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Current Protein & Peptide Science

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ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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Mini-Review Article

Exercise and Metabolic Health: The Emerging Roles of Novel Exerkines

Author(s): İbrahim Türkel, Berkay Özerkliğ, Muhammed M. Atakan, Selin Aktitiz, Şükran N. Koşar and Burak Yazgan*

Volume 23, Issue 7, 2022

Published on: 26 August, 2022

Page: [437 - 455] Pages: 19

DOI: 10.2174/1389203723666220629163524

Price: $65

Abstract

Physical inactivity is a major cause of chronic diseases. It shortens the health span by lowering the age of the first chronic disease onset, which leads to decreased quality of life and increased mortality risk. On the other hand, physical exercise is considered a miracle cure in the primary prevention of at least 35 chronic diseases, including obesity, insulin resistance, and type 2 diabetes. However, despite many scientific attempts to unveil the health benefits conferred by regular exercise, the underlying molecular mechanisms driving such benefits are not fully explored. Recent research shows that exercise-induced bioactive molecules, named exerkines, might play a critical role in the regulation of metabolic homeostasis and thus prevent metabolic diseases. Here we summarize the current understanding of the health-promoting effects of exerkines secreted from skeletal muscle, adipose tissue, bone, and liver, including MOTS-c, BDNF, miR-1, 12,13-diHOME, irisin, SPX, OC, GDF15, and FGF21 on obesity, insulin resistance, and type 2 diabetes. Identifying the systemic health benefits of exerkines may open a new area for the discovery of new pharmacological strategies for the prevention and management of metabolic diseases.

Keywords: Exercise, exerkines, obesity, insulin resistance, type 2 diabetes, MOTS-c, spexin, 12, 13-diHOME.

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Graphical Abstract

[1]
Booth, F.W.; Roberts, C.K.; Laye, M.J. Lack of exercise is a major cause of chronic diseases. Compr. Physiol., 2012, 2(2), 1143-1211.
[http://dx.doi.org/10.1002/cphy.c110025] [PMID: 23798298]
[2]
Tremmel, M.; Gerdtham, U.G.; Nilsson, P.M.; Saha, S. Economic burden of obesity: A systematic literature review. Int. J. Environ. Res. Public Health, 2017, 14(4), 435.
[http://dx.doi.org/10.3390/ijerph14040435] [PMID: 28422077]
[3]
Guthold, R.; Stevens, G.A.; Riley, L.M.; Bull, F.C. Worldwide trends in insufficient physical activity from 2001 to 2016: A pooled analy-sis of 358 population-based surveys with 1•9 million participants. Lancet Glob. Health, 2018, 6(10), e1077-e1086.
[http://dx.doi.org/10.1016/S2214-109X(18)30357-7] [PMID: 30193830]
[4]
WHO. 2017. Available from: http://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight
[5]
Sarma, S.; Sockalingam, S.; Dash, S. Obesity as a multisystem disease: Trends in obesity rates and obesity-related complications. Diabetes Obes. Metab., 2021, 23(Suppl. 1), 3-16.
[http://dx.doi.org/10.1111/dom.14290] [PMID: 33621415]
[6]
Piché, M.E.; Tchernof, A.; Després, J.P. Obesity phenotypes, diabetes, and cardiovascular diseases. Circ. Res., 2020, 126(11), 1477-1500.
[http://dx.doi.org/10.1161/CIRCRESAHA.120.316101] [PMID: 32437302]
[7]
Sylow, L.; Richter, E.A. Current advances in our understanding of exercise as medicine in metabolic disease. Curr. Opin. Physiol., 2019, 12, 12-19.
[http://dx.doi.org/10.1016/j.cophys.2019.04.008]
[8]
Prieto, D.; Contreras, C.; Sánchez, A. Endothelial dysfunction, obesity and insulin resistance. Curr. Vasc. Pharmacol., 2014, 12(3), 412-426.
[http://dx.doi.org/10.2174/1570161112666140423221008] [PMID: 24846231]
[9]
Susruta, A.; Susruta, S. Uttar Tantra, 2008, 56(6), 413.
[10]
Warburton, D.E.; Nicol, C.W.; Bredin, S.S. Health benefits of physical activity: The evidence. CMAJ, 2006, 174(6), 801-809.
[http://dx.doi.org/10.1503/cmaj.051351] [PMID: 16534088]
[11]
Fatone, C.; Guescini, M.; Balducci, S.; Battistoni, S.; Settequattrini, A.; Pippi, R.; Stocchi, L.; Mantuano, M.; Stocchi, V.; De Feo, P. Two weekly sessions of combined aerobic and resistance exercise are sufficient to provide beneficial effects in subjects with Type 2 diabetes mellitus and metabolic syndrome. J. Endocrinol. Invest., 2010, 33(7), 489-495.
[http://dx.doi.org/10.1007/BF03346630] [PMID: 20142634]
[12]
Haskell, W.L.; Lee, I.M.; Pate, R.R.; Powell, K.E.; Blair, S.N.; Franklin, B.A.; Macera, C.A.; Heath, G.W.; Thompson, P.D.; Bauman, A. Physical activity and public health: Updated recommendation for adults from the American college of sports medicine and the American heart association. Med. Sci. Sports Exerc., 2007, 39(8), 1423-1434.
[http://dx.doi.org/10.1249/mss.0b013e3180616b27] [PMID: 17762377]
[13]
Anton, S.D.; Hida, A.; Mankowski, R.; Layne, A.; Solberg, L.M.; Mainous, A.G.; Buford, T. Nutrition and exercise in sarcopenia. Curr. Protein Pept. Sci., 2018, 19(7), 649-667.
[http://dx.doi.org/10.2174/1389203717666161227144349] [PMID: 28029078]
[14]
Hawley, J.A. Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance. Diabetes Metab. Res. Rev., 2004, 20(5), 383-393.
[http://dx.doi.org/10.1002/dmrr.505] [PMID: 15343584]
[15]
Febbraio, M.A. Exercise metabolism in 2016: Health benefits of exercise - more than meets the eye! Nat. Rev. Endocrinol., 2017, 13(2), 72-74.
[http://dx.doi.org/10.1038/nrendo.2016.218] [PMID: 28051119]
[16]
Booth, F.W.; Tseng, B.S.; Flück, M.; Carson, J.A. Molecular and cellular adaptation of muscle in response to physical training. Acta Physiol. Scand., 1998, 162(3), 343-350.
[http://dx.doi.org/10.1046/j.1365-201X.1998.0326e.x] [PMID: 9578380]
[17]
Flück, M.; Hoppeler, H. Molecular basis of skeletal muscle plasticity--from gene to form and function. Rev. Physiol. Biochem. Pharmacol., 2003, 146, 159-216.
[http://dx.doi.org/10.1007/s10254-002-0004-7] [PMID: 12605307]
[18]
Hawley, J.A.; Hargreaves, M.; Joyner, M.J.; Zierath, J.R. Integrative biology of exercise. Cell, 2014, 159(4), 738-749.
[http://dx.doi.org/10.1016/j.cell.2014.10.029] [PMID: 25417152]
[19]
Whitham, M.; Febbraio, M.A. The ever-expanding myokinome: Discovery challenges and therapeutic implications. Nat. Rev. Drug Discov., 2016, 15(10), 719-729.
[http://dx.doi.org/10.1038/nrd.2016.153] [PMID: 27616294]
[20]
Pedersen, B.K.; Akerstrom, T.C.; Nielsen, A.R.; Fischer, C.P. Role of myokines in exercise and metabolism. J. Appl. Physiol., 2007, 103(3), 1093-1098.
[21]
Magliulo, L.; Bondi, D.; Pini, N.; Marramiero, L.; Di Filippo, E.S. The wonder exerkines-novel insights: A critical state-of-the-art review. Mol. Cell. Biochem., 2022, 477(1), 105-113.
[http://dx.doi.org/10.1007/s11010-021-04264-5] [PMID: 34554363]
[22]
Lee, T.H.; Formolo, D.A.; Kong, T.; Lau, S.W.; Ho, C.S.; Leung, R.Y.H.; Hung, F.H.; Yau, S.Y. Potential exerkines for physical exercise-elicited pro-cognitive effects: Insight from clinical and animal research. Int. Rev. Neurobiol., 2019, 147, 361-395.
[http://dx.doi.org/10.1016/bs.irn.2019.06.002] [PMID: 31607361]
[23]
Chow, L.S.; Gerszten, R.E.; Taylor, J.M.; Pedersen, B.K.; van Praag, H.; Trappe, S.; Febbraio, M.A.; Galis, Z.S.; Gao, Y.; Haus, J.M.; Lan-za, I.R.; Lavie, C.J.; Lee, C.H.; Lucia, A.; Moro, C.; Pandey, A.; Robbins, J.M.; Stanford, K.I.; Thackray, A.E.; Villeda, S.; Watt, M.J.; Xia, A.; Zierath, J.R.; Goodpaster, B.H.; Snyder, M.P. Exerkines in health, resilience and disease. Nat. Rev. Endocrinol., 2022, 18(5), 273-289.
[http://dx.doi.org/10.1038/s41574-022-00641-2] [PMID: 35304603]
[24]
McGee, S.L.; Hargreaves, M. Exercise adaptations: Molecular mechanisms and potential targets for therapeutic benefit. Nat. Rev. Endocrinol., 2020, 16(9), 495-505.
[http://dx.doi.org/10.1038/s41574-020-0377-1] [PMID: 32632275]
[25]
Reddy, A.; Bozi, L.H.M.; Yaghi, O.K.; Mills, E.L.; Xiao, H.; Nicholson, H.E.; Paschini, M.; Paulo, J.A.; Garrity, R.; Laznik-Bogoslavski, D.; Ferreira, J.C.B.; Carl, C.S.; Sjøberg, K.A.; Wojtaszewski, J.F.P.; Jeppesen, J.F.; Kiens, B.; Gygi, S.P.; Richter, E.A.; Mathis, D.; Chouchani, E.T. pH-gated succinate secretion regulates muscle remodeling in response to exercise. Cell, 2020, 183(1), 62-75.e17.
[http://dx.doi.org/10.1016/j.cell.2020.08.039] [PMID: 32946811]
[26]
Nalbandian, M.; Takeda, M. Lactate as a signaling molecule that regulates exercise-induced adaptations. Biology (Basel), 2016, 5(4), 38.
[http://dx.doi.org/10.3390/biology5040038] [PMID: 27740597]
[27]
Atakan, M.M. Koşar, S.N.; Güzel, Y.; Tin, H.T.; Yan, X. The role of exercise, diet, and cytokines in preventing obesity and improving adipose tissue. Nutrients, 2021, 13(5), 1459.
[http://dx.doi.org/10.3390/nu13051459] [PMID: 33922998]
[28]
Pedersen, B.K.; Steensberg, A.; Schjerling, P. Muscle-derived interleukin-6: Possible biological effects. J. Physiol., 2001, 536(Pt 2), 329-337.
[http://dx.doi.org/10.1111/j.1469-7793.2001.0329c.xd] [PMID: 11600669]
[29]
Ostrowski, K.; Rohde, T.; Zacho, M.; Asp, S.; Pedersen, B.K. Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J. Physiol., 1998, 508(Pt 3), 949-953.
[http://dx.doi.org/10.1111/j.1469-7793.1998.949bp.x] [PMID: 9518745]
[30]
Kirk, B.; Feehan, J.; Lombardi, G.; Duque, G. Muscle, bone, and fat crosstalk: The biological role of myokines, osteokines, and adi-pokines. Curr. Osteoporos. Rep., 2020, 18(4), 388-400.
[http://dx.doi.org/10.1007/s11914-020-00599-y] [PMID: 32529456]
[31]
Safdar, A.; Saleem, A.; Tarnopolsky, M.A. The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat. Rev. Endocrinol., 2016, 12(9), 504-517.
[http://dx.doi.org/10.1038/nrendo.2016.76] [PMID: 27230949]
[32]
Yang, F.T.; Stanford, K.I. Batokines: Mediators of inter-tissue communication (a mini-review). Curr. Obes. Rep., 2022, 11(1), 1-9.
[http://dx.doi.org/10.1007/s13679-021-00465-7] [PMID: 34997461]
[33]
Henriksen, T.; Green, C.; Pedersen, B.K. Myokines in myogenesis and health. Recent Pat. Biotechnol., 2012, 6(3), 167-171.
[http://dx.doi.org/10.2174/1872208311206030167] [PMID: 23092437]
[34]
Lee, C.; Zeng, J.; Drew, B.G.; Sallam, T.; Martin-Montalvo, A.; Wan, J.; Kim, S.J.; Mehta, H.; Hevener, A.L.; de Cabo, R.; Cohen, P. The mitochondrial-derived peptide MOTS-c promotes metabolic homeostasis and reduces obesity and insulin resistance. Cell Metab., 2015, 21(3), 443-454.
[http://dx.doi.org/10.1016/j.cmet.2015.02.009] [PMID: 25738459]
[35]
Ramanjaneya, M.; Bettahi, I.; Jerobin, J.; Chandra, P.; Abi Khalil, C.; Skarulis, M.; Atkin, S.L.; Abou-Samra, A.B. Mitochondrial-derived peptides are down regulated in diabetes subjects. Front. Endocrinol. (Lausanne), 2019, 10, 331.
[http://dx.doi.org/10.3389/fendo.2019.00331] [PMID: 31214116]
[36]
Ramanjaneya, M.; Jerobin, J.; Bettahi, I.; Bensila, M.; Aye, M.; Siveen, K.S.; Sathyapalan, T.; Skarulis, M.; Abou-Samra, A.B.; Atkin, S.L. Lipids and insulin regulate mitochondrial-derived peptide (MOTS-c) in PCOS and healthy subjects. Clin. Endocrinol. (Oxf.), 2019, 91(2), 278-287.
[http://dx.doi.org/10.1111/cen.14007] [PMID: 31066084]
[37]
Du, C.; Zhang, C.; Wu, W.; Liang, Y.; Wang, A.; Wu, S.; Zhao, Y.; Hou, L.; Ning, Q.; Luo, X. Circulating MOTS-c levels are decreased in obese male children and adolescents and associated with insulin resistance. Pediatr. Diabetes, 2018, 19(6), 1058-1064.
[http://dx.doi.org/10.1111/pedi.12685] [PMID: 29691953]
[38]
Dieli-Conwright, C.M.; Sami, N.; Norris, M.K.; Wan, J.; Kumagai, H.; Kim, S.J.; Cohen, P. Effect of aerobic and resistance exercise on the mitochondrial peptide MOTS-c in hispanic and non-hispanic white breast cancer survivors. Sci. Rep., 2021, 11(1), 16916.
[http://dx.doi.org/10.1038/s41598-021-96419-z] [PMID: 34413391]
[39]
Yong, C.Q.Y.; Tang, B.L. A mitochondrial encoded messenger at the nucleus. Cells, 2018, 7(8), 105.
[http://dx.doi.org/10.3390/cells7080105] [PMID: 30104535]
[40]
Zarse, K.; Ristow, M. A mitochondrially encoded hormone ameliorates obesity and insulin resistance. Cell Metab., 2015, 21(3), 355-356.
[http://dx.doi.org/10.1016/j.cmet.2015.02.013] [PMID: 25738453]
[41]
Lu, H.; Wei, M.; Zhai, Y.; Li, Q.; Ye, Z.; Wang, L.; Luo, W.; Chen, J.; Lu, Z. MOTS-c peptide regulates adipose homeostasis to prevent ovariectomy-induced metabolic dysfunction. J. Mol. Med. (Berl.), 2019, 97(4), 473-485.
[http://dx.doi.org/10.1007/s00109-018-01738-w] [PMID: 30725119]
[42]
Kim, S.J.; Miller, B.; Mehta, H.H.; Xiao, J.; Wan, J.; Arpawong, T.E.; Yen, K.; Cohen, P. The mitochondrial-derived peptide MOTS-c is a regulator of plasma metabolites and enhances insulin sensitivity. Physiol. Rep., 2019, 7(13), e14171.
[http://dx.doi.org/10.14814/phy2.14171] [PMID: 31293078]
[43]
Yin, Y.; Pan, Y.; He, J.; Zhong, H.; Wu, Y.; Ji, C.; Liu, L.; Cui, X. The mitochondrial-derived peptide MOTS-c relieves hyperglycemia and insulin resistance in gestational diabetes mellitus. Pharmacol. Res., 2022, 175, 105987.
[http://dx.doi.org/10.1016/j.phrs.2021.105987] [PMID: 34798268]
[44]
Li, S.; Laher, I. Exercise pills: At the starting line. Trends Pharmacol. Sci., 2015, 36(12), 906-917.
[http://dx.doi.org/10.1016/j.tips.2015.08.014] [PMID: 26439443]
[45]
Reynolds, J.C.; Lai, R.W.; Woodhead, J.S.T.; Joly, J.H.; Mitchell, C.J.; Cameron-Smith, D.; Lu, R.; Cohen, P.; Graham, N.A.; Benayoun, B.A.; Merry, T.L.; Lee, C. MOTS-c is an exercise-induced mitochondrial-encoded regulator of age-dependent physical decline and muscle homeostasis. Nat. Commun., 2021, 12(1), 470.
[http://dx.doi.org/10.1038/s41467-020-20790-0] [PMID: 33473109]
[46]
Cataldo, L.R.; Fernández-Verdejo, R.; Santos, J.L.; Galgani, J.E. Plasma MOTS-c levels are associated with insulin sensitivity in lean but not in obese individuals. J. Investig. Med., 2018, 66(6), 1019-1022.
[http://dx.doi.org/10.1136/jim-2017-000681] [PMID: 29593067]
[47]
Guo, Q.; Chang, B.; Yu, Q.L.; Xu, S.T.; Yi, X.J.; Cao, S.C. Adiponectin treatment improves insulin resistance in mice by regulating the expression of the mitochondrial-derived peptide MOTS-c and its response to exercise via APPL1-SIRT1-PGC-1. Diabetologia, 2020, 63(12), 2675-2688.
[http://dx.doi.org/10.1007/s00125-020-05269-3] [PMID: 32880686]
[48]
Yang, B.; Yu, Q.; Chang, B.; Guo, Q.; Xu, S.; Yi, X.; Cao, S. MOTS-c interacts synergistically with exercise intervention to regulate PGC-1α expression, attenuate insulin resistance and enhance glucose metabolism in mice via AMPK signaling pathway. Biochim. Biophys. Acta Mol. Basis Dis., 2021, 1867(6), 166126.
[http://dx.doi.org/10.1016/j.bbadis.2021.166126] [PMID: 33722744]
[49]
Cotman, C.W.; Engesser-Cesar, C. Exercise enhances and protects brain function. Exerc. Sport Sci. Rev., 2002, 30(2), 75-79.
[http://dx.doi.org/10.1097/00003677-200204000-00006] [PMID: 11991541]
[50]
Mattson, M.P.; Maudsley, S.; Martin, B. BDNF and 5-HT: A dynamic duo in age-related neuronal plasticity and neurodegenerative disor-ders. Trends Neurosci., 2004, 27(10), 589-594.
[http://dx.doi.org/10.1016/j.tins.2004.08.001] [PMID: 15374669]
[51]
Tyler, W.J.; Alonso, M.; Bramham, C.R.; Pozzo-Miller, L.D. From acquisition to consolidation: On the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem., 2002, 9(5), 224-237.
[http://dx.doi.org/10.1101/lm.51202] [PMID: 12359832]
[52]
Lessmann, V.; Brigadski, T. Mechanisms, locations, and kinetics of synaptic BDNF secretion: An update. Neurosci. Res., 2009, 65(1), 11-22.
[http://dx.doi.org/10.1016/j.neures.2009.06.004] [PMID: 19523993]
[53]
Barde, Y.A.; Edgar, D.; Thoenen, H. Purification of a new neurotrophic factor from mammalian brain. EMBO J., 1982, 1(5), 549-553.
[http://dx.doi.org/10.1002/j.1460-2075.1982.tb01207.x] [PMID: 7188352]
[54]
Metsis, M.; Timmusk, T.; Arenas, E.; Persson, H. Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc. Natl. Acad. Sci. USA, 1993, 90(19), 8802-8806.
[http://dx.doi.org/10.1073/pnas.90.19.8802] [PMID: 8415610]
[55]
Binder, D.K.; Scharfman, H.E. Brain-derived neurotrophic factor. Growth Factors, 2004, 22(3), 123-131.
[http://dx.doi.org/10.1080/08977190410001723308] [PMID: 15518235]
[56]
Brigadski, T.; Leßmann, V. The physiology of regulated BDNF release. Cell Tissue Res., 2020, 382(1), 15-45.
[http://dx.doi.org/10.1007/s00441-020-03253-2] [PMID: 32944867]
[57]
Huang, E.J.; Reichardt, L.F. Neurotrophins: Roles in neuronal development and function. Annu. Rev. Neurosci., 2001, 24, 677-736.
[http://dx.doi.org/10.1146/annurev.neuro.24.1.677] [PMID: 11520916]
[58]
Seidler, K.; Barrow, M. Intermittent fasting and cognitive performance - Targeting BDNF as potential strategy to optimise brain health. Front. Neuroendocrinol., 2022, 65, 100971.
[http://dx.doi.org/10.1016/j.yfrne.2021.100971] [PMID: 34929259]
[59]
Ventriglia, M.; Zanardini, R.; Bonomini, C.; Zanetti, O.; Volpe, D.; Pasqualetti, P.; Gennarelli, M.; Bocchio-Chiavetto, L. Serum brain-derived neurotrophic factor levels in different neurological diseases. BioMed Res. Int., 2013, 2013, 901082.
[http://dx.doi.org/10.1155/2013/901082] [PMID: 24024214]
[60]
Siuda, J. Patalong-Ogiewa, M.; Żmuda, W.; Targosz-Gajniak, M.; Niewiadomska, E.; Matuszek, I.; Jędrzejowska-Szypułka, H.; Lewin-Kowalik, J.; Rudzińska-Bar, M. Cognitive impairment and BDNF serum levels. Neurol. Neurochir. Pol., 2017, 51(1), 24-32.
[http://dx.doi.org/10.1016/j.pjnns.2016.10.001] [PMID: 28341039]
[61]
Xie, B.; Zhou, H.; Liu, W.; Yu, W.; Liu, Z.; Jiang, L.; Zhang, R.; Cui, D.; Shi, Z.; Xu, S. Evaluation of the diagnostic value of peripheral BDNF levels for Alzheimer’s disease and mild cognitive impairment: Results of a meta-analysis. Int. J. Neurosci., 2020, 130(3), 218-230.
[http://dx.doi.org/10.1080/00207454.2019.1667794] [PMID: 31518516]
[62]
Matthews, V.B.; Aström, M.B.; Chan, M.H.; Bruce, C.R.; Krabbe, K.S.; Prelovsek, O.; Akerström, T.; Yfanti, C.; Broholm, C.; Mortensen, O.H.; Penkowa, M.; Hojman, P.; Zankari, A.; Watt, M.J.; Bruunsgaard, H.; Pedersen, B.K.; Febbraio, M.A. Brain-derived neurotrophic fac-tor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein ki-nase. Diabetologia, 2009, 52(7), 1409-1418.
[http://dx.doi.org/10.1007/s00125-009-1364-1] [PMID: 19387610]
[63]
Mowla, S.J.; Farhadi, H.F.; Pareek, S.; Atwal, J.K.; Morris, S.J.; Seidah, N.G.; Murphy, R.A. Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J. Biol. Chem., 2001, 276(16), 12660-12666.
[http://dx.doi.org/10.1074/jbc.M008104200] [PMID: 11152678]
[64]
Nakagawa, T.; Tsuchida, A.; Itakura, Y.; Nonomura, T.; Ono, M.; Hirota, F.; Inoue, T.; Nakayama, C.; Taiji, M.; Noguchi, H. Brain-derived neurotrophic factor regulates glucose metabolism by modulating energy balance in diabetic mice. Diabetes, 2000, 49(3), 436-444.
[http://dx.doi.org/10.2337/diabetes.49.3.436] [PMID: 10868966]
[65]
Mousavi, K.; Jasmin, B.J. BDNF is expressed in skeletal muscle satellite cells and inhibits myogenic differentiation. J. Neurosci., 2006, 26(21), 5739-5749.
[http://dx.doi.org/10.1523/JNEUROSCI.5398-05.2006] [PMID: 16723531]
[66]
Kernie, S.G.; Liebl, D.J.; Parada, L.F. BDNF regulates eating behavior and locomotor activity in mice. EMBO J., 2000, 19(6), 1290-1300.
[http://dx.doi.org/10.1093/emboj/19.6.1290] [PMID: 10716929]
[67]
Duan, W.; Guo, Z.; Jiang, H.; Ware, M.; Mattson, M.P. Reversal of behavioral and metabolic abnormalities, and insulin resistance syn-drome, by dietary restriction in mice deficient in brain-derived neurotrophic factor. Endocrinology, 2003, 144(6), 2446-2453.
[http://dx.doi.org/10.1210/en.2002-0113] [PMID: 12746306]
[68]
Tsuchida, A.; Nonomura, T.; Nakagawa, T.; Itakura, Y.; Ono-Kishino, M.; Yamanaka, M.; Sugaru, E.; Taiji, M.; Noguchi, H. Brain-derived neurotrophic factor ameliorates lipid metabolism in diabetic mice. Diabetes Obes. Metab., 2002, 4(4), 262-269.
[http://dx.doi.org/10.1046/j.1463-1326.2002.00206.x] [PMID: 12099975]
[69]
Yamanaka, M.; Itakura, Y.; Ono-Kishino, M.; Tsuchida, A.; Nakagawa, T.; Taiji, M. Intermittent administration of brain-derived neu-rotrophic factor (BDNF) ameliorates glucose metabolism and prevents pancreatic exhaustion in diabetic mice. J. Biosci. Bioeng., 2008, 105(4), 395-402.
[http://dx.doi.org/10.1263/jbb.105.395] [PMID: 18499057]
[70]
Krabbe, K.S.; Nielsen, A.R.; Krogh-Madsen, R.; Plomgaard, P.; Rasmussen, P.; Erikstrup, C.; Fischer, C.P.; Lindegaard, B.; Petersen, A.M.; Taudorf, S.; Secher, N.H.; Pilegaard, H.; Bruunsgaard, H.; Pedersen, B.K. Brain-derived neurotrophic factor (BDNF) and type 2 dia-betes. Diabetologia, 2007, 50(2), 431-438.
[http://dx.doi.org/10.1007/s00125-006-0537-4] [PMID: 17151862]
[71]
Li, B.; Lang, N.; Cheng, Z.F. Serum levels of brain-derived neurotrophic factor are associated with diabetes risk, complications, and obesi-ty: A cohort study from chinese patients with type 2 diabetes. Mol. Neurobiol., 2016, 53(8), 5492-5499.
[http://dx.doi.org/10.1007/s12035-015-9461-2] [PMID: 26454822]
[72]
Gajewska, E. Sobieska, M.; Łojko, D.; Wieczorowska-Tobis, K.; Suwalska, A. Obesity itself does not influence BDNF serum levels in adults. Eur. Rev. Med. Pharmacol. Sci., 2014, 18(21), 3246-3250.
[PMID: 25487935]
[73]
Boyuk, B.; Degirmencioglu, S.; Atalay, H.; Guzel, S.; Acar, A.; Celebi, A.; Ekizoglu, I.; Simsek, C. Relationship between levels of brain-derived neurotrophic factor and metabolic parameters in patients with type 2 diabetes mellitus. J. Diabetes Res., 2014, 2014, 978143.
[http://dx.doi.org/10.1155/2014/978143] [PMID: 25587547]
[74]
Suwa, M.; Kishimoto, H.; Nofuji, Y.; Nakano, H.; Sasaki, H.; Radak, Z.; Kumagai, S. Serum brain-derived neurotrophic factor level is increased and associated with obesity in newly diagnosed female patients with type 2 diabetes mellitus. Metabolism, 2006, 55(7), 852-857.
[http://dx.doi.org/10.1016/j.metabol.2006.02.012] [PMID: 16784955]
[75]
Sandrini, L.; Di Minno, A.; Amadio, P.; Ieraci, A.; Tremoli, E.; Barbieri, S.S. Association between obesity and circulating brain-derived neurotrophic factor (BDNF) levels: Systematic review of literature and meta-analysis. Int. J. Mol. Sci., 2018, 19(8), 2281.
[http://dx.doi.org/10.3390/ijms19082281] [PMID: 30081509]
[76]
Davarpanah, M.; Shokri-Mashhadi, N.; Ziaei, R.; Saneei, P. A systematic review and meta-analysis of association between brain-derived neurotrophic factor and type 2 diabetes and glycemic profile. Sci. Rep., 2021, 11(1), 13773.
[http://dx.doi.org/10.1038/s41598-021-93271-z] [PMID: 34215825]
[77]
Rozanska, O.; Uruska, A.; Zozulinska-Ziolkiewicz, D. Brain-derived neurotrophic factor and diabetes. Int. J. Mol. Sci., 2020, 21(3), 841.
[http://dx.doi.org/10.3390/ijms21030841] [PMID: 32012942]
[78]
Fujinami, A.; Ohta, K.; Obayashi, H.; Fukui, M.; Hasegawa, G.; Nakamura, N.; Kozai, H.; Imai, S.; Ohta, M. Serum brain-derived neu-rotrophic factor in patients with type 2 diabetes mellitus: Relationship to glucose metabolism and biomarkers of insulin resistance. Clin. Biochem., 2008, 41(10-11), 812-817.
[http://dx.doi.org/10.1016/j.clinbiochem.2008.03.003] [PMID: 18402781]
[79]
Huang, T.; Larsen, K.T.; Ried-Larsen, M.; Møller, N.C.; Andersen, L.B. The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: A review. Scand. J. Med. Sci. Sports, 2014, 24(1), 1-10.
[http://dx.doi.org/10.1111/sms.12069] [PMID: 23600729]
[80]
Dinoff, A.; Herrmann, N.; Swardfager, W.; Lanctôt, K.L. The effect of acute exercise on blood concentrations of brain-derived neu-rotrophic factor in healthy adults: A meta-analysis. Eur. J. Neurosci., 2017, 46(1), 1635-1646.
[http://dx.doi.org/10.1111/ejn.13603] [PMID: 28493624]
[81]
Dinoff, A.; Herrmann, N.; Swardfager, W.; Liu, C.S.; Sherman, C.; Chan, S.; Lanctôt, K.L. The effect of exercise training on resting con-centrations of peripheral brain-derived neurotrophic factor (BDNF): A meta-analysis. PLoS One, 2016, 11(9), e0163037.
[http://dx.doi.org/10.1371/journal.pone.0163037] [PMID: 27658238]
[82]
Rasmussen, P.; Brassard, P.; Adser, H.; Pedersen, M.V.; Leick, L.; Hart, E.; Secher, N.H.; Pedersen, B.K.; Pilegaard, H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol., 2009, 94(10), 1062-1069.
[http://dx.doi.org/10.1113/expphysiol.2009.048512] [PMID: 19666694]
[83]
Gómez-Pinilla, F.; Ying, Z.; Opazo, P.; Roy, R.R.; Edgerton, V.R. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur. J. Neurosci., 2001, 13(6), 1078-1084.
[http://dx.doi.org/10.1046/j.0953-816x.2001.01484.x] [PMID: 11285004]
[84]
Pedersen, B.K.; Pedersen, M.; Krabbe, K.S.; Bruunsgaard, H.; Matthews, V.B.; Febbraio, M.A. Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals. Exp. Physiol., 2009, 94(12), 1153-1160.
[http://dx.doi.org/10.1113/expphysiol.2009.048561] [PMID: 19748969]
[85]
Cefis, M.; Chaney, R.; Quirié, A.; Santini, C.; Marie, C.; Garnier, P.; Prigent-Tessier, A. Endothelial cells are an important source of BDNF in rat skeletal muscle. Sci. Rep., 2022, 12(1), 311.
[http://dx.doi.org/10.1038/s41598-021-03740-8] [PMID: 35013359]
[86]
Ha, M.; Kim, V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol., 2014, 15(8), 509-524.
[http://dx.doi.org/10.1038/nrm3838] [PMID: 25027649]
[87]
O’Brien, J.; Hayder, H.; Zayed, Y.; Peng, C. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. (Lausanne), 2018, 9, 402.
[http://dx.doi.org/10.3389/fendo.2018.00402] [PMID: 30123182]
[88]
Liang, Y.; Ridzon, D.; Wong, L.; Chen, C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics, 2007, 8, 166.
[http://dx.doi.org/10.1186/1471-2164-8-166] [PMID: 17565689]
[89]
Zhang, X.; Zuo, X.; Yang, B.; Li, Z.; Xue, Y.; Zhou, Y.; Huang, J.; Zhao, X.; Zhou, J.; Yan, Y.; Zhang, H.; Guo, P.; Sun, H.; Guo, L.; Zhang, Y.; Fu, X.D. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell, 2014, 158(3), 607-619.
[http://dx.doi.org/10.1016/j.cell.2014.05.047] [PMID: 25083871]
[90]
Rodrigues, A.C.; Spagnol, A.R.; Frias, F.T.; de Mendonça, M.; Araújo, H.N.; Guimarães, D.; Silva, W.J.; Bolin, A.P.; Murata, G.M.; Silvei-ra, L. Intramuscular injection of miR-1 reduces insulin resistance in obese mice. Front. Physiol., 2021, 12, 676265.
[http://dx.doi.org/10.3389/fphys.2021.676265] [PMID: 34295259]
[91]
Kahn, B.B.; Alquier, T.; Carling, D.; Hardie, D.G. AMP-activated protein kinase: Ancient energy gauge provides clues to modern under-standing of metabolism. Cell Metab., 2005, 1(1), 15-25.
[http://dx.doi.org/10.1016/j.cmet.2004.12.003] [PMID: 16054041]
[92]
Mihaylova, M.M.; Shaw, R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol., 2011, 13(9), 1016-1023.
[http://dx.doi.org/10.1038/ncb2329] [PMID: 21892142]
[93]
Frias, Fde. T.; de Mendonça, M.; Martins, A.R.; Gindro, A.F.; Cogliati, B.; Curi, R.; Rodrigues, A.C. MyomiRs as markers of insulin re-sistance and decreased myogenesis in skeletal muscle of diet-induced obese mice. Front. Endocrinol. (Lausanne), 2016, 7, 76.
[http://dx.doi.org/10.3389/fendo.2016.00076] [PMID: 27445979]
[94]
Feng, B.; Cao, Y.; Chen, S.; Ruiz, M.; Chakrabarti, S. Reprint of: MiRNA-1 regulates endothelin-1 in diabetes. Life Sci., 2014, 118(2), 275-280.
[http://dx.doi.org/10.1016/j.lfs.2014.10.001] [PMID: 25307117]
[95]
Ringholm, S.; Biensø, R.S.; Kiilerich, K.; Guadalupe-Grau, A.; Aachmann-Andersen, N.J.; Saltin, B.; Plomgaard, P.; Lundby, C.; Wojtaszewski, J.F.; Calbet, J.A.; Pilegaard, H. Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab., 2011, 301(4), E649-E658.
[http://dx.doi.org/10.1152/ajpendo.00230.2011] [PMID: 21750272]
[96]
Russell, A.P.; Lamon, S.; Boon, H.; Wada, S.; Güller, I.; Brown, E.L.; Chibalin, A.V.; Zierath, J.R.; Snow, R.J.; Stepto, N.; Wadley, G.D.; Akimoto, T. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J. Physiol., 2013, 591(18), 4637-4653.
[http://dx.doi.org/10.1113/jphysiol.2013.255695] [PMID: 23798494]
[97]
Nielsen, S.; Scheele, C.; Yfanti, C.; Akerström, T.; Nielsen, A.R.; Pedersen, B.K.; Laye, M.J. Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J. Physiol., 2010, 588(Pt 20), 4029-4037.
[http://dx.doi.org/10.1113/jphysiol.2010.189860] [PMID: 20724368]
[98]
Mueller, M.; Breil, F.A.; Lurman, G.; Klossner, S.; Flück, M.; Billeter, R.; Däpp, C.; Hoppeler, H. Different molecular and structural adap-tations with eccentric and conventional strength training in elderly men and women. Gerontology, 2011, 57(6), 528-538.
[http://dx.doi.org/10.1159/000323267] [PMID: 21311168]
[99]
Drummond, M.J.; McCarthy, J.J.; Fry, C.S.; Esser, K.A.; Rasmussen, B.B. Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am. J. Physiol. Endocrinol. Metab., 2008, 295(6), E1333-E1340.
[http://dx.doi.org/10.1152/ajpendo.90562.2008] [PMID: 18827171]
[100]
Stanford, K.I.; Lynes, M.D.; Takahashi, H.; Baer, L.A.; Arts, P.J.; May, F.J.; Lehnig, A.C.; Middelbeek, R.J.W.; Richard, J.J.; So, K.; Chen, E.Y.; Gao, F.; Narain, N.R.; Distefano, G.; Shettigar, V.K.; Hirshman, M.F.; Ziolo, M.T.; Kiebish, M.A.; Tseng, Y.H.; Coen, P.M.; Good-year, L.J. 12,13-dihome: An exercise-induced lipokine that increases skeletal muscle fatty acid uptake. Cell Metab., 2018, 27(5), 1111-1120.e3.
[http://dx.doi.org/10.1016/j.cmet.2018.03.020] [PMID: 29719226]
[101]
Pinckard, K.M.; Shettigar, V.K.; Wright, K.R.; Abay, E.; Baer, L.A.; Vidal, P.; Dewal, R.S.; Das, D.; Duarte-Sanmiguel, S.; Hernández-Saavedra, D.; Arts, P.J.; Lehnig, A.C.; Bussberg, V.; Narain, N.R.; Kiebish, M.A.; Yi, F.; Sparks, L.M.; Goodpaster, B.H.; Smith, S.R.; Prat-ley, R.E.; Lewandowski, E.D.; Raman, S.V.; Wold, L.E.; Gallego-Perez, D.; Coen, P.M.; Ziolo, M.T.; Stanford, K.I. A novel endocrine role for the bat-released lipokine 12,13-dihome to mediate cardiac function. Circulation, 2021, 143(2), 145-159.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.049813] [PMID: 33106031]
[102]
Lynes, M.D.; Leiria, L.O.; Lundh, M.; Bartelt, A.; Shamsi, F.; Huang, T.L.; Takahashi, H.; Hirshman, M.F.; Schlein, C.; Lee, A.; Baer, L.A.; May, F.J.; Gao, F.; Narain, N.R.; Chen, E.Y.; Kiebish, M.A.; Cypess, A.M.; Blüher, M.; Goodyear, L.J.; Hotamisligil, G.S.; Stanford, K.I.; Tseng, Y.H. The cold-induced lipokine 12,13-diHOME promotes fatty acid transport into brown adipose tissue. Nat. Med., 2017, 23(5), 631-637.
[http://dx.doi.org/10.1038/nm.4297] [PMID: 28346411]
[103]
Vasan, S.K.; Noordam, R.; Gowri, M.S.; Neville, M.J.; Karpe, F.; Christodoulides, C. The proposed systemic thermogenic metabolites succinate and 12,13-diHOME are inversely associated with adiposity and related metabolic traits: Evidence from a large human cross-sectional study. Diabetologia, 2019, 62(11), 2079-2087.
[http://dx.doi.org/10.1007/s00125-019-4947-5] [PMID: 31309263]
[104]
Schuchardt, J.P.; Schmidt, S.; Kressel, G.; Dong, H.; Willenberg, I.; Hammock, B.D.; Hahn, A.; Schebb, N.H. Comparison of free serum oxylipin concentrations in hyper- vs. normolipidemic men. Prostaglandins Leukot. Essent. Fatty Acids, 2013, 89(1), 19-29.
[http://dx.doi.org/10.1016/j.plefa.2013.04.001] [PMID: 23694766]
[105]
Wang, W.; Yang, J.; Qi, W.; Yang, H.; Wang, C.; Tan, B.; Hammock, B.D.; Park, Y.; Kim, D.; Zhang, G. Lipidomic profiling of high-fat diet-induced obesity in mice: Importance of cytochrome P450-derived fatty acid epoxides. Obesity (Silver Spring), 2017, 25(1), 132-140.
[http://dx.doi.org/10.1002/oby.21692] [PMID: 27891824]
[106]
Peres Valgas da Silva, C.; Hernández-Saavedra, D.; White, J.D.; Stanford, K.I. Cold and exercise: Therapeutic tools to activate brown adi-pose tissue and combat obesity. Biology (Basel), 2019, 8(1), 9.
[http://dx.doi.org/10.3390/biology8010009] [PMID: 30759802]
[107]
Nieman, D.C.; Shanely, R.A.; Luo, B.; Meaney, M.P.; Dew, D.A.; Pappan, K.L. Metabolomics approach to assessing plasma 13- and 9-hydroxy-octadecadienoic acid and linoleic acid metabolite responses to 75-km cycling. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2014, 307(1), R68-R74.
[http://dx.doi.org/10.1152/ajpregu.00092.2014] [PMID: 24760997]
[108]
Nayor, M.; Shah, R.V.; Miller, P.E.; Blodgett, J.B.; Tanguay, M.; Pico, A.R.; Murthy, V.L.; Malhotra, R.; Houstis, N.E.; Deik, A.; Pierce, K.A.; Bullock, K.; Dailey, L.; Velagaleti, R.S.; Moore, S.A.; Ho, J.E.; Baggish, A.L.; Clish, C.B.; Larson, M.G.; Vasan, R.S.; Lewis, G.D. Metabolic architecture of acute exercise response in middle-aged adults in the community. Circulation, 2020, 142(20), 1905-1924.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.050281] [PMID: 32927962]
[109]
Görgens, S.W.; Eckardt, K.; Jensen, J.; Drevon, C.A.; Eckel, J. Exercise and regulation of adipokine and myokine production. Prog. Mol. Biol. Transl. Sci., 2015, 135, 313-336.
[http://dx.doi.org/10.1016/bs.pmbts.2015.07.002] [PMID: 26477920]
[110]
Boström, P.; Wu, J.; Jedrychowski, M.P.; Korde, A.; Ye, L.; Lo, J.C.; Rasbach, K.A.; Boström, E.A.; Choi, J.H.; Long, J.Z.; Kajimura, S.; Zingaretti, M.C.; Vind, B.F.; Tu, H.; Cinti, S.; Højlund, K.; Gygi, S.P.; Spiegelman, B.M.A.A. PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature, 2012, 481(7382), 463-468.
[http://dx.doi.org/10.1038/nature10777] [PMID: 22237023]
[111]
Hofmann, T.; Elbelt, U.; Stengel, A. Irisin as a muscle-derived hormone stimulating thermogenesis--a critical update. Peptides, 2014, 54, 89-100.
[http://dx.doi.org/10.1016/j.peptides.2014.01.016] [PMID: 24472856]
[112]
Huh, J.Y.; Panagiotou, G.; Mougios, V.; Brinkoetter, M.; Vamvini, M.T.; Schneider, B.E.; Mantzoros, C.S. FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism, 2012, 61(12), 1725-1738.
[http://dx.doi.org/10.1016/j.metabol.2012.09.002] [PMID: 23018146]
[113]
Perakakis, N.; Triantafyllou, G.A.; Fernández-Real, J.M.; Huh, J.Y.; Park, K.H.; Seufert, J.; Mantzoros, C.S. Physiology and role of irisin in glucose homeostasis. Nat. Rev. Endocrinol., 2017, 13(6), 324-337.
[http://dx.doi.org/10.1038/nrendo.2016.221] [PMID: 28211512]
[114]
Roca-Rivada, A.; Castelao, C.; Senin, L.L.; Landrove, M.O.; Baltar, J.; Belén Crujeiras, A.; Seoane, L.M.; Casanueva, F.F.; Pardo, M. FNDC5/irisin is not only a myokine but also an adipokine. PLoS One, 2013, 8(4), e60563.
[http://dx.doi.org/10.1371/journal.pone.0060563] [PMID: 23593248]
[115]
Polyzos, S.A.; Mathew, H.; Mantzoros, C.S. Irisin: A true, circulating hormone. Metabolism, 2015, 64(12), 1611-1618.
[http://dx.doi.org/10.1016/j.metabol.2015.09.001] [PMID: 26422316]
[116]
Lee, P.; Linderman, J.D.; Smith, S.; Brychta, R.J.; Wang, J.; Idelson, C.; Perron, R.M.; Werner, C.D.; Phan, G.Q.; Kammula, U.S.; Kebe-bew, E.; Pacak, K.; Chen, K.Y.; Celi, F.S. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab., 2014, 19(2), 302-309.
[http://dx.doi.org/10.1016/j.cmet.2013.12.017] [PMID: 24506871]
[117]
Puigserver, P.; Wu, Z.; Park, C.W.; Graves, R.; Wright, M.; Spiegelman, B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 1998, 92(6), 829-839.
[http://dx.doi.org/10.1016/S0092-8674(00)81410-5] [PMID: 9529258]
[118]
Zhang, Y.; Li, R.; Meng, Y.; Li, S.; Donelan, W.; Zhao, Y.; Qi, L.; Zhang, M.; Wang, X.; Cui, T.; Yang, L.J.; Tang, D. Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes, 2014, 63(2), 514-525.
[http://dx.doi.org/10.2337/db13-1106] [PMID: 24150604]
[119]
Vaughan, R.A.; Gannon, N.P.; Barberena, M.A.; Garcia-Smith, R.; Bisoffi, M.; Mermier, C.M.; Conn, C.A.; Trujillo, K.A. Characterization of the metabolic effects of irisin on skeletal muscle in vitro. Diabetes Obes. Metab., 2014, 16(8), 711-718.
[http://dx.doi.org/10.1111/dom.12268] [PMID: 24476050]
[120]
Xiong, X.Q.; Chen, D.; Sun, H.J.; Ding, L.; Wang, J.J.; Chen, Q.; Li, Y.H.; Zhou, Y.B.; Han, Y.; Zhang, F.; Gao, X.Y.; Kang, Y.M.; Zhu, G.Q. FNDC5 overexpression and irisin ameliorate glucose/lipid metabolic derangements and enhance lipolysis in obesity. Biochim. Biophys. Acta, 2015, 1852(9), 1867-1875.
[http://dx.doi.org/10.1016/j.bbadis.2015.06.017] [PMID: 26111885]
[121]
de Oliveira, M.; Mathias, L.S.; Rodrigues, B.M.; Mariani, B.G.; Graceli, J.B.; De Sibio, M.T.; Castro Olimpio, R.M.; Fontes Moretto, F.C.; Deprá, I.C.; Nogueira, C.R. The roles of triiodothyronine and irisin in improving the lipid profile and directing the browning of human ad-ipose subcutaneous cells. Mol. Cell. Endocrinol., 2020, 506, 110744.
[http://dx.doi.org/10.1016/j.mce.2020.110744] [PMID: 32027943]
[122]
Chen, N.; Li, Q.; Liu, J.; Jia, S. Irisin, an exercise-induced myokine as a metabolic regulator: An updated narrative review. Diabetes Metab. Res. Rev., 2016, 32(1), 51-59.
[http://dx.doi.org/10.1002/dmrr.2660] [PMID: 25952527]
[123]
Moreno-Navarrete, J.M.; Ortega, F.; Serrano, M.; Guerra, E.; Pardo, G.; Tinahones, F.; Ricart, W.; Fernández-Real, J.M. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J. Clin. Endocrinol. Metab., 2013, 98(4), E769-E778.
[http://dx.doi.org/10.1210/jc.2012-2749] [PMID: 23436919]
[124]
Sengupta, P.; Dutta, S.; Karkada, I.R.; Akhigbe, R.E.; Chinni, S.V. Irisin, energy homeostasis and male reproduction. Front. Physiol., 2021, 12, 746049.
[http://dx.doi.org/10.3389/fphys.2021.746049] [PMID: 34621189]
[125]
Crujeiras, A.B.; Zulet, M.A.; Lopez-Legarrea, P.; de la Iglesia, R.; Pardo, M.; Carreira, M.C.; Martínez, J.A.; Casanueva, F.F. Association between circulating irisin levels and the promotion of insulin resistance during the weight maintenance period after a dietary weight-lowering program in obese patients. Metabolism, 2014, 63(4), 520-531.
[http://dx.doi.org/10.1016/j.metabol.2013.12.007] [PMID: 24439241]
[126]
Qiu, S.; Cai, X.; Yin, H.; Zügel, M.; Sun, Z.; Steinacker, J.M.; Schumann, U. Association between circulating irisin and insulin resistance in non-diabetic adults: A meta-analysis. Metabolism, 2016, 65(6), 825-834.
[http://dx.doi.org/10.1016/j.metabol.2016.02.006] [PMID: 27173461]
[127]
Aydin, S.; Aydin, S.; Kuloglu, T.; Yilmaz, M.; Kalayci, M.; Sahin, I.; Cicek, D. Alterations of irisin concentrations in saliva and serum of obese and normal-weight subjects, before and after 45 min of a Turkish bath or running. Peptides, 2013, 50, 13-18.
[http://dx.doi.org/10.1016/j.peptides.2013.09.011] [PMID: 24096106]
[128]
Choi, Y-K.; Kim, M-K.; Bae, K.H.; Seo, H-A.; Jeong, J-Y.; Lee, W-K.; Kim, J-G.; Lee, I-K.; Park, K-G. Serum irisin levels in new-onset type 2 diabetes. Diabetes Res. Clin. Pract., 2013, 100(1), 96-101.
[http://dx.doi.org/10.1016/j.diabres.2013.01.007] [PMID: 23369227]
[129]
Blüher, S.; Panagiotou, G.; Petroff, D.; Markert, J.; Wagner, A.; Klemm, T.; Filippaios, A.; Keller, A.; Mantzoros, C.S. Effects of a 1-year exercise and lifestyle intervention on irisin, adipokines, and inflammatory markers in obese children. Obesity (Silver Spring), 2014, 22(7), 1701-1708.
[http://dx.doi.org/10.1002/oby.20739] [PMID: 24644099]
[130]
Handschin, C.; Spiegelman, B.M. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature, 2008, 454(7203), 463-469.
[http://dx.doi.org/10.1038/nature07206] [PMID: 18650917]
[131]
Lira, V.A.; Benton, C.R.; Yan, Z.; Bonen, A. PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab., 2010, 299(2), E145-E161.
[http://dx.doi.org/10.1152/ajpendo.00755.2009] [PMID: 20371735]
[132]
Fox, J.; Rioux, B.V.; Goulet, E.D.B.; Johanssen, N.M.; Swift, D.L.; Bouchard, D.R.; Loewen, H.; Sénéchal, M. Effect of an acute exercise bout on immediate post-exercise irisin concentration in adults: A meta-analysis. Scand. J. Med. Sci. Sports, 2018, 28(1), 16-28.
[http://dx.doi.org/10.1111/sms.12904] [PMID: 28453881]
[133]
Qiu, S.; Cai, X.; Sun, Z.; Schumann, U.; Zügel, M.; Steinacker, J.M. Chronic exercise training and circulating irisin in adults: A meta-analysis. Sports Med., 2015, 45(11), 1577-1588.
[http://dx.doi.org/10.1007/s40279-014-0293-4] [PMID: 26392122]
[134]
Jandova, T.; Buendía-Romero, A.; Polanska, H.; Hola, V.; Rihova, M.; Vetrovsky, T.; Courel-Ibáñez, J.; Steffl, M. Long-term effect of exercise on irisin blood levels-systematic review and meta-analysis. Healthcare (Basel), 2021, 9(11), 1438.
[http://dx.doi.org/10.3390/healthcare9111438] [PMID: 34828485]
[135]
Murawska-Cialowicz, E.; Wojna, J.; Zuwala-Jagiello, J. Crossfit training changes brain-derived neurotrophic factor and irisin levels at rest, after wingate and progressive tests, and improves aerobic capacity and body composition of young physically active men and women. J. Physiol. Pharmacol., 2015, 66(6), 811-821.
[136]
Safarimosavi, S.; Mohebbi, H.; Rohani, H. High-intensity interval vs. continuous endurance training: Preventive effects on hormonal changes and physiological adaptations in prediabetes patients. J. Strength Cond. Res., 2021, 35(3), 731-738.
[http://dx.doi.org/10.1519/JSC.0000000000002709] [PMID: 29939900]
[137]
Tsuchiya, Y.; Ijichi, T.; Goto, K. Effect of sprint training on resting serum irisin concentration - Sprint training once daily vs. twice every other day. Metabolism, 2016, 65(4), 492-495.
[http://dx.doi.org/10.1016/j.metabol.2015.12.006] [PMID: 26975541]
[138]
Dundar, A.; Kocahan, S.; Sahin, L. Associations of apelin, leptin, irisin, ghrelin, insulin, glucose levels, and lipid parameters with physical activity during eight weeks of regular exercise training. Arch. Physiol. Biochem., 2021, 127(4), 291-295.
[http://dx.doi.org/10.1080/13813455.2019.1635622] [PMID: 31290696]
[139]
Löffler, D.; Müller, U.; Scheuermann, K.; Friebe, D.; Gesing, J.; Bielitz, J.; Erbs, S.; Landgraf, K.; Wagner, I.V.; Kiess, W.; Körner, A. Serum irisin levels are regulated by acute strenuous exercise. J. Clin. Endocrinol. Metab., 2015, 100(4), 1289-1299.
[http://dx.doi.org/10.1210/jc.2014-2932] [PMID: 25625801]
[140]
Huang, J.; Wang, S.; Xu, F.; Wang, D.; Yin, H.; Lai, Q.; Liao, J.; Hou, X.; Hu, M. Exercise training with dietary restriction enhances circu-lating irisin level associated with increasing endothelial progenitor cell number in obese adults: An intervention study. PeerJ, 2017, 5, e3669.
[http://dx.doi.org/10.7717/peerj.3669] [PMID: 28828264]
[141]
Norheim, F.; Langleite, T.M.; Hjorth, M.; Holen, T.; Kielland, A.; Stadheim, H.K.; Gulseth, H.L.; Birkeland, K.I.; Jensen, J.; Drevon, C.A. The effects of acute and chronic exercise on PGC-1α irisin and browning of subcutaneous adipose tissue in humans. FEBS J., 2014, 281(3), 739-749.
[http://dx.doi.org/10.1111/febs.12619] [PMID: 24237962]
[142]
Briken, S.; Rosenkranz, S.C.; Keminer, O.; Patra, S.; Ketels, G.; Heesen, C.; Hellweg, R.; Pless, O.; Schulz, K.H.; Gold, S.M. Effects of exercise on Irisin, BDNF and IL-6 serum levels in patients with progressive multiple sclerosis. J. Neuroimmunol., 2016, 299, 53-58.
[http://dx.doi.org/10.1016/j.jneuroim.2016.08.007] [PMID: 27725121]
[143]
Kim, H.J.; Lee, H.J.; So, B.; Son, J.S.; Yoon, D.; Song, W. Effect of aerobic training and resistance training on circulating irisin level and their association with change of body composition in overweight/obese adults: A pilot study. Physiol. Res., 2016, 65(2), 271-279.
[http://dx.doi.org/10.33549/physiolres.932997] [PMID: 26447516]
[144]
Tsuchiya, Y.; Ando, D.; Takamatsu, K.; Goto, K. Resistance exercise induces a greater irisin response than endurance exercise. Metabolism, 2015, 64(9), 1042-1050.
[http://dx.doi.org/10.1016/j.metabol.2015.05.010] [PMID: 26081427]
[145]
Zhao, J.; Su, Z.; Qu, C.; Dong, Y. Effects of 12 weeks resistance training on serum irisin in older male adults. Front. Physiol., 2017, 8, 171.
[http://dx.doi.org/10.3389/fphys.2017.00171] [PMID: 28382004]
[146]
Tsuchiya, Y.; Ando, D.; Goto, K.; Kiuchi, M.; Yamakita, M.; Koyama, K. High-intensity exercise causes greater irisin response compared with low-intensity exercise under similar energy consumption. Tohoku J. Exp. Med., 2014, 233(2), 135-140.
[http://dx.doi.org/10.1620/tjem.233.135] [PMID: 24910199]
[147]
Mirabeau, O.; Perlas, E.; Severini, C.; Audero, E.; Gascuel, O.; Possenti, R.; Birney, E.; Rosenthal, N.; Gross, C. Identification of novel peptide hormones in the human proteome by hidden Markov model screening. Genome Res., 2007, 17(3), 320-327.
[http://dx.doi.org/10.1101/gr.5755407] [PMID: 17284679]
[148]
Kim, D.K.; Yun, S.; Son, G.H.; Hwang, J.I.; Park, C.R.; Kim, J.I.; Kim, K.; Vaudry, H.; Seong, J.Y. Coevolution of the spex-in/galanin/kisspeptin family: Spexin activates galanin receptor type II and III. Endocrinology, 2014, 155(5), 1864-1873.
[http://dx.doi.org/10.1210/en.2013-2106] [PMID: 24517231]
[149]
Gu, L.; Ma, Y.; Gu, M.; Zhang, Y.; Yan, S.; Li, N.; Wang, Y.; Ding, X.; Yin, J.; Fan, N.; Peng, Y. Spexin peptide is expressed in human endocrine and epithelial tissues and reduced after glucose load in type 2 diabetes. Peptides, 2015, 71, 232-239.
[http://dx.doi.org/10.1016/j.peptides.2015.07.018] [PMID: 26211893]
[150]
Porzionato, A.; Rucinski, M.; Macchi, V.; Stecco, C.; Malendowicz, L.K.; De Caro, R. Spexin expression in normal rat tissues. J. Histochem. Cytochem., 2010, 58(9), 825-837.
[http://dx.doi.org/10.1369/jhc.2010.956300] [PMID: 20530460]
[151]
Wong, M.K.H.; He, M.; Sze, K.H.; Huang, T.; Ko, W.K.W.; Bian, Z.X.; Wong, A.O.L. Mouse spexin: (I) NMR solution structure, docking models for receptor binding, and histological expression at tissue level. Front. Endocrinol. (Lausanne), 2021, 12, 681646.
[http://dx.doi.org/10.3389/fendo.2021.681646] [PMID: 34276561]
[152]
Walewski, J.L.; Ge, F.; Lobdell, H.I.V.; Levin, N.; Schwartz, G.J.; Vasselli, J.R.; Pomp, A.; Dakin, G.; Berk, P.D. Spexin is a novel human peptide that reduces adipocyte uptake of long chain fatty acids and causes weight loss in rodents with diet-induced obesity. Obesity (Silver Spring), 2014, 22(7), 1643-1652.
[http://dx.doi.org/10.1002/oby.20725] [PMID: 24550067]
[153]
Gonzalez-Gil, A.M.; Elizondo-Montemayor, L. The role of exercise in the interplay between myokines, hepatokines, osteokines, adi-pokines, and modulation of inflammation for energy substrate redistribution and fat mass loss: A review. Nutrients, 2020, 12(6), 1899.
[http://dx.doi.org/10.3390/nu12061899] [PMID: 32604889]
[154]
Behrooz, M.; Vaghef-Mehrabany, E.; Maleki, V.; Pourmoradian, S.; Fathifar, Z.; Ostadrahimi, A. Spexin status in relation to obesity and its related comorbidities: A systematic review. J. Diabetes Metab. Disord., 2020, 19(2), 1943-1957.
[http://dx.doi.org/10.1007/s40200-020-00636-8] [PMID: 33520870]
[155]
Türkel, İ.; Memi, G.; Yazgan, B. Impact of spexin on metabolic diseases and inflammation: An updated minireview. Exp. Biol. Med. (Maywood), 2022, 247(7), 567-573.
[http://dx.doi.org/10.1177/15353702211072443] [PMID: 35068225]
[156]
Yu, M.; Wang, M.; Han, S.; Han, L.; Kan, Y.; Zhao, J.; Yu, X.; Yan, J.; Jin, Y.; Zhang, Z.; Shang, W.; Fang, P. Spexin ameliorates skeletal muscle insulin resistance through activation of GAL2 receptor. Eur. J. Pharmacol., 2022, 917, 174731.
[http://dx.doi.org/10.1016/j.ejphar.2021.174731] [PMID: 34973950]
[157]
Yazgan, B. Avcı F.; Memi, G.; Tastekin, E. Inflammatory response and matrix metalloproteinases in chronic kidney failure: Modulation by adropin and spexin. Exp. Biol. Med. (Maywood), 2021, 246(17), 1917-1927.
[http://dx.doi.org/10.1177/15353702211012417] [PMID: 34024143]
[158]
Mills, E.G.; Izzi-Engbeaya, C.; Abbara, A.; Comninos, A.N.; Dhillo, W.S. Functions of galanin, spexin and kisspeptin in metabolism, mood and behaviour. Nat. Rev. Endocrinol., 2021, 17(2), 97-113.
[http://dx.doi.org/10.1038/s41574-020-00438-1] [PMID: 33273729]
[159]
Ge, J.F.; Walewski, J.L.; Anglade, D.; Berk, P.D. Regulation of hepatocellular fatty acid uptake in mouse models of fatty liver disease with and without functional leptin signaling: Roles of nfkb and srebp-1c and the effects of spexin. Semin. Liver Dis., 2016, 36(4), 360-372.
[http://dx.doi.org/10.1055/s-0036-1597248] [PMID: 27997977]
[160]
Gu, L.; Ding, X.; Wang, Y.; Gu, M.; Zhang, J.; Yan, S.; Li, N.; Song, Z.; Yin, J.; Lu, L.; Peng, Y. Spexin alleviates insulin resistance and inhibits hepatic gluconeogenesis via the FoxO1/PGC-1α pathway in high-fat-diet-induced rats and insulin resistant cells. Int. J. Biol. Sci., 2019, 15(13), 2815-2829.
[http://dx.doi.org/10.7150/ijbs.31781] [PMID: 31853220]
[161]
Kolodziejski, P.A.; Leciejewska, N.; Chmurzynska, A.; Sassek, M.; Szczepankiewicz, A.; Szczepankiewicz, D.; Malek, E.; Strowski, M.Z.; Checinska-Maciejewska, Z.; Nowak, K.W.; Pruszynska-Oszmalek, E. 30-Day spexin treatment of mice with diet-induced obesity (DIO) and type 2 diabetes (T2DM) increases insulin sensitivity, improves liver functions and metabolic status. Mol. Cell. Endocrinol., 2021, 536, 111420.
[http://dx.doi.org/10.1016/j.mce.2021.111420] [PMID: 34384849]
[162]
El-Saka, M.H.; Abo El Gheit, R.E.; El Saadany, A.; Alghazaly, G.M.; Marea, K.E.; Madi, N.M. Effect of spexin on renal dysfunction in experimentally obese rats: Potential mitigating mechanisms via galanin receptor-2. Arch. Physiol. Biochem., 2021. [Online epub a head of print], 1-10.
[http://dx.doi.org/10.1080/13813455.2021.1887265] [PMID: 33632048]
[163]
Said, M.A.; Nafeh, N.Y.; Abdallah, H.A. Spexin alleviates hypertension, hyperuricaemia, dyslipidemia and insulin resistance in high fruc-tose diet induced metabolic syndrome in rats via enhancing PPAR-ɣ and AMPK and inhibiting IL-6 and TNF-. Arch. Physiol. Biochem., 2021, 1-6.
[http://dx.doi.org/10.1080/13813455.2021.1899242] [PMID: 33721543]
[164]
Kumar, S.; Hossain, J.; Nader, N.; Aguirre, R.; Sriram, S.; Balagopal, P.B. Decreased circulating levels of spexin in obese children. J. Clin. Endocrinol. Metab., 2016, 101(7), 2931-2936.
[http://dx.doi.org/10.1210/jc.2016-1177] [PMID: 27218269]
[165]
Behrooz, M.; Vaghef-Mehrabany, E.; Ostadrahimi, A. Different spexin level in obese vs normal weight children and its relationship with obesity related risk factors. Nutr. Metab. Cardiovasc. Dis., 2020, 30(4), 674-682.
[http://dx.doi.org/10.1016/j.numecd.2019.11.008] [PMID: 32139252]
[166]
Kołodziejski, P.A.; Pruszyńska-Oszmałek, E.; Korek, E.; Sassek, M.; Szczepankiewicz, D.; Kaczmarek, P.; Nogowski, L.; Maćkowiak, P.; Nowak, K.W.; Krauss, H.; Strowski, M.Z. Serum levels of spexin and kisspeptin negatively correlate with obesity and insulin resistance in women. Physiol. Res., 2018, 67(1), 45-56.
[http://dx.doi.org/10.33549/physiolres.933467] [PMID: 29137471]
[167]
Bitarafan, V.; Esteghamati, A.; Azam, K.; Yosaee, S.; Djafarian, K. Comparing serum concentration of spexin among patients with meta-bolic syndrome, healthy overweight/obese, and normal-weight individuals. Med. J. Islam. Repub. Iran, 2019, 33, 93.
[http://dx.doi.org/10.47176/mjiri.33.93] [PMID: 31696087]
[168]
Karaca, A.; Bakar-Ates, F.; Ersoz-Gulcelik, N. Decreased spexin levels in patients with type 1 and type 2 diabetes. Med. Princ. Pract., 2018, 27(6), 549-554.
[http://dx.doi.org/10.1159/000493482] [PMID: 30184546]
[169]
Guler, A. Demir, . Decreased levels of spexin are associated with hormonal and metabolic disturbance in subjects with polycystic ovary syndrome. J. Obstet. Gynaecol., 2021, 41(3), 408-413.
[http://dx.doi.org/10.1080/01443615.2020.1737660] [PMID: 32293212]
[170]
Zhang, L.; Li, G.; She, Y.; Zhang, Z. Low levels of spexin and adiponectin may predict insulin resistance in patients with non-alcoholic fatty liver. Pract. Lab. Med., 2021, 24, e00207.
[http://dx.doi.org/10.1016/j.plabm.2021.e00207] [PMID: 33665291]
[171]
Ceylan, H.I. Saygın, Ö.; Özel Türkcü, Ü. Assessment of acute aerobic exercise in the morning versus evening on asprosin, spexin, lipocalin-2, and insulin level in overweight/obese versus normal weight adult men. Chronobiol. Int., 2020, 37(8), 1252-1268.
[http://dx.doi.org/10.1080/07420528.2020.1792482] [PMID: 32741294]
[172]
Fathi, R. The effect of single session of interval aerobic exercise on serum spexin levels in active young men. J. Sport Physiol. Phys. Ac-tiv., 2016, 10, 37-46.
[173]
Mohammadi, A.; Bijeh, N.; Moazzami, M. Kazem Khodaei; Rahimi, N. Effect of exercise training on spexin level, appetite, lipid accu-mulation product, visceral adiposity index, and body composition in adults with type 2 diabetes. Biol. Res. Nurs., 2022, 24(2), 152-162.
[http://dx.doi.org/10.1177/10998004211050596] [PMID: 34719994]
[174]
Khadir, A.; Kavalakatt, S.; Madhu, D.; Devarajan, S.; Abubaker, J.; Al-Mulla, F.; Tiss, A. Spexin as an indicator of beneficial effects of exercise in human obesity and diabetes. Sci. Rep., 2020, 10(1), 10635.
[http://dx.doi.org/10.1038/s41598-020-67624-z] [PMID: 32606431]
[175]
Al-Daghri, N.M.; Wani, K.; Yakout, S.M.; Al-Hazmi, H.; Amer, O.E.; Hussain, S.D.; Sabico, S.; Ansari, M.G.A.; Al-Musharaf, S.; Alenad, A.M.; Alokail, M.S.; Clerici, M. Favorable changes in fasting glucose in a 6-month self-monitored lifestyle modification programme in-versely affects spexin levels in females with prediabetes. Sci. Rep., 2019, 9(1), 9454.
[http://dx.doi.org/10.1038/s41598-019-46006-0] [PMID: 31263247]
[176]
Baldelli, R.; Coudert, A.E.; Del Fattore, A. Editorial: Advances in the endocrine role of the skeleton. Front. Endocrinol. (Lausanne), 2020, 11, 591085.
[http://dx.doi.org/10.3389/fendo.2020.591085] [PMID: 33178138]
[177]
Diaz-Franco, M.C.; Franco-Diaz de Leon, R.; Villafan-Bernal, J.R. Osteocalcin GPRC6A: An update of its clinical and biological mul-ti organic interactions. (Review) Mol. Med. Rep., 2019, 19(1), 15-22.
[PMID: 30431093]
[178]
Price, P.A.; Otsuka, A.A.; Poser, J.W.; Kristaponis, J.; Raman, N. Characterization of a gamma-carboxyglutamic acid-containing protein from bone. Proc. Natl. Acad. Sci. USA, 1976, 73(5), 1447-1451.
[http://dx.doi.org/10.1073/pnas.73.5.1447] [PMID: 1064018]
[179]
Price, P.A.; Poser, J.W.; Raman, N. Primary structure of the gamma-carboxyglutamic acid-containing protein from bovine bone. Proc. Natl. Acad. Sci. USA, 1976, 73(10), 3374-3375.
[http://dx.doi.org/10.1073/pnas.73.10.3374] [PMID: 1068450]
[180]
Mizokami, A.; Kawakubo-Yasukochi, T.; Hirata, M. Osteocalcin and its endocrine functions. Biochem. Pharmacol., 2017, 132, 1-8.
[http://dx.doi.org/10.1016/j.bcp.2017.02.001] [PMID: 28189726]
[181]
Booth, S.L.; Centi, A.; Smith, S.R.; Gundberg, C. The role of osteocalcin in human glucose metabolism: Marker or mediator? Nat. Rev. Endocrinol., 2013, 9(1), 43-55.
[http://dx.doi.org/10.1038/nrendo.2012.201] [PMID: 23147574]
[182]
Ducy, P. The role of osteocalcin in the endocrine cross-talk between bone remodelling and energy metabolism. Diabetologia, 2011, 54(6), 1291-1297.
[http://dx.doi.org/10.1007/s00125-011-2155-z] [PMID: 21503740]
[183]
Moser, S.C.; van der Eerden, B.C.J. Osteocalcin-a versatile bone-derived hormone. Front. Endocrinol. (Lausanne), 2019, 9, 794.
[http://dx.doi.org/10.3389/fendo.2018.00794] [PMID: 30687236]
[184]
Ferron, M.; Lacombe, J. Regulation of energy metabolism by the skeleton: Osteocalcin and beyond. Arch. Biochem. Biophys., 2014, 561, 137-146.
[http://dx.doi.org/10.1016/j.abb.2014.05.022] [PMID: 24893146]
[185]
Lee, N.K.; Sowa, H.; Hinoi, E.; Ferron, M.; Ahn, J.D.; Confavreux, C.; Dacquin, R.; Mee, P.J.; McKee, M.D.; Jung, D.Y.; Zhang, Z.; Kim, J.K.; Mauvais-Jarvis, F.; Ducy, P.; Karsenty, G. Endocrine regulation of energy metabolism by the skeleton. Cell, 2007, 130(3), 456-469.
[http://dx.doi.org/10.1016/j.cell.2007.05.047] [PMID: 17693256]
[186]
Fulzele, K.; Riddle, R.C.; DiGirolamo, D.J.; Cao, X.; Wan, C.; Chen, D.; Faugere, M.C.; Aja, S.; Hussain, M.A.; Brüning, J.C.; Clemens, T.L. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell, 2010, 142(2), 309-319.
[http://dx.doi.org/10.1016/j.cell.2010.06.002] [PMID: 20655471]
[187]
Mohammad Rahimi, G.R.; Niyazi, A.; Alaee, S. The effect of exercise training on osteocalcin, adipocytokines, and insulin resistance: A systematic review and meta-analysis of randomized controlled trials. Osteoporos. Int., 2021, 32(2), 213-224.
[188]
Bador, K.M.; Wee, L.D.; Halim, S.A.; Fadi, M.F.; Santhiran, P.; Rosli, N.F.; Mustafa, N. Serum osteocalcin in subjects with metabolic syn-drome and central obesity. Diabetes Metab. Syndr., 2016, 10(1)(Suppl. 1), S42-S45.
[http://dx.doi.org/10.1016/j.dsx.2015.09.009] [PMID: 26482049]
[189]
Yeap, B.B.; Chubb, S.A.; Flicker, L.; McCaul, K.A.; Ebeling, P.R.; Beilby, J.P.; Norman, P.E. Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur. J. Endocrinol., 2010, 163(2), 265-272.
[http://dx.doi.org/10.1530/EJE-10-0414] [PMID: 20501596]
[190]
Otani, T.; Mizokami, A.; Kawakubo-Yasukochi, T.; Takeuchi, H.; Inai, T.; Hirata, M. The roles of osteocalcin in lipid metabolism in adi-pose tissue and liver. Adv. Biol. Regul., 2020, 78, 100752.
[http://dx.doi.org/10.1016/j.jbior.2020.100752] [PMID: 32992234]
[191]
Mera, P.; Laue, K.; Ferron, M.; Confavreux, C.; Wei, J.; Galán-Díez, M.; Lacampagne, A.; Mitchell, S.J.; Mattison, J.A.; Chen, Y.; Bacchet-ta, J.; Szulc, P.; Kitsis, R.N.; de Cabo, R.; Friedman, R.A.; Torsitano, C.; McGraw, T.E.; Puchowicz, M.; Kurland, I.; Karsenty, G. Oste-ocalcin signaling in myofibers is necessary and sufficient for optimum adaptation to exercise. Cell Metab., 2016, 23(6), 1078-1092.
[http://dx.doi.org/10.1016/j.cmet.2016.05.004] [PMID: 27304508]
[192]
Lin, C.F.; Huang, T.H.; Tu, K.C.; Lin, L.L.; Tu, Y.H.; Yang, R.S. Acute effects of plyometric jumping and intermittent running on serum bone markers in young males. Eur. J. Appl. Physiol., 2012, 112(4), 1475-1484.
[http://dx.doi.org/10.1007/s00421-011-2108-8] [PMID: 21837450]
[193]
Hiam, D.; Landen, S.; Jacques, M.; Voisin, S.; Alvarez-Romero, J.; Byrnes, E.; Chubb, P.; Levinger, I.; Eynon, N. Osteocalcin and its forms respond similarly to exercise in males and females. Bone, 2021, 144, 115818.
[http://dx.doi.org/10.1016/j.bone.2020.115818] [PMID: 33338665]
[194]
Hiam, D.; Voisin, S.; Yan, X.; Landen, S.; Jacques, M.; Papadimitriou, I.D.; Munson, F.; Byrnes, E.; Brennan-Speranza, T.C.; Levinger, I.; Eynon, N. The association between bone mineral density gene variants and osteocalcin at baseline, and in response to exercise: The gene smart study. Bone, 2019, 123, 23-27.
[http://dx.doi.org/10.1016/j.bone.2019.03.015] [PMID: 30878522]
[195]
Levinger, I.; Zebaze, R.; Jerums, G.; Hare, D.L.; Selig, S.; Seeman, E. The effect of acute exercise on undercarboxylated osteocalcin in obese men. Osteoporos. Int., 2011, 22(5), 1621-1626.
[196]
Jürimäe, J.; Vaiksaar, S.; Purge, P.; Jürimäe, T. Adiponectin and osteocalcin responses to rowing exercise, and the relationship to substrate oxidation in female rowers. Physiol. Int., 2016, 103(2), 220-230.
[PMID: 28639861]
[197]
Mohammad, R.G.R.; Bijeh, N.; Rashidlamir, A. Effects of exercise training on serum preptin, undercarboxylated osteocalcin and high mo-lecular weight adiponectin in adults with metabolic syndrome. Exp. Physiol., 2020, 105(3), 449-459.
[http://dx.doi.org/10.1113/EP088036] [PMID: 31869474]
[198]
Levinger, I.; Jerums, G.; Stepto, N.K.; Parker, L.; Serpiello, F.R.; McConell, G.K.; Anderson, M.; Hare, D.L.; Byrnes, E.; Ebeling, P.R.; Seeman, E. The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men. J. Bone Miner. Res., 2014, 29(12), 2571-2576.
[http://dx.doi.org/10.1002/jbmr.2285] [PMID: 24861730]
[199]
Kurgan, N.; McKee, K.; Calleja, M.; Josse, A.R.; Klentrou, P. Cytokines, adipokines, and bone markers at rest and in response to plyome-tric exercise in obese vs normal weight adolescent females. Front. Endocrinol. (Lausanne), 2020, 11, 531926.
[http://dx.doi.org/10.3389/fendo.2020.531926] [PMID: 33362710]
[200]
Rochette, L.; Zeller, M.; Cottin, Y.; Vergely, C. Insights into mechanisms of gdf15 and receptor gfral: Therapeutic targets. Trends Endocrinol. Metab., 2020, 31(12), 939-951.
[http://dx.doi.org/10.1016/j.tem.2020.10.004] [PMID: 33172749]
[201]
Wischhusen, J.; Melero, I.; Fridman, W.H. Growth/differentiation factor-15 (gdf-15): From biomarker to novel targetable immune check-point. Front. Immunol., 2020, 11, 951.
[http://dx.doi.org/10.3389/fimmu.2020.00951] [PMID: 32508832]
[202]
Lee, S.E.; Kang, S.G.; Choi, M.J.; Jung, S.B.; Ryu, M.J.; Chung, H.K.; Chang, J.Y.; Kim, Y.K.; Lee, J.H.; Kim, K.S.; Kim, H.J.; Lee, H.K.; Yi, H.S.; Shong, M. Growth differentiation factor 15 mediates systemic glucose regulatory action of t-helper type 2 cytokines. Diabetes, 2017, 66(11), 2774-2788.
[http://dx.doi.org/10.2337/db17-0333] [PMID: 28874416]
[203]
Johnen, H.; Lin, S.; Kuffner, T.; Brown, D.A.; Tsai, V.W.; Bauskin, A.R.; Wu, L.; Pankhurst, G.; Jiang, L.; Junankar, S.; Hunter, M.; Fair-lie, W.D.; Lee, N.J.; Enriquez, R.F.; Baldock, P.A.; Corey, E.; Apple, F.S.; Murakami, M.M.; Lin, E.J.; Wang, C.; During, M.J.; Sainsbury, A.; Herzog, H.; Breit, S.N. Tumor-induced anorexia and weight loss are mediated by the TGF-beta superfamily cytokine MIC-1. Nat. Med., 2007, 13(11), 1333-1340.
[http://dx.doi.org/10.1038/nm1677] [PMID: 17982462]
[204]
Gerstein, H.C.; Pare, G.; Hess, S.; Ford, R.J.; Sjaarda, J.; Raman, K.; McQueen, M.; Lee, S.; Haenel, H.; Steinberg, G.R.; Investigators, O. Growth differentiation factor 15 as a novel biomarker for metformin. Diabetes Care, 2017, 40(2), 280-283.
[http://dx.doi.org/10.2337/dc16-1682] [PMID: 27974345]
[205]
Mullican, S.E.; Lin-Schmidt, X.; Chin, C.N.; Chavez, J.A.; Furman, J.L.; Armstrong, A.A.; Beck, S.C.; South, V.J.; Dinh, T.Q.; Cash-Mason, T.D.; Cavanaugh, C.R.; Nelson, S.; Huang, C.; Hunter, M.J.; Rangwala, S.M. GFRAL is the receptor for GDF15 and the ligand promotes weight loss in mice and nonhuman primates. Nat. Med., 2017, 23(10), 1150-1157.
[http://dx.doi.org/10.1038/nm.4392] [PMID: 28846097]
[206]
Yang, L.; Chang, C.C.; Sun, Z.; Madsen, D.; Zhu, H.; Padkjær, S.B.; Wu, X.; Huang, T.; Hultman, K.; Paulsen, S.J.; Wang, J.; Bugge, A.; Frantzen, J.B.; Nørgaard, P.; Jeppesen, J.F.; Yang, Z.; Secher, A.; Chen, H.; Li, X.; John, L.M.; Shan, B.; He, Z.; Gao, X.; Su, J.; Hansen, K.T.; Yang, W.; Jørgensen, S.B. GFRAL is the receptor for GDF15 and is required for the anti-obesity effects of the ligand. Nat. Med., 2017, 23(10), 1158-1166.
[http://dx.doi.org/10.1038/nm.4394] [PMID: 28846099]
[207]
Wollert, K.C.; Kempf, T.; Wallentin, L. Growth differentiation factor 15 as a biomarker in cardiovascular disease. Clin. Chem., 2017, 63(1), 140-151.
[http://dx.doi.org/10.1373/clinchem.2016.255174] [PMID: 28062617]
[208]
Chung, H.K.; Ryu, D.; Kim, K.S.; Chang, J.Y.; Kim, Y.K.; Yi, H.S.; Kang, S.G.; Choi, M.J.; Lee, S.E.; Jung, S.B.; Ryu, M.J.; Kim, S.J.; Kweon, G.R.; Kim, H.; Hwang, J.H.; Lee, C.H.; Lee, S.J.; Wall, C.E.; Downes, M.; Evans, R.M.; Auwerx, J.; Shong, M. Growth differentia-tion factor 15 is a myomitokine governing systemic energy homeostasis. J. Cell Biol., 2017, 216(1), 149-165.
[http://dx.doi.org/10.1083/jcb.201607110] [PMID: 27986797]
[209]
Strelau, J.; Strzelczyk, A.; Rusu, P.; Bendner, G.; Wiese, S.; Diella, F.; Altick, A.L.; von Bartheld, C.S.; Klein, R.; Sendtner, M.; Unsicker, K. Progressive postnatal motoneuron loss in mice lacking GDF-15. J. Neurosci., 2009, 29(43), 13640-13648.
[http://dx.doi.org/10.1523/JNEUROSCI.1133-09.2009] [PMID: 19864576]
[210]
Baek, S.J.; Okazaki, R.; Lee, S.H.; Martinez, J.; Kim, J.S.; Yamaguchi, K.; Mishina, Y.; Martin, D.W.; Shoieb, A.; McEntee, M.F.; Eling, T.E. Nonsteroidal anti-inflammatory drug-activated gene-1 over expression in transgenic mice suppresses intestinal neoplasia. Gastroenterology, 2006, 131(5), 1553-1560.
[http://dx.doi.org/10.1053/j.gastro.2006.09.015] [PMID: 17101328]
[211]
Macia, L.; Tsai, V.W.; Nguyen, A.D.; Johnen, H.; Kuffner, T.; Shi, Y.C.; Lin, S.; Herzog, H.; Brown, D.A.; Breit, S.N.; Sainsbury, A. Mac-rophage inhibitory cytokine 1 (MIC-1/GDF15) decreases food intake, body weight and improves glucose tolerance in mice on normal & obesogenic diets. PLoS One, 2012, 7(4), e34868.
[http://dx.doi.org/10.1371/journal.pone.0034868] [PMID: 22514681]
[212]
Min, K.W.; Liggett, J.L.; Silva, G.; Wu, W.W.; Wang, R.; Shen, R.F.; Eling, T.E.; Baek, S.J. NAG-1/GDF15 accumulates in the nucleus and modulates transcriptional regulation of the Smad pathway. Oncogene, 2016, 35(3), 377-388.
[http://dx.doi.org/10.1038/onc.2015.95] [PMID: 25893289]
[213]
Kleinert, M.; Clemmensen, C.; Sjøberg, K.A.; Carl, C.S.; Jeppesen, J.F.; Wojtaszewski, J.F.P.; Kiens, B.; Richter, E.A. Exercise increases circulating GDF15 in humans. Mol. Metab., 2018, 9, 187-191.
[http://dx.doi.org/10.1016/j.molmet.2017.12.016] [PMID: 29398617]
[214]
Campderrós, L.; Sánchez-Infantes, D.; Villarroya, J.; Nescolarde, L.; Bayès-Genis, A.; Cereijo, R.; Roca, E.; Villarroya, F. Altered GDF15 and FGF21 levels in response to strenuous exercise: A study in marathon runners. Front. Physiol., 2020, 11, 550102.
[http://dx.doi.org/10.3389/fphys.2020.550102] [PMID: 33329017]
[215]
Zhang, H.; Fealy, C.E.; Kirwan, J.P. Exercise training promotes a GDF15-associated reduction in fat mass in older adults with obesity. Am. J. Physiol. Endocrinol. Metab., 2019, 316(5), E829-E836.
[http://dx.doi.org/10.1152/ajpendo.00439.2018] [PMID: 30860878]
[216]
Fisher, F.M.; Maratos-Flier, E. Understanding the physiology of FGF21. Annu. Rev. Physiol., 2016, 78, 223-241.
[http://dx.doi.org/10.1146/annurev-physiol-021115-105339] [PMID: 26654352]
[217]
Liu, M.; Cao, H.; Hou, Y.; Sun, G.; Li, D.; Wang, W. Liver plays a major role in fgf-21 mediated glucose homeostasis. Cell. Physiol. Biochem., 2018, 45(4), 1423-1433.
[http://dx.doi.org/10.1159/000487568] [PMID: 29462809]
[218]
Minard, A.Y.; Tan, S.X.; Yang, P.; Fazakerley, D.J.; Domanova, W.; Parker, B.L.; Humphrey, S.J.; Jothi, R.; Stöckli, J.; James, D.E. mTORC1 is a major regulatory node in the fgf21 signaling network in adipocytes. Cell Rep., 2016, 17(1), 29-36.
[http://dx.doi.org/10.1016/j.celrep.2016.08.086] [PMID: 27681418]
[219]
Kliewer, S.A.; Mangelsdorf, D.J. A dozen years of discovery: Insights into the physiology and pharmacology of FGF21. Cell Metab., 2019, 29(2), 246-253.
[http://dx.doi.org/10.1016/j.cmet.2019.01.004] [PMID: 30726758]
[220]
Izumiya, Y.; Bina, H.A.; Ouchi, N.; Akasaki, Y.; Kharitonenkov, A.; Walsh, K. FGF21 is an Akt-regulated myokine. FEBS Lett., 2008, 582(27), 3805-3810.
[http://dx.doi.org/10.1016/j.febslet.2008.10.021] [PMID: 18948104]
[221]
Tezze, C.; Romanello, V.; Desbats, M.A.; Fadini, G.P.; Albiero, M.; Favaro, G.; Ciciliot, S.; Soriano, M.E.; Morbidoni, V.; Cerqua, C.; Loefler, S.; Kern, H.; Franceschi, C.; Salvioli, S.; Conte, M.; Blaauw, B.; Zampieri, S.; Salviati, L.; Scorrano, L.; Sandri, M. Age-associated loss of opa1 in muscle impacts muscle mass, metabolic homeostasis, systemic inflammation, and epithelial senescence. Cell Metab., 2017, 25(6), 1374-1389.e6.
[http://dx.doi.org/10.1016/j.cmet.2017.04.021] [PMID: 28552492]
[222]
Hojman, P.; Pedersen, M.; Nielsen, A.R.; Krogh-Madsen, R.; Yfanti, C.; Akerstrom, T.; Nielsen, S.; Pedersen, B.K. Fibroblast growth fac-tor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes, 2009, 58(12), 2797-2801.
[http://dx.doi.org/10.2337/db09-0713] [PMID: 19720803]
[223]
Xu, J.; Lloyd, D.J.; Hale, C.; Stanislaus, S.; Chen, M.; Sivits, G.; Vonderfecht, S.; Hecht, R.; Li, Y.S.; Lindberg, R.A.; Chen, J.L.; Jung, D.Y.; Zhang, Z.; Ko, H.J.; Kim, J.K.; Véniant, M.M. Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes, 2009, 58(1), 250-259.
[http://dx.doi.org/10.2337/db08-0392] [PMID: 18840786]
[224]
Xu, J.; Stanislaus, S.; Chinookoswong, N.; Lau, Y.Y.; Hager, T.; Patel, J.; Ge, H.; Weiszmann, J.; Lu, S.C.; Graham, M.; Busby, J.; Hecht, R.; Li, Y.S.; Li, Y.; Lindberg, R.; Véniant, M.M. Acute glucose-lowering and insulin-sensitizing action of FGF21 in insulin-resistant mouse models--association with liver and adipose tissue effects. Am. J. Physiol. Endocrinol. Metab., 2009, 297(5), E1105-E1114.
[http://dx.doi.org/10.1152/ajpendo.00348.2009] [PMID: 19706786]
[225]
Staiger, H.; Keuper, M.; Berti, L.; Hrabe de Angelis, M.; Häring, H.U. Fibroblast growth factor 21-metabolic role in mice and men. Endocr. Rev., 2017, 38(5), 468-488.
[http://dx.doi.org/10.1210/er.2017-00016] [PMID: 28938407]
[226]
Fujii, N.; Uta, S.; Kobayashi, M.; Sato, T.; Okita, N.; Higami, Y. Impact of aging and caloric restriction on fibroblast growth factor 21 sig-naling in rat white adipose tissue. Exp. Gerontol., 2019, 118, 55-64.
[http://dx.doi.org/10.1016/j.exger.2019.01.001] [PMID: 30620889]
[227]
Fazeli, P.K.; Lun, M.; Kim, S.M.; Bredella, M.A.; Wright, S.; Zhang, Y.; Lee, H.; Catana, C.; Klibanski, A.; Patwari, P.; Steinhauser, M.L. FGF21 and the late adaptive response to starvation in humans. J. Clin. Invest., 2015, 125(12), 4601-4611.
[http://dx.doi.org/10.1172/JCI83349] [PMID: 26529252]
[228]
Cuevas-Ramos, D.; Almeda-Valdés, P.; Meza-Arana, C.E.; Brito-Córdova, G.; Gómez-Pérez, F.J.; Mehta, R.; Oseguera-Moguel, J.; Aguilar-Salinas, C.A. Exercise increases serum fibroblast growth factor 21 (FGF21) levels. PLoS One, 2012, 7(5), e38022.
[http://dx.doi.org/10.1371/journal.pone.0038022] [PMID: 22701542]
[229]
Kim, K.H.; Kim, S.H.; Min, Y.K.; Yang, H.M.; Lee, J.B.; Lee, M.S. Acute exercise induces FGF21 expression in mice and in healthy hu-mans. PLoS One, 2013, 8(5), e63517.
[http://dx.doi.org/10.1371/journal.pone.0063517] [PMID: 23667629]
[230]
Tanimura, Y.; Aoi, W.; Takanami, Y.; Kawai, Y.; Mizushima, K.; Naito, Y.; Yoshikawa, T. Acute exercise increases fibroblast growth factor 21 in metabolic organs and circulation. Physiol. Rep., 2016, 4(12), e12828.
[http://dx.doi.org/10.14814/phy2.12828] [PMID: 27335433]

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