scholarly journals Muscle nonshivering thermogenesis in a feral mammal

2018 ◽  
Author(s):  
Julia Nowack ◽  
Sebastian G. Vetter ◽  
Gabrielle Stalder ◽  
Johanna Painer ◽  
Maria Kral ◽  
...  

AbstractWhile 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.

1998 ◽  
Vol 78 (2) ◽  
pp. 339-358 ◽  
Author(s):  
MARIA FLOREZ-DUQUET ◽  
ROGER B. McDONALD

Florez-Duquet, Maria, and Roger B. McDonald. Cold-Induced Thermoregulation and Biological Aging. Physiol. Rev. 78: 339–358, 1998. — Aging is associated with diminished cold-induced thermoregulation (CIT). The mechanisms accounting for this phenomenon have yet to be clearly elucidated but most likely reflect a combination of increased heat loss and decreased metabolic heat production. The inability of the aged subject to reduce heat loss during cold exposure is associated with diminished reactive tone of the cutaneous vasculature and, to a lesser degree, alterations in the insulative properties of body fat. Cold-induced metabolic heat production via skeletal muscle shivering thermogenesis and brown adipose tissue nonshivering thermogenesis appears to decline with age. Few investigations have directly linked diminished skeletal muscle shivering thermogenesis with the age-related reduction in cold-induced thermoregulatory capacity. Rather, age-related declines in skeletal muscle mass and metabolic activity are cited as evidence for decreased heat production via shivering. Reduced mass, GDP binding to brown fat mitochondria, and uncoupling protein (UCP) levels are cited as evidence for attenuated brown adipose tissue cold-induced nonshivering thermogenic capacity during aging. The age-related reduction in brown fat nonshivering thermogenic capacity most likely reflects altered cellular signal transduction rather than changes in neural and hormonal signaling. The discussion in this review focuses on how alterations in CIT during the life span may offer insight into possible mechanisms of biological aging. Although the preponderance of evidence presented here demonstrates that CIT declines with chronological time, the mechanism reflecting this attenuated function remains to be elucidated. The inability to draw definitive conclusions regarding biological aging and CIT reflects the lack of a clear definition of aging. It is unlikely that the mechanisms accounting for the decline in cold-induced thermoregulation during aging will be determined until biological aging is more precisely defined.


2018 ◽  
Vol 22 (2) ◽  
pp. 265-272 ◽  
Author(s):  
Y. V. Piskunova ◽  
A. Y. Kazantceva ◽  
A. V. Baklanov ◽  
N. M. Bazhan

The lethal yellow mutation in agouti loci (Ay mutation) reduces the activity of melanocortin (MC) receptors and causes hyperphagia, obesity and type two diabetes mellitus in aging mice (Ay mice). It is unknown if changes in distinct elements of the metabolic system such as white adipose tissue (WAT) and brown adipose tissue (BAT), and skeletal muscle will manifest before the development of obesity. The aim of this work was to measure the relative gene expression of key proteins that regulate carbohydrate-lipid metabolism in WAT, BAT and skeletal muscle in Ay mice before the development of obesity. C57Bl/6J mice bearing a dominant autosomal mutation Ay (Ay /a mice) and mice of the standard genotype (a/a mice, control) have been studied in three age groups: 10, 15 and 30 weeks. The relative mRNA level of genes was measured by real-time PCR in skeletal muscles (uncoupling protein 3 (Ucp3) and carnitine palmitoyl transferase 1b (Cpt1b) (free fatty acids oxidation), solute carrier family 2 (facilitated glucose transporter), member 4 (Slc2a4) (glucose uptake)), in WAT lipoprotein lipase (Lpl) (triglyceride deposition), hormone-sensitive lipase (Lipe) (lipid mobilization), and Slc2a4 (glucose uptake)), and in BAT: uncoupling protein 1 (Ucp1) (energy expenditure). The expression of Cpt1b was reduced in young Ay mice (10 weeks), there was no transient peak of transcription of Cpt1b, Ucp3 in skeletal muscle tissue and Lipe, Slc2a4 in WAT in early adult Ay mice (15 weeks), which was noted in а/а mice. Reduction of the transcriptional activity of the studied genes in skeletal muscle and white adipose tissue can initiate the development of melanocortin obesity in Ay mice.


1997 ◽  
Vol 272 (2) ◽  
pp. C565-C571 ◽  
Author(s):  
P. E. Mozdziak ◽  
E. Schultz ◽  
R. G. Cassens

The role of satellite cells and DNA unit size in determining skeletal muscle growth was studied after mitotic activity was inhibited in the left pectoralis thoracicus of 2-wk-old tom turkeys by means of a 25-Gy dose of irradiation. Toms were killed and muscle weights were obtained 1 (n = 5), 4 (n = 6), 7 (n = 6), and 15 (n = 4) wk after irradiation. Satellite cell mitotic activity and DNA unit size were determined using enzymatically isolated myofiber segments and image analysis. Irradiated and nonirradiated muscle weights increased (P < 0.01) between all ages examined, but irradiated muscle weights were significantly (P < 0.01) lower than nonirradiated muscle weights at 4, 7, and 15 wk after irradiation. Satellite cell mitotic activity was lower (P < 0.01) in irradiated than in nonirradiated muscles at 1 and 4 wk after irradiation and resulted in a significant reduction (P < 0.05) in the number of myofiber nuclei per millimeter at 4 and 7 wk after irradiation. Satellite cell mitotic activity was higher (P < 0.05) in irradiated than in nonirradiated muscles at 7 wk after irradiation, but at 15 wk after irradiation it had fallen to low levels in both muscles. There was no significant (P > 0.10) difference in DNA unit size between muscles at any time, but there was an age-related increase (P < 0.01) for both muscles. Irradiation reduced muscle growth through a transient reduction in myonuclear production at a critical time (3-6 wk of age) in posthatch skeletal muscle development. The age-related increase in DNA unit size was not accelerated to compensate for the reduction in myonuclear accretion. Thus it appears that muscle growth potential is governed mostly by myonuclear accretion and to a lesser extent by DNA unit size.


1981 ◽  
Vol 241 (3) ◽  
pp. R185-R189
Author(s):  
S. J. Wickler

Nonshivering thermogenesis (NST) is a major contributor to total heat production capabilities of Peromyscus and the magnitude of the NST response increases dramatically in winter-acclimatized animals. To directly assess the contribution from skeletal muscle to this NST, a hindlimb perfusion system was developed for Peromyscus. Oxygen consumption was then measured with and without norepinephrine (the mediator of NST) in freshly captured animals in summer and winter. Norepinephrine (NE) was infused at 0.001, 0.01, and 0.1 micrograms . g hindlimb muscle-1 . min-1. Vascular resistance (VR), calculated as arterial pressure divided by flow rate, increased during all NE infusions. At doses of 0.001 and 0.01, VR stabilized after approximately 10 min, but at 0.1 VR continued to rise. Resting oxygen consumption was 0.817 +/- 0.037 and 0.805 +/- 0.049 mumol O2 . g-1 . min-1 in summer (n = 8) and winter (n = 7) animals, respectively. There was no apparent increase in oxygen consumption with any dosage of NE. It appears that the increase in NST in winter animals is not due to an increased NST in skeletal muscle.


2014 ◽  
Vol 307 (11) ◽  
pp. E1020-E1029 ◽  
Author(s):  
Ruy A. Louzada ◽  
Maria C. S. Santos ◽  
João Paulo A. Cavalcanti-de-Albuquerque ◽  
Igor F. Rangel ◽  
Andrea C. F. Ferreira ◽  
...  

During cold acclimation, shivering is progressively replaced by nonshivering thermogenesis. Brown adipose tissue (BAT) and skeletal muscle are relevant for nonshivering thermogenesis, which depends largely on thyroid hormone. Since the skeletal muscle fibers progressively adapt to cold exposure through poorly defined mechanisms, our intent was to determine whether skeletal muscle type 2 deiodinase (D2) induction could be implicated in the long-term skeletal muscle cold acclimation. We demonstrate that in the red oxidative soleus muscle, D2 activity increased 2.3-fold after 3 days at 4°C together with the brown adipose tissue D2 activity, which increased 10-fold. Soleus muscle and BAT D2 activities returned to the control levels after 10 days of cold exposure, when an increase of 2.8-fold in D2 activity was detected in white glycolytic gastrocnemius but not in red oxidative gastrocnemius fibers. Propranolol did not prevent muscle D2 induction, but it impaired the decrease of D2 in BAT and soleus after 10 days at 4°C. Cold exposure is accompanied by increased oxygen consumption, UCP3, and PGC-1α genes expression in skeletal muscles, which were partialy prevented by propranolol in soleus and gastrocnemius. Serum total and free T3 is increased during cold exposure in rats, even after 10 days, when BAT D2 is already normalized, suggesting that skeletal muscle D2 activity contributes significantly to circulating T3 under this adaptive condition. In conclusion, cold exposure is accompanied by concerted changes in the metabolism of BAT and oxidative and glycolytic skeletal muscles that are paralleled by type 2 deiodinase activation.


2013 ◽  
Vol 126 (8) ◽  
pp. 581-592 ◽  
Author(s):  
Gwenael Layec ◽  
Joel D. Trinity ◽  
Corey R. Hart ◽  
Seong-Eun Kim ◽  
Henderik Jonathan Groot ◽  
...  

The present study reveals that impaired skeletal muscle efficiency potentially contributes to the age-related decline in exercise capacity and may explain the altered haemodynamic response to exercise in the elderly.


Endocrinology ◽  
2008 ◽  
Vol 149 (12) ◽  
pp. 6262-6271 ◽  
Author(s):  
Ana Paula Arruda ◽  
Luisa A. Ketzer ◽  
Mariana Nigro ◽  
Antonio Galina ◽  
Denise P. Carvalho ◽  
...  

Brown adipose tissue (BAT) is involved in rat and mice thermoregulation, and heat produced by BAT depends on the concerted action of thyroid hormones and catecholamines. Little is known about cold-induced thermogenesis in mammals that have little or no BAT, such as rabbits. In these animals, thermogenesis primarily occurs in skeletal muscle. In this work, we have studied the effect of cold acclimation (4 C for 10 d) in normal and hypothyroid rabbits. It is known that hypothyroid rats die after a few hours of cold exposure. We now show that, different from rats, hypothyroid rabbits sustain their body temperature and survive after 10 d cold exposure. When compared with rabbits kept at room temperature, the muscles of cold-exposed rabbits showed a dark red color characteristic of oxidative muscle fibers. According to this pattern, we observed that in both normal and hypothyroid rabbits, cold exposure promotes an increase in oxygen consumption by skeletal muscle mitochondria. Moreover, in red muscle, cold acclimation induces an increase in the expression and activity of sarcoplasmic reticulum Ca2+ ATPase isoform 1 (SERCA1), one of the muscle enzymes involved in heat production. We conclude that rabbit cold tolerance is probably related to increased muscle oxidative metabolism and heat production by SERCA1 and that these changes are not completely dependent on normal thyroid function.


1993 ◽  
Vol 265 (5) ◽  
pp. R1076-R1083 ◽  
Author(s):  
C. Duchamp ◽  
H. Barre

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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