A Single Bout of Ultra-Endurance Exercise Reveals Early Signs of Muscle Aging in Master Athletes.

Cécile Coudy-Gandilhon, Marine Gueugneau, Christophe Chambon, Daniel Taillandier, Lydie Combaret, Cécile Polge, Guillaume Y Millet, Léonard Féasson, Daniel Béchet
Author Information
  1. Cécile Coudy-Gandilhon: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France.
  2. Marine Gueugneau: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France. ORCID
  3. Christophe Chambon: Université Clermont Auvergne, INRAE, Metabolomic and Proteomic Exploration Facility, F-63000 Clermont-Ferrand, France.
  4. Daniel Taillandier: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France.
  5. Lydie Combaret: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France. ORCID
  6. Cécile Polge: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France. ORCID
  7. Guillaume Y Millet: Université de Lyon, UJM-Saint-Etienne, Inter-University Laboratory of Human Movement Biology, EA 7424, F-42023 Saint-Etienne, France. ORCID
  8. Léonard Féasson: Université de Lyon, UJM-Saint-Etienne, Inter-University Laboratory of Human Movement Biology, EA 7424, F-42023 Saint-Etienne, France. ORCID
  9. Daniel Béchet: Université Clermont Auvergne, INRAE, UNH, Unité de Nutrition Humaine, CRNH Auvergne, F-63000 Clermont-Ferrand, France. ORCID

Abstract

Middle-aged and master endurance athletes exhibit similar physical performance and long-term muscle adaptation to aerobic exercise. Nevertheless, we hypothesized that the short-term plasticity of the skeletal muscle might be distinctly altered for master athletes when they are challenged by a single bout of prolonged moderate-intensity exercise. Six middle-aged (37Y) and five older (50Y) master highly-trained athletes performed a 24-h treadmill run (24TR). muscle biopsies were collected before and after the run and assessed for proteomics, fiber morphometry, intramyocellular lipid droplets (LD), mitochondrial oxidative activity, extracellular matrix (ECM), and micro-vascularisation. Before 24TR, muscle fiber type morphometry, intramyocellular LD, oxidative activity, ECM and micro-vascularisation were similar between master and middle-aged runners. For 37Y runners, 24TR was associated with ECM thickening, increased capillary-to-fiber interface, and an 89% depletion of LD in type-I fibers. In contrast, for 50Y runners, 24TR did not alter ECM and capillarization and poorly depleted LDs. Moreover, an impaired succinate dehydrogenase activity and functional class scoring of proteomes suggested reduced oxidative phosphorylation post-24TR exclusively in 50Y muscle. Collectively, our data support that middle-aged and master endurance athletes exhibit distinct transient plasticity in response to a single bout of ultra-endurance exercise, which may constitute early signs of muscle aging for master athletes.

Keywords

References

  1. Proc Nutr Soc. 1995 Mar;54(1):107-21 [PMID: 7568245]
  2. Histochem Cell Biol. 1999 Oct;112(4):271-6 [PMID: 10550611]
  3. Front Physiol. 2020 Mar 19;11:253 [PMID: 32265741]
  4. Nat Biotechnol. 2014 Mar;32(3):223-6 [PMID: 24727771]
  5. J Physiol. 2007 Nov 15;585(Pt 1):231-9 [PMID: 17884919]
  6. Acta Neurol Scand. 1979 Jun;59(6):317-23 [PMID: 484204]
  7. J Neurol Sci. 1989 Dec;94(1-3):29-40 [PMID: 2614471]
  8. J Physiol. 2004 Jan 15;554(Pt 2):559-69 [PMID: 14578492]
  9. Can J Appl Physiol. 1997 Feb;22(1):11-22 [PMID: 9018404]
  10. Mol Cell Proteomics. 2014 Jan;13(1):283-94 [PMID: 24217021]
  11. Magnes Res. 2019 Aug 1;32(3):72-82 [PMID: 32162608]
  12. J Gerontol. 1977 Jan;32(1):33-7 [PMID: 830731]
  13. PLoS One. 2014 Dec 04;9(12):e113637 [PMID: 25474696]
  14. Clin Physiol Funct Imaging. 2003 Nov;23(6):337-43 [PMID: 14617264]
  15. J Cachexia Sarcopenia Muscle. 2018 Oct;9(5):929-946 [PMID: 29989354]
  16. Springerplus. 2014 Nov 25;3:693 [PMID: 25520912]
  17. J Gerontol A Biol Sci Med Sci. 2019 Apr 23;74(5):608-615 [PMID: 30137216]
  18. Am J Hematol. 2020 Nov;95(11):1257-1268 [PMID: 32681734]
  19. Scand J Med Sci Sports. 2011 Feb;21(1):54-61 [PMID: 19883385]
  20. J Appl Physiol (1985). 2010 May;108(5):1224-33 [PMID: 20167672]
  21. BMC Genomics. 2014 Dec 23;15:1165 [PMID: 25532418]
  22. J Biomed Nanotechnol. 2014 Oct;10(10):2464-507 [PMID: 25992406]
  23. Cell Metab. 2013 Feb 5;17(2):162-84 [PMID: 23395166]
  24. J Physiol. 2008 Jan 1;586(1):55-63 [PMID: 17717011]
  25. Acta Physiol Scand. 1987 Jul;130(3):513-20 [PMID: 3630729]
  26. Histochem Cell Biol. 2010 Sep;134(3):307-17 [PMID: 20711601]
  27. J Appl Physiol (1985). 2012 May;112(9):1529-37 [PMID: 22345427]
  28. Age Ageing. 2019 Jul 1;48(4):601 [PMID: 31081853]
  29. Ir J Med Sci. 2011 Mar;180(1):129-34 [PMID: 20512663]
  30. J Appl Physiol (1985). 2002 Oct;93(4):1185-95 [PMID: 12235013]
  31. Am J Physiol Endocrinol Metab. 2010 Feb;298(2):E257-69 [PMID: 19903866]
  32. Med Sci Sports Exerc. 2007 Dec;39(12):2160-70 [PMID: 18046187]
  33. J Gerontol A Biol Sci Med Sci. 2015 May;70(5):566-76 [PMID: 24939997]
  34. Exp Gerontol. 2016 Apr;76:80-8 [PMID: 26826452]
  35. J Muscle Res Cell Motil. 1989 Jun;10(3):221-8 [PMID: 2760192]
  36. Acta Physiol Scand. 1979 Nov;107(3):257-61 [PMID: 539455]
  37. Front Physiol. 2016 Dec 12;7:613 [PMID: 28018241]
  38. Nucleic Acids Res. 2019 Jan 8;47(D1):D607-D613 [PMID: 30476243]
  39. J Appl Physiol (1985). 2009 Mar;106(3):804-12 [PMID: 19131480]
  40. Cell. 2014 Nov 6;159(4):738-49 [PMID: 25417152]
  41. PLoS Comput Biol. 2012;8(2):e1002375 [PMID: 22383865]
  42. Sports Med. 2014 May;44 Suppl 1:S87-96 [PMID: 24791920]
  43. Cold Spring Harb Perspect Med. 2018 Mar 1;8(3): [PMID: 28432116]
  44. Aging Cell. 2014 Apr;13(2):254-62 [PMID: 24245531]
  45. Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9440-5 [PMID: 12883005]
  46. Horm Metab Res. 2001 Feb;33(2):63-6 [PMID: 11294494]
  47. J Physiol. 2003 Dec 1;553(Pt 2):611-25 [PMID: 14514877]
  48. Angiogenesis. 2014 Jul;17(3):499-509 [PMID: 24668225]
  49. Int J Mol Sci. 2021 Apr 19;22(8): [PMID: 33921590]
  50. Bioinformatics. 2016 May 15;32(10):1502-8 [PMID: 26787660]
  51. Sports Med. 2015 Nov;45 Suppl 1:S23-32 [PMID: 26553490]

Grants

  1. CAP 20-25/French government IDEX-ISITE initiative 16-IDEX-0001
  2. NCT 00428779/University Hospital of Saint-Etienne (France)
  3. CERA Sarcopenie n°30/Caisse d'Epargne Rhone Alpes

MeSH Term

Aging
Athletes
Exercise
Humans
Middle Aged
Muscle, Skeletal
Physical Endurance

Word Cloud

Created with Highcharts 10.0.0musclemasterathletesexercise24TRECMmiddle-aged50YLDoxidativeactivityrunnersenduranceexhibitsimilarplasticityskeletalsinglebout37Yrunfibermorphometryintramyocellularlipiddropletsextracellularmatrixmicro-vascularisationagingMiddle-agedphysicalperformancelong-termadaptationaerobicNeverthelesshypothesizedshort-termmightdistinctlyalteredchallengedprolongedmoderate-intensitySixfiveolderhighly-trainedperformed24-htreadmillbiopsiescollectedassessedproteomicsmitochondrialtypeassociatedthickeningincreasedcapillary-to-fiberinterface89%depletiontype-IfiberscontrastaltercapillarizationpoorlydepletedLDsMoreoverimpairedsuccinatedehydrogenasefunctionalclassscoringproteomessuggestedreducedphosphorylationpost-24TRexclusivelyCollectivelydatasupportdistincttransientresponseultra-endurancemayconstituteearlysignsSingleBoutUltra-EnduranceExerciseRevealsEarlySignsMuscleAgingMasterAthletescapillaries

Similar Articles

Cited By