TALE factors use two distinct functional modes to control an essential zebrafish gene expression program

Ladam, Franck; Stanney, William; Donaldson, Ian J.; Yildiz, Ozge; Bobola, Nicoletta; Sagerström, Charles G.

doi:10.7554/elife.36144

Cited by 25 publications

(37 citation statements)

References 91 publications

(165 reference statements)

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“…Many of these sites are also occupied by nucleosomes, consistent with previous reports that Pbx TFs possess pioneer activity (Magnani et al, 2011). While we find maternally deposited TALE TFs bound at genomic elements near genes activated at ZGA, they are also bound near genes active later in development (Ladam et al, 2018), suggesting that TALE TFs may have a dual role. Notably, we further demonstrated that a subset of TALE-occupied sites is associated with nearby binding motifs for the NF-Y TF.…”

Section: Introductionsupporting

confidence: 90%

“…in gastrulation or organogenesis) also act at the ZGA. Accordingly, we recently reported that two TFs of the TALE family (Prep1 and Pbx4) -that were originally defined as cooperating with Hox proteins in the activation of tissue-specific gene expression during organogenesis -actually occupy their genomic binding sites already during maternal stages of zebrafish embryogenesis (Ladam et al, 2018). Many of these sites are also occupied by nucleosomes, consistent with previous reports that Pbx TFs possess pioneer activity (Magnani et al, 2011).…”

Section: Introductionsupporting

confidence: 88%

“…This similarity in phenotypes is likely due to the fact that multiple TALE factors act together in larger protein complexes, which are rendered ineffective when one or more TALE factors are disrupted (reviewed in Merabet and Mann, 2016)). In preliminary experiments we recently observed abnormal anterior development also upon disruption of NF-Y function (Ladam et al, 2018). Here we extend this analysis to directly compare disruption of TALE factors (using the dominant negative PBCAB construct reported previously; (Choe et al, 2002)) to disruption of NF-Y function (using the previously reported NF-YA dominant negative construct; (Mantovani et al, 1994)) and find smaller heads in both cases ( Figure 1A-D).…”

Section: Nf-y and Tale Tfs Are Required For Formation Of Anterior Embmentioning

confidence: 95%

“…Notably, we further demonstrated that a subset of TALE-occupied sites is associated with nearby binding motifs for the NF-Y TF. NF-Y was originally discovered as a ubiquitous basal transcription factor (reviewed in (Dolfini et al, 2012)), but has recently been shown to be maternally deposited in zebrafish, to form protein complexes with TALE TFs and to possess pioneer activity (Ladam et al, 2018;Nardini et al, 2013;Oldfield et al, 2014). Recent work identified NF-Y binding sites near genes activated at ZGA in mouse embryos (Gao et al, 2018;Lu et al, 2016), but NF-Y also binds near many genes acting at later stages of development (Oldfield et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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TALE and NF-Y co-occupancy marks enhancers of developmental control genes during zygotic genome activation in zebrafish

Stanney

Ladam

Donaldson

et al. 2019

Preprint

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Animal embryogenesis is initiated by maternal factors, but zygotic genome activation (ZGA) shifts control to the embryo at early blastula stages. ZGA is thought to be mediated by specialized maternally deposited transcription factors (TFs), but here we demonstrate that NF-Y and TALE -TFs with known later roles in embryogenesis -cooccupy unique genomic elements at zebrafish ZGA. We show that these elements are selectively associated with early-expressed genes involved in transcriptional regulation and possess enhancer activity in vivo. In contrast, we find that elements individually occupied by either NF-Y or TALE are associated with genes acting later in development -such that NF-Y controls a cilia gene expression program while TALE TFs control expression of hox genes. We conclude that NF-Y and TALE have a shared role at ZGA, but separate roles later during development, demonstrating that combinations of known TFs can regulate subsets of key developmental genes at vertebrate ZGA.

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Section: Introductionsupporting

confidence: 90%

Section: Introductionsupporting

confidence: 88%

Section: Nf-y and Tale Tfs Are Required For Formation Of Anterior Embmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

TALE and NF-Y co-occupancy marks enhancers of developmental control genes during zygotic genome activation in zebrafish

Stanney

Ladam

Donaldson

et al. 2019

Preprint

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“…One such candidate factor is NFYA. It has previously been shown that NFYA binds to DNA in combination with TALE factors during zebrafish blastula stages [68], promotes chromatin accessibility and enhances the binding of Oct4, Sox2 and Nanog in embryonic stem cells [69], and establishes open chromatin during mouse ZGA [11]. Future studies will reveal whether NFYA cooperates with Pou5f3, Sox19b and Nanog in transcriptional priming during zebrafish ZGA.…”

Section: Pou5f3 Sox19b and Nanog Establish Chromatin Accessibilitymentioning

confidence: 87%

Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

Pálfy

Schulze

Valen

et al. 2019

Preprint

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In many organisms, early embryonic development is driven by maternally provided factors until the controlled onset of transcription during zygotic genome activation. The regulation of chromatin accessibility and its relationship to gene activity during this transition remains poorly understood. Here, we generated chromatin accessibility maps from genome activation until the onset of lineage specification. During this period, chromatin accessibility increases at regulatory elements. This increase is independent of RNA polymerase II-mediated transcription, with the exception of the hyper-transcribed miR-430 locus. Instead, accessibility often precedes the transcription of associated genes. Loss of the maternal transcription factors Pou5f3, Sox19b, and Nanog, which are known to be required for zebrafish genome activation, results in decreased accessibility at regulatory elements. Importantly, the accessibility of regulatory regions, especially when established by Pou5f3, Sox19b and Nanog, is predictive for future transcription.Our results show that the maternally provided transcription factors Pou5f3, Sox19b, and Nanog open up chromatin and prime genes for activity during zygotic genome activation in zebrafish.

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The TALE never ends: A comprehensive overview of the role of PBX1, a TALE transcription factor, in human developmental defects

et al. 2022

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PBX1 is a highly conserved atypical homeodomain transcription factor (TF) belonging to the TALE (three amino acid loop extension) family. Dimerized with other TALE proteins, it can interact with numerous partners and reach dozens of regulating sequences, suggesting its role as a pioneer factor. PBX1 is expressed throughout the embryonic stages (as early as the blastula stage) in vertebrates. In human, PBX1 germline variations are linked to syndromic renal anomalies (CAKUTHED). In this review, we summarized available data on PBX1 functions, PBX1‐deficient animal models, and PBX1 germline variations in humans. Two types of genetic alterations were identified in PBX1 gene. PBX1 missense variations generate a severe phenotype including lung hypoplasia, cardiac malformations, and sexual development defects (DSDs). Conversely, truncating variants generate milder phenotypes (mainly cryptorchidism and deafness). We suggest that defects in PBX1 interactions with various partners, including proteins from the HOX (HOXA7, HOXA10, etc.), WNT (WNT9B, WNT3), and Polycomb (BMI1, EED) families are responsible for abnormal proliferation and differentiation of the embryonic mesenchyme. These alterations could explain most of the defects observed in humans. However, some phenotype variability (especially DSDs) remains poorly understood. Further studies are needed to explore the TALE family in greater depth.

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TALE factors use two distinct functional modes to control an essential zebrafish gene expression program

Cited by 25 publications

References 91 publications

TALE and NF-Y co-occupancy marks enhancers of developmental control genes during zygotic genome activation in zebrafish

TALE and NF-Y co-occupancy marks enhancers of developmental control genes during zygotic genome activation in zebrafish

Chromatin accessibility established by Pou5f3, Sox19b and Nanog primes genes for activity during zebrafish genome activation

The TALE never ends: A comprehensive overview of the role of PBX1, a TALE transcription factor, in human developmental defects

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