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1.
Dev Biol ; 453(2): 180-190, 2019 09 15.
Artigo em Inglês | MEDLINE | ID: mdl-31211947

RESUMO

A major challenge in vertebrate evolution is to identify the gene regulatory mechanisms that facilitated the origin of neural crest cells and placodes from ancestral precursors in invertebrates. Here, we show in lamprey, a primitively jawless vertebrate, that the transcription factor Snail is expressed simultaneously throughout the neural plate, neural plate border, and pre-placodal ectoderm in the early embryo and is then upregulated in the CNS throughout neurogenesis. Using CRISPR/Cas9-mediated genome editing, we demonstrate that Snail plays functional roles in all of these embryonic domains or their derivatives. We first show that Snail patterns the neural plate border by repressing lateral expansion of Pax3/7 and activating nMyc and ZicA. We also present evidence that Snail is essential for DlxB-mediated establishment of the pre-placodal ectoderm but is not required for SoxB1a expression during formation of the neural plate proper. At later stages, Snail regulates formation of neural crest-derived and placode-derived PNS neurons and controls CNS neural differentiation in part by promoting cell survival. Taken together with established functions of invertebrate Snail genes, we identify a pan-bilaterian mechanism that extends to jawless vertebrates for regulating neurogenesis that is dependent on Snail transcription factors. We propose that ancestral vertebrates deployed an evolutionarily conserved Snail expression domain in the CNS and PNS for neurogenesis and then acquired derived functions in neural crest and placode development by recruitment of regulatory genes downstream of neuroectodermal Snail activity. Our results suggest that Snail regulatory mechanisms in vertebrate novelties such as the neural crest and placodes may have emerged from neurogenic roles that originated early in bilaterian evolution.


Assuntos
Evolução Biológica , Lampreias/embriologia , Lampreias/genética , Crista Neural/metabolismo , Neurogênese , Fatores de Transcrição da Família Snail/metabolismo , Animais , Diferenciação Celular/genética , Sobrevivência Celular/genética , Ectoderma/embriologia , Ectoderma/metabolismo , Regulação da Expressão Gênica no Desenvolvimento , Modelos Biológicos , Sistema Nervoso/embriologia , Sistema Nervoso/metabolismo , Neurogênese/genética , Neurônios/citologia , Filogenia , Fatores de Transcrição da Família Snail/genética
2.
Dev Biol ; 428(1): 176-187, 2017 08 01.
Artigo em Inglês | MEDLINE | ID: mdl-28624345

RESUMO

The acquisition of neural crest cells was a key step in the origin of the vertebrate body plan. An outstanding question is how neural crest cells acquired their ability to undergo an epithelial-mesenchymal transition (EMT) and migrate extensively throughout the vertebrate embryo. We tested if differential regulation of classical cadherins-a highly conserved feature of neural crest EMT and migration in jawed vertebrates-mediates these cellular behaviors in lamprey, a basal jawless vertebrate. Lamprey has single copies of the type I and type II classical cadherins (CadIA and CadIIA). CadIIA is expressed in premigratory neural crest, and requires the transcription factor Snail for proper expression, yet CadIA is never expressed in the neural tube during neural crest development, suggesting that differential regulation of classical cadherin expression is not required to initiate neural crest migration in basal vertebrates. We hypothesize that neural crest cells evolved by retention of regulatory programs linking distinct mesenchymal and multipotency properties, and emigrated from the neural tube without differentially regulating type I/type II cadherins. Our results point to the coupling of mesenchymal state and multipotency as a key event facilitating the origin of migratory neural crest cells.


Assuntos
Caderinas/metabolismo , Movimento Celular/fisiologia , Lampreias/embriologia , Crista Neural/embriologia , Fatores de Transcrição da Família Snail/metabolismo , Sequência de Aminoácidos , Animais , Caderinas/genética , Diferenciação Celular/fisiologia , Transição Epitelial-Mesenquimal/fisiologia , Regulação da Expressão Gênica no Desenvolvimento , Crista Neural/citologia , Tubo Neural/metabolismo , Alinhamento de Sequência
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