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Transcriptional modulation of mitochondria biogenesis pathway at and above critical speed in mice

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Abstract

High- or moderate-intensity endurance training leads to mitochondrial biogenesis via the peroxisome proliferator-activated receptor γ co-activator 1α (PGC-1α)/mitochondrial transcription factor A (Tfam) signaling pathway. Although this pathway is stimulated during acute exercise, the relationship between its activity and the intensity of the exercise has not been characterized. In animal studies, individualized running speeds have not previously been assessed. Here, we sought to determine whether this pathway was modulated after a bout of exhaustive exercise at different relative intensities (at and over critical speed (CS)). Our starting hypotheses were that (i) exercise-induced overexpression of PGC-1α in skeletal muscle falls at intensities above CS, and (ii) transcriptional activity of the mitochondrial biogenesis signaling cascade is intensity-sensitive at and above CS. To test these hypothesis, male Friend Virus B-Type mice were divided into a control group and three exercise groups (exercising at CS, peak velocity (vPeak) and 150 % CS, respectively). mRNA expression levels for genes involved in mitochondrial biogenesis signaling were analyzed in the quadriceps muscle. PGC-1α was overexpressed at all exercise intensities. We also identified that, PGC-1α mRNA expression was negatively correlated with exercise intensity and blood lactate levels but not with maximal oxygen uptake, vPeak, or CS. Expression of the PGC-1α co-activator peroxisome proliferator-activated receptor β was negatively correlated with the exercise intensity. In contrast, expression levels of Tfam were dissociated from exercise intensity. Our data indicate that at the intensities used in endurance training, the expression of mitochondrial biogenesis genes is finely modulated by the relative intensity of exhaustive exercise.

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Abbreviations

\( {\dot{\text{V}}\text{O}}_{{ 2 {\text{max}}}} \) :

Maximal oxygen uptake

PGC-1α:

Peroxisome proliferator-activated receptor-γ coactivator-1α

CS:

Critical speed

PPARβ:

Peroxisome proliferator-activated receptor beta

Tfam:

Mitochondrial transcription factor A

Sirt-1:

Sirtuin 1

VO2 :

Oxygen consumption

vPeak:

Peak velocity

[La] rest:

Blood lactate concentration at rest

C t :

Critical threshold

AMPK:

AMP-activated protein kinase

miRNA:

microRNA

References

  1. Nader GA (2006) Concurrent strength and endurance training: from molecules to man. Med Sci Sports Exerc 38(11):1965–1970. doi:10.1249/01.mss.0000233795.39282.33

    Article  PubMed  Google Scholar 

  2. Jacobs RA, Fluck D, Bonne TC, Burgi S, Christensen PM, Toigo M, Lundby C (2013) Improvements in exercise performance with high-intensity interval training coincide with an increase in skeletal muscle mitochondrial content and function. J Appl Physiol 115(6):785–793. doi:10.1152/japplphysiol.00445.2013

    Article  PubMed  Google Scholar 

  3. Ziemann E, Grzywacz T, Luszczyk M, Laskowski R, Olek RA, Gibson AL (2011) Aerobic and anaerobic changes with high-intensity interval training in active college-aged men. J Strength Cond Res 25(4):1104–1112. doi:10.1519/JSC.0b013e3181d09ec9

    Article  PubMed  Google Scholar 

  4. Astorino TA, Allen RP, Roberson DW, Jurancich M (2012) Effect of high-intensity interval training on cardiovascular function, VO2max, and muscular force. J Strength Cond Res 26(1):138–145. doi:10.1519/JSC.0b013e318218dd77

    Article  PubMed  Google Scholar 

  5. Tonkonogi M, Sahlin K (1997) Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status. Acta Physiol Scand 161(3):345–353. doi:10.1046/j.1365-201X.1997.00222.x

    Article  CAS  PubMed  Google Scholar 

  6. Burgomaster KA, Hughes SC, Heigenhauser GJ, Bradwell SN, Gibala MJ (2005) Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. J Appl Physiol 98(6):1985–1990. doi:10.1152/japplphysiol.01095.2004

    Article  PubMed  Google Scholar 

  7. Lanza IR, Nair KS (2010) Mitochondrial metabolic function assessed in vivo and in vitro. Curr Opin Clin Nutr Metab Care 13(5):511–517. doi:10.1097/MCO.0b013e32833cc93d

    Article  PubMed Central  PubMed  Google Scholar 

  8. Strasser B (2013) Physical activity in obesity and metabolic syndrome. Ann N Y Acad Sci 1281:141–159. doi:10.1111/j.1749-6632.2012.06785.x

    Article  PubMed Central  PubMed  Google Scholar 

  9. Landry BW, Driscoll SW (2012) Physical activity in children and adolescents. PM & R 4(11):826–832. doi:10.1016/j.pmrj.2012.09.585

    Article  Google Scholar 

  10. Bartlett JD, Joo CH, Jeong TS, Louhelainen J, Cochran AJ, Gibala MJ, Gregson W, Close GL, Drust B, Morton JP (2012) Matched work high-intensity interval and continuous running induce similar increases in PGC-1alpha mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle. J Appl Physiol 112(7):1135–1143. doi:10.1152/japplphysiol.01040.2011

    Article  CAS  PubMed  Google Scholar 

  11. Holloszy JO (2008) Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharmacol 59(Suppl 7):5–18

    PubMed  Google Scholar 

  12. Laursen PB (2010) Training for intense exercise performance: high-intensity or high-volume training? Scand J Med Sci Sports 20(Suppl 2):1–10. doi:10.1111/j.1600-0838.2010.01184.x

    Article  PubMed  Google Scholar 

  13. Uguccioni G, D’Souza D, Hood DA (2010) Regulation of PPARgamma coactivator-1alpha function and expression in muscle: effect of exercise. PPAR Res. doi:10.1155/2010/937123

    PubMed Central  PubMed  Google Scholar 

  14. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, Gobelet C, Meier CA, Bell DR, Kralli A, Giacobino JP, Deriaz O (2003) Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 52(12):2874–2881

    Article  CAS  PubMed  Google Scholar 

  15. Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M (2009) Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol 106(3):929–934. doi:10.1152/japplphysiol.90880.2008

    Article  CAS  PubMed  Google Scholar 

  16. Koves TR, Li P, An J, Akimoto T, Slentz D, Ilkayeva O, Dohm GL, Yan Z, Newgard CB, Muoio DM (2005) Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280(39):33588–33598. doi:10.1074/jbc.M507621200

    Article  CAS  PubMed  Google Scholar 

  17. Adser H, Wojtaszewski JF, Jakobsen AH, Kiilerich K, Hidalgo J, Pilegaard H (2011) Interleukin-6 modifies mRNA expression in mouse skeletal muscle. Acta Physiol 202(2):165–173. doi:10.1111/j.1748-1716.2011.02269.x

    Article  CAS  Google Scholar 

  18. Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, Barron N, McCaffrey N, Moyna NM, Zierath JR, O’Gorman DJ (2010) Exercise intensity-dependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol 588(10):1779–1790. doi:10.1113/jphysiol.2010.188011

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Serpiello FR, McKenna MJ, Bishop DJ, Aughey RJ, Caldow MK, Cameron-Smith D, Stepto NK (2012) Repeated sprints alter signaling related to mitochondrial biogenesis in humans. Med Sci Sports Exerc 44(5):827–834. doi:10.1249/MSS.0b013e318240067e

    Article  CAS  PubMed  Google Scholar 

  20. Tadaishi M, Miura S, Kai Y, Kawasaki E, Koshinaka K, Kawanaka K, Nagata J, Oishi Y, Ezaki O (2011) Effect of exercise intensity and AICAR on isoform-specific expressions of murine skeletal muscle PGC-1alpha mRNA: a role of beta(2)-adrenergic receptor activation. Am J Physiol Endocrinol Metab 300(2):E341–E349. doi:10.1152/ajpendo.00400.2010

    Article  CAS  PubMed  Google Scholar 

  21. Nordsborg NB, Lundby C, Leick L, Pilegaard H (2010) Relative workload determines exercise-induced increases in PGC-1alpha mRNA. Med Sci Sports Exerc 42(8):1477–1484. doi:10.1249/MSS.0b013e3181d2d21c

    Article  CAS  PubMed  Google Scholar 

  22. Billat VL, Mouisel E, Roblot N, Melki J (2005) Inter-and intrastrain variation in mouse critical running speed. J Appl Physiol 98(4):1258–1263. doi:10.1152/japplphysiol.00991.2004

    Article  PubMed  Google Scholar 

  23. Copp SW, Hirai DM, Musch TI, Poole DC (2010) Critical speed in the rat: implications for hindlimb muscle blood flow distribution and fibre recruitment. J Physiol 588(Pt 24):5077–5087. doi:10.1113/jphysiol.2010.198382

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Edgett BA, Foster WS, Hankinson PB, Simpson CA, Little JP, Graham RB, Gurd BJ (2013) Dissociation of increases in PGC-1alpha and its regulators from exercise intensity and muscle activation following acute exercise. PLoS One 8(8):e71623. doi:10.1371/journal.pone.0071623

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Psilander N, Wang L, Westergren J, Tonkonogi M, Sahlin K (2010) Mitochondrial gene expression in elite cyclists: effects of high-intensity interval exercise. Eur J Appl Physiol 110(3):597–606. doi:10.1007/s00421-010-1544-1

    Article  PubMed  Google Scholar 

  26. Wang L, Psilander N, Tonkonogi M, Ding S, Sahlin K (2009) Similar expression of oxidative genes after interval and continuous exercise. Med Sci Sports Exerc 41(12):2136–2144. doi:10.1249/MSS.0b013e3181abc1ec

    Article  CAS  PubMed  Google Scholar 

  27. Mathai AS, Bonen A, Benton CR, Robinson DL, Graham TE (2008) Rapid exercise-induced changes in PGC-1alpha mRNA and protein in human skeletal muscle. J Appl Physiol 105(4):1098–1105. doi:10.1152/japplphysiol.00847.2007

    Article  CAS  PubMed  Google Scholar 

  28. Le Moyec L, Mille-Hamard L, Triba MN, Breuneval C, Petot H, Billat VL (2012) NMR metabolomics for assessment of exercise effects with mouse biofluids. Anal Bioanal Chem 404(2):593–602. doi:10.1007/s00216-012-6165-6

    Article  PubMed  Google Scholar 

  29. Tobina T, Yoshioka K, Hirata A, Mori S, Kiyonaga A, Tanaka H (2011) Peroxisomal proliferator-activated receptor gamma co-activator-1 alpha gene expression increases above the lactate threshold in human skeletal muscle. J Sports Med Phys Fit 51(4):683–688

    CAS  Google Scholar 

  30. Russell AP, Hesselink MK, Lo SK, Schrauwen P (2005) Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J 19(8):986–988. doi:10.1096/fj.04-3168fje

    CAS  PubMed  Google Scholar 

  31. Watt MJ, Southgate RJ, Holmes AG, Febbraio MA (2004) Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) alpha and delta and PPAR coactivator 1alpha in human skeletal muscle, but not lipid regulatory genes. J Mol Endocrinol 33(2):533–544. doi:10.1677/jme.1.01499

    Article  CAS  PubMed  Google Scholar 

  32. Kang C, O’Moore KM, Dickman JR, Ji LL (2009) Exercise activation of muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling is redox sensitive. Free Radic Biol Med 47(10):1394–1400. doi:10.1016/j.freeradbiomed.2009.08.007

    Article  CAS  PubMed  Google Scholar 

  33. Spangenburg EE, Brown DA, Johnson MS, Moore RL (2009) Alterations in peroxisome proliferator-activated receptor mRNA expression in skeletal muscle after acute and repeated bouts of exercise. Mol Cell Biochem 332(1–2):225–231. doi:10.1007/s11010-009-0195-1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Norrbom J, Sundberg CJ, Ameln H, Kraus WE, Jansson E (1985) Gustafsson T (2004) PGC-1alpha mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J Appl Physiol 96(1):189–194. doi:10.1152/japplphysiol.00765.2003

    Article  Google Scholar 

  35. Wang L, Sahlin K (2012) The effect of continuous and interval exercise on PGC-1alpha and PDK4 mRNA in type I and type II fibres of human skeletal muscle. Acta Physiol 204(4):525–532. doi:10.1111/j.1748-1716.2011.02354.x

    Article  CAS  Google Scholar 

  36. Yeo WK, McGee SL, Carey AL, Paton CD, Garnham AP, Hargreaves M, Hawley JA (2010) Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen. Exp Physiol 95(2):351–358. doi:10.1113/expphysiol.2009.049353

    Article  CAS  PubMed  Google Scholar 

  37. Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355. doi:10.1038/nature02871

    Article  CAS  PubMed  Google Scholar 

  38. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  CAS  PubMed  Google Scholar 

  39. Aoi W, Naito Y, Mizushima K, Takanami Y, Kawai Y, Ichikawa H, Yoshikawa T (2010) The microRNA miR-696 regulates PGC-1alpha in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab 298(4):E799–E806. doi:10.1152/ajpendo.00448.2009

    Article  CAS  PubMed  Google Scholar 

  40. Yamamoto H, Morino K, Nishio Y, Ugi S, Yoshizaki T, Kashiwagi A, Maegawa H (2012) MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am J Physiol Endocrinol Metab 303(12):E1419–E1427. doi:10.1152/ajpendo.00097.2012

    Article  CAS  PubMed  Google Scholar 

  41. Bori Z, Zhao Z, Koltai E, Fatouros IG, Jamurtas AZ, Douroudos II, Terzis G, Chatzinikolaou A, Sovatzidis A, Draganidis D, Boldogh I, Radak Z (2012) The effects of aging, physical training, and a single bout of exercise on mitochondrial protein expression in human skeletal muscle. Exp Gerontol 47(6):417–424. doi:10.1016/j.exger.2012.03.004

    Article  CAS  PubMed  Google Scholar 

  42. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451(7181):1008–1012. doi:10.1038/nature06613

    Article  CAS  PubMed  Google Scholar 

  43. Scarpulla RC (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88(2):611–638. doi:10.1152/physrev.00025.2007

    Article  CAS  PubMed  Google Scholar 

  44. Dumke CL, Mark Davis J, Angela Murphy E, Nieman DC, Carmichael MD, Quindry JC, Travis Triplett N, Utter AC, Gross Gowin SJ, Henson DA, McAnulty SR, McAnulty LS (2009) Successive bouts of cycling stimulates genes associated with mitochondrial biogenesis. Eur J Appl Physiol 107(4):419–427. doi:10.1007/s00421-009-1143-1

    Article  CAS  PubMed  Google Scholar 

  45. Smith BK, Mukai K, Lally JS, Maher AC, Gurd BJ, Heigenhauser GJ, Spriet LL, Holloway GP (2013) AMP-activated protein kinase is required for exercise-induced peroxisome proliferator-activated receptor co-activator 1 translocation to subsarcolemmal mitochondria in skeletal muscle. J Physiol 591(Pt 6):1551–1561. doi:10.1113/jphysiol.2012.245944

    Article  PubMed Central  PubMed  Google Scholar 

  46. Stepto NK, Benziane B, Wadley GD, Chibalin AV, Canny BJ, Eynon N, McConell GK (2012) Short-term intensified cycle training alters acute and chronic responses of PGC1alpha and Cytochrome C oxidase IV to exercise in human skeletal muscle. PLoS One 7(12):e53080. doi:10.1371/journal.pone.0053080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Perry CG, Lally J, Holloway GP, Heigenhauser GJ, Bonen A, Spriet LL (2010) Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol 588(Pt 23):4795–4810. doi:10.1113/jphysiol.2010.199448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Pilegaard H, Saltin B, Neufer PD (2003) Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546(Pt 3):851–858

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA (2011) Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem 286(12):10605–10617. doi:10.1074/jbc.M110.211466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Daussin FN, Rasseneur L, Bouitbir J, Charles AL, Dufour SP, Geny B, Burelle Y, Richard R (2012) Different timing of changes in mitochondrial functions following endurance training. Med Sci Sports Exerc 44(2):217–224. doi:10.1249/MSS.0b013e31822b0bd4

    Article  CAS  PubMed  Google Scholar 

  51. Popov DV, Zinovkin RA, Karger EM, Tarasova OS, Vinogradova OL (2013) The effect of aerobic exercise on the expression of genes in skeletal muscles of trained and untrained men. Hum Physiol 39(2):190–195

    Article  CAS  Google Scholar 

  52. Ljubicic V, Joseph AM, Saleem A, Uguccioni G, Collu-Marchese M, Lai RY, Nguyen LM, Hood DA (2010) Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. Biochim Biophys Acta 3:223–234. doi:10.1016/j.bbagen.2009.07.031

    Article  Google Scholar 

  53. Slivka D, Heesch M, Dumke C, Cuddy J, Hailes W, Ruby B (2013) Effects of post-exercise recovery in a cold environment on muscle glycogen, PGC-1alpha, and downstream transcription factors. Cryobiology 66(3):250–255. doi:10.1016/j.cryobiol.2013.02.005

    Article  CAS  PubMed  Google Scholar 

  54. Bishop DJ, Granata C, Eynon N (2014) Can we optimise the exercise training prescription to maximise improvements in mitochondria function and content? Biochim Biophys Acta 4:1266–1275. doi:10.1016/j.bbagen.2013.10.012

    Article  Google Scholar 

  55. Mazzatti DJ, Smith MA, Oita RC, Lim FL, White AJ, Reid MB (2008) Muscle unloading-induced metabolic remodeling is associated with acute alterations in PPARdelta and UCP-3 expression. Physiol Genomics 34(2):149–161. doi:10.1152/physiolgenomics.00281.2007

    Article  CAS  PubMed  Google Scholar 

  56. de Lange P, Farina P, Moreno M, Ragni M, Lombardi A, Silvestri E, Burrone L, Lanni A, Goglia F (2006) Sequential changes in the signal transduction responses of skeletal muscle following food deprivation. FASEB J 20(14):2579–2581. doi:10.1096/fj.06-6025fje

    Article  PubMed  Google Scholar 

  57. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA (2005) Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J 19(11):1498–1500. doi:10.1096/fj.04-3149fje

    CAS  PubMed  Google Scholar 

  58. Ehrenborg E, Krook A (2009) Regulation of skeletal muscle physiology and metabolism by peroxisome proliferator-activated receptor delta. Pharmacol Rev 61(3):373–393. doi:10.1124/pr.109.001560

    Article  CAS  PubMed  Google Scholar 

  59. Nemoto S, Fergusson MM, Finkel T (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1alpha. J Biol Chem 280(16):16456–16460. doi:10.1074/jbc.M501485200

    Article  CAS  PubMed  Google Scholar 

  60. Aquilano K, Vigilanza P, Baldelli S, Pagliei B, Rotilio G, Ciriolo MR (2010) Peroxisome proliferator-activated receptor gamma co-activator 1alpha (PGC-1alpha) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem 285(28):21590–21599. doi:10.1074/jbc.M109.070169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Gurd BJ, Yoshida Y, McFarlan JT, Holloway GP, Moyes CD, Heigenhauser GJ, Spriet L, Bonen A (2011) Nuclear SIRT1 activity, but not protein content, regulates mitochondrial biogenesis in rat and human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 301(1):R67–R75. doi:10.1152/ajpregu.00417.2010

    Article  CAS  PubMed  Google Scholar 

  62. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J (2009) AMPK regulates energy expenditure by modulating NAD + metabolism and SIRT1 activity. Nature 458(7241):1056–1060. doi:10.1038/nature07813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Pardo PS, Mohamed JS, Lopez MA, Boriek AM (2011) Induction of Sirt1 by mechanical stretch of skeletal muscle through the early response factor EGR1 triggers an antioxidative response. J Biol Chem 286(4):2559–2566. doi:10.1074/jbc.M110.149153

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Handschin C, Spiegelman BM (2008) The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 454(7203):463–469. doi:10.1038/nature07206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Moflehi D, Kok LY, Tengku-Kamalden TF, Amri S (2012) Effect of single-session aerobic exercise with varying intensities on lipid peroxidation and muscle-damage markers in sedentary males. Glob J Health Sci 4(4):48–54. doi:10.5539/gjhs.v4n4p48

    PubMed  Google Scholar 

  66. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 282(1):194–199. doi:10.1074/jbc.M606116200

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. UBIAE, INSERM U902, Université Evry-Val d’Essonne, Bd Francois Mitterrand, Batiment Maupertuis, 91025, Evry, France

    L. Mille-Hamard, C. Breuneval & V. L. Billat

  2. C3M, INSERM 1065, Université Nice-Sophia-Antipolis, Nice, France

    A. S. Rousseau & P. Grimaldi

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  1. L. Mille-Hamard
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  2. C. Breuneval
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Correspondence to L. Mille-Hamard.

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Mille-Hamard, L., Breuneval, C., Rousseau, A.S. et al. Transcriptional modulation of mitochondria biogenesis pathway at and above critical speed in mice. Mol Cell Biochem 405, 223–232 (2015). https://doi.org/10.1007/s11010-015-2413-3

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