synthesis or replisome stability. We found that the changes in replication patterns commonly observed upon RIF1 depletion are induced by DNA replication stress. The data suggest that RIF1 encases replication factories to ensure the organization of replication clusters against chromatin rearrangements induced by DNA replication stress.

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Section: Rif1 Localizes Near Replisomessupporting

confidence: 90%

Section: Rif1 Depletion Reduces Ipond Pull Down Efficiency Without Afmentioning

confidence: 99%

The organizer of chromatin topology RIF1 ensures cellular resilience to DNA replication stress

Ribeyre

Lebdy

Patouillard

et al. 2019

Preprint

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show abstract

“…The six different categories of binding site we have found together form a profile that differs significantly from the binding patterns described for Rif1 in other organisms. S. pombe Rif1 binds sequences with a tendency to form G4 DNA structures . While we generally see no such tendency for S. cerevisiae Rif1 (Fig C and Table EV2), an intriguing possibility is that single stranded DNA exposed by transcription or impaired DNA replication may form G4 DNA that binds Rif1.…”

Section: Discussionmentioning

confidence: 73%

Budding yeast Rif1 binds to replication origins and protects DNA at blocked replication forks

et al. 2018

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Despite its evolutionarily conserved function in controlling DNA replication, the chromosomal binding sites of the budding yeast Rif1 protein are not well understood. Here, we analyse genome‐wide binding of budding yeast Rif1 by chromatin immunoprecipitation, during G1 phase and in S phase with replication progressing normally or blocked by hydroxyurea. Rif1 associates strongly with telomeres through interaction with Rap1. By comparing genomic binding of wild‐type Rif1 and truncated Rif1 lacking the Rap1‐interaction domain, we identify hundreds of Rap1‐dependent and Rap1‐independent chromosome interaction sites. Rif1 binds to centromeres, highly transcribed genes and replication origins in a Rap1‐independent manner, associating with both early and late‐initiating origins. Interestingly, Rif1 also binds around activated origins when replication progression is blocked by hydroxyurea, suggesting association with blocked forks. Using nascent DNA labelling and DNA combing techniques, we find that in cells treated with hydroxyurea, yeast Rif1 stabilises recently synthesised DNA. Our results indicate that, in addition to controlling DNA replication initiation, budding yeast Rif1 plays an ongoing role after initiation and controls events at blocked replication forks.

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“…In this work, we characterized the critical roles of G-quadruplexes in chromatin structures. G-quadruplexes were thought to regulate local chromatin structures through exclusion of nucleosome [37,38], gene transcription [9,55], and co-binding with proteins [56]. However, the relationship between G-quadruplexes and three-dimensional chromosome organization was unknown.…”

Section: Discussionmentioning

confidence: 99%

Integrative characterization of G-Quadruplexes in the three-dimensional chromatin structure

Hou

Zhang

et al. 2019

Epigenetics

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DNA molecules are highly compacted in the eukaryotic nucleus where distal regulatory elements reach their targets through three-dimensional chromosomal interactions. G-quadruplexes, stable four-stranded non-canonical DNA structures, can change local chromatin organization through the exclusion of nucleosomes. However, the relationship between G-quadruplexes and higher-order genome organization remains unknown. Here, we found that G-quadruplexes are significantly enriched at boundaries of topological associated domains (TADs). Architectural protein occupancy, which plays critical roles in the formation of TADs, was highly correlated with the content of G-quadruplexes at TAD boundaries. Moreover, adjacent boundaries containing G-quadruplexes frequently interacted with each other because of the high enrichment of architectural protein binding sites. Similar to CCCTC-binding factor (CTCF) binding sites, G-quadruplexes also showed strong insulation ability in the separation of adjacent regions. Additionally, the insulation ability of CTCF binding sites and TAD boundaries was significantly reinforced by G-quadruplexes. Furthermore, G-quadruplex motifs on different strands were associated with the orientation of CTCF binding sites. These findings suggest a potential role for G-quadruplexes in loop extrusion. The enrichment of transcription factor binding sites (TFBSs) around regulatory elements containing G-quadruplexes led to frequent interactions between regulatory elements containing G-quadruplexes. Intriguingly, more than 99% of G-quadruplexes overlapped with TFBSs. The binding sites of CTCF and cohesin proteins were preferentially located surrounding G-quadruplexes. Accordingly, we proposed a new mechanism of long-distance gene regulation in which G-quadruplexes are involved in distal interactions between enhancers and promoters.

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Oligomer formation and G-quadruplex binding by purified murine Rif1 protein, a key organizer of higher-order chromatin architecture

Cited by 41 publications

References 74 publications

The organizer of chromatin topology RIF1 ensures cellular resilience to DNA replication stress

The organizer of chromatin topology RIF1 ensures cellular resilience to DNA replication stress

Budding yeast Rif1 binds to replication origins and protects DNA at blocked replication forks

Integrative characterization of G-Quadruplexes in the three-dimensional chromatin structure

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