Sarcolipin Is a Key Determinant of the Basal Metabolic Rate, and Its Overexpression Enhances Energy Expenditure and Resistance against Diet-induced Obesity

Maurya, Santosh K.; Bal, Naresh C.; Sopariwala, Danesh H.; Pant, Meghna; Rowland, Leslie A.; Shaikh, Sana; Periasamy, Muthu

doi:10.1074/jbc.m115.636878

Cited by 138 publications

(162 citation statements)

References 45 publications

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“…Moreover, the ability to recruit SLN/SERCA-mediated muscle-based NST without significantly affecting muscle maturation and function will be favorably selected for, specifically in non-tropical climates where temperature and food availability dramatically fluctuate seasonally. Recent studies from our lab further show that SLN increases fatigue resistance of muscle while increasing energy expenditure and contributes to thermogenesis (Maurya et al, 2015;Rowland et al, 2015;Sopariwala et al, 2015). Collectively, these findings along with our data suggest that SLN is an important marker of muscle-based thermogenesis.…”

Section: Resultssupporting

confidence: 65%

Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis?

Pant

Bal

Periasamy

2015

Journal of Experimental Biology

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Neonatal mice have a greater thermogenic need than adult mice and may require additional means of heat production, other than the established mechanism of brown adipose tissue (BAT). We and others recently discovered a novel mediator of skeletal muscle-based thermogenesis called sarcolipin (SLN) that acts by uncoupling sarcoendoplasmic reticulum Ca 2+ -ATPase (SERCA). In addition, we have shown that SLN expression is downregulated during neonatal development in rats. In this study we probed two questions: (1) is SLN expression developmentally regulated in neonatal mice?; and (2) if so, will cold adaptation override this? Our data show that SLN expression is higher during early neonatal stages and is gradually downregulated in fast twitch skeletal muscles. Interestingly, we demonstrate that cold acclimation of neonatal mice can prevent downregulation of SLN expression. This observation suggests that SLN-mediated thermogenesis can be recruited to a greater extent during extreme physiological need, in addition to BAT.

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Section: Resultssupporting

confidence: 65%

Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis?

Pant

Bal

Periasamy

2015

Journal of Experimental Biology

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“…Heat can be generated under neuronal control in skeletal muscle through the uncoupling of sarcoplasmic reticulum Ca 2+ -ATPase (SERCA) mediated by sarcolipin (Sln) (Mall et al, 2006;Bal et al, 2012;Newman, Mezentseva & Badyaev, 2013;Maurya et al, 2015;. During a typical muscle fibre contraction, heat is dissipated when (i) ATP is hydrolyzed during the actual fibre contraction by myosin ATPase, (ii) when the Ca 2+ that is released following the neuronal stimulus and which initiates the muscle fibre contraction is pumped back from the cytosol into the lumen of the sarcoplasmic reticulum via SERCA, and (iii) by Na + /K + ATPase when the resting ion gradients and membrane potential are restored following the release of the Ca 2+ (Bal et al, 2012).…”

Section: (D) Endogenous Uncoupled Respiration In Skeletal Musclementioning

confidence: 99%

A phenology of the evolution of endothermy in birds and mammals

2016

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Recent palaeontological data and novel physiological hypotheses now allow a timescaled reconstruction of the evolution of endothermy in birds and mammals. A three-phase iterative model describing how endothermy evolved from Permian ectothermic ancestors is presented. In Phase One I propose that the elevation of endothermy - increased metabolism and body temperature (T ) - complemented large-body-size homeothermy during the Permian and Triassic in response to the fitness benefits of enhanced embryo development (parental care) and the activity demands of conquering dry land. I propose that Phase Two commenced in the Late Triassic and Jurassic and was marked by extreme body-size miniaturization, the evolution of enhanced body insulation (fur and feathers), increased brain size, thermoregulatory control, and increased ecomorphological diversity. I suggest that Phase Three occurred during the Cretaceous and Cenozoic and involved endothermic pulses associated with the evolution of muscle-powered flapping flight in birds, terrestrial cursoriality in mammals, and climate adaptation in response to Late Cenozoic cooling in both birds and mammals. Although the triphasic model argues for an iterative evolution of endothermy in pulses throughout the Mesozoic and Cenozoic, it is also argued that endothermy was potentially abandoned at any time that a bird or mammal did not rely upon its thermal benefits for parental care or breeding success. The abandonment would have taken the form of either hibernation or daily torpor as observed in extant endotherms. Thus torpor and hibernation are argued to be as ancient as the origins of endothermy itself, a plesiomorphic characteristic observed today in many small birds and mammals.

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“…Samples were processed by the core facility, and images were obtained using a Tecnai G2 Spirit transmission electron microscope (FEI, Hillsboro, OR) at various magnifications. SDH activity staining was performed on sections of TA muscles as described earlier (52). respiration (non-phosphorylating inner membrane proton leak) was measured following the addition of saturating concentrations of malate (2 M) and glutamate (500 mM).…”

Section: Methodsmentioning

confidence: 99%

“…Western Blotting-Protein levels were quantified using a Western blotting technique following a protocol published previously (14,52 , and SLN (1:1000 dilution) antibodies were custom-generated in the laboratory of Dr. Periasamy. RyR1 and Thr(P) 2848 -RyR 1 antibodies (used at 1:1000 and 1:500 dilutions, respectively) were generated in the laboratory of Dr. Wehrens using the regular and phospho-peptide QSAQpTYD-PREGYC.…”

Section: Measurement Of Mitochondrial Respiration-measurementmentioning

confidence: 99%

Increased Reliance on Muscle-based Thermogenesis upon Acute Minimization of Brown Adipose Tissue Function

Bal

Maurya

Singh

et al. 2016

Journal of Biological Chemistry

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Skeletal muscle has been suggested as a site of nonshivering thermogenesis (NST) besides brown adipose tissue (BAT). Studies in birds, which do not contain BAT, have demonstrated the importance of skeletal muscle-based NST. However, musclebased NST in mammals remains poorly characterized. We recently reported that sarco/endoplasmic reticulum Ca 2؉ cycling and that its regulation by SLN can be the basis for muscle NST. Because of the dominant role of BAT-mediated thermogenesis in rodents, the role of muscle-based NST is less obvious. In this study, we investigated whether muscle will become an important site of NST when BAT function is conditionally minimized in mice. We surgically removed interscapular BAT (iBAT, which constitutes ϳ70% of total BAT) and exposed the mice to prolonged cold (4°C) for 9 days. The iBAT-ablated mice were able to maintain optimal body temperature (ϳ35-37°C) during the entire period of cold exposure. After 4 days in the cold, both sham controls and iBAT-ablated mice stopped shivering and resumed routine physical activity, indicating that they are cold-adapted. The iBAT-ablated mice showed higher oxygen consumption and decreased body weight and fat mass, suggesting an increased energy cost of cold adaptation. The skeletal muscles in these mice underwent extensive remodeling of both the sarcoplasmic reticulum and mitochondria, including alteration in the expression of key components of Ca 2؉ handling and mitochondrial metabolism. These changes, along with increased sarcolipin expression, provide evidence for the recruitment of NST in skeletal muscle. These studies collectively suggest that skeletal muscle becomes the major site of NST when BAT activity is minimized.

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Sarcolipin Is a Key Determinant of the Basal Metabolic Rate, and Its Overexpression Enhances Energy Expenditure and Resistance against Diet-induced Obesity

Cited by 138 publications

References 45 publications

Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis?

Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis?

A phenology of the evolution of endothermy in birds and mammals

Increased Reliance on Muscle-based Thermogenesis upon Acute Minimization of Brown Adipose Tissue Function

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