Hypothalamic-Pituitary-Thyroid Axis Crosstalk With the Hypothalamic-Pituitary-Gonadal Axis and Metabolic Regulation in the Eurasian Tree Sparrow During Mating and Non-mating Periods.

Ghulam Nabi,Xuelu Liu,Chuan Jiang,Yanfeng Sun,Yinchao Hao,Yang Wang,Dongming Li,Yuefeng Wu,Juyong Li

doi:10.3389/fendo.2020.00303

Ghulam Nabi, Xuelu Liu + Show 7 more

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https://doi.org/10.3389/fendo.2020.00303

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Abstract

Reproduction is an energetically costly phenomenon. Therefore, to optimize reproductive success, male birds invest enough energetic resources for maintaining well-developed testes. The hypothalamic–pituitary–thyroid (HPT) axis in birds can crosstalk with the hypothalamic–pituitary–gonadal (HPG) axis, thus orchestrating both the reproduction and metabolism. However, until now, how the free-living birds timely optimize both the energy metabolism and reproduction via HPT-axis is not understood. To uncover this physiological mechanism, we investigated the relationships among body mass, testis size, plasma hormones including thyroid-stimulating hormone (TSH), thyroxine (T4), triiodothyronine (T3), metabolites including glucose (Glu), triglyceride (TG), total cholesterol (TC), uric acid (UA), diencephalon mRNA expressions of type 2 (Dio2) and 3 (Dio3) iodothyronine deiodinase enzymes, thyrotropin-releasing hormone (TRH), thyroid-stimulating hormone (TSH), gonadotropin-releasing hormone I (GnRH-I), and gonadotropin-inhibitory hormone (GnIH) in a male Eurasian tree sparrow (ETS, Passer montanus). We found significantly larger testis size; elevated diencephalon Dio2 and TRH mRNA expressions, plasma T3, and UA levels; and significantly lowered Glu, TG, and TC levels during mating relative to the non-mating stages in male ETSs. However, Dio3, TSH, GnRH-I, and GnIH mRNA expression did not vary with the stage. Furthermore, life-history stage dependent variation in plasma T3 had both direct effects on the available energy substrates and indirect effects on body mass and testis size, indicating a complex regulation of metabolic pathways through the HPT- and HPG-axes. The identified differences and relationships in mRNA expression, plasma T3 and metabolites, and testis size in male ETSs contribute to our understanding how free-living birds adjust their molecular, endocrinal, and biochemical features to orchestrate their reproductive physiology and metabolism for the maintenance of well-developed testes.

Highlights

The hypothalamic–pituitary–thyroid (HPT) axis in both birds and other vertebrates appears to have similar functions in general [1]
The increase of thyrotropin-releasing hormone (TRH) in the hypothalamus stimulates the production of thyroid-stimulating hormone (TSH) in the pars distalis [6], which further acts on the thyroid glands to secrete T3 and T4 Thyroid hormones (THs) [1, 6]
Among the correlation results of 17 measured variables (Figure 1), plasma T3 levels positively correlated with diencephalon TRH mRNA expression (ρ = 0.641), plasma uric acid (UA) levels (ρ = 0.638), and testis size (ρ = 0. 639), respectively

Summary

Introduction

The hypothalamic–pituitary–thyroid (HPT) axis in both birds and other vertebrates appears to have similar functions in general [1]. Thyroid hormones (THs) are considered as essential biomarkers of an animal energy expenditure [2]. The activation of thyroid signaling modulates energy expenditure through both the central and peripheral pathways [3]. The increase of thyrotropin-releasing hormone (TRH) in the hypothalamus stimulates the production of thyroid-stimulating hormone (TSH) in the pars distalis [6], which further acts on the thyroid glands to secrete T3 and T4 THs [1, 6]. HPT-axis in birds regulates the basal metabolic rate (BMR) and several plasma metabolic parameters [7, 8]. The central molecular and cellular mechanisms regulating seasonality and metabolic adjustment to photoperiod are poorly understood [9]

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