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

Nowack, Julia; Giroud, Sylvain; Arnold, W.; Ruf, T.

doi:10.3389/fphys.2017.00889

Cited by 127 publications

(115 citation statements)

References 133 publications

Supporting

Mentioning

112

Contrasting

Order By: Relevance

“…This 'futile' cycle of calcium releases sufficient heat to warm the visionary system and adjacent brain areas to above surrounding water temperatures [35]. 'Futile' pumping of calcium may also occur in skeletal muscle of mammals to facilitate muscle nonshivering thermogenesis [28,29,36]. Another heat-producing process is lipid 'futile' cycling, defined as the simultaneous occurrence of lipolysis and lipogenesis to increase ATP turnover in adipocytes, which may occur in adipose tissue of mammals [37].…”

Section: Mechanisms Of Thermogenesismentioning

confidence: 99%

Importance of adipocyte browning in the evolution of endothermy

Jastroch

Seebacher

2020

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

Endothermy changes the relationship between organisms and their environment fundamentally, and it is therefore of major ecological and evolutionary significance. Endothermy is characterized by non-shivering thermogenesis, that is metabolic heat production in the absence of muscular activity. In many eutherian mammals, brown adipose tissue (BAT) is an evolutionary innovation that facilitates non-shivering heat production in mitochondria by uncoupling food-derived substrate oxidation from chemical energy (ATP) production. Consequently, energy turnover is accelerated resulting in increased heat release. The defining characteristics of BAT are high contents of mitochondria and vascularization, and the presence of uncoupling protein 1. Recent insights, however, reveal that a range of stimuli such as exercise, diet and the immune system can cause the browning of white adipocytes, thereby increasing energy expenditure and heat production even in the absence of BAT. Here, we review the molecular mechanisms that cause browning of white adipose tissue, and their potential contribution to thermoregulation. The significance for palaeophysiology lies in the presence of adipose tissue and the mechanisms that cause its browning and uncoupling in all amniotes. Hence, adipocytes may have played a role in the evolution of endothermy beyond the more specific evolution of BAT in eutherians. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

show abstract

Section: Mechanisms Of Thermogenesismentioning

confidence: 99%

Importance of adipocyte browning in the evolution of endothermy

Jastroch

Seebacher

2020

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

show abstract

“…To defend against hypothermia, mammals have evolved various thermogenic mechanisms, ranging from skeletal muscle shivering to non-shivering, adaptive thermogenesis [1][2][3][4][5]. Although short-lived, shivering is the fast contraction of skeletal muscles during which heat is released via the hydrolysis of ATP [6]. Another early mechanism to regulate body temperature is vasoconstriction, which helps to mitigate heat loss [7], but its duration and relative contribution to homeothermy, especially in the context of adaptive thermogenesis, is often underappreciated.…”

Section: Introductionmentioning

confidence: 99%

14-3-3ζ mediates an alternative, non-thermogenic mechanism to reduce heat loss and improve cold tolerance

Diallo

Dussault²,

Noll³

et al. 2019

Preprint

View full text Add to dashboard Cite

Running title: 14-3-3ζ over-expression improves cold tolerance in male mice AbstractAdaptive thermogenesis, which is partly mediated by sympathetic input on brown adipose tissue (BAT), is a mechanism of heat production in response to prolonged cold that relies upon the actions of Uncoupling Protein-1 (UCP1). Moreover, various stimuli, including norepinephrine and FGF-21, promote the conversion of inguinal white adipocytes to beige adipocytes, which represent a secondary cell type that can contribute to adaptive thermogenesis. Although we previously identified an essential role of the molecular scaffold 14-3-3ζ in adipogenesis, one of the earliest, identified functions of 14-3-3ζ is its regulatory effects on the activity of tyrosine hydroxylase, the rate-limiting enzyme in the synthesis of norepinephrine. This suggests that 14-3-3z could influence adaptive thermogenesis via actions on BAT activation or the beiging of white adipocytes. Herein, we report that transgenic over-expression of 14-3-3ζ (TAP) in male mice significantly improved tolerance to acute (3 hrs) and chronic (3 days) cold (4 o C) exposure. In response to cold,increased UCP1 expression in beige inguinal white tissue (iWAT) and BAT was observed in TAP mice following chronic cold exposure, in addition to significantly elevated body temperature. Of note was the paradoxical finding that cold-induced increases in body temperature were associated with significantly decreased energy expenditure in TAP mice. The marked improvements in cold tolerance were not due to changes in sensitivity to b-adrenergic stimulation; instead over-expression of 14-3-3z significantly decreased thermal conductance and heat loss in mice via increased peripheral vasoconstriction. Despite displaying elevations in cold-induced UCP1 expression in brown or beige adipocytes, these findings suggest alternative mechanisms that can be activated to mitigate heat loss during chronic cold exposure. Collectively, our results point to novel roles of 14-3-3ζ in regulating non-thermogenic mechanisms that regulate body temperature.

show abstract

“…The regulation of a high and stable body temperature (T b ) independent of climatic conditions is one of the most important mechanisms that arose during the evolution of mammals and birds. After decades of intensive research, it is now well-understood how mammals possessing brown adipose tissue (BAT) - a specialised thermogenic organ - are able to maintain an optimal T b even in cold environments by using nonshivering thermogenesis (NST) [reviewed in 1], However, only ~20% of endothermic birds and mammals actually possess BAT [2]. NST in BAT requires thermogenic functional uncoupling protein 1 (UCP1) that alters proton conductance in the inner mitochondrial membrane, leading to heat generation instead of ATP production [3, 4], Functional UCP1 has not been found, however, in marsupials or monotremes [5] and typically substantial amounts of BAT are present only in neonates of large-bodied mammals [6, 7, but see: 8].…”

Section: Introductionmentioning

confidence: 99%

“…It was long believed that species without thermogenic functional UCP1 rely solely on shivering, a process that on its own is insufficient for the maintenance of a stable T b during cold exposure in UCP1 knockout mice [11]. However, a second mechanism of NST in muscle, which had been studied in vitro for a long time [12-15], has recently been shown to play an important role in thermoregulation in mice lacking functional BAT [11], The mechanism is so far only confirmed as an additional form of NST in rodents in which the wildtype possesses BAT [11, 16-20], but assumed to occur in all mammals [2, 21]. Furthermore, muscle NST is discussed as a heat production mechanism that played an important role for the evolution of a high T b , i.e.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Muscle nonshivering thermogenesis in a feral mammal

Nowack

Vetter

Stalder

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

While small mammals and neonates are able to maintain an optimal body temperature (Tb) independent of ambient conditions by producing heat via nonshivering thermogenesis (NST) in the brown adipose tissue (BAT), larger mammals and other mammals lacking BAT were long believed to rely primarily on shivering and behavioural adaptations. However, recently, a second mechanism of NST was found in skeletal muscle that could play an important role in thermoregulation of such species. Muscle NST is independent of muscle contractions and produces heat based on the activity of an ATPase pump in the sarcoplasmic reticulum (SERCA1a) and controlled by the protein sarcolipin. To evaluate whether muscle NST could indeed play an important role in thermoregulation in species lacking BAT, we investigated the thermogenic capacities of new-born wild boar piglets. During cold exposure over the first 5 days of life, total heat production was improved while shivering intensity decreased, indicating an increasing contribution of NST. Sampling skeletal muscle tissue for analyses of SERCA activity as well as gene expression of SERCA1a and sarcolipin, we found an age-related increase in all three variables as well as in Tb. Hence, the improved thermogenesis during the development of wild boars is not due to shivering but explained by the observed increase in SERCA activity. Our results suggest that muscle NST may be the primary mechanism of heat production during cold stress in large mammals lacking BAT, strengthening the hypothesis that muscle NST has likely played an important role in the evolution of endothermy.

show abstract

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

Cited by 127 publications

References 133 publications

Importance of adipocyte browning in the evolution of endothermy

Importance of adipocyte browning in the evolution of endothermy

14-3-3ζ mediates an alternative, non-thermogenic mechanism to reduce heat loss and improve cold tolerance

Muscle nonshivering thermogenesis in a feral mammal

Contact Info

Product

Resources

About