Chiffon triggers global histone H3 acetylation and expression of developmental genes in <i>Drosophila</i> embryos

Torres-Zelada, Eliana F.; George, Smitha; Blum, Hannah R.; Weake, Vikki M.

doi:10.1242/jcs.259132

Cited by 6 publications

(8 citation statements)

References 44 publications

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“…Drosophila Gcn5 shares the domains that are common to all Gcn5 homologues, including the PCAF (P300/CBP‐associated factor) domain (73–323 aa), Gcn5‐N‐Acetyltransferase domain (514–598 aa) and bromodomain (717–795 aa), which binds acetylated lysine (Figure 3a) (Carré et al, 2005; Nagy & Tora, 2007). In addition, in Drosophila and other insects, Gcn5 shares a similar domain architecture with the mammalian Gcn5 paralogs that include the metazoan‐specific N‐terminal domain (Torres‐Zelada et al, 2022) (Figure S2, Supplementary file 2).…”

Section: Resultsmentioning

confidence: 98%

“…Although there are four splice isoforms listed for chiffon on FlyBase (Chiffon‐RA, ‐RB, ‐RD and ‐RE) and another gene shares the chiffon promoter but encodes a distinct protein ( Hyls1 ) (Figure 1b), there is no evidence of alternative splicing in chiffon that could account for distinct production of the Chiffon‐A and Chiffon‐B proteins. Instead, uncharacterized translational mechanisms are thought to underly the switch between Chiffon‐A and Chiffon‐B expression (Torres‐Zelada et al, 2022). Chiffon interacts with the histone acetyltransferase Gcn5 and three partner proteins, Ada2b‐PA, Sgf29 and Ada3 to nucleate formation of the CHAT and a schematic illustrating the subunit composition of the Drosophila DDK and CHAT complexes are shown in Figure 1c (Torres‐Zelada et al, 2019; Torres‐Zelada & Weake, 2021).…”

Section: Resultsmentioning

confidence: 99%

“…Gcn5/KAT2A was the first nuclear histone acetyltransferase to be identified, and functions as part of multi‐subunit complexes that have key roles in gene expression and are widely conserved in yeast, Drosophila , plants and mammals (Torres‐Zelada & Weake, 2021). Recently, gene expression profiling of Drosophila embryos revealed that CHAT has an important role in regulating the expression of developmental genes, albeit partially redundant with other Gcn5‐containing complexes (Torres‐Zelada et al, 2022). Intriguingly, there is a switch between the expression of the Chiffon‐A (Cdc7 binding) and Chiffon‐B (CHAT) proteins during the early stages of embryogenesis in Drosophila .…”

Section: Introductionmentioning

confidence: 99%

“…Intriguingly, there is a switch between the expression of the Chiffon‐A (Cdc7 binding) and Chiffon‐B (CHAT) proteins during the early stages of embryogenesis in Drosophila . Chiffon‐A is expressed during and is maternally required for, the early nuclear cycles, similar to Cdc7 (Seller & O'Farrell, 2018; Torres‐Zelada et al, 2022). In contrast, Chiffon‐B only begins to appear in embryos just prior to zygotic genomic activation and is essential for zygotic development but is not maternally required for embryogenesis (Torres‐Zelada et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…Chiffon‐A is expressed during and is maternally required for, the early nuclear cycles, similar to Cdc7 (Seller & O'Farrell, 2018; Torres‐Zelada et al, 2022). In contrast, Chiffon‐B only begins to appear in embryos just prior to zygotic genomic activation and is essential for zygotic development but is not maternally required for embryogenesis (Torres‐Zelada et al, 2022). These data suggest that the unique gene structure of chiffon provides a mechanism in which to temporally separate DNA replication from transcription activation via histone acetylation in developing embryos.…”

Section: Introductionmentioning

confidence: 99%

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The interaction between the Dbf4 ortholog Chiffon and Gcn5 is conserved in Dipteran insect species

George

Blum

Torres-Zelada

et al. 2022

Insect Molecular Biology

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Chiffon is the sole Drosophila ortholog of Dbf4, the regulatory subunit for the cell‐cycle kinase Cdc7 that initiates DNA replication. In Drosophila, the chiffon gene encodes two polypeptides with independent activities. Chiffon‐A contains the conserved Dbf4 motifs and interacts with Cdc7 to form the Dbf4‐dependent Kinase (DDK) complex, which is essential for a specialized form of DNA replication. In contrast, Chiffon‐B binds the histone acetyltransferase Gcn5 to form the Chiffon histone acetyltransferase (CHAT) complex, which is necessary for histone H3 acetylation and viability. Previous studies have shown that the Chiffon‐B region is only present within insects. However, it was unclear how widely the interaction between Chiffon‐B and Gcn5 was conserved among insect species. To examine this, we performed yeast two‐hybrid assays using Chiffon‐B and Gcn5 from a variety of insect species and found that Chiffon‐B and Gcn5 interact in Diptera species such as Australian sheep blowfly and yellow fever mosquito. Protein domain analysis identified that Chiffon‐B has features of acidic transcriptional activators such as Gal4 or VP16. We propose that the CHAT complex plays a critical role in a biological process that is unique to Dipterans and could therefore be a potential target for pest control strategies.

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Section: Resultsmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The interaction between the Dbf4 ortholog Chiffon and Gcn5 is conserved in Dipteran insect species

George

Blum

Torres-Zelada

et al. 2022

Insect Molecular Biology

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Prenatal LPS leads to increases in RAS expression within the PVN and overactivation of sympathetic outflow in offspring rats

Hao,

Long,

Fan

et al. 2024

Hypertens Res

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The renin-angiotensin system (RAS) and the sympathetic nervous system (SNS) are two major blood pressure-regulating systems. The link between the renal and cerebral RAS axes was provided by reflex activation of renal afferents and efferent sympathetic nerves. There is a self-sustaining enhancement of the brain and the intrarenal RAS. In this study, prenatal exposure to lipopolysaccharide (LPS) led to increased RAS activity in the paraventricular nucleus (PVN) and overactivation of sympathetic outflow, accompanied by increased production of reactive oxygen species (ROS) and disturbances between inhibitory and excitatory neurons in PVN. The AT1 receptor blocker losartan and α2 adrenergic receptor agonist clonidine in the PVN significantly decreased renal sympathetic nerve activity (RSNA) and synchronously reduced systolic blood pressure. Prenatal LPS stimulation caused H3 acetylation at H3K9 and H3K14 in the PVN, which suggested that epigenetic changes are involved in transmitting the prenatal adverse stimulative information to the next generation. Additionally, melatonin treatment during pregnancy reduced RAS activity and ROS levels in the PVN; balanced the activity of inhibitory and excitatory neurons in the PVN; increased urine sodium secretion; reduced RSNA and blood pressure. In conclusion, prenatal LPS leads to increased RAS expression within the PVN and overactivation of the sympathetic outflow, thereby contributing to hypertension in offspring rats. Melatonin is expected to be a promising agent for preventing prenatal LPS exposure-induced hypertension.

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Epigenetic inheritance and gene expression regulation in early Drosophila embryos

Ciabrelli,

Atinbayeva,

Pane

et al. 2024

EMBO Rep

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Precise spatiotemporal regulation of gene expression is of paramount importance for eukaryotic development. The maternal-to-zygotic transition (MZT) during early embryogenesis in Drosophila involves the gradual replacement of maternally contributed mRNAs and proteins by zygotic gene products. The zygotic genome is transcriptionally activated during the first 3 hours of development, in a process known as “zygotic genome activation” (ZGA), by the orchestrated activities of a few pioneer factors. Their decisive role during ZGA has been characterized in detail, whereas the contribution of chromatin factors to this process has been historically overlooked. In this review, we aim to summarize the current knowledge of how chromatin regulation impacts the first stages of Drosophila embryonic development. In particular, we will address the following questions: how chromatin factors affect ZGA and transcriptional silencing, and how genome architecture promotes the integration of these processes early during development. Remarkably, certain chromatin marks can be intergenerationally inherited, and their presence in the early embryo becomes critical for the regulation of gene expression at later stages. Finally, we speculate on the possible roles of these chromatin marks as carriers of epialleles during transgenerational epigenetic inheritance (TEI).

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Chiffon triggers global histone H3 acetylation and expression of developmental genes in Drosophila embryos

Cited by 6 publications

References 44 publications

The interaction between the Dbf4 ortholog Chiffon and Gcn5 is conserved in Dipteran insect species

The interaction between the Dbf4 ortholog Chiffon and Gcn5 is conserved in Dipteran insect species

Prenatal LPS leads to increases in RAS expression within the PVN and overactivation of sympathetic outflow in offspring rats

Epigenetic inheritance and gene expression regulation in early Drosophila embryos

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