Exercise is mitochondrial medicine for muscle

Ashley N. Oliveira, David A. Hood

Sports Medicine and Health Science ›› 2019, Vol. 1 ›› Issue (1) : 11-18. DOI: 10.1016/j.smhs.2019.08.008
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Exercise is mitochondrial medicine for muscle

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Abstract

Mitochondria are vital organelles that provide energy for muscle function. When these organelles become dysfunctional, they produce less energy as well as excessive levels of reactive oxygen species which can trigger muscle atrophy, weakness and loss of endurance. In this review, molecular evidence is provided to show that exercise serves as a useful therapeutic countermeasure to overcome mitochondrial dysfunction, even when key regulators of organelle biogenesis are absent. These findings illustrate the complexity and compensatory nature of exercise-induced molecular signaling to transcription, as well as to post-transcriptional events within the mitochondrial synthesis and degradation (i.e. turnover) pathways. Beginning with the first bout of contractile activity, exercise exerts a medicinal effect to improve mitochondrial health and whole muscle function.

Keywords

Mitochondria / Muscle / Exercise / Health / Aging / Metabolism / Training

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Ashley N. Oliveira, David A. Hood. Exercise is mitochondrial medicine for muscle. Sports Medicine and Health Science, 2019, 1(1): 11‒18 https://doi.org/10.1016/j.smhs.2019.08.008

References

[[1]]
S.E. Calvo, K.R. Clauser, V.K. Mootha. MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins. Nucleic Acids Res, 44 (D1) ( 2016), pp. D1251-D1257, DOI: 10.1093/nar/gkv1003
[[2]]
P. Mitchell. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature, 191 ( 1961), pp. 144-148
[[3]]
G. Petrosillo, F.M. Ruggiero, G. Paradies. Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria. FASEB J, 17 (15) ( 2003), pp. 2202-2208, DOI: 10.1096/fj.03-0012com
[[4]]
M. Frank, S. Duvezin-Caubet, S. Koob, et al.. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta Mol Cell Res, 1823 (12) ( 2012), pp. 2297-2310, DOI: 10.1016/j.bbamcr.2012.08.007
[[5]]
P. Heusch, M. Canton, S. Aker, et al.. The contribution of reactive oxygen species and p 38 mitogen-activated protein kinase to myofilament oxidation and progression of heart failure in rabbits. Br J Pharmacol, 160 (6) ( 2010), pp. 1408-1416, DOI: 10.1111/j.1476-5381.2010.00793.x
[[6]]
E. Barbieri, P. Sestili.Reactive oxygen species in skeletal muscle signaling. J Signal Transduct, 2012 ( 2012), p. 982794, DOI: 10.1155/2012/982794
[[7]]
B.B. Lowell, B.M. Spiegelman. Towards a molecular understanding of adaptive thermogenesis. Nature, 404 (6778) ( 2000), pp. 652-660, DOI: 10.1038/35007527
[[8]]
S.P. Kirkwood, E.A. Munn, G.A. Brooks. Mitochondrial reticulum in limb skeletal muscle. Am J Physiol, 251 (3 Pt 1) ( 1986), pp. C395-C402
[[9]]
H. Hoppeler. Exercise-induced ultrastructural changes in skeletal muscle. Int J Sports Med, 07 (04) ( 1986), pp. 187-204, DOI: 10.1055/s-2008-1025758
[[10]]
D.A. Hood. Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol, 90 (3) ( 2001), pp. 1137-1157
[[11]]
A.M. Cogswell, R.J. Stevens, D.A. Hood. Properties of skeletal muscle mitochondria from subsarcolemmal and intermyofibrillar isolated regions. Am J Physiol, 264 (Pt 1) ( 1993), pp. C383-C389
[[12]]
M. Picard, K. White, D.M. Turnbull. Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study. J Appl Physiol ( 2013), DOI: 10.1152/japplphysiol.01096.2012
[[13]]
R. Ferreira, R. Vitorino, R.M.P. Alves, et al.. Subsarcolemmal and intermyofibrillar mitochondria proteome differences disclose functional specializations in skeletal muscle. Proteomics, 10 (17) ( 2010), pp. 3142-3154, DOI: 10.1002/pmic.201000173
[[14]]
A.E. Vincent, K. White, T. Davey, et al.. Quantitative 3D mapping of the human skeletal muscle mitochondrial network. Cell Rep, 26 (4) ( 2019), pp. 996-1009, DOI: 10.1038/nature22814.Trans-kingdom
[[15]]
M. Molnar, G. Kovacs. Mitochondrial diseases. Handb Clin Neurol, 145 ( 2017), pp. 147-155, DOI: 10.1016/B978-0-12-802395-2.00010-9
[[16]]
J.O. Holloszy. Biochemical adaptations in muscle. J Biol Chem, 242 (9) ( 1967), pp. 2278-2282
[[17]]
P.D. Gollnick, R.B. Armstrong, B. Saltin, C.W. Saubert, W.L. Sembrowich, R.E. Shepherd. Effect of training on enzyme activity and fiber composition of human skeletal muscle. J Appl Physiol, 34 (1) ( 1973), pp. 107-111
[[18]]
K.A. Burgomaster, K.R. Howarth, S.M. Phillips, et al.. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol, 5861 ( 2008), pp. 151-160, DOI: 10.1113/jphysiol.2007.142109
[[19]]
J.D. Bartlett, C. Hwa Joo, T.-S. Jeong, et al.. Matched work high-intensity interval and continuous running induce similar increases in PGC-1 mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle. J Appl Physiol, 112 (7) ( 2012), pp. 1135-1143, DOI: 10.1152/japplphysiol.01040.2011
[[20]]
M.J. MacInnis, M.J. Gibala. Physiological adaptations to interval training and the role of exercise intensity. J Physiol, 595 (9) ( 2017), pp. 2915-2930, DOI: 10.1113/JP273196
[[21]]
T. Groennebaek, K. Vissing.Impact of resistance training on skeletal muscle mitochondrial biogenesis, content, and function. Front Physiol, 15 (8) ( 2017), p. 713, DOI: 10.3389/fphys.2017.00713
[[22]]
J. MacDougall, D. Sale, J. Moroz, G. Elder, J. Sutton, H. Howald. Mitochondrial volume density in human skeletal muscle following heavy resistance training. Med Sci Sport, 11 (2) ( 1979), pp. 164-166
[[23]]
C. Porter, P.T. Reidy, N. Bhattarai, L.S. Sidossis, B.B. Rasmussen. Resistance exercise training alters mitochondrial function in human skeletal muscle. Hum Skelet Muscle Med Sci Sport Exerc, 47 (9) ( 2015), pp. 1922-1931, DOI: 10.1249/MSS.0000000000000605
[[24]]
V. Ljubicic, A.-M. Joseph, P.J. Adhihetty, et al.. Molecular basis for an attenuated mitochondrial adaptive plasticity in aged skeletal muscle. Aging (Albany NY), 1 (9) ( 2009), pp. 818-830
[[25]]
P. Puigserver, G. Adelmant, Z. Wu, et al.. Activation of PPARgamma coactivator-1 through transcription factor docking. Science, 286 (5443) ( 1999), pp. 1368-1371
[[26]]
J. Lin, C. Handschin, B.M. Spiegelman. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metabol, 1 (6) ( 2005), pp. 361-370, DOI: 10.1016/j.cmet.2005.05.004
[[27]]
M.B. Hock, A. Kralli. Transcriptional control of mitochondrial biogenesis and function. Annu Rev Physiol, 71 (1) ( 2009), pp. 177-203, DOI: 10.1146/annurev.physiol.010908.163119
[[28]]
D.A. Hood, J.M. Memme, A.N. Oliveira, M. Triolo. Maintenance of skeletal muscle mitochondria in health, exercise, and aging. Annu Rev Physiol, 81 (1) ( 2019), DOI: 10.1146/annurev-physiol-020518-114310. annurev-physiol-020518-114310
[[29]]
J.A. Calvo, T.G. Daniels, X. Wang, et al.. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J Appl Physiol, 104 (5) ( 2008), pp. 1304-1312, DOI: 10.1152/japplphysiol.01231.2007
[[30]]
J. Lin, H. Wu, P.T. Tarr, et al.. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature, 418 (6899) ( 2002), pp. 797-801, DOI: 10.1038/nature00904
[[31]]
P.J. Adhihetty, G. Uguccioni, L. Leick, J. Hidalgo, H. Pilegaard, D.A. Hood. The role of PGC-1 on mitochondrial function and apoptotic susceptibility in muscle. AJP Cell Physiol, 297 (1) ( 2009), pp. C217-C225, DOI: 10.1152/ajpcell.00070.2009
[[32]]
B. Chabi, V. Ljubicic, K.J. Menzies, J.H. Huang, A. Saleem, D a Hood. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell, 7 (1) ( 2008), pp. 2-12, DOI: 10.1111/j.1474-9726.2007.00347.x
[[33]]
H.N. Carter, M. Pauly, L.D. Tryon, D.A. Hood. Effect of contractile activity on PGC-1α transcription in young and aged skeletal muscle. J Appl Physiol, 124 (6) ( 2018), pp. 1605-1615, DOI: 10.1152/japplphysiol.01110.2017
[[34]]
H. Pilegaard, B. Saltin, P.D. Neufer. Exercise induces transient transcriptional activation of the PGC-1$α$ gene in human skeletal muscle. J Physiol, 546 (3) ( 2003), pp. 851-858, DOI: 10.1113/jphysiol.2002.034850
[[35]]
G.C. Rowe, R. El-Khoury, I.S. Patten, P. Rustin, Z. Arany. PGC-1 a is dispensable for exercise-induced mitochondrial biogenesis in skeletal muscle. PLoS One, 7 (7) ( 2012), Article e41817, DOI: 10.1371/journal.pone.0041817
[[36]]
L. Leick, J.F.P. Wojtaszewski, S.J. Johansen, et al.. PGC-1α is not mandatory for exercise-and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab, 294 (2) ( 2008), pp. 463-474
[[37]]
L. Leick, S.S. Lyngby, J.F. Wojtasewski, H. Pilegaard. PGC-1α is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp Gerontol, 45 (5) ( 2010), pp. 336-342, DOI: 10.1016/J.EXGER.2010.01.011
[[38]]
D.P. Lane. Cancer. p53, guardian of the genome. Nature, 358 (6381) ( 1992), pp. 15-16, DOI: 10.1038/358015a0
[[39]]
K. Beyfuss, D.A. Hood. A systematic review of p53 regulation of oxidative stress in skeletal muscle. Redox Rep, 23 (1) ( 2018), pp. 100-117, DOI: 10.1080/13510002.2017.1416773
[[40]]
A. Saleem, P.J. Adhihetty, D.A. Hood. Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol Genom, 3 ( 2009), pp. 58-66, DOI: 10.1152/physiolgenomics.90346.2008
[[41]]
V. Ljubicic, A.-M. Joseph, A. Saleem, et al.. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. Biochim Biophys Acta Gen Subj, 1800 (3) ( 2010), pp. 223-234, DOI: 10.1016/j.bbagen.2009.07.031
[[42]]
S. Matoba, J.-G. Kang, W.D. Patino, et al.. p 53 regulates mitochondrial metabolism. Science, 312 (5780) ( 2006), pp. 1650-1653. 80-
[[43]]
K. Beyfuss, A.T. Erlich, M. Triolo, D.A. Hood.The role of p 53 in determining mitochondrial adaptations to endurance training in skeletal muscle. Sci Rep, 8 (1) ( 2018), p. 14710, DOI: 10.1038/s41598-018-32887-0
[[44]]
J. Zhuang, W.M. Kamp, J. Li, et al.. Forkhead Box O3A (FOXO3) and the mitochondrial disulfide relay carrier (CHCHD4) regulate p53 protein nuclear activity in response to exercise. J Biol Chem, 291 (48) ( 2016), pp. 24819-24827, DOI: 10.1074/jbc.M116.745737
[[45]]
K. Heyne, S. Mannebach, E. Wuertz, K.X. Knaup, M. Mahyar-Roemer, K. Roemer. Identification of a putative p53 binding sequence within the human mitochondrial genome. FEBS Lett, 578 ( 2004), pp. 198-202, DOI: 10.1016/j.febslet.2004.10.099
[[46]]
J.-H. Park, J. Zhuang, J. Li, P.M. Hwang. p 53 as guardian of the mitochondrial genome. FEBS Lett, 590 (7) ( 2016), pp. 924-934, DOI: 10.1016/j.physbeh.2017.03.040
[[47]]
G. Achanta, R. Sasaki, L. Feng, et al.. Novel role of p 53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J, 24 (19) ( 2005), pp. 3482-3492, DOI: 10.1038/sj.emboj.7600819
[[48]]
A. Safdar, K. Khrapko, J.M. Flynn, et al.. Exercise-induced mitochondrial p 53 repairs mtDNA mutations in mutator mice. Skelet Muscle, 6 (7) ( 2016), DOI: 10.1186/s13395-016-0075-9
[[49]]
J.-Y. Park, P.-Y. Wang, T. Matsumoto, et al.. p 53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res, 105 (7) ( 2009), pp. 705-712, DOI: 10.1161/CIRCRESAHA.109.205310
[[50]]
A. Saleem, D.A. Hood. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53-Tfam-mitochondrial DNA complex in skeletal muscle. J Physiol, 591 (14) ( 2013), pp. 3625-3636
[[51]]
A. Saleem, S. Iqbal, Y. Zhang, D.A. Hood. Effect of p53 on mitochondrial morphology, import and assembly in skeletal muscle. Am J Physiol Cell Physiol, 308 ( 2015), pp. C319-C329, DOI: 10.1152/ajpcell.00253.2014
[[52]]
L. Mouchiroud, R.H. Houtkooper, N. Moullan, et al.. The NAD(+)/Sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell, 154 (2) ( 2013), pp. 430-441, DOI: 10.1016/j.cell.2013.06.016
[[53]]
K. Aquilano, P. Vigilanza, S. Baldelli, B. Pagliei, G. Rotilio, M.R. Ciriolo. Peroxisome proliferator-activated receptor γ co-activator 1 α (PGC-1α) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem, 285 (28) ( 2010), pp. 21590-21599, DOI: 10.1074/jbc.M109.070169
[[54]]
B.L. Tang. Sirt1 and the mitochondria. Mol Cells, 39 (2) ( 2016), pp. 87-95, DOI: 10.14348/molcells.2016.2318
[[55]]
H.S. Ghosh, M. McBurney, P.D. Robbins. SIRT 1 negatively regulates the mammalian target of rapamycin. PLoS One, 5 (2) ( 2010), pp. 1-8, DOI: 10.1371/journal.pone.0009199
[[56]]
F. Ng, B.L. Tang. Sirtuins' modulation of autophagy. J Cell Physiol, 228 (12) ( 2013), pp. 2262-2270
[[57]]
Nirmala Hariharan, Yasuhiro Maejima, Jun Nakae, Jihye Paik, Ronald A. DePinho J. S. Deacetylation of FoxO by Sirt 1 Plays an Essential Role in Mediating Starvation-Induced Autophagy in Cardiac Myocytes. 185 ( 2013), pp. 974-981, DOI: 10.1038/mp.2011.182. 2
[[58]]
K.J. Menzies, K. Singh, A. Saleem, D.A. Hood. Sirtuin 1-mediated effects of exercise and resveratrol on mitochondrial biogenesis. J Biol Chem, 288 (10) ( 2013), pp. 6968-6979
[[59]]
J. Dudek. Role of cardiolipin in mitochondrial signaling pathways. Front Cell Dev Biol, 5 (90) ( 2017), pp. 1-17, DOI: 10.3389/fcell.2017.00090
[[60]]
K.L. Wicks, D.A. Hood. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am J Physiol Cell Physiol, 260 (29) ( 1991), pp. C841-C850
[[61]]
O. Ostojic, M.F.N. O'Leary, K. Singh, K.J. Menzies, A. Vainshtein, D.A. Hood. The effects of chronic muscle use and disuse on cardiolipin metabolism. J Appl Physiol, 114 (4) ( 2013), pp. 444-452, DOI: 10.1152/japplphysiol.01312.2012
[[62]]
K. Singh, D.A. Hood. Effect of denervation-induced muscle disuse on mitochondrial protein import. Am J Cell Physiol, 300 ( 2011), pp. C138-C145
[[63]]
M. Takahashi, D.A. Hood. Chronic stimulation-induced changes in mitochondria and performance in rat skeletal muscle. J Appl Physiol, 74 (2) ( 1993), pp. 934-941
[[64]]
S. Backes, J.M. Herrmann.Protein translocation into the intermembrane space and matrix of mitochondria: mechanisms and driving forces. Front Mol Biosci, 4 ( 2017), p. 83, DOI: 10.3389/fmolb.2017.00083
[[65]]
N. Wiedemann, N. Pfanner. Mitochondrial machineries for protein import and assembly. Annu Rev Biochem, 86 (1) ( 2017), pp. 685-714, DOI: 10.1146/annurev-biochem-060815-014352
[[66]]
M. Takahashi, A. Chesley, D. Freyssenet, D.A. Hood. Contractile activity-induced adaptations in the mitochondrial protein import system. Am J Physiol, 274 (5 Pt 1) ( 1998), pp. C1380-C1387, DOI: 10.1152/ajpcell.1998.274.5.C1380
[[67]]
Y. Zhang, S. Iqbal, M.F.N. O'Leary, et al.. Altered mitochondrial morphology and defective protein import reveal novel roles for Bax and/or Bak in skeletal muscle. AJP Cell Physiol, 305 (5) ( 2013), pp. C502-C511, DOI: 10.1152/ajpcell.00058.2013
[[68]]
B. Glancy, L.M. Hartnell, C.A. Combs, et al.. Power grid protection of the muscle mitochondrial reticulum. Cell Rep ( 2017), DOI: 10.1016/j.celrep.2017.03.063
[[69]]
P. Mishra, D.C. Chan. Metabolic regulation of mitochondrial dynamics. J Cell Biol, 212 (4) ( 2016), pp. 379-387, DOI: 10.1083/jcb.201511036
[[70]]
D.C. Chan. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet, 46 (1) ( 2012), pp. 265-287, DOI: 10.1146/annurev-genet-110410-132529
[[71]]
O.C. Losón, Z. Song, H. Chen, D.C. Chan. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell, 24 (5) ( 2013), pp. 659-667, DOI: 10.1091/mbc.E12-10-0721
[[72]]
S. Iqbal, O. Ostojic, K. Singh, A.-M. Joseph, D.A. Hood. Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve, 48 (6) ( 2013), pp. 963-970, DOI: 10.1002/mus.23838
[[73]]
S. Pickles, P. Vigié, R.J. Youle.Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol, 28 (4) ( 2018), pp. R170-R185, DOI: 10.1016/J. CUB.2018.01.004
[[74]]
S.M. Jin, M. Lazarou, C. Wang, L.A. Kane, D.P. Narendra, R.J. Youle. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol, 191 (5) ( 2010), pp. 933-942, DOI: 10.1083/jcb.201008084
[[75]]
D.P. Narendra, S.M. Jin, A. Tanaka, et al.. PINK 1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol, 8 (1) ( 2010), DOI: 10.1371/journal.pbio.1000298
[[76]]
N. Mizushima, T. Yoshimori, Y. Ohsumi. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol, 27 (1) ( 2011), pp. 107-132, DOI: 10.1146/annurev-cellbio-092910-154005
[[77]]
A. Vainshtein, L.D. Tryon, M. Pauly, D.A. Hood. Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle. Am J Physiol Cell Physiol, 308 (9) ( 2015), pp. C710-C719, DOI: 10.1152/ajpcell.00380.2014
[[78]]
J.C. Drake, R.C. Laker, R.J. Wilson, M. Zhang, Z. Yan. Exercise-induced mitophagy in skeletal muscle occurs in the absence of stabilization of Pink1 on mitochondria. Cell Cycle, 18 (1) ( 2019), pp. 1-6, DOI: 10.1080/15384101.2018.1559556
[[79]]
C.C.W. Chen, A.T. Erlich, M.J. Crilly, D.A. Hood. Parkin is required for exercise-induced mitophagy in muscle: impact of aging. Am J Physiol Metab, 315 (3) ( 2018), pp. E404-E415, DOI: 10.1152/ajpendo.00391.2017
[[80]]
G. Mansueto, A. Armani, C. Viscomi, et al.. Transcription factor EB controls metabolic flexibility during exercise. Cell Metabol, 25 (1) ( 2017), pp. 182-196, DOI: 10.1016/j.cmet.2016.11.003
[[81]]
N. Pastore, A. Vainshtein, T.J. Klisch, et al.. TFE 3 regulates whole-body energy metabolism in cooperation with TFEB. EMBO Mol Med, 9 (5) ( 2017), pp. 605-621, DOI: 10.15252/emmm.201607204
[[82]]
A. Roczniak-Ferguson, C.S. Petit, F. Froehlich, et al.. The transcription factor TFEB links mTORC 1 signaling to transcriptional control of lysosome homeostasis. Sci Signal, 5 (228) ( 2012), p. ra42, DOI: 10.1126/scisignal.2002790
[[83]]
C. Settembre, R. Zoncu, D.L. Medina, et al.. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J, 31 (5) ( 2012), pp. 1095-1108, DOI: 10.1038/emboj.2012.32
[[84]]
G. Napolitano, A. Ballabio. TFEB at a glance. J Cell Sci, 129 ( 2016), pp. 2475-2481
[[85]]
D.L. Medina, S. Di Paola, I. Peluso, et al.. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol, 17 (3) ( 2015), pp. 288-299, DOI: 10.1038/ncb3114
[[86]]
Y. Guan, J.C. Drake, Z. Yan. Exercise-induced mitophagy in skeletal muscle and heart. Exerc Sport Sci Rev, 47 (3) ( 2019), pp. 151-156, DOI: 10.1249/JES.0000000000000192
[[87]]
Y. Kim, M. Triolo, A.T. Erlich, D.A. Hood. Regulation of autophagic and mitophagic flux during chronic contractile activity-induced muscle adaptations. Pflüg Arch - Eur J Physiol (October 2018), pp.1-10, DOI: 10.1007/s00424-018-2225-x
[[88]]
V. Ljubicic, D.A. Hood. Specific attenuation of protein kinase phosphorylation in muscle with a high mitochondrial content. Am J Physiol Metab, 297 (3) ( 2009), pp. E749-E758, DOI: 10.1152/ajpendo.00130.2009
[[89]]
Y. Kim, D.A. Hood. Regulation of the autophagy system during chronic contractile activity-induced muscle adaptations. Phys Rep, 5 (14) ( 2017), Article e13307, DOI: 10.14814/phy2.13307
[[90]]
S.E. Alway, J.S. Mohamed, M.J. Myers. Mitochondria initiate and regulate sarcopenia. Exerc Sport Sci Rev, 45 (2) ( 2017), pp. 58-69, DOI: 10.1249/JES.0000000000000101
[[91]]
R. Calvani, A.-M. Joseph, P.J. Adhihetty, et al.. Mitochondrial pathways in sarcopenia of aging and disuse muscle atrophy. Biol Chem, 394 (3) ( 2013), pp. 393-414, DOI: 10.1515/hsz-2012-0247
[[92]]
R.T. Hepple.Mitochondrial involvement and impact in aging skeletal muscle. Front Aging Neurosci, 6 ( 2014), p. 211, DOI: 10.3389/fnagi.2014.00211
[[93]]
V. Romanello, M. Sandri. Mitochondrial quality control and muscle mass maintenance. Front Physiol, 6 (422) ( 2016), pp. 1-21, DOI: 10.3389/fphys.2015.00422
[[94]]
H.N. Carter, C.C.W. Chen, D.A. Hood. Mitochondria, muscle health, and exercise with advancing age. Physiology, 30 (3) ( 2015), pp. 208-223, DOI: 10.1152/physiol.00039.2014
[[95]]
H.N. Carter, Y. Kim, A.T. Erlich, D. Zarrin-khat, D.A. Hood. Autophagy and mitophagy flux in young and aged skeletal muscle following chronic contractile activity. J Physiol (July 2018), DOI: 10.1113/JP275998
[[96]]
M.F. O'Leary, A. Vainshtein, S. Iqbal, O. Ostojic, D a Hood. Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle. Am J Physiol Cell Physiol, 304 (5) ( 2013), pp. C422-C430, DOI: 10.1152/ajpcell.00240.2012
[[97]]
V. Ljubicic, D.A. Hood. Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell, 8 (4) ( 2009), pp. 394-404, DOI: 10.1111/j.1474-9726.2009.00483.x
[[98]]
E. Koltai, N. Hart, A.W. Taylor, et al.. Age-associated declines in mitochondrial biogenesis and protein quality control factors are minimized by exercise training. Am J Physiol Integr Comp Physiol, 303 (2) ( 2012), pp. R127-R134, DOI: 10.1152/ajpregu.00337.2011

The work was funded by Natural Sciences and Engineering Research Council (NSERC) and Canadian Institutes of Health Research (CIHR) grants to D.A.H. A.N.O. is the recipient of an NSERC CGS-D. D.A.H. is the recipient of a Canada Research Chair in Cell Physiology.

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