Effects of dietary polyunsaturated fatty acids on mitochondrial metabolism in mammalian hibernation

Abstract

SUMMARYThirteen-lined ground squirrels (Spermophilus tridecemlineatus) were fed one of four isocaloric, isolipemic diets containing 16, 22, 35 or 55 mg linoleic acid (18:2n-6) per gram. Mitochondrial properties were compared between hibernating and summer active states, and between diet groups. As in other studies, state 3 respiration was significantly reduced in hibernation, but only in animals fed the 22 mg g -1 18:2 diet. In the other diet groups, there was no difference in state 3 respiration between the hibernating and summer active groups. In the 22 mg g -1 18:2 diet group, there was no difference in mitochondrial proton conductance between hibernating and summer active animals, again in agreement with earlier studies. However, for all other diet groups, mitochondrial proton conductance was significantly reduced during hibernation. Mitochondrial phospholipid fatty acids changed significantly with hibernation, including increases in unsaturation indices and n-6/n-3, but no differences were found among diet groups. Mitochondrial proton conductance in hibernation showed a positive correlation with the content of linoleic acid (18:2) and arachidonic acid (20:4) in mitochondrial phospholipids. Lipid peroxidation was higher in mitochondria from hibernating animals, probably due to higher unsaturation, but there was no effect of dietary 18:2 on this pattern. Despite the dietary effects on mitochondrial metabolism, all animals hibernated with no differences in bout durations, body temperatures or whole-animal metabolic rates among the diet groups. The reduced mitochondrial proton leak in the 15, 35 and 55 mg g -1 18:2 diet groups might compensate for the inability to suppress respiration, permitting whole-animal energy savings over the hibernation season.

Regulation of succinate-fueled mitochondrial respiration in liver and skeletal muscle of hibernating thirteen-lined ground squirrels

“…With saturating (10mmoll -1 ) succinate levels, the extent of suppression (52 and 33% in liver and skeletal muscle, respectively, compared with IBE) was comparable to previous studies (Gehnrich and Aprille, 1988;Muleme et al, 2006;Gerson et al, 2008;Armstrong and Staples, 2010;Chung et al, 2011;Brown et al, 2012), but the extent of suppression tended to decline with succinate concentration. For example, with 1mmoll -1 succinate, the extent of suppression was 42% in liver and 12.5% in skeletal muscle.…”

“…We chose to examine succinate-fuelled metabolism in the present study because (i) it is the most common substrate used in studies of mitochondrial metabolism in hibernating animals, and (ii) it allowed us to examine changes to an important segment of the electron transport chain without confounding effects from upstream processes that may be differentially regulated, for example, to shift fuel use away from carbohydrates rather than to suppress metabolism per se (Buck et al, 2002). For the most part, the results confirmed observations in previous studies made using saturating succinate concentrations (Gehnrich and Aprille, 1988;Muleme et al, 2006;Gerson et al, 2008;Armstrong and Staples, 2010;Chung et al, 2011;Brown et al, 2012), but two important facts were revealed by the present study. First, the degree of mitochondrial metabolic suppression during torpor is lower at sub-saturating compared with saturating succinate levels because torpid mitochondria are less sensitive to changes in succinate concentration than IBE mitochondria.…”

Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oysterCrassostrea gigas

“…Regulation of respiration rates, coupling and phosphorylation efficiency during short-term hypoxia are presumably controlled by several adjustments of the respiratory chain. Reduction of state 3 could result from inhibition of the phosphorylation system (reactions that generate or utilize ATP), the substrate oxidation system (reactions responsible for generating proton motive force) or both (Gerson et al, 2008). The increase of CCO activity during hypoxia in oysters (reported per nmol of cytochrome a) is unlikely a candidate for respiratory inhibition but suggests an involvement of this complex in response to hypoxia.…”

Mimicking the natural doping of migrant sandpipers in sedentary quails:effects of dietary n-3 fatty acids on muscle membranes and PPAR expression

“…Diet and in vitro manipulations have been used to alter the fatty acid composition of phospholipids. The resulting changes in membrane fluidity, permeability, n-3/n-6 ratio, and local molecular environment play important roles in modulating the activities of key membrane proteins (Gerson et al, 2008;Guderley et al, 2008;Murphy, 1990;Stillwell et al, 1997). They include enzymes from oxidative pathways, ATPases, hormone receptors and ion channels [carnitine palmitoyl transferase (CPT) (Guo et al, 2005;Power and Newsholme, 1997); citrate synthase (CS) (Miyasaka et al, 1996); Na + /K + -ATPase; insulin receptor (Corcoran et al, 2007); Na + and Ca 2+ channels (Leaf et al, 2005)].…”