CAF-1-induced oligomerization of histones H3/H4 and mutually exclusive interactions with Asf1 guide H3/H4 transitions among histone chaperones and DNA

Liu, Wallace H.; Roemer, Sarah C.; Port, Alex M.; Churchill, Mair E. A.

doi:10.1093/nar/gkx729

Cited by 7 publications

(2 citation statements)

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“…Its role in promoting nucleosome assembly on nascent DNA strands was first identified in an SV40-based in vitro study (Smith and Stillman 1989). More recent studies found that CAF-1 receives nascent H3-H4 dimers from Asf1, facilitates the dimerization of H3-H4 to form (H3-H4)2 tetramers and deposits them onto the newly replicated DNA through an interaction with PCNA (Shibahara and Stillman 1999;Liu et al 2016Liu et al , 2017. In addition, CAF-1 exhibits a high affinity for the post-translational modification H3K56ac, present on nascent H3-H4 in yeast, suggesting that CAF-1 contributes to the deposition of new histones (Li et al 2008;Masumoto et al 2005).…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal kinetics of CAF-1-dependent chromatin maturation ensures transcription fidelity during S-phase

Chen

MacAlpine

Hartemink

et al. 2023

Preprint

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Proper maintenance of epigenetic information after replication is dependent on the rapid assembly and maturation of chromatin. Chromatin Assembly Complex 1 (CAF-1) is a conserved histone chaperone that deposits (H3-H4)2tetramers as part of the replication-dependent chromatin assembly process. Loss of CAF-1 leads to a delay in chromatin maturation, albeit with minimal impact on steady-state chromatin structure. However, the mechanisms by which CAF-1 mediates the deposition of (H3-H4)2tetramers and the phenotypic consequences of CAF-1-associated assembly defects are not well understood. We used nascent chromatin occupancy profiling to track the spatiotemporal kinetics of chromatin maturation in both wild-type (WT) and CAF-1 mutant yeast cells. Our results show that loss of CAF-1 leads to a heterogeneous rate of nucleosome assembly, with some nucleosomes maturing at near WT kinetics and others exhibiting significantly slower maturation kinetics. The slow-to-mature nucleosomes are enriched in intergenic and poorly transcribed regions, suggesting that transcription-dependent assembly mechanisms can reset the slow-to-mature nucleosomes following replication. Nucleosomes with slow maturation kinetics are also associated with poly(dA:dT) sequences, which implies that CAF-1 deposits histones in a manner that counteracts resistance from the inflexible DNA sequence, promoting the formation of histone octamers as well as ordered nucleosome arrays. In addition, we demonstrate that the delay in chromatin maturation is accompanied by a transient and S-phase specific loss of gene silencing and transcriptional regulation, revealing that the DNA replication program can directly shape the chromatin landscape and modulate gene expression through the process of chromatin maturation.

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Section: Introductionmentioning

confidence: 99%

Spatiotemporal kinetics of CAF-1-dependent chromatin maturation ensures transcription fidelity during S-phase

Chen

MacAlpine

Hartemink

et al. 2023

Preprint

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“…Notably, the ASF1histone complex represents a particular challenge. Firstly, the binding affinity is in the nanomolar range (Liu et al, 2012). Secondly, the binding interface is rather flat, extended (1,360 Å 2 ), and exhibits distant shallow pockets (Agez et al, 2007;English et al, 2006;Natsume et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Design on a Rational Basis of High-Affinity Peptides Inhibiting the Histone Chaperone ASF1

Bakail

Gaubert

Andréani

et al. 2019

Cell Chemical Biology

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Inheritance of Histone (H3/H4): A Binary Choice?

Francis

Sihou

2021

Trends in Biochemical Sciences

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Histones carry information in the form of post-translational modifications (PTMs). For this information to be propagated through cell cycles, parental histones and their PTMs need to be maintained at the same genomic locations. Yet, during DNA replication, every nucleosome in the genome is disrupted to allow passage of the replisome. Recent data have identified histone chaperone activities that are intrinsic components of the replisome and implicate them in maintaining parental histones during DNA replication. We propose that structural and kinetic coordination between DNA replication and replisome-associated histone chaperone activities ensures positional inheritance of histones and their PTMs. When this coordination is perturbed, histones may instead be recycled to random genomic locations by alternative histone chaperones. Controlling Histone InheritanceA well-accepted although largely untested hypothesis is that histone PTMs serve as epigenetic information to regulate gene expression. The information content of histone PTMs depends on their placement at specific genomic locations. For this information to be heritable, the linkage between DNA sequence and modifications must be preserved. Yet, during DNA replication, every nucleosome in the genome is disrupted, and the number of nucleosomes is doubled. Thus, if histone modifications carry epigenetic information, there must be mechanisms to maintain them at specific genomic locations, which we refer to as histone inheritance, and the precision of these mechanisms constrains the memory capacity of histone PTMs (Figure 1, paths 1 and 2). Parental histones can also be recycled through a soluble pool and deposited randomly on nascent DNA (Figure 1, path 3). Recent work has identified histone chaperones that act at DNA replication forks, including those that are part of the DNA replication machinery itself, and described the inheritance patterns of parental histones on the genome. We summarize this work and use it to propose a model for how the fate of parental histones is controlled. HighlightsParental histones can be inherited close to their starting DNA sequence (i.e., with positional memory).Histone chaperone activities intrinsic to the replisome may mediate positional memory.A binary choice may be made for each (H3/H4) 2 between recycling through a soluble pool and redeposition with positional memory.

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CAF-1-induced oligomerization of histones H3/H4 and mutually exclusive interactions with Asf1 guide H3/H4 transitions among histone chaperones and DNA

Cited by 7 publications

References 2 publications

Spatiotemporal kinetics of CAF-1-dependent chromatin maturation ensures transcription fidelity during S-phase

Spatiotemporal kinetics of CAF-1-dependent chromatin maturation ensures transcription fidelity during S-phase

Design on a Rational Basis of High-Affinity Peptides Inhibiting the Histone Chaperone ASF1

Inheritance of Histone (H3/H4): A Binary Choice?

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