Activation of brain steroidogenesis and neurogenesis during the gonadal differentiation in protandrous black porgy, Acanthopagrus schlegelii

Abstract

The early brain development, at the time of gonadal differentiation was investigated using a protandrous teleost, black porgy. This natural model of monosex juvenile fish avoids the potential complexity of sexual dimorphism. Brain neurogenesis was evaluated by histological analyses of the diencephalon, at the time of testicular differentiation (in fish between 90 and 150 days after hatching). Increases in the number of both Nissl-stained total brain cells, and Pcna-immunostained proliferative brain cells were observed in specific area of the diencephalon, such as ventromedialis thalami and posterior preoptic area, revealing brain cell proliferation. qPCR analyses showed significantly higher expression of the radial glial cell marker blbp and neuron marker bdnf. Strong immunohistochemical staining of Blbp and extended cellular projections were observed. A peak expression of aromatase (cyp19a1b), as well as an increase in estradiol (E2 ) content were also detected in the early brain. These data demonstrate that during gonadal differentiation, the early brain exhibits increased E2 synthesis, cell proliferation, and neurogenesis. To investigate the role of E2 in early brain, undifferentiated fish were treated with E2 or aromatase inhibitor (AI). E2 treatment upregulated brain cyp19a1b and blbp expression, and enhanced brain cell proliferation. Conversely, AI reduced brain cell proliferation. Castration experiment did not influence the brain gene expression patterns and the brain cell number. Our data clearly support E2 biosynthesis in the early brain, and that brain E2 induces neurogenesis. These peak activity patterns in the early brain occur at the time of gonad differentiation but are independent of the gonads.

Early life low intensity stress experience modifies acute stress effects on juvenile brain cell proliferation of European sea bass ( D. Labrax )

“…In agreement with previous studies in other teleost species [36][37], a populations of mitotically active cells were found to express the early neuronal marker TUC-4, within Dm, PGZ and VCe M (double-labeled BrdU-TUC-4), or BLBP stem cells (BrdU-BLBP) in PGZ and Dm.…”

“…To determine the phenotype of proliferating cells double immunofluorescence experiments were performed in adjacent sections, using an early neuronal marker, (Turned On After Division, TOAD, TUC-4) and a glial marker brain lipid binding protein (BLBP) [36][37]. …”

Androgen induced cellular proliferation, neurogenesis, and generation of GnRH3 neurons in the brain of mature female Mozambique tilapia

“…On the contrary, Lin et al . 49 showed that estradiol treatment in the early brain development enhanced cellular proliferation and gene expressions of aromatase and radial glial cell marker ( Blbp ) in black porgy indicating a stimulatory effect of estradiol on the proliferation and development of radial glial cells in the fish brain 49 . Research studies reporting the androgen-induced neurogenesis in vertebrates are much less compared to those that reporting neurogenesis induced by oestrogen.…”

Direct and Indirect Effects of Sex Steroids on Gonadotrope Cell Plasticity in the Teleost Fish Pituitary

“…An anti-proliferative effect of E2 was also seen in adult female zebrafish, where the number of proliferating cells labelled with BrdU decreased in several neurogenic brain regions, including the POA ( 214 ). However, opposite effects were observed in juvenile black porgy treated with E2, where levels of brain aromatase and numbers of proliferative cells increased ( 259 ). A significant reduction in brain cell proliferation was observed after treatment with an aromatase inhibitor, while castration did not affect the number of brain cells.…”