Sox8 remodels the cranial ectoderm to generate the ear

Buzzi, Ailin Leticia; Chen, Jingchen; Thiery, Alexandre P; Delile, Julien; Streit, Andrea

doi:10.1073/pnas.2118938119

Cited by 7 publications

(9 citation statements)

References 80 publications

(103 reference statements)

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“…Hybridisation chain reaction v3 (HCR) was carried out as previously described (Buzzi et al, 2022; Choi et al, 2018). Embryos were fixed in 4% PFA for 1h at room temperature, dehydrated in a series of methanol in PBT, and stored overnight at −20°C.…”

Section: Methodsmentioning

confidence: 99%

A gradient border model for cell fate decisions at the neural plate border

Thiery

Buzzi

Hamrud

et al. 2022

Preprint

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The vertebrate neural plate border is a transient territory at the edge of the neural plate containing precursors for all ectodermal derivatives: the neural plate, neural crest, placodes, and epidermis. Elegant functional experiments in a range of vertebrate models have provided an in-depth understanding of gene regulatory interactions within the ectoderm. However, these experiments conducted at tissue level have raised seemingly contradictory models for fate allocation of individual cells. Here, we carry out single cell RNA sequencing of chick ectoderm from primitive streak to neurulation stage, to explore cell state diversity and heterogeneity. We identify and characterise the dynamics of gene modules containing key factors known to regulate ectodermal cell fates, allowing us to model the order in which these fates are specified. Furthermore, we find that genes previously classified as neural plate border specifiers typically exhibit dynamic expression patterns and are biased towards either placodal or neural crest fates. Instead, given its transient and heterogenous characteristics, the neural plate border should be defined based on the co-expression of alternative placodal and neural crest gene modules. Finally, we propose a gradient border model for cell fate choice at the neural plate border, with the probability of cell fate allocation closely tied to the spatiotemporal positioning of cells.

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Section: Methodsmentioning

confidence: 99%

A gradient border model for cell fate decisions at the neural plate border

Thiery

Buzzi

Hamrud

et al. 2022

Preprint

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“…Recent work on otic placode development in chicken embryos (Buzzi et al, 2022) suggests that another of the chondrostean lateral line mechanosensory-restricted transcription factors we identified, Sox8 , could play an even earlier role than Foxg1 . ( Sox8 was expressed in ampullary organs as well as neuromasts in cartilaginous fishes, however, suggesting lineage-specific divergence of expression between cartilaginous and bony vertebrates.)…”

Section: Discussionmentioning

confidence: 93%

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

Minařík

Modrell

Gillis

et al. 2023

Preprint

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In electroreceptive jawed vertebrates, embryonic lateral line placodes give rise to electrosensory ampullary organs as well as mechanosensory neuromasts. Previous reports of shared gene expression suggest that conserved mechanisms underlie electroreceptor and mechanosensory hair cell development and that electroreceptors evolved as a transcriptionally related 'sister cell type' to hair cells. We previously identified only one transcription factor gene, Neurod4, as ampullary organ-restricted in the developing lateral line system of a chondrostean ray-finned fish, the Mississippi paddlefish (Polyodon spathula). The other 16 transcription factor genes we previously validated in paddlefish were expressed in both ampullary organs and neuromasts. Here, we used our published lateral line organ-enriched gene-set (arising from differential bulk RNA-seq in late-larval paddlefish), together with a candidate gene approach, to identify 23 transcription factor genes expressed in the developing lateral line system of a more experimentally tractable chondrostean, the sterlet (Acipenser ruthenus, a small sturgeon), and/or that of paddlefish. Twelve are expressed in both ampullary organs and neuromasts, consistent with conservation of molecular mechanisms. Six are novel electrosensory-restricted transcription factor genes (Irx5, Satb2, Insm1, Sp5, MafA and Rorc), and five are the first-reported mechanosensory-restricted transcription factor genes (Foxg1, Sox8, Isl1, Hmx2 and Rorb). However, as previously reported, Sox8 is expressed in ampullary organs as well as neuromasts in a shark (Scyliorhinus canicula), suggesting the existence of lineage-specific differences between cartilaginous and ray-finned fishes. Overall, our results support the hypothesis that ampullary organs and neuromasts develop via largely conserved transcriptional mechanisms, and identify multiple transcription factors potentially involved in the formation of electrosensory versus mechanosensory lateral line organs.

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“…Recent work on otic placode development in chicken embryos ( Buzzi et al, 2022 ) suggests that another of the chondrostean lateral line mechanosensory-restricted transcription factor genes we identified, Sox8 , could play an even earlier role than Foxg1 . ( Sox8 was expressed in ampullary organs as well as neuromasts in cartilaginous fishes, however, suggesting lineage-specific divergence of expression between cartilaginous and bony vertebrates.)…”

Section: Discussionmentioning

confidence: 93%

“…( Sox8 was expressed in ampullary organs as well as neuromasts in cartilaginous fishes, however, suggesting lineage-specific divergence of expression between cartilaginous and bony vertebrates.) Sox8 in chicken lies upstream of all other transcription factor genes in the otic gene regulatory network, including Foxg1 ( Buzzi et al, 2022 ). Ectopic expression of Sox8 in cranial ectoderm drives the formation of ectopic otic vesicles and neurons ( Buzzi et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…Sox8 in chicken lies upstream of all other transcription factor genes in the otic gene regulatory network, including Foxg1 ( Buzzi et al, 2022 ). Ectopic expression of Sox8 in cranial ectoderm drives the formation of ectopic otic vesicles and neurons ( Buzzi et al, 2022 ). In paddlefish, Sox8 displays a similar expression pattern to Foxg1 in elongating lateral line primordia and neuromasts.…”

Section: Discussionmentioning

confidence: 99%

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Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

Minařík,

Modrell,

Gillis

et al. 2024

Front. Cell Dev. Biol.

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In electroreceptive jawed vertebrates, embryonic lateral line placodes give rise to electrosensory ampullary organs as well as mechanosensory neuromasts. Previous reports of shared gene expression suggest that conserved mechanisms underlie electroreceptor and mechanosensory hair cell development and that electroreceptors evolved as a transcriptionally related “sister cell type” to hair cells. We previously identified only one transcription factor gene, Neurod4, as ampullary organ-restricted in the developing lateral line system of a chondrostean ray-finned fish, the Mississippi paddlefish (Polyodon spathula). The other 16 transcription factor genes we previously validated in paddlefish were expressed in both ampullary organs and neuromasts. Here, we used our published lateral line organ-enriched gene-set (arising from differential bulk RNA-seq in late-larval paddlefish), together with a candidate gene approach, to identify 25 transcription factor genes expressed in the developing lateral line system of a more experimentally tractable chondrostean, the sterlet (Acipenser ruthenus, a small sturgeon), and/or that of paddlefish. Thirteen are expressed in both ampullary organs and neuromasts, consistent with conservation of molecular mechanisms. Seven are electrosensory-restricted on the head (Irx5, Irx3, Insm1, Sp5, Satb2, Mafa and Rorc), and five are the first-reported mechanosensory-restricted transcription factor genes (Foxg1, Sox8, Isl1, Hmx2 and Rorb). However, as previously reported, Sox8 is expressed in ampullary organs as well as neuromasts in a catshark (Scyliorhinus canicula), suggesting the existence of lineage-specific differences between cartilaginous and ray-finned fishes. Overall, our results support the hypothesis that ampullary organs and neuromasts develop via largely conserved transcriptional mechanisms, and identify multiple transcription factors potentially involved in the formation of electrosensory versus mechanosensory lateral line organs.

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Sox8 remodels the cranial ectoderm to generate the ear

Cited by 7 publications

References 80 publications

A gradient border model for cell fate decisions at the neural plate border

A gradient border model for cell fate decisions at the neural plate border

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

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