1,710
Views
1
CrossRef citations to date
0
Altmetric
Review

Regulatory effects and mechanisms of exercise on activation of brown adipose tissue (BAT) and browning of white adipose tissue (WAT)

, , , &
Article: 2266147 | Received 03 Jul 2023, Accepted 27 Sep 2023, Published online: 09 Oct 2023

References

  • Collaboration n c d r F. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet (London, England). 2017;390(10113):2627–10. doi: 10.1016/S0140-6736(17)32129-3
  • Zhang J, Wang H, Wang Z, et al. Prevalence and stabilizing trends in overweight and obesity among children and adolescents in China, 2011-2015. BMC Public Health. 2018;18(1):571. doi: 10.1186/s12889-018-5483-9
  • Skinner AC, Ravanrbakht SN, Skelton JA, et al. Prevalence of obesity and severe obesity in US children, 1999-2016. Pediatrics. 2018;141(3):e20173459. doi: 10.1542/peds.2017-3459
  • Lobstein T, Jackson-Leach R. Planning for the worst: estimates of obesity and comorbidities in school‐age children in 2025. Pediatr Obes. 2016;11(5):321–325. doi: 10.1111/ijpo.12185
  • Guo C, Huijun W, Bing Z. Advances in childhood and adolescent obesity research. J Hyg Res. 2020;49(3):516–522+526.
  • Lobstein T. Prevalence and costs of obesity. Medicine. 2011;39(1):11–13. doi: 10.1016/j.mpmed.2010.10.001
  • Martin AR, Chung S, Koehler K. Is exercise a match for Cold exposure? Common molecular framework for adipose tissue Browning. Int J Sports Med. 2020;41(7):427–442. doi: 10.1055/a-1100-7118
  • Vidal P, Stanford KI. Exercise-induced adaptations to adipose tissue thermogenesis. Front Endocrinol query. 2020;11:270. doi: 10.3389/fendo.2020.00270
  • Kopelman PG. Obesity as a medical problem. Nature. 2000;404(6778):635–643. doi: 10.1038/35007508
  • Han JC, Lawlor DA, Kimm SY. Childhood obesity. Lancet. 2010;375(9727):1737–1748. doi: 10.1016/S0140-6736(10)60171-7
  • Sun W, Man Q, Lili L, et al. Effects of high-intensity interval training on fat loss in overweight and obese female college students: a meta-analysis. Chin J Sch Health. 2021;42(10):1480–1486.
  • Wang L, Li F. Progress in the study of exercise to promote Browning of white adipose tissue. Chin J Integr Med. 2020;39(6):486–490.
  • Lu M. Effects of high-intensity interval training on lipid metabolism and chronic inflammation in obese organism. Geno Appl Biol. 2020;39(9):4310–4317.
  • Billon N, Iannarelli P, Monteiro MC, et al. The generation of adipocytes by the neural crest. Development. 2007;134(12):2283–2292. doi: 10.1242/dev.002642
  • Berry R, Rodeheffer MS. Characterization of the adipocyte cellular lineage in vivo. Nat Cell Biol. 2013;15(3):302–308. doi: 10.1038/ncb2696
  • Cinti S. UCP1 protein: the molecular hub of adipose organ plasticity. Biochimie. 2017;134:71–76. doi: 10.1016/j.biochi.2016.09.008
  • Coelho M, Oliveira T, Fernandes R. Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci. 2013;9(2):191–200. doi: 10.5114/aoms.2013.33181
  • Miranda CS, Silva-Veiga F, Martins FF, et al. PPAR-alpha activation counters brown adipose tissue whitening: a comparative study between high-fat and high-fructose-fed mice.Nutrition. 2020;78:110791. doi:10.1016/j.nut.2020.110791
  • Inagaki T, Sakai J, Kajimura S. Transcriptional and epigenetic control of brown and beige adipose cell fate and function. Nat Rev Mol Cell Biol. 2017;18(8):527. doi: 10.1038/nrm.2017.72
  • Ong FJ, Ahmed BA, Oreskovich SM, et al. Recent advances in the detection of brown adipose tissue in adult humans: a review. Clin Sci (Lond). 2018;132(10):1039–1054. doi: 10.1042/CS20170276
  • Seale P, Bjork B, Yang W, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008;454(7207):961–967. doi: 10.1038/nature07182
  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360(15):1500–1508. doi: 10.1056/NEJMoa0808718
  • Ruiz JR, Martinez-Tellez B, Sanchez-Delgado G, et al. Regulation of energy balance by brown adipose tissue: at least three potential roles for physical activity. Br J Sports Med. 2015;49(15):972–973. doi: 10.1136/bjsports-2014-094537
  • Valente A, Jamurtas AZ, Koutedakis Y, et al. Molecular pathways linking non-shivering thermogenesis and obesity: focusing on brown adipose tissue development. BiolRev Camb Philos Soc. 2015;90(1):77–88. doi: 10.1111/brv.12099
  • Van Marken Lichtenbelt WD, Vanhommerig JW. SmuldersNM, et a1. Cold-activated brown adipose tissue in healthy men.N. Engl J Med. 2009;360(15):1500–1508. doi: 10.1056/NEJMoa0808718
  • Kaisanlahti A, Glumoff T. Browning of white fat: agents and implications for beige adipose tissue to type 2 diabetes. J Physiol Biochem. 2018;75(1):1–10. doi: 10.1007/s13105-018-0658-5
  • Ikeda K, Maretich P, Kajimura S. The common and distinct features of Brown and beige adipocytes. Trends Endocrinol Metab. 2018;29(3):191–200. doi: 10.1016/j.tem.2018.01.001
  • WU J, Bostrom P, Sparks LM, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150(2):366–376. doi: 10.1016/j.cell.2012.05.016
  • Lin C, Hong Q. The relationship between mitochondrial quality control and beige adipocytes [J/OL]. Chinese J Biochem Mol Biol. 10.13865/j.cnki.cjbmb.2020.09.1335
  • Kajimura S, Spiegelman BM, Seale P. Brown and beige fat: physiological roles beyond heat generation. Cell Metab. 2015;22(4):546–559. doi: 10.1016/j.cmet.2015.09.007
  • Nedergaard J, Cannon B. How brown is brown fat? It depends where you look. Nature Med. 2013;19(5):540–541. doi: 10.1038/nm.3187
  • Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol. 2014;10(1):24–36. doi: 10.1038/nrendo.2013.204
  • Zouhal H, Jacob C, Delamarche P, et al. Catecholamines and the effects of exercise, training and gender. Sports Med. 2008;38(5):401–423. doi: 10.2165/00007256-200838050-00004
  • Merlin J, Evans BA, Dehvari N, et al. Could burning fat start with a brite spark? Pharmacological and nutritional ways to promote thermogenesis. Molecular Nutrition Food Resquery. 2016;60(1):18–42. doi: 10.1002/mnfr.201500251
  • Mendez-Gutierrez A, Osuna-Prieto FJ, Aguilera CM, et al. Endocrine mechanisms connecting exercise to brown adipose tissue metabolism: a human perspective. Curr Diab Rep. 2020;20(9):40. doi: 10.1007/s11892-020-01319-7
  • Bostrom P, Wu J, Jedrychowski MP, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis.Nature. 2012;481(7382):463–468. doi: 10.1038/nature10777
  • Roberts LD, Bostrom P, J F O, et al. β-Aminoisobutyric acid induces browning of white fat and hepaticβ-oxidation and is inversely correlated with car diometabolic risk factors. Cell Metab. 2014;19(1):96–108. doi: 10.1016/j.cmet.2013.12.003
  • Huang T, Xiaokai L. Review on the Association between exercise and adipose tissue Browning. China Sport Science. 2016;36(7):71–78.
  • Dunstan D. Diabetes: exercise and T2DM-move muscles more often! Nat Rev Endocrinol. 2011;7(4):189–190. doi: 10.1038/nrendo.2011.35
  • Tanaka R, Fuse S, Kuroiwa M, et al. Vigorous-intensity physical activities are associated with high brown adipose tissue density in humans. Int J Environ Res Public Health. 2020;17(8):2796. doi: 10.3390/ijerph17082796
  • Vosselman MJ, Hoeks J, Brans B, et al. Low brown adipose tissue activity in endurance-trained compared with lean sedentary men. Int J Obes (Lond). 2015;39(12):1696–1702. doi: 10.1038/ijo.2015.130
  • Singhal V, Maffazioli GD, Ackerman KE, et al. Effect of chronic athletic activity on brown fat in young women. PLoS One. 2016;11(5):e0156353. doi: 10.1371/journal.pone.0156353
  • Sanchez-Delgado G, Martinez-Tellez B, Olza J, et al. Activating brown adipose tissue through exercise(ACTIBATE)in young adults: rationale, design and methodology [J].Contemp Clin trials. 2015;45(Pt B):416–425. doi: 10.1016/j.cct.2015.11.004
  • Rothwell NJ, Stock MJ. Lulxuskonsumption, diet-induced the rmogenesis and brown fat: the case in favour. BrMed. 1983;64(1):19–23. doi: 10.1042/cs0640019
  • Wu J, Cohen P, Spiegelman BM. Adaptive the rmogenesis in adipocytes: is beige the new brown?.Genes Dev. Genes Dev. 2013;27(3):234–250. doi: 10.1101/gad.211649.112
  • Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277–359. doi: 10.1152/physrev.00015.2003
  • Vegiopoulos A, Muller-Decker K, Strzoda D, et al. Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328(5982):1158–1161. doi: 10.1126/science.1186034
  • Li W, Li Q. PGC-1α and obesity. Mod Med J. 2006(3):204–206.
  • Song G, Deng YM, Xu, Y et al. Effects of exercise on mRNA expression of brown adipose tissue function-regulated genes in rats with high-fat diet during the growth period. Chin J Integr Med. 2021;40(1):29–37.
  • Hansen JS, Clemmesen JO, Secher NH, et al. Glucagon-to-insulin ratio is pivotal for splanchnic regulation of FGF-21 in humans. Molecular Metabolism. 2015;4(8):551–560. doi: 10.1016/j.molmet.2015.06.001
  • Fisher FM, Chui PC, Antonellis PJ, et al. Obesity is an FGF21 resistant State. Diabetes. 2010;59(11):2781–2789. doi: 10.2337/db10-0193
  • Véniant MM, Sivits G, Helmering J, et al. Pharmacologic effects of FGF21 are Independent of the “Browning” of white adipose tissue. Cell Metabolism. 2015;21(5):731–738. doi: 10.1016/j.cmet.2015.04.019
  • Slusher AL, Whitehurst M, Zoeller RF, et al. Attenuated fibroblast growth factor 21 response to acute aerobic exercise in obese individuals. Nutrition, Metabolism And Cardiovascular Diseases. 2015;25(9):839–845. doi: 10.1016/j.numecd.2015.06.002
  • Xu X, Ying Z, Cai M, et al. Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue.Am. J Physiol Regul Integr Comp Physiol. 2011;300(5):R1115–1125. doi: 10.1152/ajpregu.00806.2010
  • Lehnig AC, Stanford KI. Exercise-induced adaptations to white and brown adipose tissue. J Exp Biol. 2018;221(Pt Suppl 1):jeb161570. doi: 10.1242/jeb.161570
  • Fu P, Lijing G, Rongxin Z, et al. Studies on aerobic exercise modulating genes and pathways associated with inflammation of brown adipose tissue in obese mice. Chin J Integr Med. 2018;37(9):764–771.
  • Wang J, Xiaohong W. Feng Weidou.Exercise training inhibiting TGFp pathway and improving D-Glactose injection–induced senescent muscle loss in rat. China Sport Science. 2014;34(10):72–77.
  • Nguyen MT, Favelyukis S, Nguyen AK, et al. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-Dependent Pathways[j]. J Biol Chem. 2007;282(48):35279–35292. doi: 10.1074/jbc.M706762200
  • Zhang Y, Hongbing Z. Effects of 8 week swimming exercise intervention on inflammatory cytokines and adipokines in mice with high-fat diet. Chin J Rehabil Med. 2020;35(3):301–305.
  • Zhang J, Yanmei N, Li F. Browning of white fat – a new target of exercise weight loss. Chin J Integr Med. 2014;33(8):826–829+840.
  • Srivastava S, Veech RL. Brown and brite: the fat soldiers in the anti-obesity fight. Front Physiol query. 2019;10(38). doi: 10.3389/fphys.2019.00038
  • Thyagarajan B, Foster MT. Beiging of white adipose tissue as a therapeutic strategy for weight loss in humans . Hormone molecular biology and clinical investigation. 2017;31(2): doi: 10.1515/hmbci-2017-0016.
  • Fu P, Lijing G, Yang H. The effect of exercise on function of brown adipose tissue and its mechanism. China Sport Science. 2018;38(11):92–97.
  • Haiping D. Anti-resistance ladder climbing exercise with MSTN antibodies and combined intervention to regulate brown fat glucose metabolism and molecular mechanism [D]. Xian: Shaanxi Normal University; 2016.
  • May FJ, Baer LA, Lehnig AC, et al. Lipidomic adaptations in white and brown adipose tissue in response to exercise demonstrates molecular species-specific remodeling. Cell Rep. 2017;18(6):1558–1572. doi: 10.1016/j.celrep.2017.01.038
  • Guo Y, Peijie C, Weihua X. Mitochondrial dysfunction and exercise regulation in adipose tissue during obesity. Chinese J Biochem Mol Biol. 2020;36(10):1145–1150.
  • Han J, Meng Q, Shen L, et al. Interleukin-6 induces fat loss in cancer cachexia by promoting white adipose tissue lipolysis and browning. Lipids Health Dis. 2018;17(1):14. doi: 10.1186/s12944-018-0657-0
  • De Matteis R, Lucertini F, Guescini M, et al. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr Metab Cardiovasc Dis. 2013;23(6):582–590. doi: 10.1016/j.numecd.2012.01.013
  • De Farias JM, Bom KF, Tromm CB, et al. Effect of physical training on the adipose tissue of diet-induced obesity mice: interaction between reactive oxygen species and lipolysis. Horm Metab Res. 2013;45(3):190–196. doi: 10.1055/s-0032-1323740
  • Lira VA, Benton CR, Yan Z, et al. PGC-1 alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab. 2010;299(2):1451–1461. doi: 10.1152/ajpendo.00755.2009
  • Wu MV, Bikopoulos G, Hung S, et al. Thermogenic capacity is antagonistically regulated in classical brown and white subcutaneous fat depots by high fat diet and endurance training in rats: impact on whole-body energy expenditure. Journal Of Biological Chemistry. 2014;289(49):34129–34140. doi: 10.1074/jbc.M114.591008
  • Peppler WT, Townsend LK, Knuth CM, et al. Subcutaneous inguinal white adipose tissue is responsive to, but dispensable for, the metabolic health benefits of exercise. American Journal Of Physiology-Endocrinology And Metabolism. 2018;314(1):E66–77. doi: 10.1152/ajpendo.00226.2017
  • Xiong Y, Wu Z, Zhang B, et al. Fndc5 loss-of-function attenuates exercise-induced browning of white adipose tissue in mice. FASEB J. 2019;33(5):5876–5886. doi: 10.1096/fj.201801754RR
  • Ziegler AK, Damgaard A, Mackey AL, et al. An anti-inflammatory phenotype in visceral adipose tissue of old lean mice, augmented by exercise. Sci Rep. 2019;9(1):12069. doi: 10.1038/s41598-019-48587-2
  • Tsiloulis T, Carey AL, Bayliss J, et al. No evidence of white adipocyte browning after endurance exercise training in obese men. Int J Obes (Lond). 2018;42(4):721–727. doi: 10.1038/ijo.2017.295
  • Dinas PC, Valente A, Granzotto M, et al. Browning formation markers of subcutaneous adipose tissue in relation to resting energy expenditure, physical activity and diet in humans. Horm Mol Biol Clin Investig. 2017;31(1).
  • Wang L, Liang Y. Fibroblast growth factor 21 regulates browning of white fat: the roIe of exercise. Chin J Tissue Eng Res. 2020;24(20):3275–3280.
  • Seale P, Kajimura S, Yang W, et al. Transcriptional Control of brown fat Determination by PRDM16. Cell Metab. 2007;6(1):0–54. doi: 10.1016/j.cmet.2007.06.001
  • Fan D, Juan J, Yubo H, et al. Research progress on factors influencing browning of white fat. Chin J Diabetes Mellit. 2020;28(11):874–877.
  • Cao L, Choi EY, Liu X, et al. White to brown fat phenotypic switch induced by genetic and environmental activation of a hypothalamic-adipocyte axis [J].Cell Metab. Cell Metab. 2011;14(3):324–338. doi: 10.1016/j.cmet.2011.06.020
  • Alizadeh Pahlavani H. Exercise therapy for people with sarcopenic obesity: myokines and Adipokines as effective actors. Front Endocrinol. 2022;13:811751. doi: 10.3389/fendo.2022.811751
  • Mu WJ, Zhu JY, Chen M, et al. Exercise-Mediated Browning of white adipose tissue: its significance, mechanism and effectiveness. Int J Mol Sci. 2021;22(21):22. doi: 10.3390/ijms222111512
  • Nederveen JP, Warnier G, Di Carlo A, et al. Extracellular vesicles and exosomes: insights from exercise Science. Front Physiol. 2020;11:604274. doi: 10.3389/fphys.2020.604274
  • Li Y, Han C, Wang J, et al. Exosomes mediate the beneficial effects of exercise. Adv Exp Med Biol. 2017;1000:333–353.
  • Kim KH, Kim SH, Min YK, et al. Acute exercise induces FGF21 expression in mice and in healthy humans. PLo S One. 2013;8(5):e63517. doi: 10.1371/journal.pone.0063517
  • Moyers JS, Shiyanova TL, Mehrbod F, et al. Molecular determinants of FGF21 activity-synergy and cross-talk with PPAR gamma signaling. J Cell Physiol. 2007;210(1):1–6. doi: 10.1002/jcp.20847
  • Volpe M. Natriuretic peptides and cardio-renal disease. Int J Cardiol. 2014;176(3):630–639. doi: 10.1016/j.ijcard.2014.08.032
  • Lafontan M, Moro C, Berlan M, et al. Control of lipolysis by natriuretic peptides and cyclic GMP. Trends Endocrinol Metab. 2008;19(4):130–137. doi: 10.1016/j.tem.2007.11.006
  • Engeli S, Birkenfeld AL, Badin PM, et al. Natriuretic peptides enhance the oxidative capacity of human skeletal muscle. J Clin Invest query. 2012;122(12):4675–4679. doi: 10.1172/JCI64526
  • Bordicchia M, D L, Amri EZ, et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest. 2012;122(3):1022–1036. doi: 10.1172/JCI59701
  • Thomsen CF, Ried-Larsen M, Goetze JP, et al. Plasma proatrial natriuretic peptide associates with lipid oxidation during exercise and cardiorespiratory fitness in healthy young adults. Peptides. 2019;122(170156). doi: 10.1016/j.peptides.2019.170156
  • Tapia-Arancibia L, Rage F, Givalois L, et al. Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol. 2004;25(2):77–107. doi: 10.1016/j.yfrne.2004.04.001
  • Stanford KI, Goodyear LJ. Exercise regulation of adipose tissue. Adipocyte. 2016;5(2):153–162. doi: 10.1080/21623945.2016.1191307
  • Wrann CD, White JP, Salogiannnis J, et al. Exercise induces hippocampal BDNF through a PGC-1α/FNDC5 pathway. Cell Metabolism. 2013;18(5):649–659. doi: 10.1016/j.cmet.2013.09.008
  • Tsiloulis T, Watt MJ. Exercise and the regulation of adipose tissue metabolism. Prog Mol Biol Transl Sci. 2015;135(175–201.
  • Marinus N, Hansen D, Feys P, et al. The impact of different types of exercise training on peripheral blood brain-derived neurotrophic factor concentrations in older adults: a meta-analysis. Sports Med. 2019;49(10):1529–1546. doi: 10.1007/s40279-019-01148-z