Open AccessEstrogens regulate early embryonic development of the olfactory sensory system via estrogen-responsive glia
Author(s) -
Aya Takesono,
Paula Schirrmacher,
Aaron Scott,
Jon M. Green,
Okhyun Lee,
Matthew J. Winter,
Tetsuhiro Kudoh,
Charles R. Tyler
Publication year - 2022
Publication title -
development
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 0.15
H-Index - 36
eISSN - 1477-9129
pISSN - 0950-1991
DOI - 10.1242/dev.199860
Subject(s) - biology , neurogenesis , olfactory bulb , estrogen , synaptogenesis , olfactory system , medicine , estrogen receptor , endocrinology , olfaction , neuroscience , embryonic stem cell , microbiology and biotechnology , central nervous system , biochemistry , genetics , cancer , breast cancer , gene
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.