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Erschienen in: Sports Medicine 7/2018

19.04.2018 | Review Article

Principles of Exercise Prescription, and How They Influence Exercise-Induced Changes of Transcription Factors and Other Regulators of Mitochondrial Biogenesis

verfasst von: Cesare Granata, Nicholas A. Jamnick, David J. Bishop

Erschienen in: Sports Medicine | Ausgabe 7/2018

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Abstract

Physical inactivity represents the fourth leading risk factor for mortality, and it has been linked with a series of chronic disorders, the treatment of which absorbs ~ 85% of healthcare costs in developed countries. Conversely, physical activity promotes many health benefits; endurance exercise in particular represents a powerful stimulus to induce mitochondrial biogenesis, and it is routinely used to prevent and treat chronic metabolic disorders linked with sub-optimal mitochondrial characteristics. Given the importance of maintaining a healthy mitochondrial pool, it is vital to better characterize how manipulating the endurance exercise dose affects cellular mechanisms of exercise-induced mitochondrial biogenesis. Herein, we propose a definition of mitochondrial biogenesis and the techniques available to assess it, and we emphasize the importance of standardizing biopsy timing and the determination of relative exercise intensity when comparing different studies. We report an intensity-dependent regulation of exercise-induced increases in nuclear peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) protein content, nuclear phosphorylation of p53 (serine 15), and PGC-1α messenger RNA (mRNA), as well as training-induced increases in PGC-1α and p53 protein content. Despite evidence that PGC-1α protein content plateaus within a few exercise sessions, we demonstrate that greater training volumes induce further increases in PGC-1α (and p53) protein content, and that short-term reductions in training volume decrease the content of both proteins, suggesting training volume is still a factor affecting training-induced mitochondrial biogenesis. Finally, training-induced changes in mitochondrial transcription factor A (TFAM) protein content are regulated in a training volume-dependent manner and have been linked with training-induced changes in mitochondrial content.
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1
For interventions employing a mode of exercise for which power is not easily measurable (e.g., running or swimming), the same parameters can be determined, but velocity (v) is used instead of power.
 
Literatur
1.
Zurück zum Zitat Picard M, White K, Turnbull DM. Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study. J Appl Physiol. 2013;114(2):161–71.PubMedCrossRef Picard M, White K, Turnbull DM. Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: a quantitative three-dimensional electron microscopy study. J Appl Physiol. 2013;114(2):161–71.PubMedCrossRef
2.
Zurück zum Zitat Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol. 1993;264(2 33-2):C383–9.CrossRef Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol. 1993;264(2 33-2):C383–9.CrossRef
3.
Zurück zum Zitat Picard M, Shirihai OS, Gentil BJ, Burelle Y. Mitochondrial morphology transitions and functions: implications for retrograde signaling? Am J Physiol Regul Integr Comp Physiol. 2013;304(6):R393–406.PubMedPubMedCentralCrossRef Picard M, Shirihai OS, Gentil BJ, Burelle Y. Mitochondrial morphology transitions and functions: implications for retrograde signaling? Am J Physiol Regul Integr Comp Physiol. 2013;304(6):R393–406.PubMedPubMedCentralCrossRef
4.
Zurück zum Zitat Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev. 2006;27(7):728–35.PubMedCrossRef Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev. 2006;27(7):728–35.PubMedCrossRef
5.
Zurück zum Zitat Kroemer G, Petit P, Zamzami N, Vayssiere J, Mignotte B. The biochemistry of programmed cell death. FASEB J. 1995;9(13):1277–87.PubMedCrossRef Kroemer G, Petit P, Zamzami N, Vayssiere J, Mignotte B. The biochemistry of programmed cell death. FASEB J. 1995;9(13):1277–87.PubMedCrossRef
7.
Zurück zum Zitat Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120(4):483–95.PubMedCrossRef Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120(4):483–95.PubMedCrossRef
8.
Zurück zum Zitat Carter HN, Chen CC, Hood DA. Mitochondria, muscle health, and exercise with advancing age. Physiology. 2015;30(3):208–23.PubMedCrossRef Carter HN, Chen CC, Hood DA. Mitochondria, muscle health, and exercise with advancing age. Physiology. 2015;30(3):208–23.PubMedCrossRef
9.
Zurück zum Zitat Hesselink MK, Schrauwen-Hinderling V, Schrauwen P. Skeletal muscle mitochondria as a target to prevent or treat type 2 diabetes mellitus. Nat Rev Endocrinol. 2016;12(11):633–45.PubMedCrossRef Hesselink MK, Schrauwen-Hinderling V, Schrauwen P. Skeletal muscle mitochondria as a target to prevent or treat type 2 diabetes mellitus. Nat Rev Endocrinol. 2016;12(11):633–45.PubMedCrossRef
11.
Zurück zum Zitat 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 41-4):E580–7.PubMedCrossRef 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 41-4):E580–7.PubMedCrossRef
12.
Zurück zum Zitat Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE. Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy. J Appl Physiol. 2002;93(1):3–30.PubMedCrossRef Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE. Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy. J Appl Physiol. 2002;93(1):3–30.PubMedCrossRef
13.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
14.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
16.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
17.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
19.
Zurück zum Zitat 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.PubMed 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.PubMed
20.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
21.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
22.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
23.
Zurück zum Zitat WHO. Global health risks: mortality and burden of disease attributable to selected major risks (Geneva, Switzerland). Geneva: World Health Organization; 2009. WHO. Global health risks: mortality and burden of disease attributable to selected major risks (Geneva, Switzerland). Geneva: World Health Organization; 2009.
24.
Zurück zum Zitat Ding D, Lawson KD, Kolbe-Alexander TL, Finkelstein EA, Katzmarzyk PT, van Mechelen W, et al. The economic burden of physical inactivity: a global analysis of major non-communicable diseases. Lancet. 2016;388(10051):1311–24.PubMedCrossRef Ding D, Lawson KD, Kolbe-Alexander TL, Finkelstein EA, Katzmarzyk PT, van Mechelen W, et al. The economic burden of physical inactivity: a global analysis of major non-communicable diseases. Lancet. 2016;388(10051):1311–24.PubMedCrossRef
26.
Zurück zum Zitat Stepien KM, Heaton R, Rankin S, Murphy A, Bentley J, Sexton D, et al. Evidence of oxidative stress and secondary mitochondrial dysfunction in metabolic and non-metabolic disorders. J Clin Med. 2017;6(7):71.PubMedCentralCrossRef Stepien KM, Heaton R, Rankin S, Murphy A, Bentley J, Sexton D, et al. Evidence of oxidative stress and secondary mitochondrial dysfunction in metabolic and non-metabolic disorders. J Clin Med. 2017;6(7):71.PubMedCentralCrossRef
27.
Zurück zum Zitat Wang CH, Wang CC, Wei YH. Mitochondrial dysfunction in insulin insensitivity: implication of mitochondrial role in type 2 diabetes. Ann N Y Acad Sci. 2010;1201(1):157–65. Wang CH, Wang CC, Wei YH. Mitochondrial dysfunction in insulin insensitivity: implication of mitochondrial role in type 2 diabetes. Ann N Y Acad Sci. 2010;1201(1):157–65.
28.
Zurück zum Zitat Miller BF, Hamilton KL. A perspective on the determination of mitochondrial biogenesis. Am J Physiol Endocrinol Metab. 2012;302(5):E496–9.PubMedCrossRef Miller BF, Hamilton KL. A perspective on the determination of mitochondrial biogenesis. Am J Physiol Endocrinol Metab. 2012;302(5):E496–9.PubMedCrossRef
29.
Zurück zum Zitat Short KR. Measuring mitochondrial protein synthesis to assess biogenesis. Am J Physiol Endocrinol Metab. 2012;302(9):E1153–4.PubMedCrossRef Short KR. Measuring mitochondrial protein synthesis to assess biogenesis. Am J Physiol Endocrinol Metab. 2012;302(9):E1153–4.PubMedCrossRef
30.
Zurück zum Zitat Ryan MT, Hoogenraad NJ. Mitochondrial-nuclear communications. Annu Rev Biochem. 2007;76:701–22.PubMedCrossRef Ryan MT, Hoogenraad NJ. Mitochondrial-nuclear communications. Annu Rev Biochem. 2007;76:701–22.PubMedCrossRef
31.
Zurück zum Zitat Drake JC, Wilson RJ, Yan Z. Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle. FASEB J. 2015;30(1):13–22.PubMedCrossRefPubMedCentral Drake JC, Wilson RJ, Yan Z. Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle. FASEB J. 2015;30(1):13–22.PubMedCrossRefPubMedCentral
32.
Zurück zum Zitat Campello S, Strappazzon F, Cecconi F. Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta, Bioenerg. 2014;1837(4):451–60.CrossRef Campello S, Strappazzon F, Cecconi F. Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta, Bioenerg. 2014;1837(4):451–60.CrossRef
33.
Zurück zum Zitat Wasilewski M, Scorrano L. The changing shape of mitochondrial apoptosis. Trends Endocrinol Metab. 2009;20(6):287–94.PubMedCrossRef Wasilewski M, Scorrano L. The changing shape of mitochondrial apoptosis. Trends Endocrinol Metab. 2009;20(6):287–94.PubMedCrossRef
35.
Zurück zum Zitat Atherton PJ, Phillips BE, Wilkinson DJ. Exercise and regulation of protein metabolism. Prog Mol Biol Transl Sci. 2015;135:75–98.PubMedCrossRef Atherton PJ, Phillips BE, Wilkinson DJ. Exercise and regulation of protein metabolism. Prog Mol Biol Transl Sci. 2015;135:75–98.PubMedCrossRef
36.
Zurück zum Zitat Bishop DJ, Granata C, Eynon N. Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? Biochim Biophys Acta Gen Subj. 2014;1840(4):1266–75.CrossRef Bishop DJ, Granata C, Eynon N. Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? Biochim Biophys Acta Gen Subj. 2014;1840(4):1266–75.CrossRef
37.
Zurück zum Zitat Ritov VB, Menshikova EV, Kelley DE. Analysis of cardiolipin in human muscle biopsy. J Chromatogr B Biomed Sci Appl. 2006;831(1):63–71. Ritov VB, Menshikova EV, Kelley DE. Analysis of cardiolipin in human muscle biopsy. J Chromatogr B Biomed Sci Appl. 2006;831(1):63–71.
38.
Zurück zum Zitat Kraunsøe R, Boushel R, Hansen CN, Schjerling P, Qvortrup K, Støckel M, et al. Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity. J Physiol. 2010;588(12):2023–32.PubMedPubMedCentralCrossRef Kraunsøe R, Boushel R, Hansen CN, Schjerling P, Qvortrup K, Støckel M, et al. Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity. J Physiol. 2010;588(12):2023–32.PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
40.
Zurück zum Zitat Reichmann H, Hoppeler H, Mathieu-Costello O, Von Bergen F, Pette D. Biochemical and ultrastructural changes of skeletal muscle mitochondria after chronic electrical stimulation in rabbits. Pflügers Archiv. 1985;404(1):1–9.PubMedCrossRef Reichmann H, Hoppeler H, Mathieu-Costello O, Von Bergen F, Pette D. Biochemical and ultrastructural changes of skeletal muscle mitochondria after chronic electrical stimulation in rabbits. Pflügers Archiv. 1985;404(1):1–9.PubMedCrossRef
42.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
43.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
44.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
45.
Zurück zum Zitat Tonkonogi M, Sahlin K. Physical exercise and mitochondrial function in human skeletal muscle. Exerc Sport Sci Rev. 2002;30(3):129–37.PubMedCrossRef Tonkonogi M, Sahlin K. Physical exercise and mitochondrial function in human skeletal muscle. Exerc Sport Sci Rev. 2002;30(3):129–37.PubMedCrossRef
46.
47.
Zurück zum Zitat 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):18317.CrossRef 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):18317.CrossRef
48.
Zurück zum Zitat Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab. 2009;34(3):465–72.PubMedCrossRef Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab. 2009;34(3):465–72.PubMedCrossRef
49.
Zurück zum Zitat 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. 2016;121(2):597–600.PubMedCrossRef 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. 2016;121(2):597–600.PubMedCrossRef
50.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
51.
Zurück zum Zitat 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. 2016;121(2):601.PubMedCrossRef 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. 2016;121(2):601.PubMedCrossRef
52.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
53.
Zurück zum Zitat Seiler S, Tønnessen E. Intervals, thresholds, and long slow distance: the role of intensity and duration in endurance training. Sportscience. 2009;13:32–53. Seiler S, Tønnessen E. Intervals, thresholds, and long slow distance: the role of intensity and duration in endurance training. Sportscience. 2009;13:32–53.
54.
Zurück zum Zitat Astrand PO, Rodahl K. Textbook of work physiology. New York: McGraw Hill; 1986. Astrand PO, Rodahl K. Textbook of work physiology. New York: McGraw Hill; 1986.
55.
Zurück zum Zitat Bentley DJ, Newell J, Bishop D. Incremental exercise test design and analysis: Implications for performance diagnostics in endurance athletes. Sports Med. 2007;37(7):575–86.PubMedCrossRef Bentley DJ, Newell J, Bishop D. Incremental exercise test design and analysis: Implications for performance diagnostics in endurance athletes. Sports Med. 2007;37(7):575–86.PubMedCrossRef
56.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
57.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
58.
Zurück zum Zitat Weston KS, Wisløff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med. 2014;48(16):1227–34.PubMedCrossRef Weston KS, Wisløff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med. 2014;48(16):1227–34.PubMedCrossRef
59.
Zurück zum Zitat Girard O, Mendez-Villanueva A, Bishop D. Repeated-sprint ability—part I. Sports Med. 2011;41(8):673–94.PubMedCrossRef Girard O, Mendez-Villanueva A, Bishop D. Repeated-sprint ability—part I. Sports Med. 2011;41(8):673–94.PubMedCrossRef
60.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
61.
Zurück zum Zitat Rose AJ, Kiens B, Richter EA. Ca2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol. 2006;574(3):889–903.PubMedPubMedCentralCrossRef Rose AJ, Kiens B, Richter EA. Ca2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol. 2006;574(3):889–903.PubMedPubMedCentralCrossRef
62.
Zurück zum Zitat Lima TI, Araujo HN, Menezes ES, Sponton CH, Araújo MB, Bomfim LH, et al. Role of microRNAs on the regulation of mitochondrial biogenesis and insulin signaling in skeletal muscle. J Cell Physiol. 2017;232(5):958–66.PubMedCrossRef Lima TI, Araujo HN, Menezes ES, Sponton CH, Araújo MB, Bomfim LH, et al. Role of microRNAs on the regulation of mitochondrial biogenesis and insulin signaling in skeletal muscle. J Cell Physiol. 2017;232(5):958–66.PubMedCrossRef
63.
Zurück zum Zitat Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One. 2009;4(5):e5610.PubMedPubMedCentralCrossRef Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One. 2009;4(5):e5610.PubMedPubMedCentralCrossRef
64.
Zurück zum Zitat Baggish AL, Hale A, Weiner RB, Lewis GD, Systrom D, Wang F, et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol. 2011;589(16):3983–94.PubMedPubMedCentralCrossRef Baggish AL, Hale A, Weiner RB, Lewis GD, Systrom D, Wang F, et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol. 2011;589(16):3983–94.PubMedPubMedCentralCrossRef
65.
Zurück zum Zitat Russell AP, Lamon S, Boon H, Wada S, Güller I, Brown EL, et al. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J Physiol. 2013;591(18):4637–53.PubMedPubMedCentralCrossRef Russell AP, Lamon S, Boon H, Wada S, Güller I, Brown EL, et al. Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J Physiol. 2013;591(18):4637–53.PubMedPubMedCentralCrossRef
67.
Zurück zum Zitat Ling C, Rönn T. Epigenetic adaptation to regular exercise in humans. Drug Discovery Today. 2014;19(7):1015–8.PubMedCrossRef Ling C, Rönn T. Epigenetic adaptation to regular exercise in humans. Drug Discovery Today. 2014;19(7):1015–8.PubMedCrossRef
68.
Zurück zum Zitat Barres R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15(3):405–11.PubMedCrossRef Barres R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15(3):405–11.PubMedCrossRef
69.
Zurück zum Zitat Voisin S, Eynon N, Yan X, Bishop D. Exercise training and DNA methylation in humans. Acta Physiol. 2015;213(1):39–59.CrossRef Voisin S, Eynon N, Yan X, Bishop D. Exercise training and DNA methylation in humans. Acta Physiol. 2015;213(1):39–59.CrossRef
70.
Zurück zum Zitat Nitert MD, Dayeh T, Volkov P, Elgzyri T, Hall E, Nilsson E, et al. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes. 2012;61(12):3322–32.PubMedPubMedCentralCrossRef Nitert MD, Dayeh T, Volkov P, Elgzyri T, Hall E, Nilsson E, et al. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes. 2012;61(12):3322–32.PubMedPubMedCentralCrossRef
71.
Zurück zum Zitat Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162–84.PubMedCrossRef Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013;17(2):162–84.PubMedCrossRef
72.
Zurück zum Zitat McGinley C, Bishop DJ. Distinct protein and mRNA kinetics of skeletal muscle proton transporters following exercise can influence interpretation of adaptations to training. Exp Physiol. 2016;101(12):1565–80.PubMedCrossRef McGinley C, Bishop DJ. Distinct protein and mRNA kinetics of skeletal muscle proton transporters following exercise can influence interpretation of adaptations to training. Exp Physiol. 2016;101(12):1565–80.PubMedCrossRef
73.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
74.
Zurück zum Zitat Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159(4):738–49.PubMedCrossRef Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159(4):738–49.PubMedCrossRef
75.
Zurück zum Zitat 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.PubMed 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.PubMed
76.
Zurück zum Zitat Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr Rev. 2003;24(1):78–90.PubMedCrossRef Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr Rev. 2003;24(1):78–90.PubMedCrossRef
77.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
78.
Zurück zum Zitat Geng T, Li P, Okutsu M, Yin X, Kwek J, Zhang M, et al. PGC-1alpha plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle. Am J Physiol Cell Physiol. 2010;298(3):C572–9.PubMedCrossRef Geng T, Li P, Okutsu M, Yin X, Kwek J, Zhang M, et al. PGC-1alpha plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle. Am J Physiol Cell Physiol. 2010;298(3):C572–9.PubMedCrossRef
79.
Zurück zum Zitat Leick L, Wojtaszewski JFP, Johansen ST, Kiilerich K, Comes G, Hellsten Y, et al. PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2008;294(2):E463–74.PubMedCrossRef Leick L, Wojtaszewski JFP, Johansen ST, Kiilerich K, Comes G, Hellsten Y, et al. PGC-1α is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2008;294(2):E463–74.PubMedCrossRef
80.
81.
Zurück zum Zitat Jäger S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc Natl Acad Sci USA. 2007;104(29):12017–22.PubMedPubMedCentralCrossRef Jäger S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc Natl Acad Sci USA. 2007;104(29):12017–22.PubMedPubMedCentralCrossRef
82.
Zurück zum Zitat Bartlett JD, Joo CH, Jeong TS, Louhelainen J, Cochran AJ, Gibala MJ, et al. Matched work high-intensity interval and continuous running induce similar increases in PGC-1α mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle. J Appl Physiol. 2012;112(7):1135–43.PubMedCrossRef Bartlett JD, Joo CH, Jeong TS, Louhelainen J, Cochran AJ, Gibala MJ, et al. Matched work high-intensity interval and continuous running induce similar increases in PGC-1α mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle. J Appl Physiol. 2012;112(7):1135–43.PubMedCrossRef
83.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
84.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
85.
Zurück zum Zitat Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1α in human skeletal muscle. J Appl Physiol. 2009;106(3):929–34.PubMedCrossRef Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1α in human skeletal muscle. J Appl Physiol. 2009;106(3):929–34.PubMedCrossRef
86.
Zurück zum Zitat Little JP, Safdar A, Cermak N, Tarnopolsky MA, Gibala MJ. Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. Am J Physiol Endocrinol Metab. 2010;298(4):R912–7. Little JP, Safdar A, Cermak N, Tarnopolsky MA, Gibala MJ. Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. Am J Physiol Endocrinol Metab. 2010;298(4):R912–7.
87.
Zurück zum Zitat Brandt N, Gunnarsson TP, Hostrup M, Tybirk J, Nybo L, Pilegaard H, et al. Impact of adrenaline and metabolic stress on exercise-induced intracellular signaling and PGC-1α mRNA response in human skeletal muscle. Physiol Rep. 2016;4(14):12844.CrossRef Brandt N, Gunnarsson TP, Hostrup M, Tybirk J, Nybo L, Pilegaard H, et al. Impact of adrenaline and metabolic stress on exercise-induced intracellular signaling and PGC-1α mRNA response in human skeletal muscle. Physiol Rep. 2016;4(14):12844.CrossRef
88.
Zurück zum Zitat Aquilano K, Vigilanza P, Baldelli S, Pagliei B, Rotilio G, Ciriolo MR. Peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1 alpha) and sirtuin 1 (SIRT1) reside in mitochondria-possible direct function in mitochondrial biogenesis. J Biol Chem. 2010;285(28):21590–9.PubMedPubMedCentralCrossRef Aquilano K, Vigilanza P, Baldelli S, Pagliei B, Rotilio G, Ciriolo MR. Peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1 alpha) and sirtuin 1 (SIRT1) reside in mitochondria-possible direct function in mitochondrial biogenesis. J Biol Chem. 2010;285(28):21590–9.PubMedPubMedCentralCrossRef
89.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
90.
Zurück zum Zitat Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA. Exercise increases mitochondrial PGC-1α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem. 2011;286(12):10605–17.PubMedPubMedCentralCrossRef Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA. Exercise increases mitochondrial PGC-1α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem. 2011;286(12):10605–17.PubMedPubMedCentralCrossRef
91.
Zurück zum Zitat Heesch MW, Shute RJ, Kreiling JL, Slivka DR. Transcriptional control, but not subcellular location, of PGC-1α is altered following exercise in a hot environment. J Appl Physiol. 2016;121(3):741–9.PubMedPubMedCentralCrossRef Heesch MW, Shute RJ, Kreiling JL, Slivka DR. Transcriptional control, but not subcellular location, of PGC-1α is altered following exercise in a hot environment. J Appl Physiol. 2016;121(3):741–9.PubMedPubMedCentralCrossRef
92.
Zurück zum Zitat McGee SL, Hargreaves M. Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes. 2004;53(5):1208–14.PubMedCrossRef McGee SL, Hargreaves M. Exercise and myocyte enhancer factor 2 regulation in human skeletal muscle. Diabetes. 2004;53(5):1208–14.PubMedCrossRef
93.
Zurück zum Zitat Tachtsis B, Smiles W, Lane S, Hawley J, Camera DM. Acute endurance exercises induces nuclear p53 abundance in human skeletal muscle. Front Physiol. 2016;7:144.PubMedPubMedCentralCrossRef Tachtsis B, Smiles W, Lane S, Hawley J, Camera DM. Acute endurance exercises induces nuclear p53 abundance in human skeletal muscle. Front Physiol. 2016;7:144.PubMedPubMedCentralCrossRef
94.
Zurück zum Zitat Dumke CL, Davis JM, Murphy EA, Nieman DC, Carmichael MD, Quindry JC, et al. Successive bouts of cycling stimulates genes associated with mitochondrial biogenesis. Eur J Appl Physiol. 2009;107(4):419–27.PubMedCrossRef Dumke CL, Davis JM, Murphy EA, Nieman DC, Carmichael MD, Quindry JC, et al. Successive bouts of cycling stimulates genes associated with mitochondrial biogenesis. Eur J Appl Physiol. 2009;107(4):419–27.PubMedCrossRef
95.
Zurück zum Zitat Mathai AS, Bonen A, Benton CR, Robinson DL, Graham TE. Rapid exercise-induced changes in PGC-1α mRNA and protein in human skeletal muscle. J Appl Physiol. 2008;105(4):1098–105.PubMedCrossRef Mathai AS, Bonen A, Benton CR, Robinson DL, Graham TE. Rapid exercise-induced changes in PGC-1α mRNA and protein in human skeletal muscle. J Appl Physiol. 2008;105(4):1098–105.PubMedCrossRef
96.
Zurück zum Zitat Nordsborg NB, Lundby C, Leick L, Pilegaard H. Relative workload determines exercise-induced increases in PGC-1α mRNA. Med Sci Sports Exerc. 2010;42(8):1477–84.PubMedCrossRef Nordsborg NB, Lundby C, Leick L, Pilegaard H. Relative workload determines exercise-induced increases in PGC-1α mRNA. Med Sci Sports Exerc. 2010;42(8):1477–84.PubMedCrossRef
97.
Zurück zum Zitat Russell AP, Hesselink MKC, Lo SK, Schrauwen P. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 2005;19(8):986–8.PubMedCrossRef Russell AP, Hesselink MKC, Lo SK, Schrauwen P. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 2005;19(8):986–8.PubMedCrossRef
98.
Zurück zum Zitat Vissing K, McGee SL, Roepstorff C, Schjerling P, Hargreaves M, Kiens B. Effect of sex differences on human MEF2 regulation during endurance exercise. Am J Physiol Endocrinol Metab. 2008;294(2):E408–15.PubMedCrossRef Vissing K, McGee SL, Roepstorff C, Schjerling P, Hargreaves M, Kiens B. Effect of sex differences on human MEF2 regulation during endurance exercise. Am J Physiol Endocrinol Metab. 2008;294(2):E408–15.PubMedCrossRef
99.
Zurück zum Zitat Watt MJ, Southgate RJ, Holmes AG, Febbraio MA. Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) α and δ and PPAR coactivator 1α in human skeletal muscle, but not lipid regulatory genes. J Mol Endocrinol. 2004;33(2):533–44.PubMedCrossRef Watt MJ, Southgate RJ, Holmes AG, Febbraio MA. Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) α and δ and PPAR coactivator 1α in human skeletal muscle, but not lipid regulatory genes. J Mol Endocrinol. 2004;33(2):533–44.PubMedCrossRef
100.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
101.
Zurück zum Zitat Cluberton LJ, McGee SL, Murphy RM, Hargreaves M. Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression. J Appl Physiol. 2005;99(4):1359–63.PubMedCrossRef Cluberton LJ, McGee SL, Murphy RM, Hargreaves M. Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression. J Appl Physiol. 2005;99(4):1359–63.PubMedCrossRef
102.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
103.
Zurück zum Zitat Pilegaard H, Osada T, Andersen LT, Helge JW, Saltin B, Neufer PD. Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism. 2005;54(8):1048–55.PubMedCrossRef Pilegaard H, Osada T, Andersen LT, Helge JW, Saltin B, Neufer PD. Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism. 2005;54(8):1048–55.PubMedCrossRef
104.
Zurück zum Zitat Sriwijitkamol A, Coletta DK, Wajcberg E, Balbontin GB, Reyna SM, Barrientes J, et al. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes. 2007;56(3):836–48.PubMedCrossRef Sriwijitkamol A, Coletta DK, Wajcberg E, Balbontin GB, Reyna SM, Barrientes J, et al. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes. 2007;56(3):836–48.PubMedCrossRef
105.
Zurück zum Zitat Popov DV, Lysenko EA, Vepkhvadze TF, Kurochkina NS, Maknovskii PA, Vinogradova OL. Promoter-specific regulation of PPARGC1A gene expression in human skeletal muscle. J Mol Endocrinol. 2015;55(2):159–68.PubMedCrossRef Popov DV, Lysenko EA, Vepkhvadze TF, Kurochkina NS, Maknovskii PA, Vinogradova OL. Promoter-specific regulation of PPARGC1A gene expression in human skeletal muscle. J Mol Endocrinol. 2015;55(2):159–68.PubMedCrossRef
106.
Zurück zum Zitat Allan R, Sharples AP, Close GL, Drust B, Shepherd SO, Dutton J, et al. Postexercise cold water immersion modulates skeletal muscle PGC-1α mRNA expression in immersed and nonimmersed limbs: evidence of systemic regulation. J Appl Physiol. 2017;123(2):451–9.PubMedCrossRef Allan R, Sharples AP, Close GL, Drust B, Shepherd SO, Dutton J, et al. Postexercise cold water immersion modulates skeletal muscle PGC-1α mRNA expression in immersed and nonimmersed limbs: evidence of systemic regulation. J Appl Physiol. 2017;123(2):451–9.PubMedCrossRef
107.
Zurück zum Zitat Broatch JR, Petersen A, Bishop DJ. Cold-water immersion following sprint interval training does not alter endurance signaling pathways or training adaptations in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2017;313(4):R372–84.PubMedCrossRef Broatch JR, Petersen A, Bishop DJ. Cold-water immersion following sprint interval training does not alter endurance signaling pathways or training adaptations in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2017;313(4):R372–84.PubMedCrossRef
108.
Zurück zum Zitat Joo CH, Allan R, Drust B, Close GL, Jeong TS, Bartlett JD, et al. Passive and post-exercise cold-water immersion augments PGC-1alpha and VEGF expression in human skeletal muscle. Eur J Appl Physiol. 2016;116(11–12):2315–26.PubMedPubMedCentralCrossRef Joo CH, Allan R, Drust B, Close GL, Jeong TS, Bartlett JD, et al. Passive and post-exercise cold-water immersion augments PGC-1alpha and VEGF expression in human skeletal muscle. Eur J Appl Physiol. 2016;116(11–12):2315–26.PubMedPubMedCentralCrossRef
109.
Zurück zum Zitat 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):e74092.CrossRef 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):e74092.CrossRef
110.
Zurück zum Zitat Leick L, Plomgaard P, Grønløkke L, Al-Abaiji F, Wojtaszewski JFP, Pilegaard H. Endurance exercise induces mRNA expression of oxidative enzymes in human skeletal muscle late in recovery. Scand J Med Sci Sports. 2010;20(4):593–9.PubMedCrossRef Leick L, Plomgaard P, Grønløkke L, Al-Abaiji F, Wojtaszewski JFP, Pilegaard H. Endurance exercise induces mRNA expression of oxidative enzymes in human skeletal muscle late in recovery. Scand J Med Sci Sports. 2010;20(4):593–9.PubMedCrossRef
111.
Zurück zum Zitat Edgett BA, Foster WS, Hankinson PB, Simpson CA, Little JP, Graham RB, et al. Dissociation of increases in PGC-1α and its regulators from exercise intensity and muscle activation following acute exercise. PLoS One. 2013;8(8):e71623.PubMedPubMedCentralCrossRef Edgett BA, Foster WS, Hankinson PB, Simpson CA, Little JP, Graham RB, et al. Dissociation of increases in PGC-1α and its regulators from exercise intensity and muscle activation following acute exercise. PLoS One. 2013;8(8):e71623.PubMedPubMedCentralCrossRef
112.
Zurück zum Zitat Wang L, Psilander N, Tonkonogi M, Ding S, Sahlin K. Similar expression of oxidative genes after interval and continuous exercise. Med Sci Sports Exerc. 2009;41(12):2136–44.PubMedCrossRef Wang L, Psilander N, Tonkonogi M, Ding S, Sahlin K. Similar expression of oxidative genes after interval and continuous exercise. Med Sci Sports Exerc. 2009;41(12):2136–44.PubMedCrossRef
113.
Zurück zum Zitat Popov D, Zinovkin R, Karger E, Tarasova O, Vinogradova O. Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle. J Sports Med Phys Fitness. 2014;54(3):362–9.PubMed Popov D, Zinovkin R, Karger E, Tarasova O, Vinogradova O. Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle. J Sports Med Phys Fitness. 2014;54(3):362–9.PubMed
114.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
115.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
116.
Zurück zum Zitat Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, et al. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J. 2006;20(1):190–2.PubMedCrossRef Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, et al. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J. 2006;20(1):190–2.PubMedCrossRef
117.
Zurück zum Zitat De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, et al. Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab. 2008;294(3):E607–14.PubMedCrossRef De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, et al. Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab. 2008;294(3):E607–14.PubMedCrossRef
118.
Zurück zum Zitat Edgett BA, Bonafiglia JT, Baechler BL, Quadrilatero J, Gurd BJ. The effect of acute and chronic sprint-interval training on LRP130, SIRT3, and PGC-1α expression in human skeletal muscle. Physiol Rep. 2016;4(17):e12879.PubMedPubMedCentralCrossRef Edgett BA, Bonafiglia JT, Baechler BL, Quadrilatero J, Gurd BJ. The effect of acute and chronic sprint-interval training on LRP130, SIRT3, and PGC-1α expression in human skeletal muscle. Physiol Rep. 2016;4(17):e12879.PubMedPubMedCentralCrossRef
119.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
120.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
121.
Zurück zum Zitat 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.PubMedPubMedCentral 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.PubMedPubMedCentral
122.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
123.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
124.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
125.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
126.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
127.
Zurück zum Zitat 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.PubMedCrossRef 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.PubMedCrossRef
128.
Zurück zum Zitat 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
129.
Zurück zum Zitat Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ. 2006;13(6):1027–36.PubMedCrossRef Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ. 2006;13(6):1027–36.PubMedCrossRef
130.
131.
132.
Zurück zum Zitat Saleem A, Carter HN, Hood DA. P53 is necessary for the adaptive changes in cellular milieu subsequent to an acute bout of endurance exercise. Am J Physiol Cell Physiol. 2014;306(3):C241–9.PubMedCrossRef Saleem A, Carter HN, Hood DA. P53 is necessary for the adaptive changes in cellular milieu subsequent to an acute bout of endurance exercise. Am J Physiol Cell Physiol. 2014;306(3):C241–9.PubMedCrossRef
133.
Zurück zum Zitat Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, et al. p53 regulates mitochondrial respiration. Science. 2006;312(5780):1650–3.PubMedCrossRef Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, et al. p53 regulates mitochondrial respiration. Science. 2006;312(5780):1650–3.PubMedCrossRef
134.
Zurück zum Zitat Park JY, Wang PY, Matsumoto T, Sung HJ, Ma W, Choi JW, et al. P53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res. 2009;105(7):705–12.PubMedPubMedCentralCrossRef Park JY, Wang PY, Matsumoto T, Sung HJ, Ma W, Choi JW, et al. P53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res. 2009;105(7):705–12.PubMedPubMedCentralCrossRef
135.
Zurück zum Zitat Saleem A, Adhihetty PJ, Hood DA. Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol Genomics. 2009;37(1):58–66.PubMedCrossRef Saleem A, Adhihetty PJ, Hood DA. Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol Genomics. 2009;37(1):58–66.PubMedCrossRef
136.
Zurück zum Zitat Bergeaud M, Mathieu L, Guillaume A, Moll UM, Mignotte B, Le Floch N, et al. Mitochondrial p53 mediates a transcription-independent regulation of cell respiration and interacts with the mitochondrial F1F0-ATP synthase. Cell Cycle. 2013;12(17):3781–93.CrossRef Bergeaud M, Mathieu L, Guillaume A, Moll UM, Mignotte B, Le Floch N, et al. Mitochondrial p53 mediates a transcription-independent regulation of cell respiration and interacts with the mitochondrial F1F0-ATP synthase. Cell Cycle. 2013;12(17):3781–93.CrossRef
137.
Zurück zum Zitat Stambolsky P, Weisz L, Shats I, Klein Y, Goldfinger N, Oren M, et al. Regulation of AIF expression by p53. Cell Death Differ. 2006;13(12):2140–9.PubMedCrossRef Stambolsky P, Weisz L, Shats I, Klein Y, Goldfinger N, Oren M, et al. Regulation of AIF expression by p53. Cell Death Differ. 2006;13(12):2140–9.PubMedCrossRef
138.
Zurück zum Zitat Vahsen N, Candé C, Brière JJ, Bénit P, Joza N, Larochette N, et al. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004;23(23):4679–89.PubMedPubMedCentralCrossRef Vahsen N, Candé C, Brière JJ, Bénit P, Joza N, Larochette N, et al. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004;23(23):4679–89.PubMedPubMedCentralCrossRef
139.
Zurück zum Zitat Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genetics. 2010;6(1):e1000795.PubMedPubMedCentralCrossRef Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genetics. 2010;6(1):e1000795.PubMedPubMedCentralCrossRef
140.
Zurück zum Zitat Pich S, Bach D, Briones P, Liesa M, Camps M, Testar X, et al. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet. 2005;14(11):1405–15.PubMedCrossRef Pich S, Bach D, Briones P, Liesa M, Camps M, Testar X, et al. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet. 2005;14(11):1405–15.PubMedCrossRef
141.
Zurück zum Zitat Wang W, Cheng X, Lu J, Wei J, Fu G, Zhu F, et al. Mitofusin-2 is a novel direct target of p53. Biochem Biophys Res Commun. 2010;400(4):587–92.PubMedCrossRef Wang W, Cheng X, Lu J, Wei J, Fu G, Zhu F, et al. Mitofusin-2 is a novel direct target of p53. Biochem Biophys Res Commun. 2010;400(4):587–92.PubMedCrossRef
142.
Zurück zum Zitat Irrcher I, Ljubicic V, Kirwan AF, Hood DA. AMP-activated protein kinase-regulated activation of the PGC-1α promoter in skeletal muscle cells. PLoS One. 2008;3(10):e3614.PubMedPubMedCentralCrossRef Irrcher I, Ljubicic V, Kirwan AF, Hood DA. AMP-activated protein kinase-regulated activation of the PGC-1α promoter in skeletal muscle cells. PLoS One. 2008;3(10):e3614.PubMedPubMedCentralCrossRef
143.
Zurück zum Zitat Bartlett JD, Close GL, Drust B, Morton JP. The emerging role of p53 in exercise metabolism. Sports Med. 2014;44(3):303–9.PubMedCrossRef Bartlett JD, Close GL, Drust B, Morton JP. The emerging role of p53 in exercise metabolism. Sports Med. 2014;44(3):303–9.PubMedCrossRef
144.
Zurück zum Zitat Stocks B, Dent JR, Joanisse S, McCurdy CE, Philp A. Skeletal muscle fibre-specific knockout of p53 does not reduce mitochondrial content or enzyme activity. Front Physiol. 2017;8:941.PubMedPubMedCentralCrossRef Stocks B, Dent JR, Joanisse S, McCurdy CE, Philp A. Skeletal muscle fibre-specific knockout of p53 does not reduce mitochondrial content or enzyme activity. Front Physiol. 2017;8:941.PubMedPubMedCentralCrossRef
145.
Zurück zum Zitat Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 1997;91(3):325–34.PubMedCrossRef Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 1997;91(3):325–34.PubMedCrossRef
146.
Zurück zum Zitat Marchenko ND, Hanel W, Li D, Becker K, Reich N, Moll UM. Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-α3 binding. Cell Death Differ. 2010;17(2):255–67.PubMedCrossRef Marchenko ND, Hanel W, Li D, Becker K, Reich N, Moll UM. Stress-mediated nuclear stabilization of p53 is regulated by ubiquitination and importin-α3 binding. Cell Death Differ. 2010;17(2):255–67.PubMedCrossRef
147.
Zurück zum Zitat Saleem A, Hood DA. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53-tfam-mitochondrial DNA complex in skeletal muscle. J Physiol. 2013;591(14):3625–36.PubMedPubMedCentralCrossRef Saleem A, Hood DA. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondria and promotes a p53-tfam-mitochondrial DNA complex in skeletal muscle. J Physiol. 2013;591(14):3625–36.PubMedPubMedCentralCrossRef
148.
Zurück zum Zitat Zhuang J, Kamp WM, Li J, Liu C, Kang J-G, P-y Wang, 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. 2016;291(48):24819–27.PubMedPubMedCentralCrossRef Zhuang J, Kamp WM, Li J, Liu C, Kang J-G, P-y Wang, 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. 2016;291(48):24819–27.PubMedPubMedCentralCrossRef
149.
Zurück zum Zitat Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, Esser KA. Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol. 2002;545(1):27–41.PubMedPubMedCentralCrossRef Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, Esser KA. Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol. 2002;545(1):27–41.PubMedPubMedCentralCrossRef
150.
Zurück zum Zitat Philp A, Schenk S. Unraveling the complexities of sirt1-mediated mitochondrial regulation in skeletal muscle. Exerc Sport Sci Rev. 2013;41(3):174–81.PubMedPubMedCentralCrossRef Philp A, Schenk S. Unraveling the complexities of sirt1-mediated mitochondrial regulation in skeletal muscle. Exerc Sport Sci Rev. 2013;41(3):174–81.PubMedPubMedCentralCrossRef
151.
Zurück zum Zitat Bartlett JD, Louhelainen J, Iqbal Z, Cochran AJ, Gibala MJ, Gregson W, et al. Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: implications for mitochondrial biogenesis. Am J Physiol Regul Integr Comp Physiol. 2013;304(6):R450–8.PubMedCrossRef Bartlett JD, Louhelainen J, Iqbal Z, Cochran AJ, Gibala MJ, Gregson W, et al. Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: implications for mitochondrial biogenesis. Am J Physiol Regul Integr Comp Physiol. 2013;304(6):R450–8.PubMedCrossRef
152.
Zurück zum Zitat Hammond KM, Impey SG, Currell K, Mitchell N, Shepherd SO, Jeromson S, et al. Postexercise high-fat feeding suppresses p70S6K1 activity in human skeletal muscle. Med Sci Sports Exerc. 2016;48(11):2108–17.PubMedCrossRef Hammond KM, Impey SG, Currell K, Mitchell N, Shepherd SO, Jeromson S, et al. Postexercise high-fat feeding suppresses p70S6K1 activity in human skeletal muscle. Med Sci Sports Exerc. 2016;48(11):2108–17.PubMedCrossRef
153.
Zurück zum Zitat Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta Gene Struct Express. 2002;1576(1–2):1–14.CrossRef Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta Gene Struct Express. 2002;1576(1–2):1–14.CrossRef
154.
155.
Zurück zum Zitat Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.PubMedCrossRef Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115–24.PubMedCrossRef
156.
Zurück zum Zitat Pilegaard H, Saltin B, Neufer DP. Exercise induces transient transcriptional activation of the PGC-1α gene in human skeletal muscle. J Physiol. 2003;546(3):851–8.PubMedPubMedCentralCrossRef Pilegaard H, Saltin B, Neufer DP. Exercise induces transient transcriptional activation of the PGC-1α gene in human skeletal muscle. J Physiol. 2003;546(3):851–8.PubMedPubMedCentralCrossRef
157.
Zurück zum Zitat Norrbom J, Sundberg CJ, Ameln H, Kraus WE, Jansson E, Gustafsson T. PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J Appl Physiol. 2004;96(1):189–94.PubMedCrossRef Norrbom J, Sundberg CJ, Ameln H, Kraus WE, Jansson E, Gustafsson T. PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J Appl Physiol. 2004;96(1):189–94.PubMedCrossRef
158.
Zurück zum Zitat Slivka D, Heesch M, Dumke C, Cuddy J, Hailes W, Ruby B. Effects of post-exercise recovery in a cold environment on muscle glycogen, PGC-1 alpha, and downstream transcription factors. Cryobiology. 2013;66(3):250–5.PubMedCrossRef Slivka D, Heesch M, Dumke C, Cuddy J, Hailes W, Ruby B. Effects of post-exercise recovery in a cold environment on muscle glycogen, PGC-1 alpha, and downstream transcription factors. Cryobiology. 2013;66(3):250–5.PubMedCrossRef
159.
Zurück zum Zitat Jensen L, Gejl KD, Ørtenblad N, Nielsen JL, Bech RD, Nygaard T, et al. Carbohydrate restricted recovery from long term endurance exercise does not affect gene responses involved in mitochondrial biogenesis in highly trained athletes. Physiol Rep. 2015;3(2):e12184.PubMedPubMedCentralCrossRef Jensen L, Gejl KD, Ørtenblad N, Nielsen JL, Bech RD, Nygaard T, et al. Carbohydrate restricted recovery from long term endurance exercise does not affect gene responses involved in mitochondrial biogenesis in highly trained athletes. Physiol Rep. 2015;3(2):e12184.PubMedPubMedCentralCrossRef
160.
Zurück zum Zitat Mendham AE, Duffield R, Coutts AJ, Marino F, Boyko A, Bishop DJ. Rugby-specific small-sided games training is an effective alternative to stationary cycling at reducing clinical risk factors associated with the development of type 2 diabetes: A randomized, controlled trial. PLoS One. 2015;10(6):e0127548.PubMedPubMedCentralCrossRef Mendham AE, Duffield R, Coutts AJ, Marino F, Boyko A, Bishop DJ. Rugby-specific small-sided games training is an effective alternative to stationary cycling at reducing clinical risk factors associated with the development of type 2 diabetes: A randomized, controlled trial. PLoS One. 2015;10(6):e0127548.PubMedPubMedCentralCrossRef
161.
Zurück zum Zitat Psilander N, Frank P, Flockhart M, Sahlin K. Exercise with low glycogen increases PGC-1α gene expression in human skeletal muscle. Eur J Appl Physiol. 2013;113(4):951–63.PubMedCrossRef Psilander N, Frank P, Flockhart M, Sahlin K. Exercise with low glycogen increases PGC-1α gene expression in human skeletal muscle. Eur J Appl Physiol. 2013;113(4):951–63.PubMedCrossRef
162.
Zurück zum Zitat Psilander N, Wang L, Westergren J, Tonkonogi M, Sahlin K. Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol. 2010;110(3):607.CrossRef Psilander N, Wang L, Westergren J, Tonkonogi M, Sahlin K. Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol. 2010;110(3):607.CrossRef
163.
Zurück zum Zitat Montoya J, Perez-Martos A, Garstka HL, Wiesner RJ. Regulation of mitochondrial transcription by mitochondrial transcription factor A. Mol Cell Biochem. 1997;174(1–2):227–30.PubMedCrossRef Montoya J, Perez-Martos A, Garstka HL, Wiesner RJ. Regulation of mitochondrial transcription by mitochondrial transcription factor A. Mol Cell Biochem. 1997;174(1–2):227–30.PubMedCrossRef
164.
Zurück zum Zitat Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998;18(3):231–6.PubMedCrossRef Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998;18(3):231–6.PubMedCrossRef
165.
Zurück zum Zitat Gordon JW, Rungi AA, Inagaki H, Hood DA. Selected contribution: Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J Appl Physiol. 2001;90(1):389–96.PubMedCrossRef Gordon JW, Rungi AA, Inagaki H, Hood DA. Selected contribution: Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J Appl Physiol. 2001;90(1):389–96.PubMedCrossRef
166.
Zurück zum Zitat Popov DV, Zinovkin RA, Karger EM, Tarasova OS, Vinogradova OL. The effect of aerobic exercise on the expression of genes in skeletal muscles of trained and untrained men. Hum Physiol. 2013;39(2):190–5.CrossRef Popov DV, Zinovkin RA, Karger EM, Tarasova OS, Vinogradova OL. The effect of aerobic exercise on the expression of genes in skeletal muscles of trained and untrained men. Hum Physiol. 2013;39(2):190–5.CrossRef
167.
Zurück zum Zitat Bengtsson J, Gustafsson T, Widegren U, Jansson E, Sundberg CJ. Mitochondrial transcription factor A and respiratory complex IV increase in response to exercise training in humans. Pflugers Arch. 2001;443(1):61–6.PubMedCrossRef Bengtsson J, Gustafsson T, Widegren U, Jansson E, Sundberg CJ. Mitochondrial transcription factor A and respiratory complex IV increase in response to exercise training in humans. Pflugers Arch. 2001;443(1):61–6.PubMedCrossRef
168.
Zurück zum Zitat Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 2005;19(11):1498–500.PubMedCrossRef Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 2005;19(11):1498–500.PubMedCrossRef
169.
Zurück zum Zitat Metcalfe R, Koumanov F, Ruffino J, Stokes K, Holman G, Thompson D, et al. Physiological and molecular responses to an acute bout of reduced-exertion high-intensity interval training (REHIT). Eur J Appl Physiol. 2015;115(11):2321–34.PubMedCrossRef Metcalfe R, Koumanov F, Ruffino J, Stokes K, Holman G, Thompson D, et al. Physiological and molecular responses to an acute bout of reduced-exertion high-intensity interval training (REHIT). Eur J Appl Physiol. 2015;115(11):2321–34.PubMedCrossRef
170.
Zurück zum Zitat Slivka DR, Dumke CL, Tucker TJ, Cuddy JS, Ruby B. Human mRNA response to exercise and temperature. Int J Sports Med. 2012;33(2):94–100.PubMedCrossRef Slivka DR, Dumke CL, Tucker TJ, Cuddy JS, Ruby B. Human mRNA response to exercise and temperature. Int J Sports Med. 2012;33(2):94–100.PubMedCrossRef
171.
Zurück zum Zitat Slivka DR, Heesch MWS, Dumke CL, Cuddy JS, Hailes WS, Ruby BC. Human skeletal muscle mRNA response to a single hypoxic exercise bout. Wilderness Environ Med. 2014;25(4):462–5.PubMedCrossRef Slivka DR, Heesch MWS, Dumke CL, Cuddy JS, Hailes WS, Ruby BC. Human skeletal muscle mRNA response to a single hypoxic exercise bout. Wilderness Environ Med. 2014;25(4):462–5.PubMedCrossRef
Metadaten
Titel
Principles of Exercise Prescription, and How They Influence Exercise-Induced Changes of Transcription Factors and Other Regulators of Mitochondrial Biogenesis
verfasst von
Cesare Granata
Nicholas A. Jamnick
David J. Bishop
Publikationsdatum
19.04.2018
Verlag
Springer International Publishing
Erschienen in
Sports Medicine / Ausgabe 7/2018
Print ISSN: 0112-1642
Elektronische ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-018-0894-4

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