Nutrient regulation of somatic growth in teleost fish. The interaction between somatic growth, feeding and metabolism
Graphical abstract
Introduction
The process for achieving somatic growth consumes available nutrient and energy (De Roos et al., 2009; Lukas et al., 2011; Sousa et al., 2010). These elements are obtained from the environment by feeding and transformed by metabolic cellular reactions into cell and tissue components. Thus, in fish as well as in other vertebrates, the growth regulatory network should sense nutrient and energy levels and coordinate actions with feed intake and energy balance regulation as well as other energy consuming process such as reproduction (Blanco, 2020; Canosa et al., 2013; Pérez-Sánchez et al., 2018). Clearly, nutrient levels influence fish growth and this is used in aquaculture-related research to establish the nutritional requirements for culture species (Canada et al., 2019; Conde-Sieira et al., 2016; Gao et al., 2019b; Gómez-Requeni et al., 2012, 2013; Meng et al., 2019; Pérez-Sánchez et al., 2018; Xu et al., 2019; Ye et al., 2017) and/or for assessing the suitability of ingredient replacement (Bertucci et al., 2018; Kousoulaki et al., 2018; Uczay et al., 2019; Yao et al., 2018). Nutrient and diet composition represent one of the most relevant environmental factors influencing the somatic growth regulatory axis in fish (Moriyama et al., 2000). Thus, body growth parameters and the expression levels of genes involved in somatic growth have been used to assess the adequacy of diets and culture conditions (Bertucci et al., 2017c, 2018; Conde-Sieira et al., 2016; Dyer et al., 2004; Gómez-Requeni et al., 2004, 2005, 2012, 2013, 2019; Pérez-Sánchez et al., 2018; Picha et al., 2008; Yom Din et al., 2008). In this way, a detailed understanding of mechanisms by which nutrients are sensed by the organism and influence the metabolic and endocrine regulation of growth performance, would be important for aquaculture industry in designing better and more sustainable formulated diets. In addition, as fish share with other vertebrates the main features in terms of regulation of growth, feeding and metabolism, they could serve as good and practical models for human physiology and disease (Matsui, 2017; Volkoff, 2019). Having this in mind, the present review aims to summarize the current knowledge on somatic growth axis regulation and its interaction with both metabolism and feeding control. The influence of nutrient and nutrient sensing mechanisms on growth axis will be highlighted. In additions, gaps of knowledge will be pointed out in attempt to stimulate future research in those areas.
Section snippets
Somatic growth and growth hormone regulation in fish
The endocrine system that regulates post-natal somatic growth is referred as the somatotropic axis which consist of an ensemble of organs and hormones that includes the hypothalamus and its hypophysiotropic factors; the pituitary gland and the growth hormone (GH); the liver and peripheral tissues and the insulin-like growth factors (IGFs). In addition to growth promoting function, GH contributes to several other functions such as fuel mobilization, gonadal development, osmoregulation, feeding,
Central regulation of food intake
The control of feeding and energy balance is highly comparable between mammals and teleost fish and takes place in the integrative feeding centers of the brain (Delgado et al., 2017; Schwartz and Zeltser, 2013; Sobrino-Crespo et al., 2014; Soengas et al., 2018; Volkoff, 2016, 2019). In mammals, it is very well documented that the feeding center is integrated by several brain nuclei such as medio basal arcuate nucleus (ARC), paraventricular hypothalamic nucleus (PVH), lateral hypothalamic
Nutrient regulation of food intake and GH secretion
As described in the previous section (1. Introduction), somatic growth and food intake are two strongly interrelated processes regulated not only by food availability but also by the quality of food in terms of its nutrient composition. Therefore, one of the most important factors influencing both the appetite-regulating hormones and growth in fish is the macro- and micro-nutrient composition of their diets (Conde-Sieira and Soengas, 2017; MacKenzie et al., 1998). This topic has gained interest
Perspective
As was discussed in previous sections, diet composition impacts in the endocrine growth axis as well as in the endocrine factors regulating food intake. Factors from both systems are involved in the regulation of some other metabolic functions in fish, but a modification in the expression of the components of the growth axis and the axis regulating food intake can certainly lead to a modification in fish somatic growth. In this regard, diets are an important target to modify fish growth through
Concluding remarks
In this review we have summarized our knowledge on somatic growth regulation and its contact points with the control of food intake and energy balance in teleost fish. We have pointed out the effects of macronutrient in these regulatory networks. The nutrient and energy sensing systems serving as nexus among nutrient/energy levels and hormones were briefly describe. In systematic covering of those topics some aspects requiring more attention were also revealed.
Improving our knowledge on these
Declarations of interest
None.
Acknowledgements
Authors would like to acknowledge the financial support and fellowships provided by Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina); Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET, Argentina) and the Emerging Leaders of the Americas Program (ELAP, Canada). Besides, JIB was supported though a Discovery grant granted to Dr Markus Hecker by the National Science and Engineering Research Council (NSERC, Canada).
References (366)
- et al.
Dopaminergic innervation of the rainbow trout pituitary and stimulatory effect of dopamine on growth hormone secretion in vitro
Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
(2000) Amino acids are more important insulinotropins than glucose in a teleost fish, barfin flounder (Verasper moseri)
Gen. Comp. Endocrinol.
(2007)- et al.
Molecular cloning and genomic characterization of novel Leptin-like genes in salmonids provide new insight into the evolution of the Leptin gene family
Gen. Comp. Endocrinol.
(2013) Three new players in energy regulation: preptin, adropin and irisin
Peptides
(2014)- et al.
Effect of dietary macronutrients on the expression of cholecystokinin, leptin, ghrelin and neuropeptide Y in gilthead sea bream (Sparus aurata)
Gen. Comp. Endocrinol.
(2017) - et al.
Anatomical distribution of galanin-like immunoreactivity in the brain and pituitary of teleost fishes
Neurosci. Lett.
(1990) - et al.
Chapter 2 - hypothalamic regulation of anterior pituitary function
- et al.
Combined replacement of fish meal and oil in practical diets for fast growing juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis
Aquaculture
(2007) - et al.
The growth hormone signaling system: insights into coordinating the anabolic and catabolic actions of growth hormone
Gen. Comp. Endocrinol.
(2018) - et al.
Direct actions of macronutrient components on goldfish hepatopancreas in vitro to modulate the expression of ghr-I, ghr-II, igf-I and igf-II mRNAs
Gen. Comp. Endocrinol.
(2017)
Glucose, amino acids and fatty acids directly regulate ghrelin and NUCB2/nesfatin-1 in the intestine and hepatopancreas of goldfish (Carassius auratus) in vitro
Comp. Biochem. Physiol. Mol. Integr. Physiol.
Influence of water salinity on genes implicated in somatic growth, lipid metabolism and food intake in Pejerrey (Odontesthes bonariensis)
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
Growth hormone differentially regulates growth and growth-related gene expression in closely related fish species
Comp. Biochem. Physiol. Mol. Integr. Physiol.
Permissive effect of insulin-like growth factor I (IGF-I) on gonadotropin releasing-hormone action on in vitro growth hormone release
Tissue-specific expression of ghrelinergic and NUCB2/nesfatin-1 systems in goldfish (Carassius auratus) is modulated by macronutrient composition of diets
Comp. Biochem. Physiol., A : Molecular and Integrative Physiology
Ghrelin modulates gene and protein expression of digestive enzymes in the intestine and hepatopancreas of goldfish (Carassius auratus) via the GHS-R1a: possible roles of PLC/PKC and AC/PKA intracellular signaling pathways
Mol. Cell. Endocrinol.
Ghrelin suppresses cholecystokinin (CCK), peptide YY (PYY) and glucagon-like peptide-1 (GLP-1) in the intestine, and attenuates the anorectic effects of CCK, PYY and GLP-1 in goldfish (Carassius auratus)
Horm. Behav.
Hypothalamic nutrient sensing in the control of energy homeostasis
Behav. Brain Res.
Dietary fatty acid composition affects food intake and gut-brain satiety signaling in Senegalese sole (Solea senegalensis, Kaup 1858) larvae and post-larvae
Gen. Comp. Endocrinol.
Social cognition in fishes
Trends Cognit. Sci.
Different strategies of grass carp (Ctenopharyngodon idella) responding to insufficient or excessive dietary carbohydrate
Aquaculture
Improving growth potential in Senegalese sole (Solea senegalensis) through dietary protein
Aquaculture
Cloning, phylogenetic analysis and expression of somatolactin and its receptor in Cichlasoma dimerus: their role in long-term background color acclimation
Gen. Comp. Endocrinol.
Neuroendocrine control of growth hormone in fish
Gen. Comp. Endocrinol.
Effects of cholecystokinin and bombesin on the expression of preprosomatostatin-encoding genes in goldfish forebrain
Regul. Pept.
Characterization of neuropeptide Y expression in the brain of a perciform fish, the sea bass (Dicentrarchus labrax)
J. Chem. Neuroanat.
Peptide YY (PYY) and fish pancreatic peptide Y (PY) expression in the brain of the sea bass (Dicentrarchus labrax) as revealed by in situ hybridization
J. Comp. Neurol.
SIRT1 and other sirtuins in metabolism
Trends Endocrinol. Metabol.
Comparative aspects of GnRH-Stimulated signal transduction in the vertebrate pituitary – contributions from teleost model systems
Mol. Cell. Endocrinol.
Effects of dietary arginine levels and carbohydrate-to-lipid ratios on mRNA expression of growth-related hormones in largemouth bass, Micropterus salmoides
Gen. Comp. Endocrinol.
Leptin receptor-deficient (knockout) medaka, Oryzias latipes, show chronical up-regulated levels of orexigenic neuropeptides, elevated food intake and stage specific effects on growth and fat allocation
Gen. Comp. Endocrinol.
Responses of digestive enzymes of tambaqui (Colossoma macropomum) to dietary cornstarch changes and metabolic inferences
Comp. Biochem. Physiol. Mol. Integr. Physiol.
Carob seed germ meal in diets for meagre (Argyrosomus regius) juveniles: growth, digestive enzymes, intermediary metabolism, liver and gut histology
Aquaculture
6 - intermediary metabolism
Hepatic gene regulation by glucose and polyunsaturated fatty acids: a role for ChREBP
J. Nutr.
Growth hormone receptors in zebrafish (Danio rerio): adult and embryonic expression patterns
Gene Expr. Patterns
Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain
Mol. Cell.
Control of leptin by metabolic state and its regulatory interactions with pituitary growth hormone and hepatic growth hormone receptors and insulin like growth factors in the tilapia (Oreochromis mossambicus)
Gen. Comp. Endocrinol.
Cloning, characterization, and comparative activity of turbot IGF-I and IGF-II
Gen. Comp. Endocrinol.
Correlation of plasma IGF-I concentrations and growth rate in aquacultured finfish: a tool for assessing the potential of new diets
Aquaculture
Evolutionary origin and divergence of the growth hormone receptor family: insight from studies on sea lamprey
Gen. Comp. Endocrinol.
Three forms of gonadotropin-releasing hormone, including a novel form, in a basal salmonid, Coregonus clupeaformis
Biol. Reprod.
Characterization of trout galanin and its distribution in trout brain and pituitary
J. Comp. Neurol.
Irisin: a hope in understanding and managing obesity and metabolic syndrome
Front. Endocrinol.
Centrally administered nesfatin-1 inhibits feeding behaviour and gastroduodenal motility in mice
Neuroreport
Expression of adropin in rat brain, cerebellum, kidneys, heart, liver, and pancreas in streptozotocin-induced diabetes
Mol. Cell. Biochem.
Secretion of prolactin and growth-hormone by teleost pituitaries invitro .2. Effect of salt concentration during long-term organ-culture
J. Comp. Physiol.
Leptin is a metabolic signal to the reproductive system
Endocrinology
Innervation and control of the adenohypophysis by hypothalamic peptidergic neurons in teleost fishes: EM immunohistochemical evidence
Microsc. Res. Tech.
Cloning of somatolactin alpha, beta forms and the somatolactin receptor in Atlantic salmon: seasonal expression profile in pituitary and ovary of maturing female broodstock
Reprod. Biol. Endocrinol.
Cited by (0)
- 1
Centro Oceanográfico de Vigo, Instituto Español de Oceanografía, IEO, Subida a Radio Faro 50, 36,390 Vigo, Spain.