Skip to main content
SpringerLink
Log in

Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise

  • Short Communication
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

The purpose of this study was to evaluate whether ultra endurance exercise changes the mRNA levels of the autophagy-related and autophagy-regulatory genes. Eight men (44 ± 1 years, range: 38–50 years) took part in a 200-km running race. The average running time was 28 h 03 min ± 2 h 01 min (range: 22 h 15 min–35 h 04 min). A muscle sample was taken from the vastus lateralis 2 weeks prior to the race and 3 h after arrival. Gene expression was assessed by RT-qPCR. Transcript levels of autophagy-related genes were increased by 49% for ATG4b (P = 0.025), 57% for ATG12 (P = 0.013), 286% for Gabarapl1 (P = 0.008) and 103% for LC3b (P = 0.011). The lysosomal enzyme cathepsin L mRNA was upregulated by 123% (P = 0.003). Similarly, transcript levels of the autophagy-regulatory genes BNIP3 and BNIP3l were both increased by 113% (P = 0.031 and P = 0.007, respectively). Since upregulation of these genes has been related with an increased autophagic flux in various models, our results strongly suggest that autophagy is activated in response to ultra endurance exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Cabrera S, Marino G, Fernandez AF, Lopez-Otin C (2010) Autophagy, proteases and the sense of balance. Autophagy 6:961–963

    Article  PubMed  Google Scholar 

  • de Lange P, Moreno M, Silvestri E, Lombardi A, Goglia F, Lanni A (2007) Fuel economy in food-deprived skeletal muscle: signaling pathways and regulatory mechanisms. Faseb J 21:3431–3441

    Article  PubMed  Google Scholar 

  • Deldicque L, Atherton P, Patel R, Theisen D, Nielens H, Rennie MJ, Francaux M (2008) Effects of resistance exercise with and without creatine supplementation on gene expression and cell signaling in human skeletal muscle. J Appl Physiol 104:371–378

    Article  PubMed  CAS  Google Scholar 

  • Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C, Boncompagni S, Belia S, Wannenes F, Nicoletti C, Del Prete Z, Rosenthal N, Molinaro M, Protasi F, Fano G, Sandri M, Musaro A (2008) Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab 8:425–436

    Article  PubMed  CAS  Google Scholar 

  • Eskelinen EL, Saftig P (2009) Autophagy: a lysosomal degradation pathway with a central role in health and disease. Biochim Biophys Acta 1793:664–673

    Article  PubMed  CAS  Google Scholar 

  • Feng Z, Bai L, Yan J, Li Y, Shen W, Wang Y, Wertz K, Weber P, Zhang Y, Chen Y, Liu J (2011) Mitochondrial dynamic remodeling in strenuous exercise-induced muscle and mitochondrial dysfunction: regulatory effects of hydroxytyrosol. Free Radic Biol Med 50:1437–1446

    Article  PubMed  CAS  Google Scholar 

  • Finn PF, Dice JF (2006) Proteolytic and lipolytic responses to starvation. Nutrition 22:830–844

    Article  PubMed  CAS  Google Scholar 

  • Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB (2007) Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14:146–157

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Jamart C, Deldicque L, An GL, Lee YH, Kim CK, Raymackers JM, Francaux M (2011) Endoplasmic reticulum stress markers and ubiquitin-proteasome pathway activity in response to a 200-km run. Med Sci Sports Exerc 43:18–25

    PubMed  CAS  Google Scholar 

  • Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y (2003) A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539–545

    Article  PubMed  CAS  Google Scholar 

  • Lee EJ, Tournier C (2011) The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy. Autophagy 7:689–695

    Article  PubMed  CAS  Google Scholar 

  • Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471

    Article  PubMed  CAS  Google Scholar 

  • Mammucari C, Schiaffino S, Sandri M (2008) Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4:524–526

    PubMed  CAS  Google Scholar 

  • McCully KK, Faulkner JA (1985) Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 59:119–126

    PubMed  CAS  Google Scholar 

  • Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101–1111

    Article  PubMed  CAS  Google Scholar 

  • Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220–9231

    Article  PubMed  CAS  Google Scholar 

  • Sahlin K, Shabalina IG, Mattsson CM, Bakkman L, Fernstrom M, Rozhdestvenskaya Z, Enqvist JK, Nedergaard J, Ekblom B, Tonkonogi M (2010) Ultraendurance exercise increases the production of reactive oxygen species in isolated mitochondria from human skeletal muscle. J Appl Physiol 108:780–787

    Article  PubMed  CAS  Google Scholar 

  • Salminen A (1985) Lysosomal changes in skeletal muscles during the repair of exercise injuries in muscle fibers. Acta Physiol Scand Suppl 539:1–31

    PubMed  CAS  Google Scholar 

  • Salminen A, Vihko V (1984) Autophagic response to strenuous exercise in mouse skeletal muscle fibers. Virchows Arch B Cell Pathol Incl Mol Pathol 45:97–106

    Article  PubMed  CAS  Google Scholar 

  • Sandri M (2010) Autophagy in skeletal muscle. FEBS Lett 584:1411–1416

    Article  PubMed  CAS  Google Scholar 

  • Tarnopolsky M (2004) Protein requirements for endurance athletes. Nutrition 20:662–668

    Article  PubMed  CAS  Google Scholar 

  • Tracy K, Macleod KF (2007) Regulation of mitochondrial integrity, autophagy and cell survival by BNIP3. Autophagy 3:616–619

    PubMed  CAS  Google Scholar 

  • Wang CW, Klionsky DJ (2003) The molecular mechanism of autophagy. Mol Med 9:65–76

    PubMed  Google Scholar 

  • Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Brault JJ, Schild A, Goldberg AL (2008) Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4:378–380

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Fonds National de la Recherche Scientifique Médicale (FRSM 3.4574.03) (Belgium), by the Université Catholique de Louvain (FSR) and by the National Research Foundation of Korea Grant funded by the Korean Government (NRF-2010-413-G00007).

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. Institute of Neuroscience, Research Group in Muscle and Exercise Physiology, Université catholique de Louvain, Place Pierre de Coubertin 1, 1348, Louvain-la-Neuve, Belgium

    Cécile Jamart, Nicolas Benoit, Jean-Marc Raymackers & Marc Francaux

  2. Department of Aging and Human Physiology, Korea National Sport University, 88-15 Oryun-dong, Songpa-gu, Seoul, South Korea

    Hyo Jeong Kim & Chang Keun Kim

Authors
  1. Cécile Jamart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicolas Benoit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Marc Raymackers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hyo Jeong Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chang Keun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marc Francaux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc Francaux.

Additional information

Communicated by Håkan Westerblad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jamart, C., Benoit, N., Raymackers, JM. et al. Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise. Eur J Appl Physiol 112, 3173–3177 (2012). https://doi.org/10.1007/s00421-011-2287-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-011-2287-3

Keywords

Search

Navigation