Distinct functions and temporal regulation of methylated histone H3 during early embryogenesis

Mutlu, Beste; Chen, Huei Mei; Gutnik, Silvia; Hall, David H.; Keppler-Ross, Sabine

doi:10.1242/dev.174516

Cited by 15 publications

(32 citation statements)

References 90 publications

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“…2 E, F). As previously reported (48,49), H3K9me2 is barely detectable at fertilization in embryos under control conditions and increases through embryogenesis to be visible by gastrulation in all embryonic nuclei (48,49). H3K9me2 was still not visible in the 2-4 cell stage embryos generated from heat-shocked oocytes dissected from the maternal germline, but by gastrulation and after, the nuclei of embryos from heat-shocked oocytes had significantly higher levels of H3K9me2 ( Fig.…”

supporting

confidence: 83%

Germline activity of the heat shock factor HSF-1 programs the insulin-receptordaf-2inC. elegans

Das¹,

Min²,

Prahlad³

2021

Preprint

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The mechanisms by which maternal stress alters offspring phenotypes remain poorly understood. Here we report that the heat shock transcription factor HSF-1, activated in the C. elegans maternal germline upon stress, epigenetically programs the insulin-like receptor daf-2 by increasing repressive H3K9me2 levels throughout the daf-2 gene. This increase occurs by the recruitment of the C. elegans SETDB1 homolog MET-2 by HSF-1. Increased H3K9me2 levels at daf-2 persist in offspring to downregulate daf-2, activate the C. elegans FOXO ortholog DAF-16 and enhance offspring stress resilience. Thus, HSF-1 activity in the mother promotes the early life programming of the insulin/IGF-1 signaling (IIS) pathway and determines the strategy of stress resilience in progeny.

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supporting

confidence: 83%

Germline activity of the heat shock factor HSF-1 programs the insulin-receptordaf-2inC. elegans

Das¹,

Min²,

Prahlad³

2021

Preprint

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“…Once the embryos hatched and became L1 larvae, concentrated NA22 bacteria were added to the culture. Synchronized embryos were harvested by bleaching after ~64 hours growth when most worms carried one to two embryos, frozen in liquid nitrogen, and stored at −80°C 9,10 .…”

Section: Methodsmentioning

confidence: 99%

Neuronal control of maternal provisioning in response to social cues

Wasson

Harris

Keppler-Ross

et al. 2021

Preprint

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Mothers contribute cytoplasmic components to their progeny in a process called maternal provisioning. Provisioning is influenced by the parental environment, but the molecular pathways that transmit environmental cues from mother to progeny are not well understood. Here we show that in C. elegans, social cues modulate maternal provisioning to regulate gene silencing in offspring. Intergenerational signal transmission depends on a pheromone-sensing neuron and neuronal FMRF (Phe-Met-Arg-Phe)-like peptides. Parental FMRF signaling promotes the deposition of mRNAs for translational components in progeny, which in turn reduces gene silencing. Previous studies had implicated FMRF signaling in short-term responses such as modulated feeding behavior in response to the metabolic state1,2, but our data reveal a broader role, to coordinate energetically expensive processes such as translation and maternal provisioning. This study identifies a new pathway for intergenerational communication, distinct from previously discovered pathways involving small RNAs and chromatin, that links sensory perception to maternal provisioning.

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“…An increase in cell cycle length has been shown to control the nuclear localization of MET2. This histone methyltransferase is responsible for the timely accumulation of H3K9me2, which restricts cellular plasticity during C. elegans embryogenesis (Mutlu et al, 2019). While these examples illustrate cell cycle phase-specific influences on histone modifying enzymes, other mechanisms directly influence the inheritance of histone PTMs during S-phase.…”

Section: Discussionmentioning

confidence: 99%

Mitotic activity shapes stage-specific histone modification profiles during Xenopus embryogenesis

Pokrovsky

Forné

Straub

et al. 2020

Preprint

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Forming an embryo from a zygote poses an apparent conflict for epigenetic regulation. On one hand, the de novo induction of cell fate identities requires the establishment and subsequent maintenance of epigenetic information to harnish developmental gene expression. On the other hand, the embryo depends on cell proliferation, and every round of DNA replication dilutes preexisting histone modifications by incorporation of new unmodified histones into chromatin. Here we investigated the possible relationship between the propagation of epigenetic information and the developmental cell proliferation during Xenopus embryogenesis. We systemically inhibited cell proliferation during the G1/S-transition in gastrula embryos and followed their development until the tadpole stage. Comparing wild-type and cell cycle-arrested embryos, we show that the inhibition of cell proliferation is principally compatible with embryo survival and cellular differentiation. In parallel, we quantified by mass spectrometry the abundance of a large set of histone modification states, which reflects the developmental maturation of the embryonic epigenome. The arrested embryos developed abnormal stage-specific histone modification profiles, in which transcriptionally repressive histone marks were overrepresented. Embryos released from the cell cycle block during neurulation reverted back towards normality on morphological, molecular and epigenetic levels. These results indicate that replicational dilution of histone marks has a strong impact on developmental chromatin maturation. We propose that this influence is strong enough to control developmental decisions, specifically in cell populations that switch between resting and proliferating states such as stem cells.

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Distinct functions and temporal regulation of methylated histone H3 during early embryogenesis

Cited by 15 publications

References 90 publications

Germline activity of the heat shock factor HSF-1 programs the insulin-receptordaf-2inC. elegans

Germline activity of the heat shock factor HSF-1 programs the insulin-receptordaf-2inC. elegans

Neuronal control of maternal provisioning in response to social cues

Mitotic activity shapes stage-specific histone modification profiles during Xenopus embryogenesis

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