Nutritional state modulates growth hormone-stimulated lipolysis

Abstract

Growth hormone (GH) regulates several processes in vertebrates, including two metabolically disparate processes: promotion of growth, an anabolic action, and mobilization of stored lipid, a catabolic action. In this study, we used hepatocytes isolated from continuously fed and long-term (4weeks) fasted rainbow trout (Oncorhynchus mykiss) as a model to investigate the mechanistic basis of the anabolic and catabolic actions of GH. Our hypothesis was that nutritional state modulates the lipolytic responsiveness of cells by adjusting the signal transduction pathways to which GH links. GH stimulated lipolysis as measured by increased glycerol release in both a time- and concentration-related manner from cells of fasted fish but not from cells of fed fish. Expression of mRNAs that encode the lipolytic enzyme hormone-sensitive lipase (HSL), HSL1 and HSL2, also was stimulated by GH in cells from fasted fish and not in cells from fed fish. Activation of the signaling pathways that mediate GH action also was studied. In cells from fed fish, GH activated the JAK-STAT, PI3K-Akt, and ERK pathways, whereas in cells from fasted fish, GH activated the PLC/PKC and ERK pathways. In hepatocytes from fasted fish, blockade of PLC/PKC and of the ERK pathway inhibited GH-stimulated lipolysis and GH-stimulated HSL mRNA expression, whereas blockade of JAK-STAT or of the PI3K-Akt pathway had no effect on lipolysis or HSL expression stimulated by GH. These results indicate that during fasting GH activates the PLC/PKC and ERK pathways resulting in lipolysis but during periods of feeding GH activates a different complement of signal elements that do not promote lipolysis. These findings suggest that the responsiveness of cells to GH depends on the signal pathways to which GH links and helps resolve the growth-promoting and lipid catabolic actions of GH.

Effect of fasting and feeding on growth, intestinal morphology and enteroendocrine cell density in Rhamdia quelen juveniles

“…This fact, commonly observed in nature, is considered to be a survival process for many species of fish in situations of food deprivation (negative energy period), using different endocrine responses to prolong energy homeostasis (Silverstein & Plysetskaya, ; Wang et al., ; Won & Borski, ). During these particular metabolic states, it is known that ghrelin, NPY and growth hormone (GH) are involved in lipolytic catabolism to direct the energy of endogenous reserves to maintain basal metabolic processes instead of growth (Bergan, Kittilson & Sheridan, ; Moro et al., ; Rodrigues, Gominho‐Rosa, Cargnin‐Ferreira, de Francisco & Fracalossi, ; Won & Borski, ). This fact was particularly reported in R. quelen juveniles subjected to fasting, in which a significant increase in GH expression and decrease in liver glycogen, glucose and triglycerides to maintain constant plasma glucose and amino acids levels was observed (Barcellos, Marqueze, Trapp, Quevedo & Ferreira, ; Menezes et al., ).…”

Seasonal response of ghrelin, growth hormone, and insulin-like growth factor I in the free-ranging Florida manatee (Trichechus manatus latirostris)

“…alterations in food intake, body weight, fat content, and hormonal functions (Florant and Healy, 2012). Metabolic hormones such as ghrelin, growth hormone (GH), and insulin-like growth factor (IGF)-I function to regulate tissue-specific energy allocation and together link growth physiology, developmental age, energy balance (the amount of calories consumed versus metabolized and stored), and nutritional status (negative [fasting] or positive nutrient intake) in domestic animals (Bergan et al, 2015;Breier, 1999;Cammisotto et al, 2010;Castaneda et al, 2010;Lawrence and Fowler, 1997).…”

“…The increase of ghrelin during fasting or reduced nutrient intake stimulates the release of GH, fat oxidation, and food intake, and inhibits body weight gain and adiposity (Tschop et al, 2000). Growth hormone regulates energy deposition and mobilization through its direct action on adipose tissue (Bergan et al, 2015; Breier, 1999). During energy deficiency or periods of low nutritional status, GH stimulates lipolysis and inhibits lipogenesis (Bergan et al, 2015).…”

“…Growth hormone regulates energy deposition and mobilization through its direct action on adipose tissue (Bergan et al, 2015; Breier, 1999). During energy deficiency or periods of low nutritional status, GH stimulates lipolysis and inhibits lipogenesis (Bergan et al, 2015). The mobilization of fat from adipose tissue, or lipolysis, provides energy for maintenance (Vijayakumar et al, 2010).…”

The response of gene expression associated with intramuscular fat deposition in the longissimus dorsi muscle of Simmental × Yellow breed cattle to different energy levels of diets

“…The GH is a peptide hormone that has important functions in regulating fat metabolism. In fat metabolism, GH epromotes lipolysis and fatty acid oxidation (Bergan, Kittilson, & Sheridan, 2015), and inhibites lipogenesis (Cordoba-Chacon et al, 2015). Dietary energy level can dramatically alter serum GH concentration (Houseknecht et al, 1988), but not well GH gene expression in Simmental × Yellow breed cattle.…”