An Astyanax mexicanus mao knockout line uncovers the developmental roles of monoamine homeostasis in fish brain

An Astyanax mexicanus mao knockout line uncovers the developmental roles of monoamine homeostasis in fish brain

Monoaminergic systems are conserved in vertebrates, yet they present variations in neuroanatomy, genetic components and functions across species. MonoAmine Oxidase, or MAO, is the enzyme responsible for monoamine degradation. While mammals possess two genes, MAO‐A and MAO‐B, fish possess one single...

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Bibliographic Details
Published in:Development, growth & differentiation Vol. 65; no. 9; pp. 517 - 533
Main Authors: Alunni, Alessandro, Pierre, Constance, Torres‐Paz, Jorge, Clairet, Natacha, Langlumé, Auriane, Pavie, Marie, Escoffier‐Pirouelle, Thomas, Leblanc, Michael, Blin, Maryline, Rétaux, Sylvie
Format: Journal Article
Language:English
Published: Japan Wiley Subscription Services, Inc 01-12-2023
Wiley
Subjects:
Amine oxidase (flavin-containing)
Amines - pharmacology
Anatomy
Animals
Astyanax mexicanus
Brain - metabolism
Brain architecture
Cell cycle
CRISPR
dopamine
Dopamine receptors
Fertilization
Fishes - metabolism
Genetic diversity
Homeostasis
Hypothalamus
Life Sciences
Locomotion
Mammals - metabolism
monoamine oxidase
Monoamine Oxidase - genetics
Monoamine Oxidase - metabolism
Monoamine Oxidase - pharmacology
Neural stem cells
Neurons
proliferation
Serotonin
Serotonin - metabolism
Serotonin - pharmacology
Telencephalon
serotonin
proliferation
cell cycle
dopamine
monoamine oxidase
locomotion
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Summary:Monoaminergic systems are conserved in vertebrates, yet they present variations in neuroanatomy, genetic components and functions across species. MonoAmine Oxidase, or MAO, is the enzyme responsible for monoamine degradation. While mammals possess two genes, MAO‐A and MAO‐B, fish possess one single mao gene. To study the function of MAO and monoamine homeostasis on fish brain development and physiology, here we have generated a mao knockout line in Astyanax mexicanus (surface fish), by CRISPR/Cas9 technology. Homozygote mao knockout larvae died at 13 days post‐fertilization. Through a time‐course analysis, we report that hypothalamic serotonergic neurons undergo fine and dynamic regulation of serotonin level upon loss of mao function, in contrast to those in the raphe, which showed continuously increased serotonin levels – as expected. Dopaminergic neurons were not affected by mao loss‐of‐function. At behavioral level, knockout fry showed a transient decrease in locomotion that followed the variations in the hypothalamus serotonin neuronal levels. Finally, we discovered a drastic effect of mao knockout on brain progenitors proliferation in the telencephalon and hypothalamus, including a reduction in the number of proliferative cells and an increase of the cell cycle length. Altogether, our results show that MAO has multiple and varied effects on Astyanax mexicanus brain development. Mostly, they bring novel support to the idea that serotonergic neurons in the hypothalamus and raphe of the fish brain are different in nature and identity, and they unravel a link between monoaminergic homeostasis and brain growth. Our analysis of brain development in mao knockout larvae of the fish Astyanax mexicanus shows that MAO has multiple and varied effects. Our results bring novel support to the idea that serotonergic neurons in the hypothalamus and raphe of the fish brain are different in nature and identity, and they unravel a link between monoaminergic homeostasis and brain growth.
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content type line 23
ISSN:0012-1592
1440-169X
DOI:10.1111/dgd.12896