Uncoupling of sarcoendoplasmic reticulum calcium ATPase pump activity by sarcolipin as the basis for muscle non-shivering thermogenesis

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Abstract

Thermogenesis in endotherms relies on both shivering and non-shivering thermogenesis (NST). The role of brown adipose tissue (BAT) in NST is well recognized, but the role of muscle-based NST has been contested. However, recent studies have provided substantial evidence for the importance of muscle-based NST in mammals. This review focuses primarily on the role of sarcoplasmic reticulum (SR) Ca ²⁺ -cycling in muscle NST; specifically, it will discuss recent data showing how uncoupling of sarcoendoplasmic reticulum calcium ATPase (SERCA) (inhibition of Ca ²⁺ transport but not ATP hydrolysis) by sarcolipin (SLN) results in futile SERCA pump activity, increased ATP hydrolysis and heat production contributing to muscle NST. It will also critically examine how activation of muscle NST can be an important factor in regulating metabolic rate and whole-body energy homeostasis. In this regard, SLN has emerged as a powerful signalling molecule to promote mitochondrial biogenesis and oxidative metabolism in muscle. Furthermore, we will discuss the functional interplay between BAT and muscle, especially with respect to how reduced BAT function in mammals could be compensated by muscle-based NST. Based on the existing data, we argue that SLN-mediated thermogenesis is an integral part of muscle NST and that muscle NST potentially contributed to the evolution of endothermy within the vertebrate clade.

This article is part of the theme issue ‘Vertebrate palaeophysiology’.

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Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings.

H Barre, James Duchamp (1993)

Despite their lack of brown adipose tissue, 6-wk-old cold-acclimated muscovy ducklings (4 degrees C; CA) exhibit nonshivering thermogenesis (NST) in the cold. To determine the site of this NST, the regional distribution of blood flow was measured by the microsphere method in the thermoneutral zone (25 degrees C) and during acute exposure to cold (8 degrees C). Ducklings reared at thermal neutrality (TN), which use shivering to produce extra heat in the cold, were compared with CA ducklings, which substitute NST for shivering. Further, the contribution of skeletal muscle thermogenesis to the increased heat production in the cold was estimated by measuring leg muscle blood flow and arteriovenous difference in oxygen content [(a-v)O2] across the leg, enabling an estimation of muscle O2 consumption. During cold exposure, a similar increase in total leg muscle blood flow occurred in TN and CA ducklings (+127 and +130% respectively), while hepatic arterial blood flow increased less (+56 to +37%, respectively). This rise in blood flow was accounted for by an increase in cardiac output, which was smaller in CA than in TN ducklings, and in both groups by a redistribution of blood flow to the most thermogenic organs (skeletal muscles and liver). The (a-v)O2 across the leg was not changed by cold exposure, indicating that the increase in leg muscle O2 consumption resulted mainly from the increase in blood flow.(ABSTRACT TRUNCATED AT 250 WORDS)

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Nonshivering thermogenesis in king penguin chicks. I. Role of skeletal muscle.

James Duchamp, A Lanni, G Paulsson-Berne … (1991)

In cold-acclimatized (CA) king penguin chicks exhibiting nonshivering thermogenesis (NST), protein content and cytochrome oxidase (CO) activity of tissue homogenates were measured together with protein content, CO, and respiration rates of isolated mitochondria from skeletal muscle (gastrocnemius and pectoralis) and liver. The comparison was made with chicks reared at thermoneutrality (TN) for at least 3 wk. In CA chicks showing a NST despite the lack of brown adipose tissue, an increase in thermogenic capacity was observed in skeletal muscle in which the oxidative capacity rose (+28% and +50% in gastrocnemius and pectoralis muscles, respectively), whereas no change occurred in the liver. Oxidative capacity of skeletal muscle increased together with the development of mitochondrial inner membrane plus cristae in muscles of CA chicks contrary to their TN littermates (+30 to +50%). Subsarcolemmal mitochondria of CA chicks had a higher protein content (+65% in gastrocnemius muscle) and higher oxidative capacities than in controls. The lower respiratory control ratio of these mitochondria might result from a low ADP phosphorylation rate. No change occurred in the intermyofibrillar fraction nor in liver mitochondria. These findings together with earlier results obtained in cold-acclimated ducklings indicate the marked and suited adaptation of skeletal muscle and in particular of subsarcolemmal mitochondria allowing them to play a role in NST.

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Nonshivering thermogenesis and adaptation to fasting in king penguin chicks.

C Duchamp, H Barre, D Delage … (1989)

The ability to develop nonshivering thermogenesis (NST) and the effect of fasting on thermogenic response to cold were studied in winter-acclimatized king penguin chicks. Metabolic rate (MR) and integrated electrical muscle activity were measured at different ambient temperatures. In cold-acclimatized (5 degrees C) fed chicks, shivering threshold temperature (STT) was 9.4 degrees C lower than lower critical temperature (LCT), indicating that NST (0.7 W/kg) occurs at moderate cold, whereas in control chicks fed and reared at 25 degrees C for 3 wk, LCT and STT were similar. Chicks reared in the cold and fasting for 3 wk or 4-5 mo (natural winter fast) developed an NST of 0.8 and 2.4 W/kg, respectively, despite the fast. In fasting chicks, the intercept of the metabolic curve with the abscissa at zero MR was far below body temperature, contrasting with the classic model for heat loss. Their low LCT indicates the capacity of a large reduction in convective conductance characteristic of diving animals and allows energy sparing in moderate cold. Below LCT, conductance reincreases progressively, leading to a steeper than expected slope of the metabolic curve and allowing preservation of a threshold temperature in the shell. These results show for the first time in a wild young bird the development of NST after cold acclimatization. Further, at the temperature of cold acclimatization, an energy-sparing mechanism is shown in response to long-term fast adaptation.