Skip Navigation
Skip to contents

Diabetes Metab J : Diabetes & Metabolism Journal

Search
OPEN ACCESS

Articles

Page Path
HOME > Diabetes Metab J > Volume 41(5); 2017 > Article
Review
Obesity and Metabolic Syndrome Skeletal Muscle Thermogenesis and Its Role in Whole Body Energy Metabolism
Muthu Periasamyorcid, Jose Luis Herrera, Felipe C. G. Reis
Diabetes & Metabolism Journal 2017;41(5):327-336.
DOI: https://doi.org/10.4093/dmj.2017.41.5.327
Published online: October 24, 2017
  • 9,489 Views
  • 216 Download
  • 116 Web of Science
  • 123 Crossref
  • 124 Scopus

Sanford Burnham Prebys Medical Discovery Institute at Lake Nona, Orlando, FL, USA.

Corresponding author: Muthu Periasamy. Sanford Burnham Prebys Medical Discovery Institute at Lake Nona, 6400 Sanger Rd, Orlando, FL 32827, USA. mperiasamy@SBPdiscovery.org
• Received: August 29, 2017   • Accepted: September 8, 2017

Copyright © 2017 Korean Diabetes Association

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • Obesity and diabetes has become a major epidemic across the globe. Controlling obesity has been a challenge since this would require either increased physical activity or reduced caloric intake; both are difficult to enforce. There has been renewed interest in exploiting pathways such as uncoupling protein 1 (UCP1)-mediated uncoupling in brown adipose tissue (BAT) and white adipose tissue to increase energy expenditure to control weight gain. However, relying on UCP1-based thermogenesis alone may not be sufficient to control obesity in humans. On the other hand, skeletal muscle is the largest organ and a major contributor to basal metabolic rate and increasing energy expenditure in muscle through nonshivering thermogenic mechanisms, which can substantially affect whole body metabolism and weight gain. In this review we will describe the role of Sarcolipin-mediated uncoupling of Sarcoplasmic Reticulum Calcium ATPase (SERCA) as a potential mechanism for increased energy expenditure both during cold and diet-induced thermogenesis.
Obesity results from an imbalance in caloric intake over energy expenditure and is a major health burden with annual costs exceeding 100 billion dollars [12]. The abundance of caloric-rich diets and lack of physical activity has increased the global occurrence of obesity at an alarming rate; equally as alarming is the drastically increasing prevalence of obesity among children [34]. The World Health Organization has identified obesity as one of the major emerging chronic diseases of the 21st century. Obesity increases the risk of type 2 diabetes mellitus, hypertension, dyslipidemias, and cardiovascular disease, reducing life expectancy. Thirty-six percent of United States adults are obese and many cannot lose sufficient weight to improve health with lifestyle interventions alone. The currently available weight loss drugs cannot effectively control obesity without serious health side effects. More often than not, physicians recommend regular exercise as the most effective way of controlling weight gain, perhaps second only to dietary caloric restriction. However, it has been extremely difficult to enforce regular exercise to prevent weight gain. A recent study warns of the urgent need for safe and effective strategies to curb the rising prevalence of obesity, and medications may play more prominent role in future therapeutic regimens [5].
Skeletal muscle is the largest organ in the body; in most mammals it makes up to ~45% to 55% body mass and is a major determinant of the basal metabolic rate [678]. Importantly, muscle can be recruited to increase energy expenditure several fold through physical activity, including sports, voluntary exercise, and/or resistance weight training [91011]. Muscle is responsible for consuming nearly 80% of insulin-stimulated glucose uptake; thus, serving a major role in glucose disposal [912]. During prolonged energy demand, muscle has the ability to switch from carbohydrates to fatty acid utilization. In addition to being a contractile machine, skeletal muscle plays a central role in temperature homeostasis; it can be recruited to produce heat through shivering and nonshivering thermogenesis (NST) [1314]. There is also evidence that skeletal muscle plays an important role in diet-induced thermogenesis [1516]. Heat production through skeletal muscle shivering is a known mechanism; however, its ability to generate heat through nonshivering mechanisms is not well understood. Studies from our laboratory and others have shown that futile sarcoplasmic reticulum calcium ATPase (SERCA) pump activity induced by sarcolipin (SLN) binding can lead to increased heat production and energy expenditure in muscle (Fig. 1) [1718192021]. The primary objective of this review is to highlight recent progress on our understanding of muscle thermogenesis and their role in energy expenditure and whole body metabolism.
Muscle is the primary thermogenic organ in most vertebrates, since muscle contraction is coupled to heat production [2223]. During muscle contraction, heat is generated through both myosin-mediated adenosine triphosphate (ATP) hydrolysis and Ca2+ transport driven by the SERCA pump. It is well known that heat production in muscle is beneficial, since muscles perform better once warmed up; however, prolonged muscle activity can generate excessive amount of heat. Contraction-mediated heat production is exploited by shivering, a repetitive mode of involuntary contractions resulting in excessive heat production. High intensity shivering activates large muscles and increases glycolysis as the main source for heat production. Since no work is done during shivering, the major part of the chemical energy is liberated as heat within muscle tissue. Constant shivering can be detrimental because it exhausts the muscle and therefore, nonshivering thermogenic mechanisms have evolved to better adapt to colder environments. Many ectoderms have adapted muscle to produce partial endothermy. Among them, fish and reptiles can exploit rhythmic muscle contractions to generate local heat in times of need. To achieve cranial endothermy, for instance, certain types of fish like the opah (Lampris guttatus) have evolved regional endothermy by activating contractions of the extraocular muscles in order to elevate cranial temperatures [24]. Muscle heat production provides selective advantage for the opah: (1) it protects the central nervous system from cold and (2) enhances vision and detection of prey. Among reptiles, brooding pythons can use a type of shivering thermogenesis to keep their eggs warm to promote embryonic development, and then revert to heterothermy after brooding. These examples illustrate that contraction-based heat production has been exploited by vertebrates to achieve partial endothermy long before complete endothermy evolved in birds and mammals.
In addition to contraction-dependent heat production, certain species of deep sea fishes have evolved a unique mechanism of heat production through a continuous process of Ca2+ release and reuptake [22]. These species of fish include bill fish, sword fish, tuna, and mackerel which have modified muscle to become a heater organ. The heater organ is derived from extra ocular eye muscle which lacks the typical myofibrillar structure but is instead, densely packed with mitochondria and extensive sarcoplasmic reticulum (SR) networks in between [22]. The SR is equipped with both Ca2+ release and reuptake mechanisms found in most muscle. It is believed that neuronal stimulation depolarizes the heater organ sarcolemmal membrane leading to SR-Ca2+ release through the ryanodine receptor (RyR), subsequently activating SR-Ca2+ ATPase to transport the myoplasmic Ca2+ across SR membrane. The translocation of calcium ions from the myoplasm to the SR lumen by SERCA requires ATP hydrolysis; thus, heat is produced by SERCA's ATPase activity without needing muscle contraction. This type of heat production involves futile Ca2+ cycling which can be energetically costly. However, the increased energy demand is well supported by an abundant mitochondrial population in these specialized cells. Of note, fishes have no brown adipose tissue (BAT) so they rely primarily on striated muscle to generate heat. These studies in fish led to the suggestion that muscle can also generate heat independently of muscle contraction through futile SR Ca2+ cycling.
Skeletal muscle plays an important role in both activity-dependent and independent heat production. Even while an animal is at rest, muscle can contribute to a significant amount of basal energy expenditure and heat production due to its high metabolic activity. Among the mechanisms that contribute to basal heat production is intracellular calcium ion homeostasis driven by SERCA. The SERCA pump depends on ATP hydrolysis for Ca2+ uptake; it translocates 2 Ca2+ ions per ATP molecule hydrolyzed. In resting conditions, the SR luminal concentration of Ca2+ is high (1×10–3M) compared to low cytoplasmic Ca2+ (1×10–7M), which produces a 10,000-fold concentration gradient. Due to this strong gradient, the RyR channel is under high luminal pressure and can spontaneously leak Ca2+, a phenomenon that may be exacerbated by both physiological and pathological changes to RyR protein and or its immediate lipid environment. Malignant hyperthermia (MH), a genetic life threatening disease, is one such example where continuous Ca2+ recycling by the SR membrane can lead to excessive heat production by muscle. MH patients are susceptible to volatile anesthetics (halothane) and often end up with abnormal contracture and hyperthermia [25]. First identified in 1960 in an Australian family who lost 10 members of the family accidently during surgical anesthetics, the disease is found also in pigs, and it is now known that the genetic defect is largely due to mutations in RyR, which encodes the Ca2+ release channel present primarily in skeletal muscle [262728]. The consequence of mutations in the RyR gene is a sustained Ca2+ release following anesthetic exposure; however, the release mechanism itself is not responsible for heat production. A sustained elevation of myoplasmic Ca2+ results in (1) abnormal contracture of muscle due to inability to relax and (2) chronic SERCA pump activity due to continuous Ca2+ leak which results in excessive heat production. Thus, futile Ca2+ cycling by SERCA pump is the primary mechanism for heat production. On the other hand, a sustained level of cytoplasmic Ca2+ activates glycolysis and oxidative metabolism through Ca2+-dependent enzymes, and by Ca2+ itself entering through mitochondria uniporter and acting as a second messenger to activate key enzymes (pyruvate dehydrogenase, ATP synthase). Without pharmacological intervention this can lead to both excessive heat production and energy demand resulting in a hypermetabolic state. Since the development of the drug named dantrolene, an inhibitor of RyR, MH has been tightly controlled [29]. Studies in MH in both pigs and human have highlighted that SR Ca2+ cycling can be an important mechanism for heat production and energy expenditure. However, its contribution to the latter is often overlooked by muscle physiologists due to the belief that it is a component of contractile activity of the muscle.
SKELETAL MUSCLE, FIBER TYPES, AND THEIR ROLE IN THERMOGENESIS AND METABOLISM
Skeletal muscle is highly dependent on energy supply, and its energy demand varies by several orders of magnitude depending on its needs (active or at rest), and depending on the fiber type. Thus, energy metabolism has to be tightly regulated in order to meet varying energy requirements [30]. Mammalian skeletal muscle was initially characterized into fast and slow fiber types, based on their contractile characteristics that are determined by myosin isoforms IIb, IIa, IIx, and type I. But the skeletal muscle has also been classified into three different fiber types based on their metabolic characteristics, as follows.

Slow oxidative fibers

These fibers are found in muscle groups that are responsible for posture maintenance such as soleus muscle. The slow twitch muscle expresses type I myosin isoform, SERCA2a, and SLN. It is red in color due to high vascularization, is quite rich in mitochondria and predominantly relies on fatty acid as a substrate to meet the high-energy demands of the postural muscles. These muscles contract slowly, produce lesser force but are more resistant to fatigue, and are recruited during prolonged muscle activity such as marathon running and adaptation to cold.

Fast oxidative fibers

These fibers are abundant in most muscle groups in large mammals. These fibers express type IIA myosin isoform, SERCA1a, and SLN. They have an intermediate diameter, capillary volume and mitochondrial density. These fibers can generate explosive power for a short period and are often recruited during short burst of activities such as basketball, soccer, tennis, and hockey. They rely on both glycolysis and oxidative metabolism and have the ability to switch between carbohydrates and fatty acid utilization depending on substrate availability. These muscle fibers produce more force but they exhibit less fatigue resistance, so they are in the middle of the muscle fiber spectrum.

Fast glycolytic fibers

These muscle fibers are the fastest and they can generate the most power and speed, and they are present in large muscle groups including gastrocnemius and quadriceps. They express type 2b and 2x myosin isoforms, SERCA1a but do not contain SLN. These types of fibers are recruited in activities that require an all-out burst of power and only act for an extremely short period of time, as the total length of their contractions usually last ~7.5 milliseconds. They tend to fatigue very quickly compared to fast oxidative fibers because they rely primarily on anaerobic glycolysis to produce ATP, a process in which lactic acid accumulates and promotes a condition called acidosis, compromising muscle function.
All three types of muscle fibers are recruited during shivering-induced thermogenesis, although some studies have suggested that glycolytic fibers are most recruited during high intensity shivering in rodents and oxidative fibers during low intensity shivering. During prolonged cold adaptation shivering is completely replaced by NST and the mechanism behind NST is just only beginning to be understood.
Shivering is the most well-known form of heat production in muscle and it is activated during an acute cold exposure. Only birds and mammals have the ability to shiver, and the mechanism is similar to muscle contraction. During shivering, heat is primarily produced by the major ATP-utilizing enzymes, notably, myosin ATPase and SERCA. Although shivering is the first response to an acute cold exposure, shivering is energetically very costly and may even compromise muscle function. In addition to shivering, mammals have evolved NST mechanisms to adapt and thrive in colder climates. Pioneering studies performed in newborn mammals and rodents have shown that BAT is an important site of NST [313233]. BAT is a highly specialized organ enriched with mitochondria that expresses a mitochondrial transmembrane protein called uncoupling protein 1 (UCP1) [31323334]. Significant progress has been made towards understanding the activation and regulation of UCP1-dependent thermogenesis in BAT [353637]. However, in large mammals including humans, BAT is restricted to neonatal stages and becomes a minor component in adult life. Therefore, large mammals especially humans have to rely on muscle-based thermogenesis for temperature homeostasis [23]. Interestingly, BAT is either absent or inactive in certain endotherms, particularly in birds. In some mammals (boars and pigs), the gene encoding UCP1 is mutated and they must completely rely on muscle for thermogenesis [23]. These findings suggested that there must be other NST which may also contribute to whole body temperature (Tc).
The first evidence that skeletal muscle can also be an important site of NST comes from studies performed in avian species by Duchamp et al. [3839]. Using direct blood-flow measurements in 5-week thermoneutral- (TN, 25℃) and cold-acclimatized (CA, 4℃) ducklings (Cairina moschata), and then exposed to 8℃, they were able to show that total muscle blood flow increased equally in the TN and CA ducklings, but the CA ducklings did not shiver compared to TN. Both groups were also able to maintain Tc in the optimal range [3839]. Thus, skeletal muscles from CA ducklings were able to produce the same amount of heat as muscles from shivering TN ducklings, demonstrating the existence of NST in skeletal muscle. Although these studies identified that muscle could serve as a site of NST, they did not provide a detailed mechanism for the source of heat production. In a subsequent study, Dumonteil et al. [40] performed detailed analyses to show how changes in SERCA and RyR gene expression patterns coincided with the activation of NST. Thus, these studies indicated that enhanced Ca2+ cycling could be responsible for muscle-based NST. Studies conducted by Arruda et al. [4142] also showed that when rabbits are CA, SERCA1 expression is increased in red muscle (SERCA2 levels are unaffected) but not in white muscle. Furthermore, in vitro preparations of these CA muscles showed that cold exposure increased the heat released during ATP hydrolysis 2-fold in red muscle, in which oxidative (mitochondrial) capacity is at least 2-fold greater than white muscle. Thus, cold exposure increased the heat-generating capacity of rabbit red muscle [43]. These results also suggest that enhanced Ca2+ cycling might be involved in heat production.
The SERCA pump plays a central role in SR Ca2+ cycling and muscle contraction. By actively transporting Ca2+, it maintains a low cytosolic but a high luminal SR Ca2+ concentration. The SERCA pump in skeletal muscle is encoded by SERCA1 and SERCA2 genes; SERCA1a being the major isoform in fast twitch fibers, whereas the slow twitch/oxidative fibers express both SERCA1a and SERCA2a protein [144445]. SERCA activity is regulated by two small molecular weight proteins in muscle, namely phospholamban (PLB, 52 aa) and SLN (31 aa) [171946]. Although PLB and SLN occupy the same site on SERCA protein, they affect SERCA pump activity very differently. PLB binding inhibits SERCA pump activity (at low cytosolic Ca2+) and its inhibitory interaction is relieved by an increase in cytosolic Ca2+ and or phosphorylation of PLB. The mechanism of PLB interaction and regulation of SERCA pump activity has been extensively reviewed and therefore will not be discussed here. SLN is encoded by a single gene, composed of two exons and differs structurally from PLB. SLN expression is predominant in skeletal muscle but is also present in atrial chamber of the heart [46]. SLN protein expression is high in embryonic/neonatal skeletal muscle; whereas in adult stages it is absent in glycolytic muscle fibers but is expressed abundantly in oxidative and slow twitch muscle fibers. In comparison to rodents, SLN expression is several folds higher in large mammals (including human) due to the high proportion of oxidative/slow twitch fibers [1323].
Although SLN was discovered nearly 30 years ago, its exact function remained largely unknown. In an effort to understand its role in muscle, we began studying how SLN binding affects SERCA activity using an in vitro biochemical approach. Our biochemical studies showed that SLN binds to SERCA even at high cytoplasmic Ca2+ and remains bound to SERCA during the Ca2+ transport cycle. In contrast, PLB binding to SERCA only occurs in the Ca2+-free state; therefore, Ca2+ and PLB binding to SERCA are mutually exclusive. Interestingly, SLN binding to SERCA does not affect ATP hydrolysis, but decreases the Vmax of Ca2+ uptake by blocking Ca2+ transport into the SR lumen. Using reconstituted synthetic SLN and SERCA, Mall et al. [47] and Smith et al. [48] initially proposed the idea that SLN binding to SERCA could promote uncoupling of ATP hydrolysis from Ca2+ transport. They showed that Ca2+ accumulation in the vesicles decreased, but the heat released by SERCA increased in the presence of SLN. These studies suggested that SLN binding to SERCA promotes slippage of Ca2+ back into the cytosol and the energy from the resulting ATP hydrolysis would thus be released as heat, without any Ca2+ transport. These and other studies suggested that binding of SLN promotes futile cycling of SERCA pump, resulting in a total increase in ATP hydrolysis and heat production.
Although initial in vitro studies predicted that SLN could play a role in muscle thermogenesis, direct evidence in support of this was missing. Therefore, our laboratory generated SLN knockout mice (SLN-KO) and explored how SLN impacts muscle function and muscle-based thermogenesis [2021]. Interestingly, loss of SLN did not affect muscle growth and/or function and the KO mice could not be distinguished easily from its wild type (WT) littermates. Regarding muscle-based thermogenesis, we decided to challenge the SLN-KO mice to acute cold (4℃) in a temperature controlled Comprehensive Lab Animal Monitoring System (CLAMS) set up [20]. We surgically removed interscapular BAT (iBAT) to minimize contribution from BAT, a key contributor to thermogenesis. Surprisingly, we found that iBAT-ablated SLN-KO mice were unable to maintain their Tc; within the first 4 hours, the majority developed hypothermia, and would die if not removed from cold [20]. On the other hand, WT (iBAT-ablated control mice) were able to maintain their body Tc despite having SLN expression restricted mainly to oxidative fibers that are non-abundant in mice, what highlights the importance of SLN in muscle thermogenesis. This was further confirmed by the finding that SLN-KO mice could be rescued following reintroduction of SLN [2049]. These in vivo studies using SLN null mice validated the initial in vitro findings, which suggested that SLN interaction with SERCA promotes uncoupling of SERCA, resulting in increased ATP hydrolysis and heat production.
Unlike large mammals, rodents contain substantial BAT in their adult life and BAT is very important for cold adaptation in rodents. Interestingly, studies in UCP1-KO mice showed that while these mice are cold sensitive, they can be gradually cold adapted to 4℃, suggesting compensation by muscle-based thermogenic mechanisms [50]. Therefore, we examined if there was a cross-talk between muscle and BAT-dependent thermogenesis during cold adaptation and if they could compensate for each other when one mechanism would fail. Our studies revealed that cold adaptation in mice relies on both muscle and BAT-based thermogenesis. Interestingly, even mild cold exposure recruits both muscle and BAT-based heat production [51]. We next investigated if muscle could compensate for the loss of BAT function using either iBAT-ablated or UCP1-KO. We found that gradual cold adaptation of iBAT ablated or UCP1-KO mice upregulates SLN expression in the skeletal muscle; which suggests that muscle thermogenesis is recruited to a greater extent when BAT function is minimized [515253]. We have also shown that when iBAT was surgically removed, the mice were able to adapt to cold but at an increased energy cost [51]. The skeletal muscles in these mice underwent extensive remodeling of both SR and mitochondria, including alteration in the expression of key components of Ca2+ handling such as SLN, SERCA, and RyR1. Interestingly, when neonatal mice were cold-adapted to 4℃, the normally occurring developmental SLN downregulation in fast twitch muscle was prevented. These studies further showed that SLN/SERCA-based thermogenesis could be an important NST mechanism in skeletal muscle.
The concept of diet induced thermogenesis (DIT) was first described by Rothwell and Stock [54] and Stock [55]. They showed that rodents can increase energy expenditure in response to overfeeding to prevent excessive weight gain. They suggested that (DIT) can be beneficial to dispose excess calories and prevent metabolic diseases. The role of BAT and UCP1 has been extensively studied as a major mechanism for DIT in rodents [333637555657]. Although the detailed mechanism responsible for DIT remains less well understood, there is substantial evidence to show that diet rich in fat activates heat production in BAT due to increased sympathetic nervous system activity [58]. Since muscle is a consumer of metabolites and SLN uncoupling of SERCA can increase energy expenditure, we wanted to further explore the role of SLN in diet-induced thermogenesis in muscle. We initially showed that SLN-KO mice were prone to diet-induced obesity when fed with high fat diet (HFD); whereas WT mice showed increased SLN expression [20]. To understand the relative contribution of BAT versus skeletal muscle to DIT, UCP1-KO, SLN-KO, and SLN overexpression (SLN-OE) mice were fed with a HFD for a period of 12 weeks [5960]. A key finding was that SLN-KO mice gained comparable weight as UCP1-KO mice on HFD, suggesting that loss of muscle-based thermogenesis has similar consequences on weight gain as loss of BAT-mediated DIT [60]. This may suggest that both SLN- and UCP1-based thermogenesis contribute to DIT to a similar extent in rodents. Although SLN-KO mice had intact BAT, SLN deficiency was sufficient to cause increased obesity, which suggests that muscle-based NST is a critical component of DIT and can be very well recruited during caloric excess. We further investigated if SLN-OE in both glycolytic and oxidative muscles can be beneficial to increase fatty acid oxidative metabolism. We found that mice overexpressing SLN were significantly less obese than WT mice and were resistant to HFD-induced obesity [59]. An interesting finding was that fast glycolytic skeletal muscles such as tibialis anterior and extensor digitorum longus from SLN-OE mice showed a striking increase in mitochondrial content and upregulation of metabolic enzymes involved in fatty acid oxidation, suggesting that SLN promotes oxidative metabolism. Considering that muscle represents ~45% to 50% body mass, even small increases in the energy demand/expenditure in muscle can have significant effects on whole-body energy expenditure [1516]. These studies led us to suggest that SLN expression can create both energy demand and increase energy expenditure through increased oxidative metabolism and can be a novel mechanism to increase energy expenditure in muscle.
Obesity and diabetes have increased globally during the last two decades at an alarming rate. Many factors have contributed to the growth and prevalence of obesity. These include excessive consumption of caloric-rich diet, limited physical activity and urban life style. There are no effective treatments to reduce obesity other than caloric restriction and exercise which are difficult to enforce on a daily basis. Our hope is to look for answers within our own body and, skeletal muscle has enormous potential due to its ability to increase metabolism significantly and may be our best choice to increase energy expenditure. As a result of life style change, there is a significant reduction in physical activity, and so we have to find alternate ways to promote energy expenditure and even if it entails taking pills to enhance this process. The discovery of SLN as an uncoupler of SERCA pump provides a promising target to increase energy expenditure in muscle. The molecular basis behind NST requires further investigation towards the identification of upstream mechanisms and pathways from SLN to induce muscle NST. It is our hope that future research will endeavor to identify novel targets to pharmacologically activate energy expenditure in muscle, since this will become critical in conditions where physical activity is increasingly limited. One of the directions worth exploring is the synergistic effect of both cold and pharmacological agents known to increase energy expenditure in muscle, in a combined therapy.
Acknowledgements
We thank all the previous members of Dr. Periasamy laboratory who have contributed to the original studies cited in this review manuscript. This work was supported in part, by National Institutes of Health Grants R01-HL 088555 and R01 DK098240 and a basic Science grant from ADA 7-13-BS-131 to Muthu Periasamy.

CONFLICTS OF INTEREST: No potential conflict of interest relevant to this article was reported.

  • 1. Spiegelman BM, Flier JS. Obesity and the regulation of energy balance. Cell 2001;104:531-543. ArticlePubMed
  • 2. Lepor NE, Fouchia DD, McCullough PA. New vistas for the treatment of obesity: turning the tide against the leading cause of morbidity and cardiovascular mortality in the developed world. Rev Cardiovasc Med 2013;14:20-39. ArticlePubMed
  • 3. Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK, Flegal KM. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA 2016;315:2292-2299. ArticlePubMedPMC
  • 4. Ogden CL, Carroll MD, Fryar CD, Flegal KM. Prevalence of obesity among adults and youth: United States, 2011-2014. NCHS Data Brief 2015;(219):1-8.
  • 5. Padwal R, Li SK, Lau DC. Long-term pharmacotherapy for overweight and obesity: a systematic review and meta-analysis of randomized controlled trials. Int J Obes Relat Metab Disord 2003;27:1437-1446. ArticlePubMedPDF
  • 6. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985) 2000;89:81-88. ArticlePubMed
  • 7. Zurlo F, Nemeth PM, Choksi RM, Sesodia S, Ravussin E. Whole-body energy metabolism and skeletal muscle biochemical characteristics. Metabolism 1994;43:481-486. ArticlePubMed
  • 8. Zurlo F, Larson K, Bogardus C, Ravussin E. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 1990;86:1423-1427. ArticlePubMedPMC
  • 9. Ferrannini E, Simonson DC, Katz LD, Reichard G Jr, Bevilacqua S, Barrett EJ, Olsson M, DeFronzo RA. The disposal of an oral glucose load in patients with non-insulin-dependent diabetes. Metabolism 1988;37:79-85. ArticlePubMed
  • 10. Kelley DE. Skeletal muscle fat oxidation: timing and flexibility are everything. J Clin Invest 2005;115:1699-1702. ArticlePubMedPMC
  • 11. Turner N, Cooney GJ, Kraegen EW, Bruce CR. Fatty acid metabolism, energy expenditure and insulin resistance in muscle. J Endocrinol 2014;220:T61-T79. ArticlePubMed
  • 12. Thiebaud D, Jacot E, DeFronzo RA, Maeder E, Jequier E, Felber JP. The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man. Diabetes 1982;31:957-963. ArticlePubMedPDF
  • 13. Pant M, Bal NC, Periasamy M. Sarcolipin: a key thermogenic and metabolic regulator in skeletal muscle. Trends Endocrinol Metab 2016;27:881-892. ArticlePubMedPMC
  • 14. Periasamy M, Maurya SK, Sahoo SK, Singh S, Sahoo SK, Reis FCG, Bal NC. Role of SERCA pump in muscle thermogenesis and metabolism. Compr Physiol 2017;7:879-890. ArticlePubMedPDF
  • 15. Lowell BB, Bachman ES. Beta-adrenergic receptors, diet-induced thermogenesis, and obesity. J Biol Chem 2003;278:29385-29388. PubMed
  • 16. Maurya SK, Periasamy M. Sarcolipin is a novel regulator of muscle metabolism and obesity. Pharmacol Res 2015;102:270-275. ArticlePubMedPMC
  • 17. Sahoo SK, Shaikh SA, Sopariwala DH, Bal NC, Periasamy M. Sarcolipin protein interaction with sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA) is distinct from phospholamban protein, and only sarcolipin can promote uncoupling of the SERCA pump. J Biol Chem 2013;288:6881-6889. ArticlePubMedPMC
  • 18. Sahoo SK, Shaikh SA, Sopariwala DH, Bal NC, Bruhn DS, Kopec W, Khandelia H, Periasamy M. The N terminus of sarcolipin plays an important role in uncoupling sarco-endoplasmic reticulum Ca2+-ATPase (SERCA) ATP hydrolysis from Ca2+ transport. J Biol Chem 2015;290:14057-14067. ArticlePubMedPMC
  • 19. Shaikh SA, Sahoo SK, Periasamy M. Phospholamban and sarcolipin: are they functionally redundant or distinct regulators of the sarco(endo)plasmic reticulum calcium ATPase? J Mol Cell Cardiol 2016;91:81-91. ArticlePubMed
  • 20. Bal NC, Maurya SK, Sopariwala DH, Sahoo SK, Gupta SC, Shaikh SA, Pant M, Rowland LA, Bombardier E, Goonasekera SA, Tupling AR, Molkentin JD, Periasamy M. Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat Med 2012;18:1575-1579. ArticlePubMedPMCPDF
  • 21. Babu GJ, Bhupathy P, Timofeyev V, Petrashevskaya NN, Reiser PJ, Chiamvimonvat N, Periasamy M. Ablation of sarcolipin enhances sarcoplasmic reticulum calcium transport and atrial contractility. Proc Natl Acad Sci U S A 2007;104:17867-17872. ArticlePubMedPMC
  • 22. Block BA. Thermogenesis in muscle. Annu Rev Physiol 1994;56:535-577. ArticlePubMed
  • 23. Rowland LA, Bal NC, Periasamy M. The role of skeletal-muscle-based thermogenic mechanisms in vertebrate endothermy. Biol Rev Camb Philos Soc 2015;90:1279-1297. ArticlePubMed
  • 24. Runcie RM, Dewar H, Hawn DR, Frank LR, Dickson KA. Evidence for cranial endothermy in the opah (Lampris guttatus). J Exp Biol 2009;212(Pt 4):461-470. ArticlePubMedPMCPDF
  • 25. Rosenberg H, Pollock N, Schiemann A, Bulger T, Stowell K. Malignant hyperthermia: a review. Orphanet J Rare Dis 2015;10:93ArticlePubMedPMCPDF
  • 26. MacLennan DH. The genetic basis of malignant hyperthermia. Trends Pharmacol Sci 1992;13:330-334. ArticlePubMed
  • 27. MacLennan DH, Otsu K, Fujii J, Zorzato F, Phillips MS, O'Brien PJ, Archibald AL, Britt BA, Gillard EF, Worton RG. The role of the skeletal muscle ryanodine receptor gene in malignant hyperthermia. Symp Soc Exp Biol 1992;46:189-201. PubMed
  • 28. MacLennan DH, Phillips MS. Malignant hyperthermia. Science 1992;256:789-794. ArticlePubMed
  • 29. Sharma A, Karnik H, Kukreja S, Jagger K. Malignant hyperthermia: dantrolene sodium. A must have. Indian J Anaesth 2012;56:212-213. ArticlePubMedPMC
  • 30. Das AM, Steuerwald U, Illsinger S. Inborn errors of energy metabolism associated with myopathies. J Biomed Biotechnol 2010;2010:340849ArticlePubMedPMCPDF
  • 31. Cannon B, Houstek J, Nedergaard J. Brown adipose tissue. More than an effector of thermogenesis? Ann N Y Acad Sci 1998;856:171-187. PubMed
  • 32. Cannon B, Jacobsson A, Rehnmark S, Nedergaard J. Signal transduction in brown adipose tissue recruitment: noradrenaline and beyond. Int J Obes Relat Metab Disord 1996;20(Suppl 3):S36-S42. PubMed
  • 33. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359. ArticlePubMed
  • 34. Kozak LP, Harper ME. Mitochondrial uncoupling proteins in energy expenditure. Annu Rev Nutr 2000;20:339-363. ArticlePubMed
  • 35. Meyer CW, Willershauser M, Jastroch M, Rourke BC, Fromme T, Oelkrug R, Heldmaier G, Klingenspor M. Adaptive thermogenesis and thermal conductance in wild-type and UCP1-KO mice. Am J Physiol Regul Integr Comp Physiol 2010;299:R1396-R1406. ArticlePubMedPMC
  • 36. Kozak LP, Anunciado-Koza R. UCP1: its involvement and utility in obesity. Int J Obes (Lond) 2008;32(Suppl 7):S32-S38. ArticlePubMedPMCPDF
  • 37. Kozak LP, Koza RA. Mitochondria uncoupling proteins and obesity: molecular and genetic aspects of UCP1. Int J Obes Relat Metab Disord 1999;23(Suppl 6):S33-S37. PubMed
  • 38. Duchamp C, Barre H. Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings. Am J Physiol 1993;265(5 Pt 2):R1076-R1083. ArticlePubMed
  • 39. Duchamp C, Cohen-Adad F, Rouanet JL, Barre H. Histochemical arguments for muscular non-shivering thermogenesis in muscovy ducklings. J Physiol 1992;457:27-45. ArticlePubMedPMC
  • 40. Dumonteil E, Barre H, Meissner G. Sarcoplasmic reticulum Ca(2+)-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis. Am J Physiol 1993;265(2 Pt 1):C507-C513. ArticlePubMed
  • 41. Arruda AP, Nigro M, Oliveira GM, de Meis L. Thermogenic activity of Ca2+-ATPase from skeletal muscle heavy sarcoplasmic reticulum: the role of ryanodine Ca2+ channel. Biochim Biophys Acta 2007;1768:1498-1505. ArticlePubMed
  • 42. Arruda AP, Ketzer LA, Nigro M, Galina A, Carvalho DP, de Meis L. Cold tolerance in hypothyroid rabbits: role of skeletal muscle mitochondria and sarcoplasmic reticulum Ca2+ ATPase isoform 1 heat production. Endocrinology 2008;149:6262-6271. ArticlePubMedPDF
  • 43. de Meis L, Arruda AP, Carvalho DP. Role of sarco/endoplasmic reticulum Ca(2+)-ATPase in thermogenesis. Biosci Rep 2005;25:181-190. ArticlePubMedPDF
  • 44. Periasamy M, Kalyanasundaram A. SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 2007;35:430-442. ArticlePubMed
  • 45. Periasamy M, Huke S. SERCA pump level is a critical determinant of Ca(2+)homeostasis and cardiac contractility. J Mol Cell Cardiol 2001;33:1053-1063. ArticlePubMed
  • 46. Babu GJ, Bhupathy P, Carnes CA, Billman GE, Periasamy M. Differential expression of sarcolipin protein during muscle development and cardiac pathophysiology. J Mol Cell Cardiol 2007;43:215-222. ArticlePubMedPMC
  • 47. Mall S, Broadbridge R, Harrison SL, Gore MG, Lee AG, East JM. The presence of sarcolipin results in increased heat production by Ca(2+)-ATPase. J Biol Chem 2006;281:36597-36602. ArticlePubMed
  • 48. Smith WS, Broadbridge R, East JM, Lee AG. Sarcolipin uncouples hydrolysis of ATP from accumulation of Ca2+ by the Ca2+-ATPase of skeletal-muscle sarcoplasmic reticulum. Biochem J 2002;361(Pt 2):277-286. ArticlePubMedPMCPDF
  • 49. Sopariwala DH, Pant M, Shaikh SA, Goonasekera SA, Molkentin JD, Weisleder N, Ma J, Pan Z, Periasamy M. Sarcolipin overexpression improves muscle energetics and reduces fatigue. J Appl Physiol (1985) 2015;118:1050-1058. ArticlePubMedPMC
  • 50. Ukropec J, Anunciado RP, Ravussin Y, Hulver MW, Kozak LP. UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1-/- mice. J Biol Chem 2006;281:31894-31908. ArticlePubMed
  • 51. Bal NC, Maurya SK, Singh S, Wehrens XH, Periasamy M. Increased reliance on muscle-based thermogenesis upon acute minimization of brown adipose tissue function. J Biol Chem 2016;291:17247-17257. ArticlePubMedPMC
  • 52. Rowland LA, Bal NC, Kozak LP, Periasamy M. Uncoupling protein 1 and sarcolipin are required to maintain optimal thermogenesis, and loss of both systems compromises survival of mice under cold stress. J Biol Chem 2015;290:12282-12289. ArticlePubMedPMC
  • 53. Bal NC, Singh S, Reis FCG, Maurya SK, Pani S, Rowland LA, Periasamy M. Both brown adipose tissue and skeletal muscle thermogenesis processes are activated during mild to severe cold adaptation in mice. J Biol Chem 2017;292:16616-16625. ArticlePubMedPMC
  • 54. Rothwell NJ, Stock MJ. Diet-induced thermogenesis. Adv Nutr Res 1983;5:201-220. ArticlePubMed
  • 55. Stock MJ. The role of brown adipose tissue in diet-induced thermogenesis. Proc Nutr Soc 1989;48:189-196. ArticlePubMed
  • 56. Kozak LP. Brown fat and the myth of diet-induced thermogenesis. Cell Metab 2010;11:263-267. ArticlePubMedPMC
  • 57. Kozak LP, Koza RA, Anunciado-Koza R. Brown fat thermogenesis and body weight regulation in mice: relevance to humans. Int J Obes (Lond) 2010;34(Suppl 1):S23-S27. ArticlePubMedPDF
  • 58. Rothwell NJ, Stock MJ. Sympathetic and adrenocorticoid influences on diet-induced thermogenesis and brown fat activity in the rat. Comp Biochem Physiol A Comp Physiol 1984;79:575-579. ArticlePubMed
  • 59. Maurya SK, Bal NC, Sopariwala DH, Pant M, Rowland LA, Shaikh SA, Periasamy M. Sarcolipin is a key determinant of the basal metabolic rate, and its overexpression enhances energy expenditure and resistance against diet-induced obesity. J Biol Chem 2015;290:10840-10849. ArticlePubMedPMC
  • 60. Rowland LA, Maurya SK, Bal NC, Kozak L, Periasamy M. Sarcolipin and uncoupling protein 1 play distinct roles in diet-induced thermogenesis and do not compensate for one another. Obesity (Silver Spring) 2016;24:1430-1433. ArticlePubMedPMC
Fig. 1

Proposed mechanism to show how sarcolipin (SLN)/sarcoendoplasmic reticulum calcium APTase (SERCA) interaction affects muscle metabolism. SERCA uses adenosine triphosphate (ATP) hydrolysis to actively transport Ca2+ from the cytosol into the sarcoplasmic reticulum lumen. SLN and Ca2+ bind competitively to SERCA during Ca2+ transport. SLN binding to SERCA does not inhibit ATP hydrolysis but prevents Ca2+ transport by a mechanism named uncoupling, where Ca2+ slips back into cytosol. Uncoupling of SERCA leads to futile cycling of the SERCA pump resulting in increased ATP hydrolysis/heat production; thus, creating energy demand. Uncoupling of SERCA increases cytosolic Ca2+ acutely, thereby promoting Ca2+ entry into mitochondria matrix activating the oxidative metabolism and ATP synthesis. RyR1, ryanodine receptor 1; ADP, adenosine diphosphate; Pi, inorganic phosphate.

dmj-41-327-g001.jpg

Figure & Data

References

    Citations

    Citations to this article as recorded by  
    • Nutrition as the foundation for successful aging: a focus on dietary protein and omega-3 polyunsaturated fatty acids
      Aubree L Hawley, Jamie I Baum
      Nutrition Reviews.2024; 82(3): 389.     CrossRef
    • Seasonal adaptation of Mangalica pigs in terms of muscle morphology and metabolism
      Sangwoo Kim, Chisato Nakayama, Daisuke Kondoh, Tatsuki Okazaki, Erina Yoneda, Kisaki Tomita, Motoki Sasaki, Yuki Muranishi
      Anatomia, Histologia, Embryologia.2024;[Epub]     CrossRef
    • In vivo heat production dynamics during a contraction-relaxation cycle in rat single skeletal muscle fibers
      Ayaka Tabuchi, Yoshinori Tanaka, Hiroshi Horikawa, Takuto Tazawa, David C. Poole, Yutaka Kano
      Journal of Thermal Biology.2024; 119: 103760.     CrossRef
    • Echinacoside stimulates myogenesis and ATP-dependent thermogenesis in the skeletal muscle via the activation of D1-like dopaminergic receptors
      Kiros Haddish, Jong Won Yun
      Archives of Biochemistry and Biophysics.2024; 752: 109886.     CrossRef
    • Ectodysplasin A2 receptor signaling in skeletal muscle pathophysiology
      Sevgi Döndü Özen, Serkan Kir
      Trends in Molecular Medicine.2024; 30(5): 471.     CrossRef
    • Chronic melatonin treatment improves obesity by inducing uncoupling of skeletal muscle SERCA-SLN mediated by CaMKII/AMPK/PGC1α pathway and mitochondrial biogenesis in female and male Zücker diabetic fatty rats
      D. Salagre, M. Navarro-Alarcón, M. Villalón-Mir, B. Alcázar-Navarrete, G. Gómez-Moreno, F. Tamimi, A. Agil
      Biomedicine & Pharmacotherapy.2024; 172: 116314.     CrossRef
    • Homotaurine exhibits contrasting effects of DRD1-mediated thermogenesis-related regulators in C2C12 myoblasts and 3T3−L1 white adipocytes
      Kiros Haddish, Jong Won Yun
      Biotechnology and Bioprocess Engineering.2024;[Epub]     CrossRef
    • Hairless (Hr) Deficiency Mitigates High‐Fat Diet‐Induced Obesity and Insulin Resistance in Mice
      Hongwei Wang, Haoyu Guo, Kuicheng Zhu, Long He, Jian‐jun Yang
      Advanced Biology.2024;[Epub]     CrossRef
    • Prediction of resting energy expenditure for adolescents with severe obesity: A multi‐centre analysis
      Amy A. Rydin, Cameron Severn, Laura Pyle, Nazeen Morelli, Ashley H. Shoemaker, Stephanie T. Chung, Jack A. Yanovski, Joan C. Han, Janine A. Higgins, Kristen J. Nadeau, Claudia Fox, Aaron S. Kelly, Melanie G. Cree
      Pediatric Obesity.2024;[Epub]     CrossRef
    • Bile acid metabolism and signaling in health and disease: molecular mechanisms and therapeutic targets
      Joshua S. Fleishman, Sunil Kumar
      Signal Transduction and Targeted Therapy.2024;[Epub]     CrossRef
    • Unveiling the Potential of Natural Compounds: A Comprehensive Review on Adipose Thermogenesis Modulation
      Jaeeun Shin, Yeonho Lee, Seong Hun Ju, Young Jae Jung, Daehyeon Sim, Sung-Joon Lee
      International Journal of Molecular Sciences.2024; 25(9): 4915.     CrossRef
    • 3D Printing of Polysaccharide-Based Hydrogel Scaffolds for Tissue Engineering Applications: A Review
      Arnaud Kamdem Tamo, Lesly Dasilva Wandji Djouonkep, Naomie Beolle Songwe Selabi
      International Journal of Biological Macromolecules.2024; 270: 132123.     CrossRef
    • Remodeling of skeletal muscle myosin metabolic states in hibernating mammals
      Christopher TA Lewis, Elise G Melhedegaard, Marija M Ognjanovic, Mathilde S Olsen, Jenni Laitila, Robert AE Seaborne, Magnus Gronset, Changxin Zhang, Hiroyuki Iwamoto, Anthony L Hessel, Michel N Kuehn, Carla Merino, Nuria Amigo, Ole Frobert, Sylvain Girou
      eLife.2024;[Epub]     CrossRef
    • Relative sarcolipin (SLN) and sarcoplasmic reticulum Ca2+ ATPase (SERCA1) transcripts levels in closely related endothermic and ectothermic scombrid fishes: Implications for molecular basis of futile calcium cycle non-shivering thermogenesis (NST)
      Sean Robinson, Nicholas C. Wegner, Chugey A. Sepulveda, Jens P.C. Franck
      Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology.2024; 295: 111667.     CrossRef
    • The effect of high fat diet and endurance training on newly discovery of nonshivering-thermogenic factors under thermoneutrality in mice
      S. Daneshyar, A. Ghasemnian, Z. Mirakhori, S.J. Daneshyar
      Science & Sports.2023; 38(3): 293.     CrossRef
    • Redox‐metabolic reprogramming of skin in mice lacking functional Nrf2 under basal conditions and cold acclimation
      Tamara Zakic, Sara Stojanovic, Aleksandra Jankovic, Aleksandra Korac, Vanja Pekovic‐Vaughan, Bato Korac
      BioFactors.2023; 49(3): 600.     CrossRef
    • Rats lackingUcp1present a novel translational tool for the investigation of thermogenic adaptation during cold challenge
      Jaycob D. Warfel, Carrie M. Elks, David S. Bayless, Bolormaa Vandanmagsar, Allison C. Stone, Samuel E. Velasquez, Paola Olivares‐Nazar, Robert C. Noland, Sujoy Ghosh, Jingying Zhang, Randall L. Mynatt
      Acta Physiologica.2023;[Epub]     CrossRef
    • SENP2 knockdown in human adipocytes reduces glucose metabolism and lipid accumulation, while increases lipid oxidation
      Solveig A. Krapf, Jenny Lund, Hege G. Bakke, Tuula A. Nyman, Stefano Bartesaghi, Xiao-Rong Peng, Arild C. Rustan, G. Hege Thoresen, Eili T. Kase
      Metabolism Open.2023; 18: 100234.     CrossRef
    • Physiological and molecular mechanisms of cold-induced improvements in glucose homeostasis in humans beyond brown adipose tissue
      Sten van Beek, Dzhansel Hashim, Tore Bengtsson, Joris Hoeks
      International Journal of Obesity.2023; 47(5): 338.     CrossRef
    • Distinct Transcriptional Responses of Skeletal Muscle to Short-Term Cold Exposure in Tibetan Pigs and Bama Pigs
      Chunhuai Yang, Chunwei Cao, Jiali Liu, Ying Zhao, Jianfei Pan, Cong Tao, Yanfang Wang
      International Journal of Molecular Sciences.2023; 24(8): 7431.     CrossRef
    • Distinct and shared endothermic strategies in the heat producing tissues of tuna and other teleosts
      Baosheng Wu, Xueli Gao, Mingling Hu, Jing Hu, Tianming Lan, Tingfeng Xue, Wenjie Xu, Chenglong Zhu, Yuan Yuan, Jiangmin Zheng, Tao Qin, Peidong Xin, Ye Li, Li Gong, Chenguang Feng, Shunping He, Huan Liu, Haimeng Li, Qing Wang, Zhenhua Ma, Qiang Qiu, Kun W
      Science China Life Sciences.2023; 66(11): 2629.     CrossRef
    • Macrophage Involvement in Aging-Associated Skeletal Muscle Regeneration
      Chang-Yi Cui, Luigi Ferrucci, Myriam Gorospe
      Cells.2023; 12(9): 1214.     CrossRef
    • Anti-nucleolin aptamer, iSN04, inhibits the inflammatory responses in C2C12 myoblasts by modulating the β-catenin/NF-κB signaling pathway
      Machi Yamamoto, Mana Miyoshi, Kamino Morioka, Takakazu Mitani, Tomohide Takaya
      Biochemical and Biophysical Research Communications.2023; 664: 1.     CrossRef
    • Building Cetacean Locomotor Muscles throughout Ontogeny to Support High-Performance Swimming into Adulthood
      S R Noren
      Integrative And Comparative Biology.2023; 63(3): 785.     CrossRef
    • Filbertone, (2E)-5-methyl-2-hepten-4-one, regulates thermogenesis and lipid metabolism in skeletal muscle of a high-fat diet fed mice
      Hyemee Kim, Byungyong Ahn
      Applied Biological Chemistry.2023;[Epub]     CrossRef
    • Silencing of dopamine receptor D5 inhibits the browning of 3T3-L1 adipocytes and ATP-consuming futile cycles in C2C12 muscle cells
      Kiros Haddish, Jong Won Yun
      Archives of Physiology and Biochemistry.2023; : 1.     CrossRef
    • Dynamic of irisin secretion change after moderate-intensity chronic physical exercise on obese female
      Desiana Merawati, Sugiharto, Hendra Susanto, Ahmad Taufiq, Adi Pranoto, Dessy Amelia, Purwo Sri Rejeki
      Journal of Basic and Clinical Physiology and Pharmacology.2023; 34(4): 539.     CrossRef
    • Polyamines and Physical Activity in Musculoskeletal Diseases: A Potential Therapeutic Challenge
      Letizia Galasso, Annalisa Cappella, Antonino Mulè, Lucia Castelli, Andrea Ciorciari, Alessandra Stacchiotti, Angela Montaruli
      International Journal of Molecular Sciences.2023; 24(12): 9798.     CrossRef
    • Phosphate toxicity and SERCA2a dysfunction in sudden cardiac arrest
      Ronald B. Brown
      The FASEB Journal.2023;[Epub]     CrossRef
    • Hepatic protein kinase Cbeta deficiency mitigates late-onset obesity
      Yaoling Shu, Nikhil Gumma, Faizule Hassan, Daniel A. Branch, Lisa A. Baer, Michael C. Ostrowski, Kristin I. Stanford, Kedryn K. Baskin, Kamal D. Mehta
      Journal of Biological Chemistry.2023; 299(8): 104917.     CrossRef
    • Functional expression of the thermally activated transient receptor potential channels TRPA1 and TRPM8 in human myotubes
      Christine Skagen, Nils Gunnar Løvsletten, Lucia Asoawe, Zeineb Al-Karbawi, Arild C. Rustan, G. Hege Thoresen, Fred Haugen
      Journal of Thermal Biology.2023; 116: 103623.     CrossRef
    • Natural products as novel anti-obesity agents: insights into mechanisms of action and potential for therapeutic management
      Ummul Fathima Shaik Mohamed Sayed, Said Moshawih, Hui Poh Goh, Nurolaini Kifli, Gaurav Gupta, Sachin Kumar Singh, Dinesh Kumar Chellappan, Kamal Dua, Andi Hermansyah, Hooi Leng Ser, Long Chiau Ming, Bey Hing Goh
      Frontiers in Pharmacology.2023;[Epub]     CrossRef
    • Recent advancements in pharmacological strategies to modulate energy balance for combating obesity
      Benudhara Pati, Satyabrata Sendh, Bijayashree Sahu, Sunil Pani, Nivedita Jena, Naresh Chandra Bal
      RSC Medicinal Chemistry.2023; 14(8): 1429.     CrossRef
    • CCE and EODF as two distinct non-shivering thermogenesis models inducing weight loss
      Tianyi Xu, Juan Wang, Hongwei Shi, Xiaofang Wei, Huiling Zhang, Yunyan Ji, Shiting Lu, Yi Yan, Xiuju Yu, Xiaomao Luo, Haidong Wang
      Pflügers Archiv - European Journal of Physiology.2023; 475(8): 961.     CrossRef
    • Birth and the Pathway to Adulthood: Integration across Development, Environment, and Evolution
      Christopher J Mayerl, Terry R Dial, Mark C Mainwaring, Ashley M Heers, Rebecca Z German
      Integrative And Comparative Biology.2023; 63(3): 548.     CrossRef
    • Adipose Tissue and Metabolic Health
      Sung-Min An, Seung-Hee Cho, John C. Yoon
      Diabetes & Metabolism Journal.2023; 47(5): 595.     CrossRef
    • The RANK-RANK-L-OPG pathway: trait d’union between bone and muscle
      Giovanni Iolascon, Sara Liguori, Marco Paoletta, Federica Tomaino, Antimo Moretti
      International Journal of Bone Fragility.2023; 3(2): 56.     CrossRef
    • Warm Cells, Hot Mitochondria: Achievements and Problems of Ultralocal Thermometry
      Alexey G. Kruglov, Alexey M. Romshin, Anna B. Nikiforova, Arina Plotnikova, Igor I. Vlasov
      International Journal of Molecular Sciences.2023; 24(23): 16955.     CrossRef
    • Plant extracts in prevention of obesity
      Han-Ning Wang, Jin-Zhu Xiang, Zhi Qi, Min Du
      Critical Reviews in Food Science and Nutrition.2022; 62(8): 2221.     CrossRef
    • Transcription factor EB enhances autophagy and ameliorates palmitate‐induced insulin resistance at least partly via upregulating AMPK activity in skeletal muscle cells
      Ping Wang, Chun Guang Li, Xian Zhou, Shuzhe Ding
      Clinical and Experimental Pharmacology and Physiology.2022; 49(2): 302.     CrossRef
    • ATP-consuming futile cycles as energy dissipating mechanisms to counteract obesity
      Alexandra J. Brownstein, Michaela Veliova, Rebeca Acin-Perez, Marc Liesa, Orian S. Shirihai
      Reviews in Endocrine and Metabolic Disorders.2022; 23(1): 121.     CrossRef
    • Skeletal muscle plasticity and thermogenesis: Insights from sea otters
      Traver Wright, Melinda Sheffield-Moore
      Temperature.2022; 9(2): 119.     CrossRef
    • Augmented CCL5/CCR5 signaling in brown adipose tissue inhibits adaptive thermogenesis and worsens insulin resistance in obesity
      Pei-Chi Chan, Li-Man Hung, Jiung-Pang Huang, Yuan-Ji Day, Chao-Lan Yu, Feng-Chih Kuo, Chieh-Hua Lu, Yu-Feng Tian, Po-Shiuan Hsieh
      Clinical Science.2022; 136(1): 121.     CrossRef
    • Altered muscle mitochondrial, inflammatory and trophic markers, and reduced exercise training adaptations in type 1 diabetes
      Dean Minnock, Giosuè Annibalini, Giacomo Valli, Roberta Saltarelli, Mauricio Krause, Elena Barbieri, Giuseppe De Vito
      The Journal of Physiology.2022; 600(6): 1405.     CrossRef
    • Maternal exercise intergenerationally drives muscle-based thermogenesis via activation of apelin-AMPK signaling
      Jun Seok Son, Song Ah Chae, Liang Zhao, Hongyang Wang, Jeanene M. de Avila, Mei-Jun Zhu, Zhihua Jiang, Min Du
      eBioMedicine.2022; 76: 103842.     CrossRef
    • Ca 2+ leak through ryanodine receptor 1 regulates thermogenesis in resting skeletal muscle
      Aldo Meizoso-Huesca, Luke Pearce, Christopher J. Barclay, Bradley S. Launikonis
      Proceedings of the National Academy of Sciences.2022;[Epub]     CrossRef
    • Deep transcranial magnetic stimulation in combination with skin thermography in obesity: a window on sympathetic nervous system
      Anna Ferrulli, Sara Gandini, Giulio Cammarata, Veronica Redaelli, Stefano Massarini, Concetta Macrì, Ileana Terruzzi, Daniele Cannavaro, Fabio Luzi, Livio Luzi
      Acta Diabetologica.2022; 59(5): 729.     CrossRef
    • Knockdown of sarcolipin (SLN) impairs substrate utilization in human skeletal muscle cells
      Abel M. Mengeste, Parmeshwar Katare, Andrea Dalmao Fernandez, Jenny Lund, Hege G. Bakke, David Baker, Stefano Bartesaghi, Xiao-Rong Peng, Arild C. Rustan, G. Hege Thoresen, Eili Tranheim Kase
      Molecular Biology Reports.2022; 49(7): 6005.     CrossRef
    • The Role of Thyroid Hormones on Skeletal Muscle Thermogenesis
      Nadia Sawicka-Gutaj, Abikasinee Erampamoorthy, Ariadna Zybek-Kocik, Angelos Kyriacou, Małgorzata Zgorzalewicz-Stachowiak, Agata Czarnywojtek, Marek Ruchała
      Metabolites.2022; 12(4): 336.     CrossRef
    • SS‐31 does not prevent or reduce muscle atrophy 7 days after a 65 kdyne contusion spinal cord injury in young male mice
      Zachary A. Graham, Jennifer J. DeBerry, Christopher P. Cardozo, Marcas M. Bamman
      Physiological Reports.2022;[Epub]     CrossRef
    • Exercise, Mitohormesis, and Mitochondrial ORF of the 12S rRNA Type-C (MOTS-c)
      Tae Kwan Yoon, Chan Hee Lee, Obin Kwon, Min-Seon Kim
      Diabetes & Metabolism Journal.2022; 46(3): 402.     CrossRef
    • Insight Into the Metabolic Adaptations of Electrically Pulse-Stimulated Human Myotubes Using Global Analysis of the Transcriptome and Proteome
      Abel M. Mengeste, Nataša Nikolić, Andrea Dalmao Fernandez, Yuan Z. Feng, Tuula A. Nyman, Sander Kersten, Fred Haugen, Eili Tranheim Kase, Vigdis Aas, Arild C. Rustan, G. Hege Thoresen
      Frontiers in Physiology.2022;[Epub]     CrossRef
    • The Role of Thermogenic Fat Tissue in Energy Consumption
      Masato Horino, Kenji Ikeda, Tetsuya Yamada
      Current Issues in Molecular Biology.2022; 44(7): 3166.     CrossRef
    • Investigation of obesogenic effects of hexachlorobenzene, DDT and DDE in male rats
      Zeyad Ayad Fadhil Al-Obaidi, Cihan Süleyman Erdogan, Engin Sümer, Hüseyin Bugra Özgün, Burcu Gemici, Süleyman Sandal, Bayram Yilmaz
      General and Comparative Endocrinology.2022; 327: 114098.     CrossRef
    • Avian adjustments to cold and non‐shivering thermogenesis: whats, wheres and hows
      Punyadhara Pani, Naresh C. Bal
      Biological Reviews.2022; 97(6): 2106.     CrossRef
    • Thirty Obesity Myths, Misunderstandings, and/or Oversimplifications: An Obesity Medicine Association (OMA) Clinical Practice Statement (CPS) 2022
      Harold Edward Bays, Angela Golden, Justin Tondt
      Obesity Pillars.2022; 3: 100034.     CrossRef
    • Myogenetic Oligodeoxynucleotide Restores Differentiation and Reverses Inflammation of Myoblasts Aggravated by Cancer-Conditioned Medium
      Yuma Nihashi, Machi Yamamoto, Takeshi Shimosato, Tomohide Takaya
      Muscles.2022; 1(2): 111.     CrossRef
    • Altered skeletal muscle sarco-endoplasmic reticulum Ca2+-ATPase calcium transport efficiency after a thermogenic stimulus
      Lydia A. Heemstra, Lauren G. Koch, Steven L. Britton, Colleen M. Novak
      American Journal of Physiology-Regulatory, Integrative and Comparative Physiology.2022; 323(5): R628.     CrossRef
    • Animal Welfare Compromises Associated with Causes of Death in Neonatal Piglets
      Kirsty L. Chidgey, Nutnapong Udomteerasuwat, Patrick C. H. Morel, Fernanda Castillo-Alcala
      Animals.2022; 12(21): 2933.     CrossRef
    • Brown to White Fat Transition Overlap With Skeletal Muscle During Development of Larger Mammals: Is it a Coincidence?
      Sunil Pani, Suchanda Dey, Benudhara Pati, Unmod Senapati, Naresh C Bal
      Journal of the Endocrine Society.2022;[Epub]     CrossRef
    • Anti‐adiposity and lipid‐lowering effects of schisandrol A in diet‐induced obese mice
      Sang Ryong Kim, Hyo Jin Park, Un Ju Jung
      Journal of Food Biochemistry.2022;[Epub]     CrossRef
    • Changes in spike protein antibody titer over 90 days after the second dose of SARS-CoV-2 vaccine in Japanese dialysis patients
      Haruki Wakai, Natsumi Abe, Touno Tokuda, Rika Yamanaka, Satoshi Ebihara, Kensuke Izumaru, Daisuke Ishii, Toru Hyodo, Kazunari Yoshida
      BMC Infectious Diseases.2022;[Epub]     CrossRef
    • Organotypic cultures as aging associated disease models
      Martina M. Sanchez, Isabella A. Bagdasarian, William Darch, Joshua T. Morgan
      Aging.2022; 14(22): 9338.     CrossRef
    • Divergent remodeling of the skeletal muscle metabolome over 24 h between young, healthy men and older, metabolically compromised men
      Jan-Frieder Harmsen, Michel van Weeghel, Rex Parsons, Georges E. Janssens, Jakob Wefers, Dirk van Moorsel, Jan Hansen, Joris Hoeks, Matthijs K.C. Hesselink, Riekelt H. Houtkooper, Patrick Schrauwen
      Cell Reports.2022; 41(11): 111786.     CrossRef
    • Structural functionality of skeletal muscle mitochondria and its correlation with metabolic diseases
      Gourabamani Swalsingh, Punyadhara Pani, Naresh C. Bal
      Clinical Science.2022; 136(24): 1851.     CrossRef
    • Trans-anethole Induces Thermogenesis via Activating SERCA/SLN Axis in C2C12 Muscle Cells
      Sulagna Mukherjee, Minji Choi, Jong Won Yun
      Biotechnology and Bioprocess Engineering.2022; 27(6): 938.     CrossRef
    • Umbilical Cord-Mesenchymal Stem Cell-Conditioned Medium Improves Insulin Resistance in C2C12 Cell
      Kyung-Soo Kim, Yeon Kyung Choi, Mi Jin Kim, Jung Wook Hwang, Kyunghoon Min, Sang Youn Jung, Soo-Kyung Kim, Yong-Soo Choi, Yong-Wook Cho
      Diabetes & Metabolism Journal.2021; 45(2): 260.     CrossRef
    • Nutmeg extract potentially alters characteristics of white adipose tissue in rats
      Ronny Lesmana, Melisa Siannoto, Gaga I. Nugraha, Hanna Goenawan, Astrid K. Feinisa, Yuni S. Pratiwi, Fifi Veronica, Vita M. Tarawan, Susianti Susianti, Unang Supratman
      Veterinary Medicine and Science.2021; 7(2): 512.     CrossRef
    • Contribution of thermogenic mechanisms by male and female mice lacking pituitary adenylate cyclase-activating polypeptide in response to cold acclimation
      Ekaterina Filatov, Landon I. Short, Maeghan A. M. Forster, Simon S. Harris, Erik N. Schien, Malcolm C. Hughes, Daemon L. Cline, Colin J. Appleby, Sarah L. Gray
      American Journal of Physiology-Endocrinology and Metabolism.2021; 320(3): E475.     CrossRef
    • Skeletal muscle non-shivering thermogenesis as an attractive strategy to combat obesity
      Hanbing Li, Can Wang, Linghuan Li, Lingqiao Li
      Life Sciences.2021; 269: 119024.     CrossRef
    • Restriction of an intron size en route to endothermy
      Jana Královičová, Ivana Borovská, Reuben Pengelly, Eunice Lee, Pavel Abaffy, Radek Šindelka, Frank Grutzner, Igor Vořechovský
      Nucleic Acids Research.2021; 49(5): 2460.     CrossRef
    • Skeletal muscle specific mitochondrial dysfunction and altered energy metabolism in a murine model (oim/oim) of severe osteogenesis imperfecta
      Victoria L. Gremminger, Emily N. Harrelson, Tara K. Crawford, Adrienne Ohler, Laura C. Schulz, R. Scott Rector, Charlotte L. Phillips
      Molecular Genetics and Metabolism.2021; 132(4): 244.     CrossRef
    • Body Protein Sparing in Hibernators: A Source for Biomedical Innovation
      Fabrice Bertile, Caroline Habold, Yvon Le Maho, Sylvain Giroud
      Frontiers in Physiology.2021;[Epub]     CrossRef
    • The Genomes of Two Billfishes Provide Insights into the Evolution of Endothermy in Teleosts
      Baosheng Wu, Chenguang Feng, Chenglong Zhu, Wenjie Xu, Yuan Yuan, Mingliang Hu, Ke Yuan, Yongxin Li, Yandong Ren, Yang Zhou, Haifeng Jiang, Qiang Qiu, Wen Wang, Shunping He, Kun Wang, Guang Yang
      Molecular Biology and Evolution.2021; 38(6): 2413.     CrossRef
    • Is Upregulation of Sarcolipin Beneficial or Detrimental to Muscle Function?
      Naresh C. Bal, Subash C. Gupta, Meghna Pant, Danesh H. Sopariwala, Geoffrey Gonzalez-Escobedo, Joanne Turner, John S. Gunn, Christopher R. Pierson, Scott Q. Harper, Jill A. Rafael-Fortney, Muthu Periasamy
      Frontiers in Physiology.2021;[Epub]     CrossRef
    • Real‐Time Assessment of Mitochondrial Toxicity in HepG2 Cells Using the Seahorse Extracellular Flux Analyzer
      Jether Amos Espinosa, Grace Pohan, Michelle R. Arkin, Sarine Markossian
      Current Protocols.2021;[Epub]     CrossRef
    • Effects of Ecklonia stolonifera extract on the obesity and skeletal muscle regeneration in high-fat diet-fed mice
      Heegu Jin, Hyun-Ji Oh, Junghee Kim, Kang-Pyo Lee, Xionggao Han, Ok-Hwan Lee, Boo-Yong Lee
      Journal of Functional Foods.2021; 82: 104511.     CrossRef
    • The Effect of Dietary Intake and Nutritional Status on Anthropometric Development and Systemic Inflammation: An Observational Study
      Roxana Maria Martin-Hadmaș, Ștefan Adrian Martin, Adela Romonți, Cristina Oana Mărginean
      International Journal of Environmental Research and Public Health.2021; 18(11): 5635.     CrossRef
    • Thermographic imaging of mouse across circadian time reveals body surface temperature elevation associated with non-locomotor body movements
      Hiroyuki Shimatani, Yuichi Inoue, Yota Maekawa, Takahito Miyake, Yoshiaki Yamaguchi, Masao Doi, Nicolas Cermakian
      PLOS ONE.2021; 16(5): e0252447.     CrossRef
    • Human umbilical cord mesenchymal stem cells in type 2 diabetes mellitus: the emerging therapeutic approach
      Andreia Gomes, Pedro Coelho, Raquel Soares, Raquel Costa
      Cell and Tissue Research.2021; 385(3): 497.     CrossRef
    • Central vs. Peripheral Action of Thyroid Hormone in Adaptive Thermogenesis: A Burning Topic
      Yanis Zekri, Frédéric Flamant, Karine Gauthier
      Cells.2021; 10(6): 1327.     CrossRef
    • Myogenetic Oligodeoxynucleotide (myoDN) Recovers the Differentiation of Skeletal Muscle Myoblasts Deteriorated by Diabetes Mellitus
      Shunichi Nakamura, Shinichi Yonekura, Takeshi Shimosato, Tomohide Takaya
      Frontiers in Physiology.2021;[Epub]     CrossRef
    • Lipophorin receptor 1 (LpR1) in Drosophila muscle influences life span by regulating mitochondrial aging
      Ae-kyeong Kim, Dae-Woo Kwon, Eunbyul Yeom, Kwang-Pyo Lee, Ki-Sun Kwon, Kweon Yu, Kyu-Sun Lee
      Biochemical and Biophysical Research Communications.2021; 568: 95.     CrossRef
    • Skeletal muscle thermogenesis enables aquatic life in the smallest marine mammal
      Traver Wright, Randall W. Davis, Heidi C. Pearson, Michael Murray, Melinda Sheffield-Moore
      Science.2021; 373(6551): 223.     CrossRef
    • Myoglobin, expressed in brown adipose tissue of mice, regulates the content and activity of mitochondria and lipid droplets
      Mostafa A. Aboouf, Julia Armbruster, Markus Thiersch, Max Gassmann, Axel Gödecke, Erich Gnaiger, Glen Kristiansen, Anne Bicker, Thomas Hankeln, Hao Zhu, Thomas A. Gorr
      Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids.2021; 1866(12): 159026.     CrossRef
    • Skeletal muscle energy metabolism in obesity
      Abel M. Mengeste, Arild C. Rustan, Jenny Lund
      Obesity.2021; 29(10): 1582.     CrossRef
    • Cellular senescence in musculoskeletal homeostasis, diseases, and regeneration
      Mei Wan, Elise F. Gray-Gaillard, Jennifer H. Elisseeff
      Bone Research.2021;[Epub]     CrossRef
    • The small molecule SERCA activator CDN1163 increases energy metabolism in human skeletal muscle cells
      Abel M. Mengeste, Jenny Lund, Parmeshwar Katare, Roya Ghobadi, Hege G. Bakke, Per Kristian Lunde, Lars Eide, Gavin O’ Mahony, Sven Göpel, Xiao-Rong Peng, Eili Tranheim Kase, G. Hege Thoresen, Arild C. Rustan
      Current Research in Pharmacology and Drug Discovery.2021; 2: 100060.     CrossRef
    • Antioxidant Properties and Cytoprotective Effect of Pistacia lentiscus L. Seed Oil against 7β-Hydroxycholesterol-Induced Toxicity in C2C12 Myoblasts: Reduction in Oxidative Stress, Mitochondrial and Peroxisomal Dysfunctions and Attenuation of Cell Death
      Imen Ghzaiel, Amira Zarrouk, Thomas Nury, Michela Libergoli, Francesca Florio, Souha Hammouda, Franck Ménétrier, Laure Avoscan, Aline Yammine, Mohammad Samadi, Norbert Latruffe, Stefano Biressi, Débora Levy, Sérgio Paulo Bydlowski, Sonia Hammami, Anne Vej
      Antioxidants.2021; 10(11): 1772.     CrossRef
    • Role of Peroxisome Proliferator-Activated Receptors (PPARs) in Energy Homeostasis of Dairy Animals: Exploiting Their Modulation through Nutrigenomic Interventions
      Faiz-ul Hassan, Asif Nadeem, Zhipeng Li, Maryam Javed, Qingyou Liu, Jahanzaib Azhar, Muhammad Saif-ur Rehman, Kuiqing Cui, Saif ur Rehman
      International Journal of Molecular Sciences.2021; 22(22): 12463.     CrossRef
    • Differential Effects of 25-Hydroxyvitamin D3 versus 1α 25-Dihydroxyvitamin D3 on Adipose Tissue Browning in CKD-Associated Cachexia
      Robert H. Mak, Uwe Querfeld, Alex Gonzalez, Sujana Gunta, Wai W. Cheung
      Cells.2021; 10(12): 3382.     CrossRef
    • Effects of Starvation on Antioxidant-Related Signaling Molecules, Oxidative Stress, and Autophagy in Juvenile Chinese Perch Skeletal Muscle
      Ping Wu, Aimin Wang, Jia Cheng, Lin Chen, Yaxiong Pan, Honghui Li, Qi Zhang, Jiaqi Zhang, Wuying Chu, Jianshe Zhang
      Marine Biotechnology.2020; 22(1): 81.     CrossRef
    • Thermogenic adipocytes: lineage, function and therapeutic potential
      Alice E. Pollard, David Carling
      Biochemical Journal.2020; 477(11): 2071.     CrossRef
    • Hypoglycaemic effect of catalpol in a mouse model of high-fat diet-induced prediabetes
      Dengqiu Xu, Xiaofei Huang, Hozeifa M. Hassan, Lu Wang, Sijia Li, Zhenzhou Jiang, Luyong Zhang, Tao Wang
      Applied Physiology, Nutrition, and Metabolism.2020; 45(10): 1127.     CrossRef
    • The evolution of mechanisms involved in vertebrate endothermy
      Lucas J. Legendre, Donald Davesne
      Philosophical Transactions of the Royal Society B: Biological Sciences.2020; 375(1793): 20190136.     CrossRef
    • Uncoupling of sarcoendoplasmic reticulum calcium ATPase pump activity by sarcolipin as the basis for muscle non-shivering thermogenesis
      Naresh C. Bal, Muthu Periasamy
      Philosophical Transactions of the Royal Society B: Biological Sciences.2020; 375(1793): 20190135.     CrossRef
    • Prediction of muscle mass in arms and legs based on 3D laser-based photonic body scans’ standard dimensions in a homogenous sample of young men
      Cristine Cavegn, Frank Rühli, Nicole Bender, Kaspar Staub
      Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization.2020; 8(5): 562.     CrossRef
    • Thermogenesis in Adipose Tissue Activated by Thyroid Hormone
      Winifred W. Yau, Paul M. Yen
      International Journal of Molecular Sciences.2020; 21(8): 3020.     CrossRef
    • Interaction of a Sarcolipin Pentamer and Monomer with the Sarcoplasmic Reticulum Calcium Pump, SERCA
      John Paul Glaves, Joseph O. Primeau, Przemek A. Gorski, L. Michel Espinoza-Fonseca, M. Joanne Lemieux, Howard S. Young
      Biophysical Journal.2020; 118(2): 518.     CrossRef
    • Automated CT-derived skeletal muscle mass determination in lower hind limbs of mice using a 3D U-Net deep learning network
      Brent van der Heyden, Wouter R. P. H. van de Worp, Ardy van Helvoort, Jan Theys, Annemie M. W. J. Schols, Ramon C. J. Langen, Frank Verhaegen
      Journal of Applied Physiology.2020; 128(1): 42.     CrossRef
    • Modified creatinine index and risk for long-term infection-related mortality in hemodialysis patients: ten-year outcomes of the Q-Cohort Study
      Hokuto Arase, Shunsuke Yamada, Hiroto Hiyamuta, Masatomo Taniguchi, Masanori Tokumoto, Kazuhiko Tsuruya, Toshiaki Nakano, Takanari Kitazono
      Scientific Reports.2020;[Epub]     CrossRef
    • Ticking for Metabolic Health: The Skeletal‐Muscle Clocks
      Miguel A. Gutierrez‐Monreal, Jan‐Frieder Harmsen, Patrick Schrauwen, Karyn A. Esser
      Obesity.2020;[Epub]     CrossRef
    • Gut microbiota and regulation of myokine-adipokine function
      Francesco Suriano, Matthias Van Hul, Patrice D Cani
      Current Opinion in Pharmacology.2020; 52: 9.     CrossRef
    • P2X7 Receptor in the Management of Energy Homeostasis: Implications for Obesity, Dyslipidemia, and Insulin Resistance
      Roberto Coccurello, Cinzia Volonté
      Frontiers in Endocrinology.2020;[Epub]     CrossRef
    • Primary Active Ca2+ Transport Systems in Health and Disease
      Jialin Chen, Aljona Sitsel, Veronick Benoy, M. Rosario Sepúlveda, Peter Vangheluwe
      Cold Spring Harbor Perspectives in Biology.2020; 12(2): a035113.     CrossRef
    • Sex‐specific alterations in whole body energetics and voluntary activity in heterozygous R163C malignant hyperthermia‐susceptible mice
      Jennifer M. Rutkowsky, Trina A. Knotts, Paul D. Allen, Isaac N. Pessah, Jon J. Ramsey
      The FASEB Journal.2020; 34(6): 8721.     CrossRef
    • The Role of Exercise in the Interplay between Myokines, Hepatokines, Osteokines, Adipokines, and Modulation of Inflammation for Energy Substrate Redistribution and Fat Mass Loss: A Review
      Adrian M. Gonzalez-Gil, Leticia Elizondo-Montemayor
      Nutrients.2020; 12(6): 1899.     CrossRef
    • Emergent Coordination of the CHKB and CPT1B Genes in Eutherian Mammals: Implications for the Origin of Brown Adipose Tissue
      Bhavin V. Patel, Fanrong Yao, Aidan Howenstine, Risa Takenaka, Jacob A. Hyatt, Karen E. Sears, Brian M. Shewchuk
      Journal of Molecular Biology.2020; 432(23): 6127.     CrossRef
    • Chronic cold exposure induces mitochondrial plasticity in deer mice native to high altitudes
      Sajeni Mahalingam, Zachary A. Cheviron, Jay F. Storz, Grant B. McClelland, Graham R. Scott
      The Journal of Physiology.2020; 598(23): 5411.     CrossRef
    • Adaptive thermogenesis enhances the life-threatening response to heat in mice with an Ryr1 mutation
      Hui J. Wang, Chang Seok Lee, Rachel Sue Zhen Yee, Linda Groom, Inbar Friedman, Lyle Babcock, Dimitra K. Georgiou, Jin Hong, Amy D. Hanna, Joseph Recio, Jong Min Choi, Ting Chang, Nadia H. Agha, Jonathan Romero, Poonam Sarkar, Nicol Voermans, M. Waleed Gab
      Nature Communications.2020;[Epub]     CrossRef
    • Sclerostin Influences Exercise-Induced Adaptations in Body Composition and White Adipose Tissue Morphology in Male Mice
      Nigel Kurgan, Joshua Stoikos, Bradley J. Baranowski, Jenalyn Yumol, Roopan Dhaliwal, Jake B. Sweezey-Munroe, Val A. Fajardo, William Gittings, Rebecca E.K. Macpherson, Panagiota Klentrou
      Journal of Bone and Mineral Research.2020; 38(4): 541.     CrossRef
    • Mitochondrial dysfunction and inhibition of myoblast differentiation in mice with high‐fat‐diet‐induced pre‐diabetes
      Dengqiu Xu, Zhenzhou Jiang, Zeren Sun, Lu Wang, Guolin Zhao, Hozeifa M. Hassan, Sisi Fan, Wang Zhou, Shuangshuang Han, Luyong Zhang, Tao Wang
      Journal of Cellular Physiology.2019; 234(5): 7510.     CrossRef
    • Noninvasive and in vivo assessment of upper and lower limb skeletal muscle oxidative metabolism activity and microvascular responses to glucose ingestion in humans
      Rogério Nogueira Soares, Alessandro L. Colosio, Juan Manuel Murias, Silvia Pogliaghi
      Applied Physiology, Nutrition, and Metabolism.2019; 44(10): 1105.     CrossRef
    • Fpr2 Deficiency Alleviates Diet-Induced Insulin Resistance Through Reducing Body Weight Gain and Inhibiting Inflammation Mediated by Macrophage Chemotaxis and M1 Polarization
      Xiaofang Chen, Shu Zhuo, Tengfei Zhu, Pengle Yao, Mengmei Yang, Hong Mei, Na Li, Fengguang Ma, Ji Ming Wang, Shiting Chen, Richard D. Ye, Yu Li, Yingying Le
      Diabetes.2019; 68(6): 1130.     CrossRef
    • Taurine protects against arsenic trioxide-induced insulin resistance via ROS-Autophagy pathway in skeletal muscle
      Lei Yang, Tianming Qiu, Xiaofeng Yao, Liping Jiang, Sen Wei, Pei Pei, Zhidong Wang, Jie Bai, Xiaofang Liu, Guang Yang, Shuang Liu, Xiance Sun
      The International Journal of Biochemistry & Cell Biology.2019; 112: 50.     CrossRef
    • Increased triacylglycerol - Fatty acid substrate cycling in human skeletal muscle cells exposed to eicosapentaenoic acid
      Nils G. Løvsletten, Siril S. Bakke, Eili T. Kase, D. Margriet Ouwens, G. Hege Thoresen, Arild C. Rustan, Juan J. Loor
      PLOS ONE.2018; 13(11): e0208048.     CrossRef
    • Transient receptor potential (TRP) channels: a metabolic TR(i)P to obesity prevention and therapy
      M. Bishnoi, P. Khare, L. Brown, S. K. Panchal
      Obesity Reviews.2018; 19(9): 1269.     CrossRef
    • Pivotal Roles of Peroxisome Proliferator-Activated Receptors (PPARs) and Their Signal Cascade for Cellular and Whole-Body Energy Homeostasis
      Shreekrishna Lamichane, Babita Dahal Lamichane, Sang-Mo Kwon
      International Journal of Molecular Sciences.2018; 19(4): 949.     CrossRef
    • Antiobesity Effect ofAstilbe chinensisFranch. et Savet. Extract through Regulation of Adipogenesis and AMP-Activated Protein Kinase Pathways in 3T3-L1 Adipocyte and High-Fat Diet-Induced C57BL/6N Obese Mice
      Xian Hua Zhang, Zhiqiang Wang, Bueom-Goo Kang, Seung Hwan Hwang, Jae-Young Lee, Soon Sung Lim, Bo Huang
      Evidence-Based Complementary and Alternative Medicine.2018; 2018: 1.     CrossRef
    • Loss of P2X7 receptor function dampens whole body energy expenditure and fatty acid oxidation
      Giacomo Giacovazzo, Savina Apolloni, Roberto Coccurello
      Purinergic Signalling.2018; 14(3): 299.     CrossRef
    • Chromatin and Metabolism
      Tamaki Suganuma, Jerry L. Workman
      Annual Review of Biochemistry.2018; 87(1): 27.     CrossRef
    • Zebrafish as a Model for Obesity and Diabetes
      Liqing Zang, Lisette A. Maddison, Wenbiao Chen
      Frontiers in Cell and Developmental Biology.2018;[Epub]     CrossRef
    • Comparison between Dual-Energy X-ray Absorptiometry and Bioelectrical Impedance Analyses for Accuracy in Measuring Whole Body Muscle Mass and Appendicular Skeletal Muscle Mass
      Seo Young Lee, Soyeon Ahn, Young Ji Kim, Myoung Jin Ji, Kyoung Min Kim, Sung Hee Choi, Hak Chul Jang, Soo Lim
      Nutrients.2018; 10(6): 738.     CrossRef

    • PubReader PubReader
    • Cite this Article
      Cite this Article
      export Copy Download
      Close
      Download Citation
      Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

      Format:
      • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
      • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
      Include:
      • Citation for the content below
      Skeletal Muscle Thermogenesis and Its Role in Whole Body Energy Metabolism
      Diabetes Metab J. 2017;41(5):327-336.   Published online October 24, 2017
      Close
    • XML DownloadXML Download
    Figure
    Periasamy M, Herrera JL, Reis FCG. Skeletal Muscle Thermogenesis and Its Role in Whole Body Energy Metabolism. Diabetes Metab J. 2017;41(5):327-336.
    Received: Aug 29, 2017; Accepted: Sep 08, 2017
    DOI: https://doi.org/10.4093/dmj.2017.41.5.327.

    Diabetes Metab J : Diabetes & Metabolism Journal
    Close layer