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Endurance training modulates the muscular transcriptome response to acute exercise

  • Skeletal Muscle
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Abstract

We hypothesized that in untrained individuals (n=6) a single bout of ergometer endurance exercise provokes a concerted response of muscle transcripts towards a slow-oxidative muscle phenotype over a 24-h period. We further hypothesized this response during recovery to be attenuated after six weeks of endurance training. We monitored the expression profile of 220 selected transcripts in muscle biopsies before as well as 1, 8, and 24 h after a 30-min near-maximal bout of exercise. The generalized gene response of untrained vastus lateralis muscle peaked after 8 h of recovery (P=0.001). It involved multiple transcripts of oxidative metabolism and glycolysis. Angiogenic and cell regulatory transcripts were transiently reduced after 1 h independent of the training state. In the trained state, the induction of most transcripts 8 h after exercise was less pronounced despite a moderately higher relative exercise intensity, partially because of increased steady-state mRNA concentration, and the level of metabolic and extracellular RNAs was reduced during recovery from exercise. Our data suggest that the general response of the transcriptome for regulatory and metabolic processes is different in the trained state. Thus, the response is specifically modified with repeated bouts of endurance exercise during which muscle adjustments are established.

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References

  1. Andersen P, Henriksson J (1977) Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol 270:677–690

    PubMed  Google Scholar 

  2. Bergstrom J, Hermansen L, Hultman E, Saltin B (1967) Diet, muscle glycogen and physical performance. Acta Physiol Scand 71:140–150

    PubMed  Google Scholar 

  3. Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA, Adams GR (2005) Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98:482–488

    PubMed  Google Scholar 

  4. Booth FW, Baldwin KM (1996) Muscle plasticity: energy demanding and supply processes, Sect 12, Chap 24. In: Rowell LB, Shepherd JT (eds) Handbook of physiology. Oxford University Press, New York, pp 1075–1123

  5. Brown MD, Hudlicka O (2003) Modulation of physiological angiogenesis in skeletal muscle by mechanical forces: involvement of VEGF and metalloproteinases. Angiogenesis 6:1–14

    Article  PubMed  Google Scholar 

  6. Carter SL, Rennie CD, Hamilton SJ, Tarnopolsky (2001) Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol 79:386–392

    Article  PubMed  Google Scholar 

  7. Dapp C, Schmutz S, Hoppeler H, Fluck M (2004) Transcriptional reprogramming and ultrastructure during atrophy and recovery of mouse soleus muscle. Physiol Genomics 20:97–107

    Article  PubMed  Google Scholar 

  8. Denis C, Chatard JC, Dormois D, Linossier MT, Geyssant A, Lacour JR (1986) Effects of endurance training on capillary supply of human skeletal muscle on two age groups (20 and 60 years). J Physiol (Paris) 81:379–383

    Google Scholar 

  9. Fischer CP, Plomgaard P, Hansen AK, Pilegaard H, Saltin B, Pedersen BK (2004) Endurance training reduces the contraction-induced interleukin-6 mRNA expression in human skeletal muscle. Am J Physiol 287:E1189–E1194

    Google Scholar 

  10. Fluck M (2004) Exercise-modulated mitochondrial phenotype; sensors and gene regulation. J Muscle Res Cell Motil 25:235–237

    Article  PubMed  Google Scholar 

  11. Fluck M, Chiquet M, Schmutz S, Mayet-Sornay MH, Desplanches D (2003) Reloading of atrophied rat soleus muscle induces tenascin-C expression around damaged muscle fibers. Am J Physiol 284:R792–R801

    Google Scholar 

  12. Fluck M, Hoppeler H (2003) Molecular basis of skeletal muscle plasticity—from gene to form and function. Rev Physiol Biochem Pharmacol 146:159–216

    PubMed  Google Scholar 

  13. Hood DA (2001) Invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90:1137–1157

    PubMed  Google Scholar 

  14. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320–327

    PubMed  Google Scholar 

  15. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R (1985) Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch 403:369–376

    Article  PubMed  Google Scholar 

  16. Ingjer F (1979) Capillary supply and mitochondrial content of different skeletal muscle fiber types in untrained and endurance-trained men. A histochemical and ultrastructural study. Eur J Appl Physiol Occup Physiol 40:197–209

    Article  PubMed  Google Scholar 

  17. Kraniou Y, Cameron-Smith D, Misso M, Collier G, Hargreaves M (2000) Effects of exercise on GLUT-4 and glycogenin gene expression in human skeletal muscle. J Appl Physiol 88:794–796

    Article  PubMed  Google Scholar 

  18. Larson DE, Zahradka P, Sells BH (1991) Control points in eucaryotic ribosome biogenesis. Biochem Cell Biol 69:5–22

    PubMed  Google Scholar 

  19. Levy NS, Chung S, Furneaux H, Levy AP (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273:6417–6423

    Article  PubMed  Google Scholar 

  20. Malm C, Nyberg P, Engstrom M, Sjodin B, Lenkei R, Ekblom B, Lundberg I (2000) Immunological changes in human skeletal muscle and blood after eccentric exercise and multiple biopsies. J Physiol 529(Pt 1):243–262

    Article  PubMed  Google Scholar 

  21. Neufer PD, Ordway GA, Hand GA, Shelton JM, Richardson JA, Benjamin IJ, Williams RS (1996) Continuous contractile activity induces fiber type specific expression of HSP70 in skeletal muscle. Am J Physiol 271:C1828–C1837

    PubMed  Google Scholar 

  22. Pilegaard H, Ordway GA, Saltin B, Neufer PD (2000) Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol 279:E806–E814

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  24. Puntschart A (1994) Molekulare Adaptation des menschlichen Skelettmuskels an Ausdauertraining. Thesis/Dissertation. ETH Zürich

  25. Puntschart A, Claassen H, Jostarndt K, Hoppeler H, Billeter R (1995) mRNAs of enzymes involved in energy metabolism and mtDNA are increased in endurance-trained athletes. Am J Physiol 269:C619–C625

    PubMed  Google Scholar 

  26. Richardson RS, Wagner H, Mudaliar SR, Henry R, Noyszewski EA, Wagner PD (1999) Human VEGF gene expression in skeletal muscle: effect of acute normoxic and hypoxic exercise. Am J Physiol 277:H2247–H2252

    PubMed  Google Scholar 

  27. Richardson RS, Wagner H, Mudaliar SR, Saucedo E, Henry R, Wagner PD (2000) Exercise adaptation attenuates VEGF gene expression in human skeletal muscle. Am J Physiol 279:H772–H778

    Google Scholar 

  28. Rosler K, Hoppeler H, Conley KE, Claassen H, Gehr P, Howald H (1985) Transfer effects in endurance exercise. Adaptations in trained and untrained muscles. Eur J Appl Physiol Occup Physiol 54:355–362

    PubMed  Google Scholar 

  29. Sachs AB (1993) Messenger RNA degradation in eukaryotes. Cell 74:413–421

    Article  PubMed  Google Scholar 

  30. Saltin B, Henriksson J, Nygaard E, Andersen P, Jansson E (1977) Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners. Ann N Y Acad Sci 301:3–29

    PubMed  Google Scholar 

  31. Schmitt B, Fluck M, Decombaz J, Kreis R, Boesch C, Wittwer M, Graber F, Vogt M, Howald H, Hoppeler H (2003) Transcriptional adaptations of lipid metabolism in tibialis anterior muscle of endurance-trained athletes. Physiol Genomics 15:148–157

    PubMed  Google Scholar 

  32. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, Kooi ME (2003) The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab 88:1610–1616

    Article  PubMed  Google Scholar 

  33. Seip RL, Angelopoulos TJ, Semenkovich CF (1995) Exercise induces human lipoprotein lipase gene expression in skeletal muscle but not adipose tissue. Am J Physiol 268:E229–E236

    PubMed  Google Scholar 

  34. Seip RL, Mair K, Cole TG, Semenkovich CF (1997) Induction of human skeletal muscle lipoprotein lipase gene expression by short-term exercise is transient. Am J Physiol 272:E255–E261

    PubMed  Google Scholar 

  35. Starkie RL, Arkinstall MJ, Koukoulas I, Hawley JA, Febbraio MA (2001) Carbohydrate ingestion attenuates the increase in plasma interleukin-6, but not skeletal muscle interleukin-6 mRNA, during exercise in humans. J Physiol 533:585–591

    Article  PubMed  Google Scholar 

  36. Tunstall RJ, Mehan KA, Wadley GD, Collier GR, Bonen A, Hargreaves M, Cameron-Smith D (2002) Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am J Physiol 283:E66–E72

    Google Scholar 

  37. Turner DL, Hoppeler H, Claassen H, Vock P, Kayser B, Schena F, Ferretti G (1997) Effects of endurance training on oxidative capacity and structural composition of human arm and leg muscles. Acta Physiol Scand 161:459–464

    Article  PubMed  Google Scholar 

  38. Vissing K, Andersen JL, Schjerling P (2005) Are exercise-induced genes induced by exercise?. FASEB J 19:94–96

    PubMed  Google Scholar 

  39. Wittwer M, Billeter R, Hoppeler H, Fluck M (2004) Regulatory gene expression in skeletal muscle of highly endurance-trained humans. Acta Physiol Scand 180:217–227

    Article  PubMed  Google Scholar 

  40. Wittwer M, Fluck M, Hoppeler H, Muller S, Desplanches D, Billeter R (2002) Prolonged unloading of rat soleus muscle causes distinct adaptations of the gene profile. FASEB J 16:884–886

    PubMed  Google Scholar 

  41. Yan Z, Salmons S, Jarvis J, Booth FW (1995) Increased muscle carnitine palmitoyltransferase II mRNA after increased contractile activity. Am J Physiol 268:E277–E281

    PubMed  Google Scholar 

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Acknowledgements

The support of the Swiss National Science Foundation (grant number 31-65276.01) and the University of Bern is gratefully acknowledged. Special thanks are addressed to Franziska Graber for assistance in morphometric analyses and Ruth Vock and Hans Howald for advice on the manuscript.

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Authors and Affiliations

  1. Department of Anatomy, University of Bern, Baltzerstrasse 2, 3000, Bern 9, Switzerland

    Silvia Schmutz, Christoph Däpp, Matthias Wittwer, Michael Vogt, Hans Hoppeler & Martin Flück

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  1. Silvia Schmutz
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  2. Christoph Däpp
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  3. Matthias Wittwer
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  4. Michael Vogt
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  5. Hans Hoppeler
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  6. Martin Flück
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Correspondence to Martin Flück.

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Schmutz, S., Däpp, C., Wittwer, M. et al. Endurance training modulates the muscular transcriptome response to acute exercise. Pflugers Arch - Eur J Physiol 451, 678–687 (2006). https://doi.org/10.1007/s00424-005-1497-0

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  • DOI: https://doi.org/10.1007/s00424-005-1497-0

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