The crosstalk between BAT thermogenesis and skeletal muscle dysfunction

Yaojing Chen; Qian Hu; Changyi Wang; Tiantian Wang

doi:10.3389/fphys.2023.1132830

journal article Open Access Apr 21, 2023

The crosstalk between BAT thermogenesis and skeletal muscle dysfunction

Yaojing Chen Qian Hu

Changyi Wang Tiantian Wang

Frontiers in Physiology Vol. 14 · Frontiers Media SA

View at Publisher Save 10.3389/fphys.2023.1132830

Abstract

Metabolic defects increase the risk of skeletal muscle diseases, and muscle impairment might worsen metabolic disruption, leading to a vicious cycle. Both brown adipose tissue (BAT) and skeletal muscle play important roles in non-shivering thermogenesis to regulate energy homeostasis. BAT regulates body temperature, systemic metabolism, and seretion of batokines that have positive or negative impacts on skeletal muscle. Conversely, muscle can secrete myokines that regulate BAT function. This review explained the crosstalk between BAT and skeletal muscle, and then discussed the batokines and highlighted their impact on skeletal muscle under physiological conditions. BAT is now considered a potential therapeutic target for obesity and diabetes treatment. Moreover, manipulation of BAT may be an attractive approach for the treatment of muscle weakness by correcting metabolic deficits. Therefore, exploring BAT as a potential treatment for sarcopenia could be a promising avenue for future research.

Topics

No keywords indexed for this article. Browse by subject →

References

105

[1]

Almendro "Effects of IL-15 on rat Brown adipose tissue: Uncoupling proteins and PPARs" Obes. (Silver Spring, Md.) (2008) 10.1038/oby.2007.47

[2]

An "Discrete BDNF neurons in the paraventricular hypothalamus control feeding and energy expenditure" Cell. Metab. (2015) 10.1016/j.cmet.2015.05.008

[3]

Bal "Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals" Nat. Med. (2012) 10.1038/nm.2897

[4]

Bal "Increased reliance on muscle-based thermogenesis upon acute minimization of Brown adipose tissue function" J. Biol. Chem. (2016) 10.1074/jbc.m116.728188

[5]

Bal "Both Brown adipose tissue and skeletal muscle thermogenesis processes are activated during mild to severe cold adaptation in mice" J. Biol. Chem. (2017) 10.1074/jbc.m117.790451

[6]

Bautista "The menthol receptor TRPM8 is the principal detector of environmental cold" Nature (2007) 10.1038/nature05910

[7]

Beiroa "GLP-1 agonism stimulates Brown adipose tissue thermogenesis and browning through hypothalamic AMPK" Diabetes (2014) 10.2337/db14-0302

[8]

Betz "Targeting thermogenesis in Brown fat and muscle to treat obesity and metabolic disease" Nat. Rev. Endocrinol. (2018) 10.1038/nrendo.2017.132

[9]

Bouchi "Insulin treatment attenuates decline of muscle mass in Japanese patients with type 2 diabetes" Calcif. Tissue Int. (2017) 10.1007/s00223-017-0251-x

[10]

Bouchi "Dipeptidyl peptidase 4 inhibitors attenuates the decline of skeletal muscle mass in patients with type 2 diabetes" Diabetes Metab. Res. Rev. (2018) 10.1002/dmrr.2957

[11]

Braga "Inhibition of in vitro and in vivo Brown fat differentiation program by myostatin" Obesity (2013) 10.1002/oby.20117

[12]

Cannon "Brown adipose tissue: Function and physiological significance" Physiol. Rev. (2004) 10.1152/physrev.00015.2003

[13]

Cao "Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism" Cell. (2008) 10.1016/j.cell.2008.07.048

[14]

Chen "High plasma level of fibroblast growth factor 21 is an independent predictor of type 2 diabetes: A 5.4-year population-based prospective study in Chinese subjects" Diabetes Care (2011) 10.2337/dc11-0294

[15]

China "Globular adiponectin reverses osteo-sarcopenia and altered body composition in ovariectomized rats" Bone (2017) 10.1016/j.bone.2017.08.005

[16]

Choi "Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance" J. Clin. Investigation (2007) 10.1172/jci13579

[17]

Choi "Multifaceted physiological roles of adiponectin in inflammation and diseases" Int. J. Mol. Sci. (2020) 10.3390/ijms21041219

[18]

Conley "Mitochondrial dysfunction: Impact on exercise performance and cellular aging" Exerc. Sport Sci. Rev. (2007) 10.1249/jes.0b013e31803e88e9

[19]

Conte "Human aging and longevity are characterized by high levels of mitokines" J. Gerontol. A Biol. Sci. Med. Sci. (2019) 10.1093/gerona/gly153

[20]

Identification and Importance of Brown Adipose Tissue in Adult Humans

Aaron M. Cypess, Sanaz Lehman, Gethin Williams et al.

New England Journal of Medicine 2009 10.1056/nejmoa0810780

[21]

Duan "Interleukin-15 in obesity and metabolic dysfunction: Current understanding and future perspectives" Obes. Rev. (2017) 10.1111/obr.12567

[22]

Eguchi "Interferon regulatory factors are transcriptional regulators of adipogenesis" Cell. Metab. (2008) 10.1016/j.cmet.2007.11.002

[23]

Eknoyan "Santorio Sanctorius (1561-1636) - founding father of metabolic balance studies" Am. J. Nephrol. (1999) 10.1159/000013455

[24]

Ferrari "Longitudinal association of type 2 diabetes and insulin therapy with muscle parameters in the KORA-Age study" Acta Diabetol. (2020) 10.1007/s00592-020-01523-7

[25]

Finlin "Human adipose beiging in response to cold and mirabegron" JCI Insight (2018) 10.1172/jci.insight.121510

[26]

Finlin "The β3-adrenergic receptor agonist mirabegron improves glucose homeostasis in obese humans" J. Clin. Invest. (2020) 10.1172/jci134892

[27]

Fisher "FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis" Genes. Dev. (2012) 10.1101/gad.177857.111

[28]

Flicker "Exploring the in vivo role of the mitochondrial calcium uniporter in Brown fat bioenergetics" Cell. Rep. (2019) 10.1016/j.celrep.2019.04.013

[29]

Fujita "Mitochondrial stress and GDF15 in the pathophysiology of sepsis" Archives Biochem. Biophysics (2020) 10.1016/j.abb.2020.108668

[30]

Gamberi "Activation of autophagy by globular adiponectin is required for muscle differentiation" Biochim. Biophys. Acta (2016) 10.1016/j.bbamcr.2016.01.016

[31]

Géloën "Regulation of the level of uncoupling protein in Brown adipose tissue by insulin requires the mediation of the sympathetic nervous system" FEBS Lett. (1990) 10.1016/0014-5793(90)80941-b

[32]

Gnad "Adenosine activates Brown adipose tissue and recruits beige adipocytes via A2A receptors" Nature (2014) 10.1038/nature13816

[33]

Gnad "Adenosine/A2B receptor signaling ameliorates the effects of aging and counteracts obesity" Cell. Metab. (2020) 10.1016/j.cmet.2020.06.006

[34]

Golozoubova "Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold" Faseb J. (2001) 10.1096/fj.00-0536fje

[35]

Guerra "Brown adipose tissue-specific insulin receptor knockout shows diabetic phenotype without insulin resistance" J. Clin. Invest. (2001) 10.1172/jci13103

[36]

Hamrick "The adipokine leptin increases skeletal muscle mass and significantly alters skeletal muscle miRNA expression profile in aged mice" Biochem. Biophys. Res. Commun. (2010) 10.1016/j.bbrc.2010.08.079

[37]

Haque "Role of the sympathetic nervous system and insulin in enhancing glucose uptake in peripheral tissues after intrahypothalamic injection of leptin in rats" Diabetes (1999) 10.2337/diabetes.48.9.1706

[38]

Ikeda "UCP1 dependent and independent thermogenesis in Brown and beige adipocytes" Front. Endocrinol. (2020) 10.3389/fendo.2020.00498

[39]

Jiménez-Osorio "Curcumin and insulin resistance-Molecular targets and clinical evidences" Biofactors (2016) 10.1002/biof.1302

[40]

Johann "The role of GDF15 as a myomitokine" Cells (2021) 10.3390/cells10112990

[41]

Adiponectin and Adiponectin Receptors

Takashi Kadowaki, Toshimasa Yamauchi

Endocrine Reviews 2005 10.1210/er.2005-0005

[42]

Khan "mTORC1 regulates mitochondrial integrated stress response and mitochondrial myopathy progression" Cell. Metab. (2017) 10.1016/j.cmet.2017.07.007

[43]

Kim "Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine" Nat. Med. (2013) 10.1038/nm.3014

[44]

Kim "Growth differentiation factor-15 as a biomarker for sarcopenia in aging humans and mice" Exp. Gerontol. (2020) 10.1016/j.exger.2020.111115

[45]

Komici "Adiponectin and sarcopenia: A systematic review with meta-analysis" Front. Endocrinol. (Lausanne) (2021) 10.3389/fendo.2021.576619

[46]

Kong "Brown adipose tissue controls skeletal muscle function via the secretion of myostatin" Cell. Metab. (2018) 10.1016/j.cmet.2018.07.004

[47]

Lee "Irisin and FGF21 are cold-induced endocrine activators of Brown fat function in humans" Cell. Metab. (2014) 10.1016/j.cmet.2013.12.017

[48]

Li "TRPM8 activation improves energy expenditure in skeletal muscle and exercise endurance in mice" Gene (2018) 10.1016/j.gene.2017.10.045

[49]

Li "Circulating factors associated with sarcopenia during ageing and after intensive lifestyle intervention" J. Cachexia Sarcopenia Muscle (2019) 10.1002/jcsm.12417

[50]

Liu "Brown adipose tissue transplantation improves whole-body energy metabolism" Cell. Res. (2013) 10.1038/cr.2013.64

Showing 50 of 105 references

Cited By

14

Different Correlation Patterns Between Circulating Amino Acids and Body Temperature in Fibromyalgia Syndrome: A Cross-Sectional Study

Antonio Casas-Barragán, Francisco Molina · 2024

International Journal of Molecular...

Metrics

14

Citations

105

References

Details

Published: Apr 21, 2023
Vol/Issue: 14
License: View

Authors

Y

Yaojing Chen

State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China

Funding

National Natural Science Foundation of China

Cite This Article

Yaojing Chen, Qian Hu, Changyi Wang, et al. (2023). The crosstalk between BAT thermogenesis and skeletal muscle dysfunction. Frontiers in Physiology, 14. https://doi.org/10.3389/fphys.2023.1132830

The crosstalk between BAT thermogenesis and skeletal muscle dysfunction

You May Also Like