Muscle nonshivering thermogenesis in a feral mammal

Abstract

Muscle nonshivering thermogenesis (NST) was recently suggested to play an important role in thermoregulation of species lacking brown adipose tissue (BAT). The mechanism, which is independent of muscle contractions, produces heat based on the activity of an ATPase pump in the sarcoplasmic reticulum (SERCA1a) and is 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 newborn 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 body temperature. 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.

Transcriptome Analysis Revealed Potential Genes of Skeletal Muscle Thermogenesis in Mashen Pigs and Large White Pigs under Cold Stress

“…The initial explanation for the decrease in trembling intensity attributed it to an increase in trembling efficiency [37]. However, current suggests that the decrease is due to increased NST in muscles [23]. The results of the present study also revealed that cold stress significantly decreased (p < 0.05) the body temperature of both LW and MS pigs, in addition to significantly increasing (p < 0.05) the shivering frequency.…”

Transcriptome Analysis Revealed Potential Genes of Skeletal Muscle Thermogenesis in Mashen Pigs and Large White Pigs under Cold Stress

“…The initial explanation for the decrease in trembling intensity attributed it to an increase in trembling efficiency [37]. However, current suggests that the decrease is due to increased NST in muscles [23]. The results of the present study also revealed that cold stress significantly decreased (p < 0.05) the body temperature of both LW and MS pigs, in addition to significantly increasing (p < 0.05) the shivering frequency.…”

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

“…The data illustrate that although mass-specific heat production did not change, shivering intensity decreased, which suggests enhanced NST in the piglets. Muscles from 5day-old piglets showed higher SERCA activity and mRNA expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

“…R. Soc. B 375: 20190135 expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

Min pig skeletal muscle response to cold stress

“…In this study, SERCA1a (ATPase sarcoplasmic/endoplasmic reticulum Ca2+ transporter 1), which is generally considered to play an important role in non-shivering thermogenesis [ 19 ], was not changed significantly, but the expression level of its regulator SLN was reduced by half. This is consistent with the findings of a study in birds [ 51 ].…”

Transcriptome Analysis Revealed Potential Genes of Skeletal Muscle Thermogenesis in Mashen Pigs and Large White Pigs under Cold Stress

“…The initial explanation for the decrease in trembling intensity attributed it to an increase in trembling efficiency [37]. However, current suggests that the decrease is due to increased NST in muscles [23]. The results of the present study also revealed that cold stress significantly decreased (p < 0.05) the body temperature of both LW and MS pigs, in addition to significantly increasing (p < 0.05) the shivering frequency.…”

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

“…The data illustrate that although mass-specific heat production did not change, shivering intensity decreased, which suggests enhanced NST in the piglets. Muscles from 5day-old piglets showed higher SERCA activity and mRNA expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

“…R. Soc. B 375: 20190135 expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

Min pig skeletal muscle response to cold stress

“…In this study, SERCA1a (ATPase sarcoplasmic/endoplasmic reticulum Ca2+ transporter 1), which is generally considered to play an important role in non-shivering thermogenesis [ 19 ], was not changed significantly, but the expression level of its regulator SLN was reduced by half. This is consistent with the findings of a study in birds [ 51 ].…”

Transcriptome Analysis Revealed Potential Genes of Skeletal Muscle Thermogenesis in Mashen Pigs and Large White Pigs under Cold Stress

“…The initial explanation for the decrease in trembling intensity attributed it to an increase in trembling efficiency [37]. However, current suggests that the decrease is due to increased NST in muscles [23]. The results of the present study also revealed that cold stress significantly decreased (p < 0.05) the body temperature of both LW and MS pigs, in addition to significantly increasing (p < 0.05) the shivering frequency.…”

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

“…The data illustrate that although mass-specific heat production did not change, shivering intensity decreased, which suggests enhanced NST in the piglets. Muscles from 5day-old piglets showed higher SERCA activity and mRNA expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

“…R. Soc. B 375: 20190135 expression of SERCA as well as SLN [114]. This study clearly demonstrates that muscle NST plays a major role in these animals that lack UCP1-mediated NST and SLN plays an important role in this process.…”

Min pig skeletal muscle response to cold stress

“…In this study, SERCA1a (ATPase sarcoplasmic/endoplasmic reticulum Ca2+ transporter 1), which is generally considered to play an important role in non-shivering thermogenesis [ 19 ], was not changed significantly, but the expression level of its regulator SLN was reduced by half. This is consistent with the findings of a study in birds [ 51 ].…”