Selective upregulation of lipid metabolism in skeletal muscle of foraging juvenile king penguins: an integrative study

Teulier, Loïc; Dégletagne, Cyril; Rey, Benjamin; Tornos, J; Keime, Céline; Dinechin, Marc de; Raccurt, Mireille; Rouanet, Jean‐Louis; Roussel, Damien; Duchamp, Claude

doi:10.1098/rspb.2011.2664

Cited by 12 publications

(24 citation statements)

References 41 publications

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“…In adults, pectoralis muscle oxidative activity was further increased compared with growing chicks (Table 1) possibly in relation with further developmental maturation and the living conditions of adults that face the energetic challenges of cold water immersion, increased contractile activity during swimming at sea, and hypoxic hunting dives. Increases in skeletal muscle oxidative potential have been documented in relation with the passage from shore to marine life in juvenile king penguins (56) and with endurance exercise training or intermittent tissue hypoxia in a number of organisms (18,23,25,28).…”

Section: Discussionmentioning

confidence: 99%

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Fongy

Romestaing

Blanc

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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The ontogeny of pectoralis muscle bioenergetics was studied in growing Adélie penguin chicks during the first month after hatching and compared with adults using permeabilized fibers and isolated mitochondria. With pyruvate-malate-succinate or palmitoyl-carnitine as substrates, permeabilized fiber respiration markedly increased during chick growth (3-fold) and further rose in adults (1.4-fold). Several markers of muscle fiber oxidative activity (cytochrome oxidase, citrate synthase, hydroxyl-acyl-CoA dehydrogenase) increased 6- to 19-fold with age together with large rises in intermyofibrillar (IMF) and subsarcolemmal (SS) mitochondrial content (3- to 5-fold) and oxidative activities (1.5- to 2.4-fold). The proportion of IMF relative to SS mitochondria increased with chick age but markedly dropped in adults. Differences in oxidative activity between mitochondrial fractions were reduced in adults compared with hatched chicks. Extrapolation of mitochondrial to muscle respirations revealed similar figures with isolated mitochondria and permeabilized fibers with carbohydrate-derived but not with lipid-derived substrates, suggesting diffusion limitations of lipid substrates with permeabilized fibers. Two immunoreactive fusion proteins, mitofusin 2 (Mfn2) and optic atrophy 1 (OPA1), were detected by Western blots on mitochondrial extracts and their relative abundance increased with age. Muscle fiber respiration was positively related with Mfn2 and OPA1 relative abundance. Present data showed by two complementary techniques large ontogenic increases in muscle oxidative activity that may enable birds to face thermal emancipation and growth in childhood and marine life in adulthood. The concomitant rise in mitochondrial fusion protein abundance suggests a role of mitochondrial networks in the skeletal muscle processes of bioenergetics that enable penguins to overcome harsh environmental constraints.

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Section: Discussionmentioning

confidence: 99%

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Fongy

Romestaing

Blanc

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Although average peak of incidence differs for each individual autoimmune disease, a general trend suggests that most autoimmune diseases develop either during puberty (juvenile type diseases) or during mature reproductive life of individuals. For example, lupus erythematosus affects primarily women of childbearing age, and most frequently begins between ages of 15 and 40 years [ 49 ]. The average age of onset of multiple sclerosis is 28-30 years [ 50 ].…”

Section: Discussionmentioning

confidence: 99%

Age-related accumulation of T cells with markers of relatively stronger autoreactivity leads to functional erosion of T cells

et al. 2012

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BackgroundThymic involution is a prominent characteristic of an aging immune system. When thymic function is reduced/absent, the peripheral T cell pool is subject to the laws of peripheral T cell homeostasis that favor survival/expansion of T cell receptors with relatively higher functional avidity for self-peptide/MHC complexes. Due to difficulties in assessing the TCR avidity in polyclonal population of T cells, it is currently not known whether high avidity T cells preferentially survive in aging individuals, and what impact this might have on the function of the immune system and development of autoimmune diseases.ResultsThe phenotype of T cells from aged mice (18-24 months) indicating functional TCR avidity (CD3 and CD5 expression) correlates with the level of preserved thymic function. In mice with moderate thymic output (> 30% of peripheral CD62Lhi T cells), T cells displayed CD3lowCD5hi phenotype characteristic for high functional avidity. In old mice with drastically low numbers of CD62Lhi T cells reduced CD5 levels were found. After adult thymectomy, T cells of young mice developed CD3lowCD5hi phenotype, followed by a CD3lowCD5low phenotype. Spleens of old mice with the CD3low/CD5hi T cell phenotype displayed increased levels of IL-10 mRNA, and their T cells could be induced to secrete IL-10 in vitro. In contrast, downmodulation of CD5 was accompanied with reduced IL-10 expression and impaired anti-CD3 induced proliferation. Irrespective of the CD3/CD5 phenotype, reduced severity of experimental allergic myelitis occurred in old mice. In MTB TCRβ transgenic mice that display globally elevated TCR avidity for self peptide/MHC, identical change patterns occurred, only at an accelerated pace.ConclusionsThese findings suggest that age-associated dysfunctions of the immune system could in part be due to functional erosion of T cells devised to protect the hosts from the prolonged exposure to T cells with high-avidity for self.

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“…Once at sea, penguins' daily metabolic cost of thermoregulation is reduced by their ability to develop powerful peripheral vasoconstriction, regional hypothermia and a thick subcutaneous fat layer (Dumonteil et al, 1994;Handrich et al, 1997;Enstipp et al, 2017;Lewden et al, 2017a). Sea acclimatization is also characterized by the fuel selection of skeletal muscle towards lipid transport and oxidation, concomitant with an increase in the content and oxidative capacity of mitochondria in skeletal muscle (Teulier et al, 2012;Rey et al, 2016). These biochemical remodeling processes are associated with an increased thermogenic effect of circulating lipids on whole-body metabolism in vivo and in mitochondrial skeletal muscle in vitro (Talbot et al, 2004;Teulier et al, 2012;Rey et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Skeletal muscle metabolism in sea-acclimatized king penguins: II. Improved efficiency of mitochondrial bioenergetics

Roussel

Marmillot

Monternier

et al. 2020

Journal of Experimental Biology

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At fledging, juvenile king penguins (Aptenodytes patagonicus) must overcome the tremendous energetic constraints imposed by their marine habitat, including during sustained extensive swimming activity and deep dives in cold seawater. Both endurance swimming and skeletal muscle thermogenesis require high mitochondrial respiratory capacity while the submerged part of dive cycles repeatedly and greatly reduce oxygen availability imposing a need for solutions to conserve oxygen. The aim of the present study was to determine in vitro whether skeletal muscle mitochondria become more “thermogenic” to sustain heat production or more “economical” to conserve oxygen in sea-acclimatized immature penguins as compared with terrestrial juveniles. Rates of mitochondrial oxidative phosphorylation were measured in permeabilized fibers and mitochondria from the pectoralis muscle. Mitochondrial ATP synthesis and coupling efficiency were measured in isolated muscle mitochondria. The mitochondrial activities of respiratory chain complexes and citrate synthase were also assessed. The results showed that respiration, ATP synthesis and respiratory chain complex activities in pectoralis muscles were increased by sea acclimatization. Further, muscle mitochondria were on average 30% to 45% more energy efficient in sea-acclimatized immatures than in pre-fledging juveniles, depending on the respiratory substrate used (pyruvate; palmitoyl-carnitine). Hence, sea acclimatization favors the development of economical management of oxygen, decreasing the oxygen needed to produce a given amount of ATP. This mitochondrial phenotype may improve dive performance during the early marine life of king penguins, by extending their aerobic dive limit.

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Selective upregulation of lipid metabolism in skeletal muscle of foraging juvenile king penguins: an integrative study

Cited by 12 publications

References 41 publications

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Age-related accumulation of T cells with markers of relatively stronger autoreactivity leads to functional erosion of T cells

Skeletal muscle metabolism in sea-acclimatized king penguins: II. Improved efficiency of mitochondrial bioenergetics

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