Int J Sports Med 2020; 41(06): 349-359
DOI: 10.1055/a-1121-7851
Review
© Georg Thieme Verlag KG Stuttgart · New York

Human Skeletal Muscle Mitochondrial Adaptations Following Resistance Exercise Training

Hailey A. Parry
1   School of Kinesiology, Auburn University, Auburn, United States
,
Michael D. Roberts
1   School of Kinesiology, Auburn University, Auburn, United States
,
Andreas N. Kavazis
1   School of Kinesiology, Auburn University, Auburn, United States
› Author Affiliations
Further Information

Publication History



accepted 31 January 2020

Publication Date:
11 March 2020 (online)

Abstract

It is universally accepted that resistance training promotes increases in muscle strength and hypertrophy in younger and older populations. Although less investigated, studies largely suggest resistance training results in lower skeletal muscle mitochondrial volume; a phenomenon which has been described as a “dilution of the mitochondrial volume” via resistance training. While this phenomenon is poorly understood, it is likely a result of muscle fiber hypertrophy outpacing mitochondrial biogenesis. Critically, there is no evidence to suggest resistance training promotes a net loss in mitochondria. Further, given the numerous reports suggesting resistance training does not decrease and may even increase VO2max in previously untrained individuals, it is plausible certain aspects of mitochondrial function may be enhanced with resistance training, and this area warrants further research consideration. Finally, there are emerging data suggesting resistance training may affect mitochondrial dynamics. The current review will provide an in-depth discussion of these topics and posit future research directions which can further our understanding of how resistance training may affect skeletal muscle mitochondrial physiology.

 
  • References

  • 1 van der Bliek AM, Sedensky MM, Morgan PG. Cell biology of the mitochondrion. Genetics 2017; 207: 843-871
  • 2 Ernster L, Schatz G. Mitochondria: A historical review. J Cell Biol 1981; 91: 227s-255s
  • 3 Holloszy JO. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 1967; 242: 2278-2282
  • 4 Di Donato DM, West DW, Churchward-Venne TA. et al. Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery. Am J Physiol Endocrinol Metab 2014; 306: E1025-E1032
  • 5 Konopka AR, Suer MK, Wolff CA. et al. Markers of human skeletal muscle mitochondrial biogenesis and quality control: Effects of age and aerobic exercise training. J Gerontol A Biol Sci Med Sci 2014; 69: 371-378
  • 6 Perry CG, Lally J, Holloway GP. et al. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol 2010; 588: 4795-4810
  • 7 Jacobs RA, Fluck D, Bonne TC. et al. Improvements in exercise performance with high-intensity interval training coincide with an increase in skeletal muscle mitochondrial content and function. J Appl Physiol (1985) 2013; 115: 785-793
  • 8 Islam H, Edgett BA, Gurd BJ. Coordination of mitochondrial biogenesis by PGC-1alpha in human skeletal muscle: A re-evaluation. Metabolism 2018; 79: 42-51
  • 9 Booth FW, Ruegsegger GN, Toedebusch RG. et al. Endurance exercise and the regulation of skeletal muscle metabolism. Prog Mol Biol Transl Sci 2015; 135: 129-151
  • 10 Lundby C, Jacobs RA. Adaptations of skeletal muscle mitochondria to exercise training. Exp Physiol 2016; 101: 17-22
  • 11 Perry CGR, Hawley JA. Molecular basis of exercise-induced skeletal muscle mitochondrial biogenesis: Historical advances, current knowledge, and future challenges. Cold Spring Harb Perspect Med. 2018 8. a029686
  • 12 Folland JP, Williams AG. The adaptations to strength training: Morphological and neurological contributions to increased strength. Sports Med 2007; 37: 145-168
  • 13 Fry AC. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 2004; 34: 663-679
  • 14 Sale DG. Neural adaptation to resistance training. Med Sci Sports Exerc 1988; 20: S135-S145
  • 15 Luthi JM, Howald H, Claassen H. et al. Structural changes in skeletal muscle tissue with heavy-resistance exercise. Int J Sports Med 1986; 7: 123-127
  • 16 Moritani T, deVries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 1979; 58: 115-130
  • 17 Grimby L, Hannerz J, Hedman B. The fatigue and voluntary discharge properties of single motor units in man. J Physiol 1981; 316: 545-554
  • 18 Campos GE, Luecke TJ, Wendeln HK. et al. Muscular adaptations in response to three different resistance-training regimens: Specificity of repetition maximum training zones. Eur J Appl Physiol 2002; 88: 50-60
  • 19 Schoenfeld BJ. The mechanisms of muscle hypertrophy and their application to resistance training. J Strength Cond Res 2010; 24: 2857-2872
  • 20 Roberts MD, Haun CT, Mobley CB. et al. Physiological differences between low versus high skeletal muscle hypertrophic responders to resistance exercise training: Current perspectives and future research directions. Front Physiol 2018; 9: 834
  • 21 Schiaffino S, Dyar KA, Ciciliot S. et al. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 2013; 280: 4294-4314
  • 22 Greene NP, Nilsson MI, Washington TA. et al. Impaired exercise-induced mitochondrial biogenesis in the obese Zucker rat, despite PGC-1alpha induction, is due to compromised mitochondrial translation elongation. Am J Physiol Endocrinol Metab 2014; 306: E503-E511
  • 23 Porter C, Reidy PT, Bhattarai N. et al. Resistance exercise training alters mitochondrial function in human skeletal muscle. Med Sci Sports Exerc 2015; 47: 1922-1931
  • 24 Fiatarone MA, Marks EC, Ryan ND. et al. High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 1990; 263: 3029-3034
  • 25 Tracy BL, Ivey FM, Hurlbut D. et al. Muscle quality. II. Effects of strength training in 65- to 75-yr-old men and women. J Appl Physiol (1985) 1999; 86: 195-201
  • 26 Trappe S, Williamson D, Godard M. et al. Effect of resistance training on single muscle fiber contractile function in older men. J Appl Physiol (1985) 2000; 89: 143-152
  • 27 Melov S, Tarnopolsky MA, Beckman K. et al. Resistance exercise reverses aging in human skeletal muscle. PLoS One 2007; 2: e465
  • 28 Parise G, Brose AN, Tarnopolsky MA. Resistance exercise training decreases oxidative damage to DNA and increases cytochrome oxidase activity in older adults. Exp Gerontol 2005; 40: 173-180
  • 29 Parise G, Phillips SM, Kaczor JJ. et al. Antioxidant enzyme activity is up-regulated after unilateral resistance exercise training in older adults. Free Radic Biol Med 2005; 39: 289-295
  • 30 Chilibeck PD, Syrotuik DG, Bell GJ. The effect of strength training on estimates of mitochondrial density and distribution throughout muscle fibres. Eur J Appl Physiol Occup Physiol 1999; 80: 604-609
  • 31 Green H, Goreham C, Ouyang J. et al. Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol 1999; 276: R591-R596
  • 32 Roberts MD, Romero MA, Mobley CB. et al. Skeletal muscle mitochondrial volume and myozenin-1 protein differences exist between high versus low anabolic responders to resistance training. PeerJ 2018; 6: e5338
  • 33 Salvadego D, Domenis R, Lazzer S. et al. Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J Appl Physiol (1985) 2013; 114: 1527-1535
  • 34 MacDougall JD, Sale DG, Moroz JR. et al. Mitochondrial volume density in human skeletal muscle following heavy resistance training. Med Sci Sports 1979; 11: 164-166
  • 35 Porter C, Reidy PT, Bhattarai N. et al. Resistance exercise training alters mitochondrial function in human skeletal muscle. Med Sci Sports Exerc 2015; 47: 1922
  • 36 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
  • 37 Larsen S, Nielsen J, Hansen CN. et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol 2012; 590: 3349-3360
  • 38 Davies KJ, Packer L, Brooks GA. Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Arch Biochem Biophys 1981; 209: 539-554
  • 39 Wibom R, Hultman E, Johansson M. et al. Adaptation of mitochondrial ATP production in human skeletal muscle to endurance training and detraining. J Appl Physiol (1985) 1992; 73: 2004-2010
  • 40 Tonkonogi M, Walsh B, Svensson M. et al. Mitochondrial function and antioxidative defence in human muscle: Effects of endurance training and oxidative stress. J Physiol 2000; 528: 379-388
  • 41 Walsh B, Tonkonogi M, Sahlin K. Effect of endurance training on oxidative and antioxidative function in human permeabilized muscle fibres. Pflügers Arch 2001; 442: 420-425
  • 42 Jornayvaz FR, Shulman GI. Regulation of mitochondrial biogenesis. Essays Biochem 2010; 47: 69-84
  • 43 Islam H, Bonafiglia JT. Cooperative control of oxidative metabolism by PGC-1alpha and PPARbeta: Implications for exercise-induced mitochondrial remodelling in skeletal muscle. J Physiol 2019; 597: 4447-4449
  • 44 Puigserver P, Wu Z, Park CW. et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998; 92: 829-839
  • 45 Wu Z, Puigserver P, Andersson U. et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic co-activator PGC-1. Cell 1999; 98: 115-124
  • 46 Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 2003; 546: 851-858
  • 47 Little JP, Safdar A, Cermak N. et al. Acute endurance exercise increases the nuclear abundance of PGC-1alpha in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2010; 298: R912-R917
  • 48 Ydfors M, Fischer H, Mascher H. et al. The truncated splice variants, NT-PGC-1alpha and PGC-1alpha4, increase with both endurance and resistance exercise in human skeletal muscle. Physiol Rep 2013; 1: e00140
  • 49 Pugh JK, Faulkner SH, Jackson AP. et al. Acute molecular responses to concurrent resistance and high-intensity interval exercise in untrained skeletal muscle. Physiol Rep. 2015 3.
  • 50 Hickson RC, Bomze HA, Holloszy JO. Linear increase in aerobic power induced by a strenuous program of endurance exercise. J Appl Physiol Respir Environ Exerc Physiol 1977; 42: 372-376
  • 51 Jacobs RA, Lundby C. Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes. J Appl Physiol (1985) 2013; 114: 344-350
  • 52 Daussin FN, Zoll J, Dufour SP. et al. Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: Relationship to aerobic performance improvements in sedentary subjects. Am J Physiol Regul Integr Comp Physiol 2008; 295: R264-R272
  • 53 MacDougall JD, Sale DG, Elder GC. et al. Muscle ult1rastructural characteristics of elite powerlifters and bodybuilders. Eur J Appl Physiol Occup Physiol 1982; 48: 117-126
  • 54 Tesch PA, Komi PV, Hakkinen K. Enzymatic adaptations consequent to long-term strength training. Int J Sports Med 1987; 8 (Suppl 1) 66-69
  • 55 Haun CT, Vann CG, Osburn SC. et al. Muscle fiber hypertrophy in response to 6 weeks of high-volume resistance training in trained young men is largely attributed to sarcoplasmic hypertrophy. PLoS One 2019; 14: e0215267
  • 56 Tesch PA, Thorsson A, Colliander EB. Effects of eccentric and concentric resistance training on skeletal muscle substrates, enzyme activities and capillary supply. Acta Physiol Scand 1990; 140: 575-580
  • 57 Wang N, Hikida RS, Staron RS. et al. Muscle fiber types of women after resistance training—quantitative ultrastructure and enzyme activity. Pflügers Arch 1993; 424: 494-502
  • 58 Tang JE, Hartman JW, Phillips SM. Increased muscle oxidative potential following resistance training induced fibre hypertrophy in young men. Appl Physiol Nutr Metab 2006; 31: 495-501
  • 59 Salvadego D, Domenis R, Lazzer S. et al. Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J Appl Physiol (1985) 2013; 114: 1527-1535
  • 60 Nicholls DG, Ferguson SJ. Bioenergetics. 3rd ed. Cambridge, MA: Elsevier; 2002
  • 61 Fukuda R, Zhang H, Kim J. et al. Regulation of COX subunit composition by HIF-1: A mechanism for optimizing the efficiency of respiration in hypoxic cells. Cell 2007; 129: 111-122
  • 62 Semenza GL. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 2007; 405: 1-9
  • 63 Kon M, Ohiwa N, Honda A. et al. Effects of systemic hypoxia on human muscular adaptations to resistance exercise training. Physiol Rep 2014; 2: e12033
  • 64 Pesta D, Hoppel F, Macek C. et al. Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am J Physiol Regul Integr Comp Physiol 2011; 301: R1078-R1087
  • 65 Bakkman L, Sahlin K, Holmberg HC. et al. Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol (Oxf) 2007; 190: 243-251
  • 66 Pignanelli C, Petrick HL, Keyvani F. et al. Low-load resistance training to task-failure with and without blood flow restriction: Muscular functional and structural adaptations. Am J Physiol Regul Integr Comp Physiol. 2020 318. R284-R295
  • 67 Lim C, Kim HJ, Morton RW. et al. Resistance exercise-induced changes in muscle phenotype are load dependent. Med Sci Sports Exerc 2019; 51: 2578-2585
  • 68 Kitaoka Y, Ogasawara R, Tamura Y. et al. Effect of electrical stimulation-induced resistance exercise on mitochondrial fission and fusion proteins in rat skeletal muscle. Appl Physiol Nutr Metab 2015; 40: 1137-1142
  • 69 Hickson R, Rosenkoetter M, Brown M. Strength training effects on aerobic power and short-term endurance. Med Sci Sports Exerc 1980; 12: 336-339
  • 70 Shaw BS, Shaw I. Compatibility of concurrent aerobic and resistance training on maximal aerobic capacity in sedentary males. Cardiovasc J Afr 2009; 20: 104
  • 71 Vincent KR, Braith RW, Feldman RA. et al. Improved cardiorespiratory endurance following 6 months of resistance exercise in elderly men and women. Arch Intern Med 2002; 162: 673-678
  • 72 Baumgartner RN, Waters DL, Gallagher D. et al. Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev 1999; 107: 123-136
  • 73 Fuggle N, Shaw S, Dennison E. et al. Sarcopenia. Best Pract Res Clin Rheumatol 2017; 31: 218-242
  • 74 Distefano G, Goodpaster BH. Effects of exercise and aging on skeletal muscle. Cold Spring Harb Perspect Med. 2018 8.
  • 75 Rogers MA, Hagberg JM, Martin WH. et al. Decline in VO2max with aging in master athletes and sedentary men. J Appl Physiol (1985) 1990; : 2195-2199
  • 76 Cawthon PM, Marshall LM, Michael Y. et al. Frailty in older men: Prevalence, progression, and relationship with mortality. J Am Geriatr Soc 2007; 55: 1216-1223
  • 77 Harman D. Aging: A theory based on free radical and radiation chemistry. J Gerontol 1956; 11: 209-300
  • 78 Harman D. Free radical theory of aging. Mutation Res 1992; 275: 257-266
  • 79 Harman D. The biologic clock: The mitochondria?. J Am Geriatr Soc 1972; 20: 145-147
  • 80 Quinlan CL, Perevoshchikova IV, Hey-Mogensen M. et al. Sites of reactive oxygen species generation by mitochondria oxidizing different substrates. Redox Biol 2013; 1: 304-312
  • 81 Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13
  • 82 Wong HS, Dighe PA, Mezera V. et al. Production of superoxide and hydrogen peroxide from specific mitochondrial sites under different bioenergetic conditions. J Biol Chem 2017; 292: 16804-16809
  • 83 Willis WT, Jackman MR, Messer JI. et al. A simple hydraulic analog model of oxidative phosphorylation. Med Sci Sports Exerc 2016; 48: 990
  • 84 Holloway GP, Holwerda AM, Miotto PM. et al. Age-associated impairments in mitochondrial adp sensitivity contribute to redox stress in senescent human skeletal muscle. Cell Rep 2018; 22: 2837-2848
  • 85 Robinson MM, Dasari S, Konopka AR. et al. enhanced protein translation underlies improved metabolic and physical adaptations to different exercise training modes in young and old humans. Cell Metab 2017; 25: 581-592
  • 86 Flack KD, Davy BM, DeBerardinis M. et al. Resistance exercise training and in vitro skeletal muscle oxidative capacity in older adults. Physiol Rep. 2016 4.
  • 87 Bouitbir J, Charles AL, Echaniz-Laguna A. et al. Opposite effects of statins on mitochondria of cardiac and skeletal muscles: A 'mitohormesis' mechanism involving reactive oxygen species and PGC-1. Eur Heart J 2012; 33: 1397-1407
  • 88 Bouitbir J, Singh F, Charles AL. et al. Statins trigger mitochondrial reactive oxygen species-induced apoptosis in glycolytic skeletal muscle. Antioxid Redox Signal 2016; 24: 84-98
  • 89 Allard NAE, Schirris TJJ, Verheggen RJ. et al. Statins affect skeletal muscle performance: Evidence for disturbances in energy metabolism. J Clin Endocrinol Metab 2017; 103: 75-84
  • 90 MacDougall JD, Tarnopolsky MA, Chesley A. et al. Changes in muscle protein synthesis following heavy resistance exercise in humans: A pilot study. Acta Physiol Scand 1992; 146: 403-404
  • 91 Wang L, Mascher H, Psilander N. et al. Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J Appl Physiol (1985) 2011; 111: 1335-1344
  • 92 Lantis DJ, Farrell JW, Cantrell GS. et al. Eight weeks of high-volume resistance training improves onset of blood lactate in trained individuals. J Strength Cond Res 2017; 31: 2176-2182
  • 93 Schoenfeld BJ, Contreras B, Krieger J. et al. Resistance Training volume enhances muscle hypertrophy but not strength in trained men. Med Sci Sports Exerc 2019; 51: 94-103
  • 94 Vincent AE, White K, Davey T. et al. Quantitative 3D mapping of the human skeletal muscle mitochondrial network. Cell Rep 2019; 26: 996-1009 e1004
  • 95 Glancy B, Hartnell LM, Combs CA. et al. Power grid protection of the muscle mitochondrial reticulum. Cell Rep 2017; 19: 487-496
  • 96 Glancy B, Hartnell LM, Malide D. et al. Mitochondrial reticulum for cellular energy distribution in muscle. Nature 2015; 523: 617-620