Abstract
In teleosts, a complex interaction between several endocrine axes modulates physiological functions related to metabolism, stress, and osmoregulation. Although many studies in fish underline the interconnection between the hypothalamic–pituitary–interrenal (HPI) and hypothalamic–pituitary–thyroid (HPT) endocrine axes, their relationship with the vasotocinergic and isotocinergic systems remains unknown. The aim of the present study is therefore to shed light on the potential cross-regulations between HPT, HPI, and the vasotocinergic and isotocinergic axes in gilthead sea bream (Sparus aurata) at hypothalamic, hypophyseal, and plasma levels. Sea breams were administered with intraperitoneal slow-release implants containing different doses of vasotocin (the active peptide in vasotocinergic system) or cortisol (the last component of HPI axis). Plasma osmolality was higher in active neuropeptides vasotocin (Avt)-treated fish, indicating an osmoregulatory function of this hormone. Low concentrations of Avt increased hypothalamic arginine vasotocin precursor (avt) mRNA levels and increased Avt storage in the pituitary. Avt treatment down-regulated hypothalamic arginine vasotocin receptor v1a-type (avtrv1a), suggesting a negative paracrine co-regulation of the HPI axis due to the close location of avtrv1a and adrenocorticotropin hormone (Acth) cells in the anterior pituitary. Furthermore, the up-regulation observed in arginine vasotocin receptor v2-type (avtrv2) suggests their involvement in metabolic and cortisol-related pathways in the hypothalamus. The decrease in isotocin (It) pituitary storage and the up-regulation of it receptor, observed in the Avt-treated group, reinforce the idea of an interconnection between the vasotocinergic and isotocinergic systems. Cortisol and Avt administration each inhibited the HPI axis, down-regulating crh gene expression in the absence of variations in corticotropin releasing hormone binding protein (crhbp). Finally, both hormonal treatments activated the HPT axis via up-regulation of trh and down-regulation of thrb. Our results provide evidence for strong interactions among the Avt/It, HPI, and HPT axes of marine teleosts, particularly at the hypothalamic level.
Highlights
The endocrine system is considered a complex net of interconnected pathways, and establishing the relevance of these pathways is critical for a correct understanding of their putative relationships
The active neuropeptides vasotocin (Avt) and It content in the plasma and pituitary gland were determined using high-performance liquid chromatography (HPLC) with fluorescence detection, preceded by solid-phase extraction (SPE) based on Gozdowska et al (2006) and MartosSitcha et al (2013b)
There were no variations in avt expression during the experiment, whereas it mRNA levels were significantly higher at day 3 posttreatment, when compared to non-treated fish
Summary
The endocrine system is considered a complex net of interconnected pathways, and establishing the relevance of these pathways is critical for a correct understanding of their putative relationships. The hypothalamus–pituitary–interrenal (HPI) axis is activated in a coordinated manner leading to the release of cortisol (Wendelaar Bonga, 1997). The release of cortisol is controlled by the hypothalamic corticotrophin-releasing hormone (Crh) and the Crh binding protein (Crhbp). Crh stimulates the release of the adrenocorticotropin hormone (Acth), which is cleaved from the precursor protein proopiomelanocortin (Pomc), produced in adenohypophyseal corticotroph cells. Acth activates cortisol biosynthesis and releases in the interrenal cells dispersed throughout the head kidney (Wendelaar Bonga, 1997; Flik et al, 2006; Aluru and Vijayan, 2008; Bernier et al, 2009). Crhbp is considered an antagonist of the Crh function, due to the higher affinity of Crh for Crhbp than for Crh receptors (Huising et al, 2004)
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