Abstract
Aromatase, the key enzyme responsible for estrogen biosynthesis, is present in the brain of all vertebrates. Much evidence has accumulated that aromatase is highly and exclusively expressed in proliferating mature radial glial cells in the brain of teleost fish even in adulthood, unlike in other vertebrates. However, the physiological significance of this expression remains unknown. We recently found that aromatase is female-specifically expressed in the optic tectum of adult medaka fish. In the present study, we demonstrated that, contrary to the accepted view of the teleost brain, female-specific aromatase-expressing cells in the medaka optic tectum represent a transient subset of post-proliferative immature radial glial cells in the neural stem cell lineage. This finding led us to hypothesize that female-specific aromatase expression and consequent estrogen production causes some sex difference in the life cycle of tectal cells. As expected, the female tectum exhibited higher expression of genes indicative of cell proliferation and radial glial maturation and lower expression of an anti-apoptotic gene than did the male tectum, suggesting a female-biased acceleration of the cell life cycle. Complicating the interpretation of this result, however, is the additional observation that estrogen administration masculinized the expression of these genes in the optic tectum, while simultaneously stimulating aromatase expression. Taken together, these results provide evidence that a unique subpopulation of neural stem cells female-specifically express aromatase in the optic tectum and suggest that this aromatase expression and resultant estrogen synthesis have an impact on the life cycle of tectal cells, whether stimulatory or inhibitory.
Highlights
Aromatase, the key steroidogenic enzyme responsible for the conversion of androgens to estrogens, is present in the brain of all classes of vertebrates
Studies in various teleost species have shown that aromatase-expressing cells in the brain express glial fibrillary acidic protein (Gfap), which is a canonical marker of mature radial glial cells in teleosts, and proliferating cell nuclear antigen (Pcna), which is an established proliferation marker [6,7,12,13,14]
This concept has been repeatedly verified by analyzing the forebrain, including the preoptic area and hypothalamus, but no studies have addressed the property of aromatase-expressing cells in the optic tectum
Summary
The key steroidogenic enzyme responsible for the conversion of androgens to estrogens, is present in the brain of all classes of vertebrates. There is accumulating evidence that aromatase plays integral roles in the process of brain sexual differentiation in mammals and birds. This is best exemplified in perinatal male rodents, where extremely high levels of aromatase activity are transiently induced in the brain, and testosterone secreted from the testis is converted to estradiol-17β (E2) by the action of brain aromatase to organize male-type neural circuitry [1,2,3]. In the teleost brain, aromatase is expressed exclusively in radial glial cells, whereas neuronal cells are its primary source in the brain of other vertebrates [6,7,8,9]. It is generally accepted that aromatase-expressing cells in the teleost brain are proliferating mature radial glial cells
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