Muscle Non-shivering Thermogenesis and Its Role in the Evolution of Endothermy.

Julia Nowack,Thomas Ruf,Sylvain Giroud,Walter Arnold

doi:10.3389/fphys.2017.00889

Julia Nowack, Thomas Ruf + Show 2 more

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https://doi.org/10.3389/fphys.2017.00889

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Abstract

The development of sustained, long-term endothermy was one of the major transitions in the evolution of vertebrates. Thermogenesis in endotherms does not only occur via shivering or activity, but also via non-shivering thermogenesis (NST). Mammalian NST is mediated by the uncoupling protein 1 in the brown adipose tissue (BAT) and possibly involves an additional mechanism of NST in skeletal muscle. This alternative mechanism is based on Ca2+-slippage by a sarcoplasmatic reticulum Ca2+-ATPase (SERCA) and is controlled by the protein sarcolipin. The existence of muscle based NST has been discussed for a long time and is likely present in all mammals. However, its importance for thermoregulation was demonstrated only recently in mice. Interestingly, birds, which have evolved from a different reptilian lineage than mammals and lack UCP1-mediated NST, also exhibit muscle based NST under the involvement of SERCA, though likely without the participation of sarcolipin. In this review we summarize the current knowledge on muscle NST and discuss the efficiency of muscle NST and BAT in the context of the hypothesis that muscle NST could have been the earliest mechanism of heat generation during cold exposure in vertebrates that ultimately enabled the evolution of endothermy. We suggest that the evolution of BAT in addition to muscle NST was related to heterothermy being predominant among early endothermic mammals. Furthermore, we argue that, in contrast to small mammals, muscle NST is sufficient to maintain high body temperature in birds, which have enhanced capacities to fuel muscle NST by high rates of fatty acid import.

Highlights

The evolution of endothermy is of major interest in the understanding of mammalian and avian radiation
A commonly accepted view is that small placental mammals were able to colonize colder habitats because they are able to maintain high Body temperature (Tb) even in the cold by producing heat via non-shivering thermogenesis (NST) mediated by the uncoupling protein 1 (UCP1) in brown adipose tissue (BAT) (Chaffee et al, 1975; Foster and Frydman, 1978; Heaton et al, 1978)
In this review we summarize our current knowledge on muscle-based NST, from here on referred to as muscle NST to distinguish it from UCP1-mediated NST in BAT, and add more evidence to the hypothesis that muscle NST could have been the earliest mechanism of endogenous heat production in vertebrates

Summary

Introduction

The evolution of endothermy is of major interest in the understanding of mammalian and avian radiation. In birds there is a profound increase in SERCA activity during cold exposure-similar to muscle NST in mammals (Dumonteil et al, 1993, 1995).

Results

Conclusion