Activation of the brain-pituitary-gonadotropic axis in the black porgy Acanthopagrus schlegelii during gonadal differentiation and testis development and effect of estradiol treatment

Gen Comp Endocrinol. 2019 Sep 15:281:17-29. doi: 10.1016/j.ygcen.2019.05.008. Epub 2019 May 11.

Abstract

Previous studies revealed an estradiol (E2)-dependent peak in brain activity, including neurosteroidogenesis and neurogenesis in the black porgy during the gonadal differentiation period. The brain-pituitary-gonadotropic axis is a key regulator of reproduction and may also be involved in gonadal differentiation, but its activity and potential role in black porgy during the gonadal differentiation period is still unknown. The present study analyzed the expression of regulatory factors involved in the gonadotropic axis at the time of gonadal differentiation (90, 120, 150 days after hatching [dah]) and subsequent testicular development (180, 210, 300 dah). In agreement with previous studies, expression of brain aromatase cyp19a1b peaked at 120 dah, and this was followed by a gradual increase during testicular development. The expression of gonadotropin subunits increased slightly but not significantly during gonadal differentiation and then increased significantly at 300 dah. In contrast, the expression of brain gnrh1 and pituitary gnrh receptor 1 (gnrhr1) exhibited a pattern with two peaks, the first at 120 dah, during the period of gonadal differentiation, and the second peak during testicular development. Gonad fshr and lhcgr increased during gonadal differentiation period with highest transcript level in prespawning season during testicular development. This suggests that the early activation of brain gnrh1, pituitary gnrhr1 and gths, and gonad gthrs might be involved in the control of gonadal differentiation. E2 treatment increased brain cyp19a1b expression at each sampling time, in agreement with previous studies in black porgy and other teleosts. E2 also significantly stimulated the expression of pituitary gonadotropin subunits at all sampling times, indicating potential E2-mediated steroid feedback. In contrast, no significant effect of E2 was observed on gnrh1. Moreover, treatment of AI or E2 had no statistically significant effect on brain gnrh1 transcription levels during gonadal differentiation. This indicated that the early peak of gnrh1 expression during the gonadal differentiation period is E2-independent and therefore not directly related to the E2-dependent peak in brain neurosteroidogenesis and neurogenesis also occurring during this period in black porgy. Both E2-independent and E2-dependent mechanisms are thus involved in the peak expression of various genes in the brain of black porgy at the time of gonadal differentiation.

Keywords: Brain; Gonadal differentiation; Gonadotropic axis; Teleost; cyp19a1b; gnrh.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aromatase / genetics
  • Aromatase / metabolism
  • Aromatase Inhibitors / pharmacology
  • Brain / metabolism*
  • Estradiol / pharmacology*
  • Female
  • Gene Expression Regulation, Developmental / drug effects
  • Gonadotropins, Pituitary / genetics
  • Gonadotropins, Pituitary / metabolism
  • Male
  • Perciformes / genetics
  • Perciformes / growth & development
  • Perciformes / physiology*
  • Pituitary Gland / metabolism*
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, LHRH / genetics
  • Receptors, LHRH / metabolism
  • Sex Differentiation* / drug effects
  • Testis / drug effects
  • Testis / growth & development*
  • Testis / metabolism

Substances

  • Aromatase Inhibitors
  • Gonadotropins, Pituitary
  • Protein Subunits
  • RNA, Messenger
  • Receptors, LHRH
  • Estradiol
  • Aromatase