Seasonal Related Multifactorial Control of Pituitary Gonadotropin and Growth Hormone in Female Goldfish: Influences of Neuropeptides and Thyroid Hormone

Abstract

Female reproduction is under multifactorial control of brain-pituitary-peripheral origin. The present study provides information on seasonal changes in circulating LH and GH concentrations, as well as transcript levels for a number of genes involved in the regulation of reproduction and growth in female goldfish. We also provide information on the effects of treatments with GnRH and/or GnIH, and their interaction with T3, at three stages of gonadal recrudescence. Maximum basal concentration of LH was observed at late recrudescence (Spring) while no seasonal changes in basal serum GH levels was detected. Serum LH and GH levels were stimulated by GnRH as expected, depending on the season. GnIH stimulated basal GH concentrations in gonadally regressed fish. GnIH inhibitory action on GnRH-induced LH response was observed in late, but not in mid recrudescence. T3 actions on basal and GnRH-or GnIH-induced GH secretion were generally inhibitory, depending on season. Administration of T3 attenuated GnRH-induced LH responses in mid and late stages of gonadal recrudescence, and the presence of GnIH abolished inhibitory actions of T3 in fish at mid recrudescence. Our results also demonstrated seasonal patterns in basal and GnRH-and/or GnIH-induced transcript levels for ERα, ERβI, FSHR, aromatase, TRαI, TRβ, IGF-I, and Vtg in the liver and ovary. However, there were no clear correlations between changes in transcript levels and circulating levels of LH and GH. The results support the hypothesis that GnRH, GnIH, and T3 are contributing factors in complex reciprocal control of reproduction and growth in goldfish.

Metabolic Changes During Growth and Reproductive Phases in the Liver of Female Goldfish (Carassius auratus)

“…In general, single GnRH injection inhibited metabolic pathways related to reproductive processes, whereas double injection enhanced the pathways related to reproduction at mid recrudescence (Table 4). This is consistent with the observation that single GnRH injection decreased Vtg and IGF-I mRNA levels, which was increased following double injection with GnRH in goldfish at mid recrudescence (Ma et al, 2020b). In the present study, double injection with GnRH also enhanced taurine and hypotaurine metabolism (Figure 8; Table 4).…”

“…The observed higher concentration of tyrosine in regressed, compared to mid and late recrudescence, is correlated with higher circulating thyroid hormones (T3 and T4) in the regressed goldfish (Sohn et al, 1999). Our results combined with observed higher thyroid hormone receptor (TRβ) mRNA level in the regressed female goldfish liver (Ma et al, 2020b), provide further support for the hypothesis that thyroid hormones are essential components of growth response during the regressed gonadal phase in fish. It should be noted that the role of thyroid hormones in the control of growth is widely recognized (Cabello and Wrutniak, 1989;Nelson and Habibi, 2009).…”

“…Accordingly, the metabolic profile following double injection in the heatmap is similar to the control (Figure 8). A similar study in goldfish demonstrated that single but not double injection with GnRH significantly increased circulating GH levels and decreased Erα, ERβ1 TRα and TRβ mRNA liver transcript levels in the regressed female goldfish (Ma et al, 2020b). In the present study, single injection with GnRH significantly altered purine and pyrimidine metabolism due to decreased levels of guanosine, adenosine, uridine, cytidine and inosine and increased levels of hypoxanthine, xanthine and uric acids (Figure 8; Table 4).…”

“…A number of oviparous species, including many fishes, are seasonal breeders and follow cycles of predominantly reproductive and growth phases. Integrated control of reproduction, growth and metabolism is multifactorial, involving neurohormones, the pituitary gonadotropins (LH and FSH), growth hormone (GH), gonadal hormones, and thyroid hormones ( Zohar et al, 2009 ; Yaron, 2011 ; Habibi et al, 2012 ; Plant, 2015 ; Ma et al, 2020a ; Ma et al, 2020b ; Rajeswari et al, 2020 ; Somoza et al, 2020 ; Trudeau and Somoza, 2020 ). Ovarian follicular development starts with the growth of many small early-stage transparent oocytes accumulating neutral lipids in the ooplasm as lipid droplets (early recrudescence).…”

The Role of the Thyroid Axis in Fish

“…Studies have shown that THs may act at the pituitary level to inhibit gonadotropin secretion. Hypothyroid conditions decrease pituitary LH immunoreactivity and LH circulating levels in male recrudescent air-breathing catfish ( 249 ), and, in recrudescent goldfish, administration of T 3 decreases pituitary LH mRNA expression in males ( 251 ) and attenuates GnRH-induced LH secretion in females ( 252 ).…”