Energy restriction with protein restriction increases basal metabolism and meal-induced thermogenesis in rats

Abstract

Portha. Energy restriction with protein restriction increases basal metabolism and meal-induced thermogenesis in rats. Am J Physiol Regul Integr Comp Physiol 284: R751-R759, 2003. First published November 27, 2002 10.1152/ajpregu.00268.2002We previously observed an increased sympathetic nervous system (SNS) activity that was partly responsible for a defect in the insulin secretion response to glucose after postweaning protein-energy restriction (PER) in female rats. These results, together with other data on low-protein feeding, suggested that a low protein-toenergy ratio (P/E) in the diet could stimulate energy expenditure (EE), but direct measurements of EE have never been reported under conditions of PER. The goal of the present study was thus to quantify the changes induced by PER to body composition, the various parameters of EE, and plasma triiodothyronine levels. PER induced severe growth retardation, but the subcutaneous white and interscapular brown adipose tissue masses were preserved. Basal metabolism, meal-induced thermogenesis, and triiodothyronine levels were increased, but substrate utilization by the working muscles was unaffected. Meal-induced thermogenesis was increased by spontaneous activity in PER rats only. These results suggest that rats adapt to a low P/E in the diet by burning part of their excess nonprotein energy and storing the remaining excess in subcutaneous adipose tissue. malnutrition; brown adipose tissue; white adipose tissue; indirect calorimetry; triiodothyronine; spontaneous activity SYMPATHETIC NERVOUS SYSTEM (SNS) activity and/or the utilization of ingested energy are unchanged or moderately decreased by calorie restriction without protein restriction (12,14,16,25), but increased SNS activity has repeatedly been reported in rats fed a low-protein diet, as evidenced by elevated norepinephrine turnover in the heart and urinary norepinephrine excretion. This increased SNS activity, observed in both young and adult animals, was shown to induce an increase in interscapular brown adipose tissue (IBAT) mass and activity and sometimes in thermogenesis (26,27,34). Therefore, a low protein-to-energy ratio (P/E) in the diet was proposed as an explanation for the above disturbances in SNS activity and in the utilization of the ingested energy in response to a low-protein diet (26). During a recent study concerning the impact of postweaning protein-energy restriction (65% of normal ad libitum daily food intake, with a 5% protein diet) on glucose metabolism, we noted a considerable stimulation of SNS activity that was shown to be partly responsible for reduced glucose-stimulated insulin secretion and resistance of the hepatic glucose production pathway to insulin action (19, 24). These two phenomena were not observed when subjecting rats to energy restriction alone (65% of normal ad libitum daily food intake, with a 15% protein diet) (24). Thus these data also suggest that the impact of protein-energy restriction on SNS activity and metabolism may mainly be due to a low P/E in the diet...

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“…Similar results have been reported in rats when fed unwanted carbohydrate (Curcio et al, 1998;Even et al, 2003). Generally speaking, the dietary protein had a higher SDA coefficient compared to dietary lipid and carbohydrate in studies on fishes (Tandler and Beamish, 1979;Jobling and Davies, 1980;Peres and Oliva-Teles, 2001).…”

The Extracellular Signal–Regulated Kinase Isoform ERK1 Is Specifically Required for In Vitro and In Vivo Adipogenesis

“…We also demonstrated that the increased thermogenic response to feeding was fueled by an increased rate of glucose oxidation. It has been shown that meal-induced elevated thermogenesis may result from a higher insulin sensitivity in peripheral tissues (32)(33)(34), leading to increased glucose oxidation. These data are thus in agreement with the better insulin sensitivity observed in mutant mice.…”

Correlation of serum leptin and insulin levels of pregnant protein-restricted rats with predictive obesity variables

“…Low dietary protein produces hyperphagia (13) accompanied by an increase of basal metabolism (14) and adaptive diet-induced thermogenesis. This diet-induced thermogenesis is associated with increased mass and activity of brown adipose tissue (15), due to the stimulation of sympathetic nervous system (14).…”

“…This diet-induced thermogenesis is associated with increased mass and activity of brown adipose tissue (15), due to the stimulation of sympathetic nervous system (14). Despite elevation of energy expenditure, body fat content increases (13,16), possibly due to positive adaptation that allows part of the excess carbohydrate ingested relative to protein to be stored as lipid (14).…”

“…This diet-induced thermogenesis is associated with increased mass and activity of brown adipose tissue (15), due to the stimulation of sympathetic nervous system (14). Despite elevation of energy expenditure, body fat content increases (13,16), possibly due to positive adaptation that allows part of the excess carbohydrate ingested relative to protein to be stored as lipid (14). The increased sympathetic nervous system activity appears to contribute partly to decreased glucose-stimulated insulin secretion (17), which is compensated by enhanced glucose tolerance and insulin action seen in protein restriction (18)(19)(20).…”