Arginine Vasotocin and Cortisol Co-regulate Vasotocinergic, Isotocinergic, Stress, and Thyroid Pathways in the Gilthead Sea Bream ()

Overview

Journal Front Physiol

Date 2019 Apr 6

PMID 30949066

Citations 3

Authors

Juan Antonio Martos-Sitcha

Laura Cadiz

Magdalena Gozdowska

Ewa Kulczykowska

Gonzalo Martinez-Rodriguez

Juan Miguel Mancera

Affiliations

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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 () 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 () mRNA levels and increased Avt storage in the pituitary. Avt treatment down-regulated hypothalamic (), suggesting a negative paracrine co-regulation of the HPI axis due to the close location of and adrenocorticotropin hormone (Acth) cells in the anterior pituitary. Furthermore, the up-regulation observed in () suggests their involvement in metabolic and cortisol-related pathways in the hypothalamus. The decrease in isotocin (It) pituitary storage and the up-regulation of 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 gene expression in the absence of variations in (). Finally, both hormonal treatments activated the HPT axis via up-regulation of and down-regulation of . Our results provide evidence for strong interactions among the Avt/It, HPI, and HPT axes of marine teleosts, particularly at the hypothalamic level.

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References

Arends R, Mancera J, Munoz J, Wendelaar Bonga S, Flik G . The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J Endocrinol. 1999; 163(1):149-57. DOI: 10.1677/joe.0.1630149. View

Chatterjee A, Hsieh Y, Yu J . Molecular cloning of cDNA encoding thyroid stimulating hormone beta subunit of bighead carp Aristichthys nobilis and regulation of its gene expression. Mol Cell Endocrinol. 2001; 174(1-2):1-9. DOI: 10.1016/s0303-7207(01)00392-6. View

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

Warne J, Harding K, Balment R . Neurohypophysial hormones and renal function in fish and mammals. Comp Biochem Physiol B Biochem Mol Biol. 2002; 132(1):231-7. DOI: 10.1016/s1096-4959(01)00527-9. View

Mancera J, Laiz Carrion R, Martin del Rio M . Osmoregulatory action of PRL, GH, and cortisol in the gilthead seabream (Sparus aurata L). Gen Comp Endocrinol. 2002; 129(2):95-103. DOI: 10.1016/s0016-6480(02)00522-1. View

Sangiao-Alvarellos S, Laiz-Carrion R, Guzman J, Martin Del Rio M, Miguez J, Mancera J . Acclimation of S aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am J Physiol Regul Integr Comp Physiol. 2003; 285(4):R897-907. DOI: 10.1152/ajpregu.00161.2003. View

Laiz-Carrion R, Martin Del Rio M, Miguez J, Mancera J, Soengas J . Influence of cortisol on osmoregulation and energy metabolism in gilthead seabream Sparus aurata. J Exp Zool A Comp Exp Biol. 2003; 298(2):105-18. DOI: 10.1002/jez.a.10256. View

Bradford C, Fitzpatrick M, Schreck C . Evidence for ultra-short-loop feedback in ACTH-induced interrenal steroidogenesis in coho salmon: acute self-suppression of cortisol secretion in vitro. Gen Comp Endocrinol. 1992; 87(2):292-9. DOI: 10.1016/0016-6480(92)90034-h. View

Han Y, Liao I, Tzeng W, Yu J . Cloning of the cDNA for thyroid stimulating hormone beta subunit and changes in activity of the pituitary-thyroid axis during silvering of the Japanese eel, Anguilla japonica. J Mol Endocrinol. 2004; 32(1):179-94. DOI: 10.1677/jme.0.0320179. View

10.

Huising M, Metz J, van Schooten C, Taverne-Thiele A, Hermsen T, Verburg-van Kemenade B . Structural characterisation of a cyprinid (Cyprinus carpio L.) CRH, CRH-BP and CRH-R1, and the role of these proteins in the acute stress response. J Mol Endocrinol. 2004; 32(3):627-48. DOI: 10.1677/jme.0.0320627. View

11.

Laiz-Carrion R, Guerreiro P, Fuentes J, Canario A, Martin Del Rio M, Mancera J . Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. J Exp Zool A Comp Exp Biol. 2005; 303(7):563-76. DOI: 10.1002/jez.a.183. View

12.

Agirregoitia N, Laiz-Carrion R, Varona A, Martin del Rio M, Mancera J, Irazusta J . Distribution of peptidase activity in teleost and rat tissues. J Comp Physiol B. 2005; 175(6):433-44. DOI: 10.1007/s00360-005-0011-5. View

13.

De Groef B, Van der Geyten S, Darras V, Kuhn E . Role of corticotropin-releasing hormone as a thyrotropin-releasing factor in non-mammalian vertebrates. Gen Comp Endocrinol. 2005; 146(1):62-8. DOI: 10.1016/j.ygcen.2005.10.014. View

14.

Flik G, Klaren P, van den Burg E, Metz J, Huising M . CRF and stress in fish. Gen Comp Endocrinol. 2006; 146(1):36-44. DOI: 10.1016/j.ygcen.2005.11.005. View

15.

Gozdowska M, Kleszczynska A, Sokolowska E, Kulczykowska E . Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp Biochem Physiol B Biochem Mol Biol. 2006; 143(3):330-4. DOI: 10.1016/j.cbpb.2005.12.004. View

16.

Balment R, Lu W, Weybourne E, Warne J . Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol. 2006; 147(1):9-16. DOI: 10.1016/j.ygcen.2005.12.022. View

17.

Sangiao-Alvarellos S, Polakof S, Arjona F, Kleszczynska A, Martin Del Rio M, Miguez J . Osmoregulatory and metabolic changes in the gilthead sea bream Sparus auratus after arginine vasotocin (AVT) treatment. Gen Comp Endocrinol. 2006; 148(3):348-58. DOI: 10.1016/j.ygcen.2006.04.005. View

18.

Moon T, Mommsen T . Vasoactive peptides and phenylephrine actions in isolated teleost hepatocytes. Am J Physiol. 1990; 259(5 Pt 1):E644-9. DOI: 10.1152/ajpendo.1990.259.5.E644. View

19.

Geven E, Verkaar F, Flik G, Klaren P . Experimental hyperthyroidism and central mediators of stress axis and thyroid axis activity in common carp (Cyprinus carpio L.). J Mol Endocrinol. 2006; 37(3):443-52. DOI: 10.1677/jme.1.02144. View

20.

Arjona F, Vargas-Chacoff L, Martin del Rio M, Flik G, Mancera J, Klaren P . The involvement of thyroid hormones and cortisol in the osmotic acclimation of Solea senegalensis. Gen Comp Endocrinol. 2007; 155(3):796-803. DOI: 10.1016/j.ygcen.2007.09.007. View