Abstract
The cyp19a1 gene that encodes aromatase, the only enzyme permitting conversion of C19 aromatizable androgens into estrogens, is present as a single copy in the genome of most vertebrate species, except in teleosts in which it has been duplicated. This study aimed at investigating the brain expression of a cyp19a1 gene expressed in both gonad and brain of Japanese eel, a basal teleost. By means of immunohistochemistry and in situ hybridization, we show that cyp19a1 is expressed only in radial glial cells of the brain and in pituitary cells. Treatments with salmon pituitary homogenates (female) or human chorionic gonadotrophin (male), known to turn on steroid production in immature eels, strongly stimulated cyp19a1 messenger and protein expression in radial glial cells and pituitary cells. Using double staining studies, we also showed that aromatase-expressing radial glial cells exhibit proliferative activity in both the brain and the pituitary. Altogether, these data indicate that brain and pituitary expression of Japanese eel cyp19a1 exhibits characteristics similar to those reported for the brain specific cyp19a1b gene in teleosts having duplicated cyp19a1 genes. This supports the hypothesis that, despite the fact that eels also underwent the teleost specific genome duplication, they have a single cyp19a1 expressed in both brain and gonad. Such data also suggest that the intriguing features of brain aromatase expression in teleost fishes were not gained after the whole genome duplication and may reflect properties of the cyp19a1 gene of ancestral Actinopterygians.
Highlights
In his famous book ‘‘Evolution by Gene Duplication’’, Suzumu Ohno [1] suggested that the large size of the vertebrate genome is the result of whole genome duplications and that such events are major triggers of evolution
Our previous studies indicated that brain aromatase enzymatic activity and cyp19a1 transcript levels were significantly higher in female eels treated with fish pituitary homogenates to induce experimental ovarian development [32,38]
The present study is the first documenting the distribution of cyp19a1 mRNA and protein in the brain of a basal teleost, the Japanese eel belonging to the order Elopomorph
Summary
In his famous book ‘‘Evolution by Gene Duplication’’, Suzumu Ohno [1] suggested that the large size of the vertebrate genome is the result of whole genome duplications and that such events are major triggers of evolution. Ohno’s hypotheses have been largely confirmed and it is accepted that two distinct genome duplication events, known as 1R and 2R, occurred early in vertebrate evolution prior to the fish-tetrapod split [2]. It is believed that a third round of whole genome duplication, referred to as 3R, occurred soon after the emergence of teleost fishes [3,4]. Cyp19a1 that encodes aromatase, the only enzyme able to convert C19 aromatizable androgens into C18 estrogens [6]. As such aromatase plays crucial roles in reproductive and non-reproductive mechanisms in vertebrates [7]. Estrogens produced in the brain, sometimes referred to as neuroestrogens, exhibit neurotrophic and/or neuroprotective functions and are believed to exert strong influences on neuronal development, survival and plasticity according to complex and still partially uncovered mechanisms [10,11,12]
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