Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp

Abstract

SUMMARYAppetite suppression is a common response to hypoxia in fish that confers significant energy savings. Yet little is known about the endocrine signals involved in the regulation of food intake during chronic hypoxia. Thus, we assessed the impact of chronic hypoxia on food intake, the expression of the potent anorexigenic signal leptin and its receptor (lepr), the mRNA levels of key hypothalamic appetite-regulating genes, and the activity of the hypothalamic-pituitary-interrenal (HPI) axis in common carp, Cyprinus carpio. Fish exposed to 10% O 2 saturation for 8days were chronically anorexic and consumed on average 79% less food than normoxic controls. Hypoxia also elicited gradual and parallel increases in the expression of liver leptin-a-I, leptin-a-II, lepr and erythropoietin, a known hypoxia-responsive gene. In contrast, the liver mRNA levels of all four genes remained unchanged in normoxic fish pair-fed to the hypoxia treatment. In the hypothalamus, expression of the appetite-regulating genes were consistent with an inhibition and stimulation of hunger in the hypoxic and pair-fed fish, respectively, and reduced feed intake led to a decrease in lepr. Although both treatments elicited similar delayed increases in plasma cortisol, they were characterized by distinct HPI axis effector transcript levels and a marked differential increase in pituitary lepr expression. Together, these results show that a reduction in O 2 availability, and not feed intake, stimulates liver leptin-a expression in common carp and suggest that this pleiotropic cytokine is involved in the regulation of appetite and the endocrine stress response during chronic hypoxia.

Food deprivation reduces and leptin increases the amplitude of an active sensory and communication signal in a weakly electric fish

“…Nonetheless, hypoxia and food-deprivation effects on EODa both follow timecourses roughly consistent with the rate at which leptin treatment increased EODa, suggesting the possibility that leptin mediates EODa responses to metabolic state in both cases. Indeed, leptin mediates hypoxia responses in several species of fish (Bernier et al, 2012;Chu et al, 2010;MacDonald et al, 2014), but does so by increasing leptin expression which in turn inhibits feeding. Additional research to determine the endocrine cascades that reduce EODa in hypoxic conditions and during food deprivation will provide a more complete picture of the neuroendocrine mechanisms for managing the energetic costs of EOD production during metabolic stress in E. virescens.…”

Hypoxemia-induced leptin secretion: a mechanism for the control of food intake in diseased fish

“…While it is well established that chronic exposure to environmental hypoxia can reduce food intake in both hypoxia-sensitive and -tolerant fish species (e.g. Chabot & Dutil (1999), Pichavant et al (2001), Bernier & Craig (2005) and Bernier et al (2012)), previous studies have not directly examined the impact of hypoxemia on food intake. Herein, we show that acute infection with C. salmositica is characterized by a positive linear relationship between individual food intake and O 2 -carrying capacity.…”

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 )

“…6), a known lipolytic factor (Sheridan, 1986), while our previous work in tilapia shows LepA suppresses gene expression of hepatic hormone-sensitive and lipoprotein lipases (Baltzegar et al, 2014) suggesting a potentially lipid sparing effect of the hormone in tilapia and perhaps other fishes. As a whole, the data suggest that leptin is a key catabolic factor in tilapia, and perhaps other teleosts, as its production and/or secretion increase in response to various stressors including fasting, acute hyperosmotic challenge, and hypoxia (Baltzegar et al, 2014; Bernier et al, 2012; Fuentes et al, 2012; Kling et al, 2009b) and the hormone acts to mobilize carbohydrates and perhaps other energy substrates.…”

“…Evidence suggests that leptin increases in response to various stressors (e.g. fasting, hypoxia and acute salinity challenge; Baltzegar et al, 2014; Bernier et al, 2012; Kling et al, 2009b) and acts as a potent hyperglycemic factor, in part, through stimulation of glycogenolysis (Baltzegar et al, 2014). Consistent with this action, the preponderance of evidence in fishes indicates that leptin gene expression or circulating leptin rises with fasting when energy stores decline and falls during feeding when fat or carbohydrate stores accumulate as observed in fine flounder, Arctic charr, and rainbow trout (Fuentes et al, 2012; Jorgensen et al, 2013; Kling et al, 2009a).…”