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Estrogens regulate early embryonic development of the olfactory sensory system via estrogen-responsive glia

Takesono, Aya; Schirrmacher, Paula; Scott, Aaron; Green, Jon M; Lee, Okhyun; Winter, Matthew J; Kudoh, Tetsuhiro; (2022) Estrogens regulate early embryonic development of the olfactory sensory system via estrogen-responsive glia. Development , 149 (1) , Article dev199860. 10.1242/dev.199860. Green open access

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Abstract

Estrogens are well-known to regulate development of sexual dimorphism of the brain; however, their role in embryonic brain development prior to sex-differentiation is unclear. Using estrogen biosensor zebrafish models, we found that estrogen activity in the embryonic brain occurs from early neurogenesis specifically in a type of glia in the olfactory bulb (OB), which we name estrogen-responsive olfactory bulb (EROB) cells. In response to estrogen, EROB cells overlay the outermost layer of the OB and interact tightly with olfactory sensory neurons at the olfactory glomeruli. Inhibiting estrogen activity using an estrogen receptor antagonist, ICI182,780 (ICI), and/or EROB cell ablation impedes olfactory glomerular development, including the topological organisation of olfactory glomeruli and inhibitory synaptogenesis in the OB. Furthermore, activation of estrogen signalling inhibits both intrinsic and olfaction-dependent neuronal activity in the OB, whereas ICI or EROB cell ablation results in the opposite effect on neuronal excitability. Altering the estrogen signalling disrupts olfaction-mediated behaviour in later larval stage. We propose that estrogens act on glia to regulate development of OB circuits, thereby modulating the local excitability in the OB and olfaction-mediated behaviour.

Type: Article
Title: Estrogens regulate early embryonic development of the olfactory sensory system via estrogen-responsive glia
Open access status: An open access version is available from UCL Discovery
DOI: 10.1242/dev.199860
Publisher version: http://dx.doi.org/10.1242/dev.199860
Language: English
Additional information: This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third-party material in this article are included in the Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
Keywords: Endocrine disrupting chemicals, Transgenic zebrafish embryo, Embryogenesis, Olfactory glomerular development, Radial glia progenitor cells, Olfactory-mediated behaviour
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Cell and Developmental Biology
URI: https://discovery-pp.ucl.ac.uk/id/eprint/10195237
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