Advertisement

Sports Medicine

, Volume 48, Issue 8, pp 1809–1828 | Cite as

Training-Induced Changes in Mitochondrial Content and Respiratory Function in Human Skeletal Muscle

  • Cesare Granata
  • Nicholas A. Jamnick
  • David J. Bishop
Review Article

Abstract

A sedentary lifestyle has been linked to a number of metabolic disorders that have been associated with sub-optimal mitochondrial characteristics and an increased risk of premature death. Endurance training can induce an increase in mitochondrial content and/or mitochondrial functional qualities, which are associated with improved health and well-being and longer life expectancy. It is therefore important to better define how manipulating key parameters of an endurance training intervention can influence the content and functionality of the mitochondrial pool. This review focuses on mitochondrial changes taking place following a series of exercise sessions (training-induced mitochondrial adaptations), providing an in-depth analysis of the effects of exercise intensity and training volume on changes in mitochondrial protein synthesis, mitochondrial content and mitochondrial respiratory function. We provide evidence that manipulation of different exercise training variables promotes specific and diverse mitochondrial adaptations. Specifically, we report that training volume may be a critical factor affecting changes in mitochondrial content, whereas relative exercise intensity is an important determinant of changes in mitochondrial respiratory function. As a consequence, a dissociation between training-induced changes in mitochondrial content and mitochondrial respiratory function is often observed. We also provide evidence that exercise-induced changes are not necessarily predictive of training-induced adaptations, we propose possible explanations for the above discrepancies and suggestions for future research.

Notes

Acknowledgements

The authors acknowledge Dr. Cian McGinley, Mr. Alessandro Garofolini, Dr. Sarah Voisin and Mr. Ramón Rodriguez for their valuable help with data analysis and presentation, and their constructive critique of this manuscript.

Author contributions

Cesare Granata conducted the literature searches. Cesare Granata, Nicholas Jamnick and David Bishop analysed and interpreted the data. Cesare Granata wrote the manuscript. Cesare Granata, Nicholas Jamnick and David Bishop critically revised and contributed to the manuscript. Cesare Granata and David Bishop have primary responsibility for final content. Data analysis took place at Victoria University. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Funding

No sources of funding were used to assist in the preparation of this article.

Conflict of interest

Cesare Granata, Nicholas Jamnick and David Bishop have no conflicts of interest directly relevant to the content of this review.

Supplementary material

40279_2018_936_MOESM1_ESM.docx (1.2 mb)
Supplementary material 1 (DOCX 1,235 kb)

References

  1. 1.
    Granata C, Oliveira RSF, Little JP, Renner K, Bishop DJ. Mitochondrial adaptations to high-volume exercise training are rapidly reversed after a reduction in training volume in human skeletal muscle. FASEB J. 2016;30(10):3413–23.PubMedGoogle Scholar
  2. 2.
    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. 2013;114(3):344–50.PubMedGoogle Scholar
  3. 3.
    Jacobs RA, Rasmussen P, Siebenmann C, Díaz V, Gassmann M, Pesta D, et al. Determinants of time trial performance and maximal incremental exercise in highly trained endurance athletes. J Appl Physiol. 2011;111(5):1422–30.PubMedGoogle Scholar
  4. 4.
    Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell. 2012;148(6):1145–59.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Conley KE, Amara CE, Jubrias SA, Marcinek DJ. Mitochondrial function, fibre types and ageing: new insights from human muscle in vivo. Exp Physiol. 2007;92(2):333–9.PubMedGoogle Scholar
  6. 6.
    Luft R. The development of mitochondrial medicine. Proc Natl Acad Sci USA. 1994;91(19):8731–8.PubMedGoogle Scholar
  7. 7.
    Lowell BB, Shulman GI. Mitochondrial dysfunction and type 2 diabetes. Science. 2005;307(5708):384–7.PubMedGoogle Scholar
  8. 8.
    Mogensen M, Sahlin K, Fernström M, Glintborg D, Vind BF, Beck-Nielsen H, et al. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes. 2007;56(6):1592–9.PubMedGoogle Scholar
  9. 9.
    Wells GD, Noseworthy MD, Hamilton J, Tarnopolski M, Tein I. Skeletal muscle metabolic dysfunction in obesity and metabolic syndrome. Can J Neurol Sci. 2008;35(1):31–40.PubMedGoogle Scholar
  10. 10.
    Booth FW, Gordon SE, Carlson CJ, Hamilton MT. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol. 2000;88(2):774–87.PubMedGoogle Scholar
  11. 11.
    World Health Organization. Global health risks: mortality and burden of disease attributable to selected major risks. Geneva: World Health Organization; 2009.Google Scholar
  12. 12.
    Hawley JA. Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance. Diabetes Metab Res Rev. 2004;20(5):383–93.PubMedGoogle Scholar
  13. 13.
    Pedersen BK, Saltin B. Evidence for prescribing exercise as therapy in chronic disease. Scand J Med Sci Sports. 2006;16(Suppl. 1):3–63.PubMedGoogle Scholar
  14. 14.
    Granata C, Jamnick NA, Bishop DJ. Principles of exercise prescription, and how they influence exercise-induced changes of transcription factors and other regulators of mitochondrial biogenesis. Sports Med. 2018.  https://doi.org/10.1007/s40279-018-0894-4 (Epub ahead of print).Google Scholar
  15. 15.
    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(9):2278–82.PubMedGoogle Scholar
  16. 16.
    Burgomaster KA, Howarth KR, Phillips SM, Rakobowchuk M, Macdonald MJ, McGee SL, et al. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J Physiol. 2008;586(1):151–60.PubMedGoogle Scholar
  17. 17.
    Perry CGR, Lally J, Holloway GP, Heigenhauser GJF, Bonen A, Spriet LL. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol. 2010;588(23):4795–810.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, et al. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol. 1985;59(2):320–7.PubMedGoogle Scholar
  19. 19.
    Montero D, Lundby C. Refuting the myth of non-response to exercise training: ‘non-responders’ do respond to higher dose of training. J Physiol. 2017;595(11):3377–87.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Daussin FN, Zoll J, Dufour SP, Ponsot E, Lonsdorfer-Wolf E, Doutreleau S, 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(1):R264–72.PubMedGoogle Scholar
  21. 21.
    Meex RCR, Schrauwen-Hinderling VB, Moonen-Kornips E, Schaart G, Mensink M, Phielix E, et al. Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes. 2010;59(3):572–9.PubMedGoogle Scholar
  22. 22.
    Tonkonogi M, Walsh B, Svensson M, Sahlin K. Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress. J Physiol. 2000;528(2):379–88.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Astrand PO, Rodahl K. Textbook of work physiology. New York: McGraw Hill; 1986.Google Scholar
  24. 24.
    Adami A, Sivieri A, Moia C, Perini R, Ferretti G. Effects of step duration in incremental ramp protocols on peak power and maximal oxygen consumption. Eur J Appl Physiol. 2013;113(10):2647–53.PubMedGoogle Scholar
  25. 25.
    Morton RH. Why peak power is higher at the end of steeper ramps: an explanation based on the “critical power” concept. J Sports Sci. 2011;29(3):307–9.PubMedGoogle Scholar
  26. 26.
    Mujika I. Intense training: the key to optimal performance before and during the taper. Scand J Med Sci Sports. 2010;20(Suppl. 2):24–31.PubMedGoogle Scholar
  27. 27.
    Wibom R, Hultman E, Johansson M, Matherei K, Constantin-Teodosiu D, Schantz PG. Adaptation of mitochondrial ATP production in human skeletal muscle to endurance training and detraining. J Appl Physiol. 1992;73(5):2004–10.PubMedGoogle Scholar
  28. 28.
    Rittweger J, Winwood K, Seynnes O, De Boer M, Wilks D, Lea R, et al. Bone loss from the human distal tibia epiphysis during 24 days of unilateral lower limb suspension. J Physiol. 2006;577(1):331–7.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab. 2009;34(3):465–72.PubMedGoogle Scholar
  30. 30.
    Boushel R, Gnaiger E, Calbet JAL, Gonzalez-Alonso J, Wright-Paradis C, Sondergaard H, et al. Muscle mitochondrial capacity exceeds maximal oxygen delivery in humans. Mitochondrion. 2011;11(2):303–7.PubMedGoogle Scholar
  31. 31.
    Tonkonogi M, Sahlin K. Physical exercise and mitochondrial function in human skeletal muscle. Exerc Sport Sci Rev. 2002;30(3):129–37.PubMedGoogle Scholar
  32. 32.
    Van Der Zwaard XS, De Ruiter CJ, Noordhof DA, Sterrenburg R, Bloemers FW, De Koning JJ, et al. Maximal oxygen uptake is proportional to muscle fiber oxidative capacity, from chronic heart failure patients to professional cyclists. J Appl Physiol. 2016;121(3):636–45.PubMedGoogle Scholar
  33. 33.
    Granata C, Oliveira RSF, Little JP, Renner K, Bishop DJ. Training intensity modulates changes in PGC-1α and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle. FASEB J. 2016;30(2):959–70.PubMedGoogle Scholar
  34. 34.
    Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol. 1984;56(4):831–8.PubMedGoogle Scholar
  35. 35.
    Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, et al. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol. 2008;586(15):3701–17.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Montero D, Cathomen A, Jacobs RA, Flück D, de Leur J, Keiser S, et al. Haematological rather than skeletal muscle adaptations contribute to the increase in peak oxygen uptake induced by moderate endurance training. J Physiol. 2015;593(20):4677–88.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Moore RL, Thacker EM, Kelley GA, Musch TI, Sinoway LI, Foster VL, et al. Effect of training/detraining on submaximal exercise responses in humans. J Appl Physiol. 1987;63(5):1719–24.PubMedGoogle Scholar
  38. 38.
    Di Donato DM, West DWD, Churchward-Venne TA, Breen L, Baker SK, Phillips SM. 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(9):E1025–32.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Donges CE, Burd NA, Duffield R, Smith GC, West DWD, Short MJ, et al. Concurrent resistance and aerobic exercise stimulates both myofibrillar and mitochondrial protein synthesis in sedentary middle-aged men. J Appl Physiol. 2012;112(12):1992–2001.PubMedGoogle Scholar
  40. 40.
    Paddon-Jones D, Sheffield-Moore M, Zhang X-J, Volpi E, Wolf SE, Aarsland A, et al. Amino acid ingestion improves muscle protein synthesis in the young and elderly. Am J Physiol Endocrinol Metab. 2004;286(3):E321–8.PubMedGoogle Scholar
  41. 41.
    Moore DR, Tang JE, Burd NA, Rerecich T, Tarnopolsky MA, Phillips SM. Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. J Physiol. 2009;587(4):897–904.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Robinson MM, Dasari S, Konopka AR, Johnson ML, Manjunatha S, Esponda RR, 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(3):581–92.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, Barron N, et al. Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor γ coactivator-1α mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol. 2010;588(10):1779–90.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Bell KE, Séguin C, Parise G, Baker SK, Phillips SM. Day-to-day changes in muscle protein synthesis in recovery from resistance, aerobic, and high-intensity interval exercise in older men. J Gerontol A Biol Sci Med Sci. 2015;70(8):1024–9.PubMedGoogle Scholar
  45. 45.
    Rennie MJ, Edwards RH, Davies CM, Krywawych S, Halliday D, Waterlow JC, et al. Protein and amino acid turnover during and after exercise. Biochem Soc Trans. 1980;8(5):499–501.PubMedGoogle Scholar
  46. 46.
    Andersen G, Ørngreen MC, Preisler N, Jeppesen TD, Krag TO, Hauerslev S, et al. Protein–carbohydrate supplements improve muscle protein balance in muscular dystrophy patients after endurance exercise: a placebo-controlled crossover study. Am J Physiol Regul Integr Comp Physiol. 2015;308(2):R123–30.PubMedGoogle Scholar
  47. 47.
    Carraro F, Stuart CA, Hartl WH, Rosenblatt J, Wolfe RR. Effect of exercise and recovery on muscle protein synthesis in human subjects. Am J Physiol Endocrinol Metab. 1990;259(4):E470–6.Google Scholar
  48. 48.
    Pasiakos SM, Carbone JW. Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise. IUBMB Life. 2014;66(7):478–84.PubMedGoogle Scholar
  49. 49.
    Harber MP, Crane JD, Dickinson JM, Jemiolo B, Raue U, Trappe TA, et al. Protein synthesis and the expression of growth-related genes are altered by running in human vastus lateralis and soleus muscles. Am J Physiol Regul Integr Comp Physiol. 2009;296(3):R708–14.PubMedGoogle Scholar
  50. 50.
    Mascher H, Ekblom B, Rooyackers O, Blomstrand E. Enhanced rates of muscle protein synthesis and elevated mTOR signalling following endurance exercise in human subjects. Acta Physiol. 2011;202(2):175–84.Google Scholar
  51. 51.
    Sheffield-Moore M, Yeckel C, Volpi E, Wolf S, Morio B, Chinkes D, et al. Postexercise protein metabolism in older and younger men following moderate-intensity aerobic exercise. Am J Physiol Endocrinol Metab. 2004;287(3):E513–22.PubMedGoogle Scholar
  52. 52.
    Pikosky MA, Gaine PC, Martin WF, Grabarz KC, Ferrando AA, Wolfe RR, et al. Aerobic exercise training increases skeletal muscle protein turnover in healthy adults at rest. J Nutr. 2006;136(2):379–83.PubMedGoogle Scholar
  53. 53.
    Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab. 2004;286(1):E92–101.PubMedGoogle Scholar
  54. 54.
    Medeiros DM. Assessing mitochondria biogenesis. Methods. 2008;46(4):288–94.PubMedGoogle Scholar
  55. 55.
    Meinild Lundby AK, Jacobs RA, Gehrig S, de Leur J, Hauser M, Bonne TC, et al. Exercise training increases skeletal muscle mitochondrial volume density by enlargement of existing mitochondria and not de novo biogenesis. Acta Physiol. 2018;222(1):e12905.Google Scholar
  56. 56.
    Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol. 2007;292(3):R1271–8.PubMedGoogle Scholar
  57. 57.
    Turner DL, Hoppeler H, Claassen H, Vock P, Kayser B, Schena F, et al. Effects of endurance training on oxidative capacity and structural composition of human arm and leg muscles. Acta Physiol Scand. 1997;161(4):459–64.PubMedGoogle Scholar
  58. 58.
    Morrison D, Hughes J, Della Gatta PA, Mason S, Lamon S, Russell AP, et al. Vitamin C and E supplementation prevents some of the cellular adaptations to endurance-training in humans. Free Radic Biol Med. 2015;89:852–62.PubMedGoogle Scholar
  59. 59.
    Stepto NK, Benziane B, Wadley GD, Chibalin AV, Canny BJ, Eynon N, et al. Short-term intensified cycle training alters acute and chronic responses of PGC1α and cytochrome c oxidase IV to exercise in human skeletal muscle. PLoS One. 2012;7(12):e53080.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol. 2012;590(14):3349–60.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Jacobs I, Esbjornsson M, Sylven C, Holm I, Jansson E. Sprint training effects on muscle myoglobin, enzymes, fiber types, and blood lactate. Med Sci Sports Exerc. 1987;19(4):368–74.PubMedGoogle Scholar
  62. 62.
    Spina RJ, Chi MMY, Hopkins MG, Nemeth PM, Lowry OH, Holloszy JO. Mitochondrial enzymes increase in muscle in response to 7–10 days of cycle exercise. J Appl Physiol. 1996;80(6):2250–4.PubMedGoogle Scholar
  63. 63.
    Svedenhag J, Henriksson J, Sylven C. Dissociation of training effects on skeletal muscle mitochondrial enzymes and myoglobin in man. Acta Physiol Scand. 1983;117(2):213–8.PubMedGoogle Scholar
  64. 64.
    Green H, Grant S, Bombardier E, Ranney D. Initial aerobic power does not alter muscle metabolic adaptations to short-term training. Am J Physiol Endocrinol Metab. 1999;277(1 Pt 1):E39–48.Google Scholar
  65. 65.
    LeBlanc PJ, Peters SJ, Tunstall RJ, Cameron-Smith D, Heigenhauser GJF. Effects of aerobic training on pyruvate dehydrogenase and pyruvate dehydrogenase kinase in human skeletal muscle. J Physiol. 2004;557(2):559–70.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Egan B, O’Connor PL, Zierath JR, O’Gorman DJ. Time course analysis reveals gene-specific transcript and protein kinetics of adaptation to short-term aerobic exercise training in human skeletal muscle. PLoS One. 2013;8(9):e74098.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Murias JM, Kowalchuk JM, Ritchie D, Hepple RT, Doherty TJ, Paterson DH. Adaptations in capillarization and citrate synthase activity in response to endurance training in older and young men. J Gerontol A Biol Sci Med Sci. 2011;66(9):957–64.PubMedGoogle Scholar
  68. 68.
    Jacobs RA, Flück D, Bonne TC, Bürgi S, Christensen PM, Toigo M, 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. 2013;115(6):785–93.PubMedGoogle Scholar
  69. 69.
    Little JP, Safdar A, Bishop D, Tarnopolsky MA, Gibala MJ. An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2011;300(6):R1303–10.PubMedGoogle Scholar
  70. 70.
    Bishop DJ, Granata C, Eynon N. Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? Biochim Biophys Acta. 2014;1840(4):1266–75.PubMedGoogle Scholar
  71. 71.
    Gorostiaga EM, Walter CB, Foster C, Hickson RC. Uniqueness of interval and continuous training at the same maintained exercise intensity. Eur J Appl Physiol Occup Physiol. 1991;63(2):101–7.PubMedGoogle Scholar
  72. 72.
    MacInnis MJ, Zacharewicz E, Martin BJ, Haikalis ME, Skelly LE, Tarnopolsky MA, et al. Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. J Physiol. 2016;595(9):2955–68.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Gillen JB, Martin BJ, MacInnis MJ, Skelly LE, Tarnopolsky MA, Gibala MJ. Twelve weeks of sprint interval training improves indices of cardiometabolic health similar to traditional endurance training despite a five-fold lower exercise volume and time commitment. PLoS One. 2016;11(4):e0154075.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Granata C, Oliveira RSF, Little JP, Renner K, Bishop DJ. Sprint-interval but not continuous exercise increases PGC-1α protein content and p53 phosphorylation in nuclear fractions of human skeletal muscle. Sci Rep. 2017;7:44227.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Cochran AJR, Percival ME, Tricarico S, Little JP, Cermak N, Gillen JB, et al. Intermittent and continuous high-intensity exercise training induce similar acute but different chronic muscle adaptations. Exp Physiol. 2014;99(5):782–91.PubMedGoogle Scholar
  76. 76.
    Miller BF, Konopka AR, Hamilton KL. The rigorous study of exercise adaptations: why mRNA might not be enough. J Appl Physiol. 2016;121(2):594–6.PubMedGoogle Scholar
  77. 77.
    Pedhazur EJ. Multiple regression in behavioral research: explanation and prediction. 3rd ed. San Diego: Harcourt Brace College Publishers; 1997. p. 156–94.Google Scholar
  78. 78.
    Gollnick P, Piehl K, Saltin B. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol. 1974;241(1):45–57.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Suriano R, Edge J, Bishop D. Effects of cycle strategy and fibre composition on muscle glycogen depletion pattern and subsequent running economy. Br J Sports Med. 2010;44(6):443–8.PubMedGoogle Scholar
  80. 80.
    Vollestad NK, Blom PCS. Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand. 1985;125(3):395–405.PubMedGoogle Scholar
  81. 81.
    Scribbans TD, Edgett BA, Vorobej K, Mitchell AS, Joanisse SD, Matusiak JBL, et al. Fibre-specific responses to endurance and low volume high intensity interval training: striking similarities in acute and chronic adaptation. PLoS One. 2014;9(6):e98119.PubMedPubMedCentralGoogle Scholar
  82. 82.
    Slivka DR, Dumke CL, Hailes WS, Cuddy JS, Ruby BC. Substrate use and biochemical response to a 3,211-km bicycle tour in trained cyclists. Eur J Appl Physiol. 2012;112(5):1621–30.PubMedGoogle Scholar
  83. 83.
    Christensen PM, Gunnarsson TP, Thomassen M, Wilkerson DP, Nielsen JJ, Bangsbo J. Unchanged content of oxidative enzymes in fast-twitch muscle fibers and VO2 kinetics after intensified training in trained cyclists. Physiol Rep. 2015;3(7):e12428.PubMedPubMedCentralGoogle Scholar
  84. 84.
    McCoy M, Proietto J, Hargreaves M. Effect of detraining on GLUT-4 protein in human skeletal muscle. J Appl Physiol. 1994;77(3):1532–6.PubMedGoogle Scholar
  85. 85.
    Mettauer B, Zoll J, Sanchez H, Lampert E, Ribera F, Veksler V, et al. Oxidative capacity of skeletal muscle in heart failure patients versus sedentary or active control subjects. J Am Coll Cardiol. 2001;38(4):947–54.PubMedGoogle Scholar
  86. 86.
    Rimbert V, Boirie Y, Bedu M, Hocquette JF, Ritz P, Morio B. Muscle fat oxidative capacity is not impaired by age but by physical inactivity: association with insulin sensitivity. FASEB J. 2004;18(6):737–9.PubMedGoogle Scholar
  87. 87.
    Robach P, Siebenmann C, Jacobs RA, Rasmussen P, Nordsborg N, Pesta D, et al. The role of haemoglobin mass on VO2max following normobaric ‘live high-train low’in endurance-trained athletes. Br J Sports Med. 2012;46(11):822–7.PubMedGoogle Scholar
  88. 88.
    Roepstorff C, Schjerling P, Vistisen B, Madsen M, Steffensen CH, Rider MH, et al. Regulation of oxidative enzyme activity and eukaryotic elongation factor 2 in human skeletal muscle: influence of gender and exercise. Acta Physiol Scand. 2005;184(3):215–24.PubMedGoogle Scholar
  89. 89.
    Russell A, Wadley G, Snow R, Giacobino JP, Muzzin P, Garnham A, et al. Slow component of \(\dot{\text{V}}O_{2}\) kinetics: the effect of training status, fibre type, UCP3 mRNA and citrate synthase activity. Int J Obes. 2002;26(2):157–64.Google Scholar
  90. 90.
    Zoll J, Sanchez H, N’Guessan B, Ribera F, Lampert E, Bigard X, et al. Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle. J Physiol. 2002;543(1):191–200.PubMedPubMedCentralGoogle Scholar
  91. 91.
    Laursen PB, Jenkins DG. The scientific basis for high-intensity interval training: optimising training programmes and maximising performance in highly trained endurance athletes. Sports Med. 2002;32(1):53–73.PubMedGoogle Scholar
  92. 92.
    Londeree BR. Effect of training on lactate/ventilatory thresholds: a meta-analysis. Med Sci Sports Exerc. 1997;29(6):837–43.PubMedGoogle Scholar
  93. 93.
    Yu M, Stepto NK, Chibalin AV, Fryer LGD, Carling D, Krook A, et al. Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J Physiol. 2003;546(2):327–35.PubMedGoogle Scholar
  94. 94.
    Shepley B, MacDougall JD, Cipriano N, Sutton JR, Tarnopolsky MA, Coates G. Physiological effects of tapering in highly trained athletes. J Appl Physiol. 1992;72(2):706–11.PubMedGoogle Scholar
  95. 95.
    Chi MM, Hintz CS, Coyle EF, Martin WH 3rd, Ivy JL, Nemeth PM, et al. Effects of detraining on enzymes of energy metabolism in individual human muscle fibers. Am J Physiol. 1983;244(3):C276–87.PubMedGoogle Scholar
  96. 96.
    Luden N, Hayes E, Minchev K, Louis E, Raue U, Conley T, et al. Skeletal muscle plasticity with marathon training in novice runners. Scand J Med Sci Sports. 2012;22(5):662–70.PubMedGoogle Scholar
  97. 97.
    Madsen K, Pedersen PK, Djurhuus MS, Klitgaard NA. Effects of detraining on endurance capacity and metabolic changes during prolonged exhaustive exercise. J Appl Physiol. 1993;75(4):1444–51.PubMedGoogle Scholar
  98. 98.
    Daussin FN, Zoll J, Ponsot E, Dufour SP, Doutreleau S, Lonsdorfer E, et al. Training at high exercise intensity promotes qualitative adaptations of mitochondrial function in human skeletal muscle. J Appl Physiol. 2008;104(5):1436–41.PubMedGoogle Scholar
  99. 99.
    Starritt EC, Angus D, Hargreaves M. Effect of short-term training on mitochondrial ATP production rate in human skeletal muscle. J Appl Physiol. 1999;86(2):450–4.PubMedGoogle Scholar
  100. 100.
    Schrauwen P, Troost FJ, Xia J, Ravussin E, Saris WH. Skeletal muscle UCP2 and UCP3 expression in trained and untrained male subjects. Int J Obes Relat Metab Disord. 1999;23(9):966–72.PubMedGoogle Scholar
  101. 101.
    Lanza IR, Nair KS. Mitochondrial metabolic function assessed in vivo and in vitro. Curr Opin Clin Nutr Metab Care. 2010;13(5):511–7.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Picard M, Taivassalo T, Ritchie D, Wright KJ, Thomas MM, Romestaing C, et al. Mitochondrial structure and function are disrupted by standard isolation methods. PLoS One. 2011;6(3):e18317.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Christensen PM, Jacobs RA, Bonne T, Fluck D, Bangsbo J, Lundby C. A short period of high-intensity interval training improves skeletal muscle mitochondrial function and pulmonary oxygen uptake kinetics. J Appl Physiol. 2016;120(11):1319–27.PubMedGoogle Scholar
  104. 104.
    Irving BA, Lanza IR, Henderson GC, Rao RR, Spiegelman BM, Sreekumaran Nair K. Combined training enhances skeletal muscle mitochondrial oxidative capacity independent of age. J Clin Endocrinol Metab. 2015;100(4):1654–63.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Pesta D, Hoppel F, Macek C, Messner H, Faulhaber M, Kobel 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(4):R1078–87.PubMedGoogle Scholar
  106. 106.
    Robach P, Bonne T, Flueck D, Buergi S, Toigo M, Jacobs RA, et al. Hypoxic training: effect on mitochondrial function and aerobic performance in hypoxia. Med Sci Sports Exerc. 2014;46(10):1936–45.PubMedGoogle Scholar
  107. 107.
    Vincent G, Lamon S, Gant N, Vincent P, MacDonald J, Markworth J, et al. Changes in mitochondrial function and mitochondria associated protein expression in response to 2-weeks of high intensity interval training. Front Physiol. 2015;6:51.PubMedPubMedCentralGoogle Scholar
  108. 108.
    Walsh B, Tonkonogi M, Sahlin K. Effect of endurance training on oxidative and antioxidative function in human permeabilized muscle fibres. Pflug Arch. 2001;442(3):420–5.Google Scholar
  109. 109.
    Larsen FJ, Schiffer TA, Ørtenblad N, Zinner C, Morales-Alamo D, Willis SJ, et al. High-intensity sprint training inhibits mitochondrial respiration through aconitase inactivation. FASEB J. 2016;30(1):417–27.PubMedGoogle Scholar
  110. 110.
    Billat LV. Interval training for performance: a scientific and empirical practice. Sports Med. 2001;31(2):75–90.PubMedGoogle Scholar
  111. 111.
    Gibala MJ, Little JP, Macdonald MJ, Hawley JA. Physiological adaptations to low-volume, high-intensity interval training in health and disease. J Physiol. 2012;590(5):1077–84.PubMedPubMedCentralGoogle Scholar
  112. 112.
    Abbiss CR, Karagounis LG, Laursen PB, Peiffer JJ, Martin DT, Hawley JA, et al. Single-leg cycle training is superior to double-leg cycling in improving the oxidative potential and metabolic profile of trained skeletal muscle. J Appl Physiol. 2011;110(5):1248–55.PubMedGoogle Scholar
  113. 113.
    Costill DL, Fink WJ, Hargreaves M, King DS, Thomas R, Fielding R. Metabolic characteristics of skeletal muscle during detraining from competitive swimming. Med Sci Sports Exerc. 1985;17(3):339–43.PubMedGoogle Scholar
  114. 114.
    Rowe G, Patten I, Zsengeller ZK, El-Khoury R, Okutsu M, Bampoh S, et al. Disconnecting mitochondrial content from respiratory chain capacity in PGC-1-deficient skeletal muscle. Cell Rep. 2013;3(5):1449–56.PubMedPubMedCentralGoogle Scholar
  115. 115.
    Drake JC, Wilson RJ, Yan Z. Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle. FASEB J. 2015;30(1):13–22.PubMedGoogle Scholar
  116. 116.
    Møller AB, Vendelbo MH, Christensen B, Clasen BF, Bak AM, Jørgensen JOL, et al. Physical exercise increases autophagic signaling through ULK1 in human skeletal muscle. J Appl Physiol. 2015;118(8):971–9.PubMedGoogle Scholar
  117. 117.
    Vainshtein A, Hood DA. The regulation of autophagy during exercise in skeletal muscle. J Appl Physiol. 2016;120(6):664–73.PubMedGoogle Scholar
  118. 118.
    Lo Verso F, Carnio S, Vainshtein A, Sandri M. Autophagy is not required to sustain exercise and PRKAA1/AMPK activity but is important to prevent mitochondrial damage during physical activity. Autophagy. 2014;10(11):1883–94.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Mai S, Muster B, Bereiter-Hahn J, Jendrach M. Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence life span. Autophagy. 2012;8(1):47–62.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Nielsen J, Gejl KD, Hey-Mogensen M, Holmberg HC, Suetta C, Krustrup P, et al. Plasticity in mitochondrial cristae density allows metabolic capacity modulation in human skeletal muscle. J Physiol. 2017;595(9):2839–47.PubMedGoogle Scholar
  121. 121.
    Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell. 2013;155(1):160–71.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Greggio C, Jha P, Kulkarni SS, Lagarrigue S, Broskey NT, Boutant M, et al. Enhanced respiratory chain supercomplex formation in response to exercise in human skeletal muscle. Cell Metab. 2016;25(2):301–11.PubMedGoogle Scholar
  123. 123.
    Cogliati S, Enriquez JA, Scorrano L. Mitochondrial cristae: where beauty meets functionality. Trends Biochem Sci. 2016;41(3):261–73.PubMedGoogle Scholar
  124. 124.
    Kim SH, Koh JH, Higashida K, Jung SR, Holloszy JO, Han DH. PGC-1α mediates a rapid, exercise-induced downregulation of glycogenolysis in rat skeletal muscle. J Physiol. 2015;593(3):635–43.PubMedGoogle Scholar
  125. 125.
    Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, et al. p53 regulates mitochondrial respiration. Science. 2006;312(5780):1650–3.PubMedGoogle Scholar
  126. 126.
    Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1α expression. J Biol Chem. 2007;282(1):194–9.PubMedGoogle Scholar
  127. 127.
    Bonafiglia JT, Edgett BA, Baechler BL, Nelms MW, Simpson CA, Quadrilatero J, et al. Acute upregulation of PGC-1α mRNA correlates with training-induced increases in SDH activity in human skeletal muscle. Appl Physiol Nutr Metab. 2017;42(6):656–66.PubMedGoogle Scholar
  128. 128.
    Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, et al. Global quantification of mammalian gene expression control. Nature. 2011;473(7347):337–42.PubMedGoogle Scholar
  129. 129.
    Miller BF, Konopka AR, Hamilton KL. Last word on Viewpont: on the rigorous study of exercise adaptations: why mRNA might not be enough? J Appl Physiol (1985). 2016;121(2):601.Google Scholar
  130. 130.
    Hornberger TA, Carter HN, Figueiredo VC, Camera DM, Chaillou T, Nader GA, et al. Commentaries on Viewpoint: the rigorous study of exercise adaptations: why mRNA might not be enough. J Appl Physiol (1985). 2016;121(2):597–600.Google Scholar
  131. 131.
    Cartoni R, Léger B, Hock MB, Praz M, Crettenand A, Pich S, et al. Mitofusins 1/2 and ERRα expression are increased in human skeletal muscle after physical exercise. J Physiol. 2005;567(1):349–58.PubMedPubMedCentralGoogle Scholar
  132. 132.
    Saleem A, Carter HN, Iqbal S, Hood DA. Role of p53 within the regulatory network controlling muscle mitochondrial biogenesis. Exerc Sport Sci Rev. 2011;39(4):199–205.PubMedGoogle Scholar
  133. 133.
    Vainshtein A, Tryon LD, Pauly M, Hood DA. Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle. Am J Physiol Cell Physiol. 2015;308(9):C710–9.PubMedPubMedCentralGoogle Scholar
  134. 134.
    Mansueto G, Armani A, Viscomi C, D’Orsi L, De Cegli R, Polishchuk EV, et al. Transcription factor EB controls metabolic flexibility during exercise. Cell Metab. 2017;25(1):182–96.PubMedPubMedCentralGoogle Scholar
  135. 135.
    Vousden KH, Ryan KM. P53 and metabolism. Nat Rev Cancer. 2009;9(10):691–700.PubMedGoogle Scholar
  136. 136.
    Neufer PD, Bamman MM, Muoio DM, Bouchard C, Cooper DM, Goodpaster BH, et al. Understanding the cellular and molecular mechanisms of physical activity-induced health benefits. Cell Metab. 2015;22(1):4–11.PubMedGoogle Scholar
  137. 137.
    Safdar A, Saleem A, Tarnopolsky MA. The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat Rev Endocrinol. 2016;12(9):504–17.PubMedGoogle Scholar
  138. 138.
    Whitham M, Febbraio MA. The ever-expanding myokinome: discovery challenges and therapeutic implications. Nat Rev Drug Discov. 2016;15(10):719–29.PubMedGoogle Scholar
  139. 139.
    Bakkman L, Sahlin K, Holmberg HC, Tonkonogi M. Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol. 2007;190(3):243–51.Google Scholar
  140. 140.
    Barnett C, Carey M, Proietto J, Cerin E, Febbraio MA, Jenkins D. Muscle metabolism during sprint exercise in man: influence of sprint training. J Sci Med Sport. 2004;7(3):314–22.PubMedGoogle Scholar
  141. 141.
    Burgomaster KA, Heigenhauser GJF, Gibala MJ. Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time-trial performance. J Appl Physiol. 2006;100(6):2041–7.PubMedGoogle Scholar
  142. 142.
    Burgomaster KA, Hughes SC, Heigenhauser GJF, Bradwell SN, Gibala MJ. Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. J Appl Physiol. 2005;98(6):1985–90.PubMedGoogle Scholar
  143. 143.
    Carter SL, Rennie CD, Hamilton SJ, Tarnopolsky MA. Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol. 2001;79(5):386–92.PubMedGoogle Scholar
  144. 144.
    Chesley A, Heigenhauser GJF, Spriet LL. Regulation of muscle glycogen phosphorylase activity following short-term endurance training. Am J Physiol. 1996;270(2 Pt 1):E328–35.PubMedGoogle Scholar
  145. 145.
    Cochran AJR, Little JP, Tarnopolsky MA, Gibala MJ. Carbohydrate feeding during recovery alters the skeletal muscle metabolic response to repeated sessions of high-intensity interval exercise in humans. J Appl Physiol. 2010;108(3):628–36.PubMedGoogle Scholar
  146. 146.
    Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC, Brooks GA. Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab. 2000;278(4):E571–9.PubMedGoogle Scholar
  147. 147.
    Green HJ, Bombardier E, Burnett ME, Smith IC, Tupling SM, Ranney DA. Time-dependent effects of short-term training on muscle metabolism during the early phase of exercise. Am J Physiol Regul Integr Comp Physiol. 2009;297(5):R1383–91.PubMedGoogle Scholar
  148. 148.
    Green HJ, Helyar R, Ball-Burnett M, Kowalchuk N, Symon S, Farrance B. Metabolic adaptations to training precede changes in muscle mitochondrial capacity. J Appl Physiol. 1992;72(2):484–91.PubMedGoogle Scholar
  149. 149.
    Green HJ, Jones S, Ball-Burnett ME, Smith D, Livesey J, Farrance BW. Early muscular and metabolic adaptations to prolonged exercise training in humans. J Appl Physiol. 1991;70(5):2032–8.PubMedGoogle Scholar
  150. 150.
    Gurd BJ, Perry CG, Heigenhauser GJ, Spriet LL, Bonen A. High-intensity interval training increases SIRT1 activity in human skeletal muscle. Appl Physiol Nutr Metab. 2010;35(3):350–7.PubMedGoogle Scholar
  151. 151.
    Gurd BJ, Yoshida Y, McFarlan JT, Holloway GP, Moyes CD, Heigenhauser GJF, et al. Nuclear SIRT1 activity, but not protein content, regulates mitochondrial biogenesis in rat and human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2011;301(1):R67–75.PubMedGoogle Scholar
  152. 152.
    Harmer AR, Chisholm DJ, McKenna MJ, Hunter SK, Ruell PA, Naylor JM, et al. Sprint training increases muscle oxidative metabolism during high-intensity exercise in patients with type 1 diabetes. Diabetes Care. 2008;31(11):2097–102.PubMedPubMedCentralGoogle Scholar
  153. 153.
    Howarth KR, LeBlanc PJ, Heigenhauser GJF, Gibala MJ. Effect of endurance training on muscle TCA cycle metabolism during exercise in humans. J Appl Physiol. 2004;97(2):579–84.PubMedGoogle Scholar
  154. 154.
    Irving BA, Short KR, Nair KS, Stump CS. Nine days of intensive exercise training improves mitochondrial function but not insulin action in adult offspring of mothers with type 2 diabetes. J Clin Endocrinol Metab. 2011;96(7):E1137–41.PubMedPubMedCentralGoogle Scholar
  155. 155.
    Jeppesen J, Jordy AB, Sjøberg KA, Füllekrug J, Stahl A, Nybo L, et al. Enhanced fatty acid oxidation and FATP4 protein expression after endurance exercise training in human skeletal muscle. PLoS One. 2012;7(1):e29391.PubMedPubMedCentralGoogle Scholar
  156. 156.
    Liljedahl ME. Different responses of skeletal muscle following sprint training in men and women. Eur J Appl Physiol Occup Physiol. 1996;74(4):375–83.Google Scholar
  157. 157.
    Linossier MT, Dormois D, Perier C, Frey J, Geyssant A, Denis C. Enzyme adaptations of human skeletal muscle during bicycle short-sprint training and detraining. Acta Physiol Scand. 1997;161(4):439–45.PubMedGoogle Scholar
  158. 158.
    Little JP, Safdar A, Wilkin GP, Tarnopolsky MA, Gibala MJ. A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J Physiol. 2010;588(6):1011–22.PubMedPubMedCentralGoogle Scholar
  159. 159.
    Ma JK, Scribbans TD, Edgett BA, Boyd JC, Simpson CA, Little JP, et al. Extremely low-volume, high-intensity interval training improves exercise capacity and increases mitochondrial protein content in human skeletal muscle. Open J Mol Integr Physiol. 2013;3(4):202–10.Google Scholar
  160. 160.
    Macdougall JD, Hicks AL, Macdonald JR, McKelvie RS, Green HJ, Smith KM. Muscle performance and enzymatic adaptations to sprint interval training. J Appl Physiol. 1998;84(6):2138–42.PubMedGoogle Scholar
  161. 161.
    Masuda K, Okazaki K, Kuno S, Asano K, Shimojo H, Katsuta S. Endurance training under 2500-m hypoxia does not increase myoglobin content in human skeletal muscle. Eur J Appl Physiol. 2001;85(5):486–90.PubMedGoogle Scholar
  162. 162.
    McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ, Tarnopolsky MA. Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am J Physiol Endocrinol Metab. 2000;278(4):E580–7.PubMedGoogle Scholar
  163. 163.
    Messonnier L, Denis C, Prieur F, Lacour JR. Are the effects of training on fat metabolism involved in the improvement of performance during high-intensity exercise? Eur J Appl Physiol. 2005;94(4):434–41.PubMedGoogle Scholar
  164. 164.
    Østergård T, Andersen JL, Nyholm B, Lund S, Nair KS, Saltin B, et al. Impact of exercise training on insulin sensitivity, physical fitness, and muscle oxidative capacity in first-degree relatives of type 2 diabetic patients. Am J Physiol Endocrinol Metab. 2006;290(5):E998–1005.PubMedGoogle Scholar
  165. 165.
    Parra J, Cadefau JA, Rodas G, Amigó N, Cussö R. The distribution of rest periods affects performance and adaptations of energy metabolism induced by high-intensity training in human muscle. Acta Physiol Scand. 2000;169(2):157–65.PubMedGoogle Scholar
  166. 166.
    Perry CGR, Heigenhauser GJF, Bonen A, Spriet LL. High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl Physiol Nutr Metab. 2008;33(6):1112–23.PubMedGoogle Scholar
  167. 167.
    Putman CT, Jones NL, Hultman E, Hollidge-Horvat MG, Bonen A, McConachie DR, et al. Effects of short-term submaximal training in humans on muscle metabolism in exercise. Am J Physiol Endocrinol Metab. 1998;275(1 Pt 1):E132–9.Google Scholar
  168. 168.
    Rud B, Foss Ø, Krustrup P, Secher NH, Hallén J. One-legged endurance training: leg blood flow and oxygen extraction during cycling exercise. Acta Physiol. 2012;205(1):177–85.Google Scholar
  169. 169.
    Stannard SR, Buckley AJ, Edge JA, Thompson MW. Adaptations to skeletal muscle with endurance exercise training in the acutely fed versus overnight-fasted state. J Sci Med Sport. 2010;13(4):465–9.PubMedGoogle Scholar
  170. 170.
    Talanian JL, Galloway SDR, Heigenhauser GJF, Bonen A, Spriet LL. Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J Appl Physiol. 2007;102(4):1439–47.PubMedGoogle Scholar
  171. 171.
    Tiidus PM, Pushkarenko J, Houston ME. Lack of antioxidant adaptation to short-term aerobic training in human muscle. Am J Physiol Regul Integr Comp Physiol. 1996;271(4 Pt 2):R832–6.Google Scholar
  172. 172.
    Yfanti C, Åkerström T, Nielsen S, Nielsen AR, Mounier R, Mortensen OH, et al. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc. 2010;42(7):1388–95.PubMedGoogle Scholar
  173. 173.
    Zinner C, Morales-Alamo D, Ørtenblad N, Larsen FJ, Schiffer TA, Willis SJ, et al. The physiological mechanisms of performance enhancement with sprint interval training differ between the upper and lower extremities in humans. Front Physiol. 2016;30(7):426.Google Scholar
  174. 174.
    Hood MS, Little JP, Tarnopolsky MA, Myslik F, Gibala MJ. Low-volume interval training improves muscle oxidative capacity in sedentary adults. Med Sci Sports Exerc. 2011;43(10):1849–56.PubMedGoogle Scholar
  175. 175.
    Konopka AR, Suer MK, Wolff CA, Harber MP. 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(4):371–8.PubMedGoogle Scholar
  176. 176.
    Scalzo RL, Peltonen GL, Binns SE, Shankaran M, Giordano GR, Hartley DA, et al. Greater muscle protein synthesis and mitochondrial biogenesis in males compared with females during sprint interval training. FASEB J. 2014;28(6):2705–14.PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute for Health and SportVictoria UniversityMelbourneAustralia
  2. 2.Department of Diabetes, Central Clinical School, Faculty of Medicine, Nursing and Health SciencesMonash UniversityMelbourneAustralia
  3. 3.School of Medical and Health SciencesEdith Cowan UniversityJoondalupAustralia

Personalised recommendations