The Embryonic Linker Histone H1 Variant of Drosophila, dBigH1, Regulates Zygotic Genome Activation

Pérez-Montero, Salvador; Carbonell, Albert; Morán, Tomás; Vaquero, Alejandro; Azorı́n, Fernando

doi:10.1016/j.devcel.2013.08.011

Cited by 97 publications

(112 citation statements)

References 67 publications

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“…Apparently, the here-tested remodelers are not sufficient to set the linker length observed in vivo or in the context of Drosophila embryo extracts in vitro, suggesting that additional factors are needed. Recently, a new embryonic linker histone H1 variant, dBigH1, was discovered in Drosophila embryos (71). Lack of dBigH1 decreased the nucleosomal repeat length, making dBigH1 a candidate for setting the physiological spacing in concert with remodelers.…”

Section: Discussionmentioning

confidence: 99%

Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density

Lieleg¹,

Ketterer

Nuebler

et al. 2015

Molecular and Cellular Biology

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Arrays of regularly spaced nucleosomes are a hallmark of chromatin, but it remains unclear how they are generated. Recent genome-wide studies, in vitro and in vivo, showed constant nucleosome spacing even if the histone concentration was experimentally reduced. This counters the long-held assumption that nucleosome density determines spacing and calls for factors keeping spacing constant regardless of nucleosome density. We call this a clamping activity. Here, we show in a purified system that ISWI-and CHD1-type nucleosome remodelers have a clamping activity such that they not only generate regularly spaced nucleosome arrays but also generate constant spacing regardless of nucleosome density. This points to a functionally attractive nucleosome interaction that could be mediated either directly by nucleosome-nucleosome contacts or indirectly through the remodelers. Mutant Drosophila melanogaster ISWI without the HAND-SANT-SLIDE (HSS) domain had no detectable spacing activity even though it is known to remodel and slide nucleosomes. This suggests that the role of ISWI remodelers in generating constant spacing is not just to mediate nucleosome sliding; they actively contribute to the attractive interaction. Additional factors are necessary to set physiological spacing in absolute terms.

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Section: Discussionmentioning

confidence: 99%

Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density

Lieleg¹,

Ketterer

Nuebler

et al. 2015

Molecular and Cellular Biology

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“…41,42 Alternatively, the N:C ratio could indirectly control ZGA if it affects other MBT events not addressed in the present study, such as maternal transcript degradation and chromatin modifications, which have also been suggested to regulate ZGA. 43,44 The influence of the N:C ratio on these events remains a question for future work.…”

Section: Discussionmentioning

confidence: 99%

Regulation of zygotic genome activation and DNA damage checkpoint acquisition at the mid-blastula transition

Zhang

Kothari²,

Mullins

et al. 2014

Cell Cycle

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Following fertilization, oviparous embryos undergo rapid, mostly transcriptionally silent cleavage divisions until the mid-blastula transition (MBT), when large-scale developmental changes occur, including zygotic genome activation (ZGA) and cell cycle remodeling, via lengthening and checkpoint acquisition. Despite their concomitant appearance, whether these changes are co-regulated is unclear. Three models have been proposed to account for the timing of (ZGA). One model implicates a threshold nuclear to cytoplasmic (N:C) ratio, another stresses the importance cell cycle elongation, while the third model invokes a timer mechanism. We show that precocious Chk1 activity in pre-MBT zebrafish embryos elongates cleavage cycles, thereby slowing the increase in the N:C ratio. We find that cell cycle elongation does not lead to transcriptional activation. Rather, ZGA slows in parallel with the N:C ratio. We show further that the DNA damage checkpoint program is maternally supplied and independent of ZGA. Although pre-MBT embryos detect damage and activate Chk2 after induction of DNA double-strand breaks, the Chk1 arm of the DNA damage response is not activated, and the checkpoint is nonfunctional. Our results are consistent with the N:C ratio model for ZGA. Moreover, the ability of precocious Chk1 activity to delay pre-MBT cell cycles indicate that lack of Chk1 activity limits checkpoint function during cleavage cycles. We propose that Chk1 gain-of-function at the MBT underlies cell cycle remodeling, whereas ZGA is regulated independently by the N:C ratio.

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“…In vertebrates, several evolutionarily conserved subfamilies of H1 can be distinguished (Talbert et al, 2012) and appear to play both redundant and specific roles during development and cellular differentiation (McBryant et al, 2010). There is accumulating evidence that, in animals, regulation of the proportions of H1 variants with different dynamic behavior in chromatin is involved in controlling the accessibility of DNA to trans-acting factors (Jullien et al, 2010;Shahhoseini et al, 2010;Zhang et al, 2012a;Pérez-Montero et al, 2013;Christophorou et al, 2014).Epigenetic mechanisms, including DNA and histone modifications and active nucleosome remodeling, are major players in translating signals about environmental perturbations into adaptive responses at the transcriptional …”

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confidence: 99%

A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis

et al. 2015

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(A.J.).Linker (H1) histones play critical roles in chromatin compaction in higher eukaryotes. They are also the most variable of the histones, with numerous nonallelic variants cooccurring in the same cell. Plants contain a distinct subclass of minor H1 variants that are induced by drought and abscisic acid and have been implicated in mediating adaptive responses to stress. However, how these variants facilitate adaptation remains poorly understood. Here, we show that the single Arabidopsis (Arabidopsis thaliana) stressinducible variant H1.3 occurs in plants in two separate and most likely autonomous pools: a constitutive guard cell-specific pool and a facultative environmentally controlled pool localized in other tissues. Physiological and transcriptomic analyses of h1.3 null mutants demonstrate that H1.3 is required for both proper stomatal functioning under normal growth conditions and adaptive developmental responses to combined light and water deficiency. Using fluorescence recovery after photobleaching analysis, we show that H1.3 has superfast chromatin dynamics, and in contrast to the main Arabidopsis H1 variants H1.1 and H1.2, it has no stable bound fraction. The results of global occupancy studies demonstrate that, while H1.3 has the same overall binding properties as the main H1 variants, including predominant heterochromatin localization, it differs from them in its preferences for chromatin regions with epigenetic signatures of active and repressed transcription. We also show that H1.3 is required for a substantial part of DNA methylation associated with environmental stress, suggesting that the likely mechanism underlying H1.3 function may be the facilitation of chromatin accessibility by direct competition with the main H1 variants.Linker (H1) histones are conserved and ubiquitous structural components of eukaryotic chromatin required for the stabilization of higher order chromatin structure and are generally thought to restrict DNA accessibility. Interestingly, despite their architectural role, H1 histones were shown to be highly mobile and continuously exchanging among chromatin-binding sites (Raghuram et al., 2009). They are also the most variable of the histones, with numerous nonallelic variants coexisting in the same cell. In vertebrates, several evolutionarily conserved subfamilies of H1 can be distinguished (Talbert et al., 2012) and appear to play both redundant and specific roles during development and cellular differentiation (McBryant et al., 2010). There is accumulating evidence that, in animals, regulation of the proportions of H1 variants with different dynamic behavior in chromatin is involved in controlling the accessibility of DNA to trans-acting factors (Jullien et al., 2010;Shahhoseini et al., 2010;Zhang et al., 2012a;Pérez-Montero et al., 2013;Christophorou et al., 2014).Epigenetic mechanisms, including DNA and histone modifications and active nucleosome remodeling, are major players in translating signals about environmental perturbations into adaptive responses at the transc...

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The Embryonic Linker Histone H1 Variant of Drosophila, dBigH1, Regulates Zygotic Genome Activation

Cited by 97 publications

References 67 publications

Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density

Nucleosome Spacing Generated by ISWI and CHD1 Remodelers Is Constant Regardless of Nucleosome Density

Regulation of zygotic genome activation and DNA damage checkpoint acquisition at the mid-blastula transition

A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis

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