Eight Weeks of High-Intensity Interval Static Strength Training Improves Skeletal Muscle Atrophy and Motor Function in Aged Rats via the PGC-1α/FNDC5/UCP1 Pathway

References

• Damluji AA, Forman DE, van Diepen S, et al. American heart association council on clinical cardiology and council on cardiovascular and stroke nursing older adults in the cardiac intensive care unit: factoring geriatric syndromes in the management, prognosis, and process of care: a scientific statement from the American heart association. Circulation. 2020;141(2):e6–e32. doi:10.1161/CIR.0000000000000741.31813278
   PubMed Web of Science ®Google Scholar
• Granic A, Mendonça N, Sayer AA, et al. Effects of dietary patterns and low protein intake on sarcopenia risk in the very old: the Newcastle 85+ Study. Clin Nutr. 2020;39(1):166–173. doi:10.1016/j.clnu.2019.01.009.30709690
   PubMed Web of Science ®Google Scholar
• Marzetti E, Calvani R, Tosato M, et al. SPRINTT consortium sarcopenia: an overview. Aging Clin Exp Res. 2017;29(1):11–17. doi:10.1007/s40520-016-0704-5.28155183
   PubMed Web of Science ®Google Scholar
• Merico A, Cavinato M, Gregorio C, et al. Effects of combined endurance and resistance training in amyotrophic lateral sclerosis: a Pilot, Randomized, Controlled Study. Eur J Transl Myol. 2018;28:7278. doi:10.4081/ejtm.2018.727829686818
   PubMed Web of Science ®Google Scholar
• De Luca CJ, Kline JC. Influence of proprioceptive feedback on the firing rate and recruitment of motoneurons. J Neural Eng. 2012;9(1):016007. doi:10.1088/1741-2560/9/1/016007.22183300
   PubMed Web of Science ®Google Scholar
• Fitts RH. Effects of regular exercise training on skeletal muscle contractile function. Am J Phys Med Rehabil. 2003;82(4):320–331. doi:10.1097/01.PHM.0000059336.40487.12649660
   PubMed Web of Science ®Google Scholar
• Hurst JE, Fitts RH. Hindlimb unloading-induced muscle atrophy and loss of function: protective effect of isometric exercise. J Appl Physiol. 2003;95(4):1405–1417. doi:10.1152/japplphysiol.00516.2002.12819219
   PubMed Web of Science ®Google Scholar
• Halling JF, Jessen H, Nøhr-Meldgaard J, et al. PGC-1α regulates mitochondrial properties beyond biogenesis with aging and exercise training. Am J Physiol Endocrinol Metab. 2019;317(3):E513–25. doi:10.1152/ajpendo.00059.2019.31265325
   PubMed Web of Science ®Google Scholar
• Ringholm S, Grunnet Knudsen J, Leick L, et al. PGC-1α is required for exercise- and exercise training-induced UCP1 up-regulation in mouse white adipose tissue. PLoS One. 2013;8(5):e641. doi:10.1371/journal.pone.0064123.
   Web of Science ®Google Scholar
• Yuan H, Niu Y, Liu X, Fu L. Exercise increases the binding of MEF2A to the Cpt1b promoter in mouse skeletal muscle. Acta Physiol (Oxf). 2014;212(4):283–292. doi:10.1111/apha.12395.25213552
   PubMed Web of Science ®Google Scholar
• Kazeminasab F, Marandi SM, Ghaedi K, et al. A comparative study on the effects of high-fat diet and endurance training on the PGC-1α-FNDC5/irisin pathway in obese and nonobese male C57BL/6 mice. Appl Physiol Nutr Metab. 2018;43(7):651–662. doi:10.1139/apnm-2017-0614.29365291
   PubMed Web of Science ®Google Scholar
• Guilford BL, Parson JC, Grote CW, Vick SN, Ryals JM, Wright DE. Increased FNDC5 is associated with insulin resistance in high fat-fed mice. Physiol Rep. 2017;5(13):e13319. doi:10.14814/phy2.13319.28676551
   PubMed Web of Science ®Google Scholar
• Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA. 1990;263(22):3029–3034. doi:10.1001/jama.1990.034402200530292342214
   PubMed Web of Science ®Google Scholar
• Howell ML, Kimoto R, Morford WR. Effect of isometric and isotonic exercise programs upon muscular endurance. Res Q. 2013;33(4):536–540. doi:10.1080/10671188.1962.10762104
   Web of Science ®Google Scholar
• Dillon LM, Rebelo AP, Moraes CT. The role of PGC-1 coactivators in aging skeletal muscle and heart. IUBMB Life. 2012;64(3):231–241. doi:10.1002/iub.608.22279035
   PubMed Web of Science ®Google Scholar
• Bahreinipour M-A, Joukar S, Hovanloo F. Mild aerobic training with blood flow restriction increases the hypertrophy index and musk in both slow and fast muscles of old rats: role of PGC-1α. Life Sci. 2018;202:103–109. doi:10.1016/j.lfs.2018.03.051.29604268
   PubMed Web of Science ®Google Scholar
• Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta. 2011;1813(7):1269–1278. doi:10.1016/j.bbamcr.2010.09.019.20933024
   PubMed Web of Science ®Google Scholar
• Hoeks J, Arany Z, Phelix E, Moonen-Kornips E, Hesselink MKC, Schrauwen P. Enhanced lipid—but not carbohydrate—supported mitochondrial respiration in skeletal muscle of PGC-1α overexpressing mice. J Cell Physiol. 2012;227(3):1026–1033. doi:10.1002/jcp.22812.21520076
   PubMed Web of Science ®Google Scholar
• Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006;3(5):333–341. doi:10.1016/j.cmet.2006.04.00216679291
   PubMed Web of Science ®Google Scholar
• Zhang Y, Shen L, Zhu H, et al. PGC-1α regulates autophagy to promote fibroblast activation and tissue fibrosis. Ann Rheum Dis. 2020;79(9):1227–1233. doi:10.1136/annrheumdis-2020-21696332482644
   PubMed Web of Science ®Google Scholar
• Brault JJ, Jespersen JG, Goldberg AL. Peroxisome proliferator-activated receptor-gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem. 2010;285(25):19460–19471. doi:10.1074/jbc.M110.113092.20404331
   PubMed Web of Science ®Google Scholar
• Hood DA, Tryon LD, Vainshtein A, et al. Exercise and the regulation of mitochondrial turnover. Prog Mol Biol Transl Sci. 2015;135:99–127. doi:10.1016/bs.pmbts.2015.07.007.26477912
   PubMed Web of Science ®Google Scholar
• Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopol-sky MA. Exercise increases mitochondrial PGC-1alpha con-tent and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem. 2011;286(12):10605–10617. doi:10.1074/jbc.M110.211466.21245132
   PubMed Web of Science ®Google Scholar
• Ropelle ER, Pauli JR, Cintra DE, et al. Acute exercise modulates the Foxo1/PGC-1alpha pathway in the liver of diet-induced obesity rats. J Physiol. 2009;587(9):2069–2076. doi:10.1113/jphysiol.2008.164202.19273580
   PubMed Web of Science ®Google Scholar
• Handschin C, Spiegelman BM. The role of exercise and PGC 1alpha in inflammation and chronic disease. Nature. 2008;454(7203):463–469. doi:10.3389/fnagi.2014.00027.18650917
   PubMed Web of Science ®Google Scholar
• Ghosh S, Lertwattanarak R, Lefort N, et al. Reduction in reactive oxygen species production by mitochondria from elderly subjects with normal and impaired glucose tolerance. Diabetes. 2011;60(8):2051–2060. doi:10.2337/db11-0121.21677280
   PubMed Web of Science ®Google Scholar
• Kang C, Chung E, Diffee G, Ji LL. Exercise training attenuates aging-associated mitochondrial dysfunction in rat skeletal muscle: role of PGC-1α. Exp Gerontol. 2013;48(11):1343–1350. doi:10.1016/j.exger.2013.08.004.23994518
   PubMed Web of Science ®Google Scholar
• Norheim F, Langleite TM, Hjorth M, et al. 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. doi:10.1111/febs.12619.24237962
   PubMed Web of Science ®Google Scholar
• Huh JY, Panagiotou G, Mougios V, et al. 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. doi:10.1016/j.metabol.2012.09.002.23018146
   PubMed Web of Science ®Google Scholar
• Gouveia MC, Vella JP, Cafeo FR, Affonso Fonseca FL, Bacci MR. Association between irisin and major chronic diseases: a review. Eur Rev Med Pharmacol Sci. 2016;20(19):4072–4077.27775791
   PubMed Web of Science ®Google Scholar
• Colaianni G, Cint S, Colucci S, Grano M. Irisin and musculoskeletal health. Ann N Y Acad Sci. 2017;1402(1):5–9. doi:10.1111/nyas.13345.28437576
   PubMed Web of Science ®Google Scholar
• Boström 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/nature10777.22237023
   PubMed Web of Science ®Google Scholar
• Pyrżak B, Demkow U, Kucharska AM. Brown adipose tissue and browning agents: irisin and FGF21 in the development of obesity in children and adolescents. Adv Exp Med Biol. 2015;866:25–34. doi:10.1007/5584_2015_149.26022904
   PubMed Web of Science ®Google Scholar
• Zadegan FG, Ghaedi K, Kalantar SM, et al. Cardiac differentiation of mouse embryonic stem cells is influenced by a PPAR γ/PGC-1α-FNDC5 pathway during the stage of cardiac precursor cell formation. Eur J Cell Biol. 2015;94(6):257–266. doi:10.1016/j.ejcb.2015.04.002.25936576
   PubMed Web of Science ®Google Scholar
• Roberts MD, Bayless DS, Company JM, et al. Elevated skeletal muscle irisin precursor FNDC5 mRNA in obese OLETF rats. Metabolism. 2013;62(8):1052–1056. doi:10.1016/j.metabol.2013.02.002.23498898
   PubMed Web of Science ®Google Scholar
• Schaalan MF, Ramadan BK, Abd Elwahab AH. Synergistic effect of carnosine on browning of adipose tissue in exercised obese rats; a focus on circulating irisin levels. J Cell Physiol. 2018;233(6):5044–5057. doi:10.1002/jcp.26370.29236301
   PubMed Web of Science ®Google Scholar
• Samy DM, Ismail CA, Nassar RA. Circulating irisin concentrations in rat models of thyroid dysfunction - effect of exercise. Metabolism. 2015;64(7):804–813. doi:10.1016/j.metabol.2015.01.001.25720940
   PubMed Web of Science ®Google Scholar
• Pang M, Yang J, Rao J, et al. Time-dependent changes in increased levels of plasma irisin and muscle PGC-1α and FNDC5 after exercise in mice. Tohoku J Exp Med. 2018;244(2):93–103. doi:10.1620/tjem.244.93.29415899
   PubMed Web of Science ®Google Scholar
• Pekkala S, Wiklund PK, Hulmi JJ, et al. Are skeletal muscle FNDC5 gene expression and irisin release regulated by exercise and related to health? J Physiol. 2013;591(21):5393–5400. doi:10.1113/jphysiol.2013.263707.24000180
   PubMed Web of Science ®Google Scholar
• Fox J, Rioux BV, Goulet EDB, et al. 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. doi:10.1111/sms.12904.28453881
   PubMed Web of Science ®Google Scholar
• Raschke S, Elsen M, Gassenhuber H, et al. Evidence against a beneficial effect of irisin in humans. PLoS One. 2013;8(9):e73680. doi:10.1371/journal.pone.007368024040023
   PubMed Web of Science ®Google Scholar