The altered human serum metabolome induced by a marathon.

Zinandré Stander, Laneke Luies, Lodewyk J Mienie, Karen M Keane, Glyn Howatson, Tom Clifford, Emma J Stevenson, Du Toit Loots
Author Information
  1. Zinandré Stander: Human Metabolomics, North-West University, Private Bag X6001, Box 269, Potchefstroom, 2531, South Africa. ORCID
  2. Laneke Luies: Human Metabolomics, North-West University, Private Bag X6001, Box 269, Potchefstroom, 2531, South Africa. ORCID
  3. Lodewyk J Mienie: Human Metabolomics, North-West University, Private Bag X6001, Box 269, Potchefstroom, 2531, South Africa. ORCID
  4. Karen M Keane: Faculty of Health and Life Sciences, Department of Sport, Exercise and Rehabilitation, Northumbria University, NE1 8ST, Newcastle upon Tyne, UK. ORCID
  5. Glyn Howatson: Faculty of Health and Life Sciences, Department of Sport, Exercise and Rehabilitation, Northumbria University, NE1 8ST, Newcastle upon Tyne, UK. ORCID
  6. Tom Clifford: Faculty of Health and Life Sciences, Department of Sport, Exercise and Rehabilitation, Northumbria University, NE1 8ST, Newcastle upon Tyne, UK. ORCID
  7. Emma J Stevenson: Human Nutrition Research Centre, Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne, UK. ORCID
  8. Du Toit Loots: Human Metabolomics, North-West University, Private Bag X6001, Box 269, Potchefstroom, 2531, South Africa. dutoit.loots@nwu.ac.za. ORCID

Abstract

INTRODUCTION: Endurance races have been associated with a substantial amount of adverse effects which could lead to chronic disease and long-term performance impairment. However, little is known about the holistic metabolic changes occurring within the serum metabolome of athletes after the completion of a marathon.
OBJECTIVES: Considering this, the aim of this study was to better characterize the acute metabolic changes induced by a marathon.
METHODS: Using an untargeted two dimensional gas chromatography time-of-flight mass spectrometry metabolomics approach, pre- and post-marathon serum samples of 31 athletes were analyzed and compared to identify those metabolites varying the most after the marathon perturbation.
RESULTS: Principle component analysis of the comparative groups indicated natural differentiation due to variation in the total metabolite profiles. Elevated concentrations of carbohydrates, fatty acids, tricarboxylic acid cycle intermediates, ketones and reduced concentrations of amino acids indicated a metabolic shift between various fuel substrate systems. Additionally, elevated odd-chain fatty acids and α-hydroxy acids indicated the utilization of α-oxidation and autophagy as alternative energy-producing mechanisms. Adaptations in gut microbe-associated markers were also observed and correlated with the metabolic flexibility of the athlete.
CONCLUSION: From these results it is evident that a marathon places immense strain on the energy-producing pathways of the athlete, leading to extensive protein degradation, oxidative stress, mammalian target of rapamycin complex 1 inhibition and autophagy. A better understanding of this metabolic shift could provide new insights for optimizing athletic performance, developing more efficient nutrition regimens and identify strategies to improve recovery.

Keywords

References

  1. J Proteome Res. 2010 Dec 3;9(12):6405-16 [PMID: 20932058]
  2. Adv Nutr. 2016 Jul 15;7(4):730-4 [PMID: 27422507]
  3. Scand J Med Sci Sports. 2010 Dec;20(6):843-52 [PMID: 19883392]
  4. Clin Chim Acta. 2015 Aug 25;448:91-7 [PMID: 26115894]
  5. J Appl Physiol Respir Environ Exerc Physiol. 1984 Apr;56(4):831-8 [PMID: 6373687]
  6. Med Sci Sports Exerc. 2012 Oct;44(10):1843-5 [PMID: 22525769]
  7. J Am Diet Assoc. 2000 Apr;100(4):466-9 [PMID: 10767907]
  8. Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3698-703 [PMID: 19234110]
  9. Asia Pac J Sports Med Arthrosc Rehabil Technol. 2015 May 02;2(3):73-84 [PMID: 29264244]
  10. Methods Enzymol. 1987;141:127-43 [PMID: 3600356]
  11. J Hum Kinet. 2015 Apr 07;45:93-102 [PMID: 25964813]
  12. Med Sci Sports Exerc. 2007 Jul;39(7):1075-9 [PMID: 17596774]
  13. Biometrics. 2006 Mar;62(1):185-92 [PMID: 16542245]
  14. Biochim Biophys Acta. 2000 Apr 15;1501(1):12-24 [PMID: 10727845]
  15. FEMS Microbiol Rev. 2016 Jul;40(4):464-79 [PMID: 26975195]
  16. J Affect Disord. 1996 Apr 26;38(1):35-46 [PMID: 8735157]
  17. BMC Genomics. 2006 Jun 08;7:142 [PMID: 16762068]
  18. J Sports Sci. 2019 May;37(9):959-967 [PMID: 28346122]
  19. J Nutr. 2011 Nov;141(11):1925-30 [PMID: 21918059]
  20. Clin Chim Acta. 1976 Sep 20;71(3):477-84 [PMID: 971536]
  21. Mitochondrion. 2017 Jul;35:97-110 [PMID: 28576558]
  22. Clin Chem. 2003 Feb;49(2):286-94 [PMID: 12560353]
  23. Exp Physiol. 2008 Jan;93(1):27-42 [PMID: 18165431]
  24. J Chromatogr. 1985 Feb 27;338(1):25-32 [PMID: 4019652]
  25. Bioresour Technol. 2013 Apr;133:469-74 [PMID: 23454803]
  26. Sci Transl Med. 2010 May 26;2(33):33ra37 [PMID: 20505214]
  27. Proc Natl Acad Sci U S A. 2017 May 23;114(21):E4233-E4240 [PMID: 28484010]
  28. Clin Chem. 2005 Mar;51(3):610-7 [PMID: 15615815]
  29. Proc Natl Acad Sci U S A. 2017 Mar 28;114(13):E2616-E2623 [PMID: 28289220]
  30. J Lipid Res. 1973 Jan;14(1):69-77 [PMID: 4701555]
  31. J Neurol Sci. 1989 Dec;94(1-3):29-40 [PMID: 2614471]
  32. Open Biomed Eng J. 2015 Oct 19;9:326-9 [PMID: 26998183]
  33. PLoS One. 2014 Jun 16;9(6):e99058 [PMID: 24932507]
  34. PLoS One. 2016 Aug 03;11(8):e0160505 [PMID: 27486806]
  35. Sci Rep. 2017 Mar 23;7:44845 [PMID: 28332596]
  36. Med Sci Sports Exerc. 2012 Jun;44(6):999-1004 [PMID: 22595981]
  37. Endocrinology. 2006 Jan;147(1):179-90 [PMID: 16223859]
  38. Int J Sport Nutr Exerc Metab. 2012 Oct;22(5):392-400 [PMID: 23011657]
  39. J Sport Health Sci. 2017 Jun;6(2):179-197 [PMID: 30356594]
  40. PLoS One. 2010 May 28;5(5):e10883 [PMID: 20526369]
  41. Diabetes Care. 1992 Nov;15(11):1767-76 [PMID: 1468313]
  42. Trans Am Clin Climatol Assoc. 2003;114:149-61; discussion 162-3 [PMID: 12813917]
  43. Postepy Hig Med Dosw (Online). 2008 Sep 05;62:451-62 [PMID: 18772850]
  44. Med Sci Sports Exerc. 2012 Feb;44(2):344-51 [PMID: 21775906]
  45. Clin Chem. 2016 Aug;62(8):1159-60 [PMID: 27471246]
  46. Cell Metab. 2011 May 4;13(5):495-504 [PMID: 21531332]
  47. J Cell Sci. 2009 Oct 15;122(Pt 20):3589-94 [PMID: 19812304]
  48. Eur J Intern Med. 2011 Oct;22(5):e36-8 [PMID: 21925040]
  49. Eur J Appl Physiol. 2012 May;112(5):1679-88 [PMID: 21879351]
  50. Pediatr Res. 1989 Jan;25(1):11-4 [PMID: 2919111]
  51. Mol Aspects Med. 2016 Aug;50:56-87 [PMID: 27106402]
  52. J Sports Sci. 2011;29 Suppl 1:S91-9 [PMID: 21916794]
  53. Circulation. 2013 Jan 22;127(3):340-8 [PMID: 23258601]
  54. Brain Behav Immun. 2006 Nov;20(6):578-84 [PMID: 16554145]
  55. Nat Commun. 2014 Oct 27;5:5338 [PMID: 25345524]
  56. Am J Physiol Endocrinol Metab. 2014 Oct 1;307(7):E539-52 [PMID: 25096178]

MeSH Term

Adult
Autophagy
Energy Metabolism
Female
Humans
Male
Metabolome
Middle Aged
Proteolysis
Running

Word Cloud

Created with Highcharts 10.0.0metabolicmarathonacidsserumindicatedperformancechangesmetabolomeathletesbetterinducedidentifyconcentrationsfattyshiftautophagyenergy-producingmarkersathleteINTRODUCTION:Enduranceracesassociatedsubstantialamountadverseeffectsleadchronicdiseaselong-termimpairmentHoweverlittleknownholisticoccurringwithincompletionOBJECTIVES:ConsideringaimstudycharacterizeacuteMETHODS:Usinguntargetedtwodimensionalgaschromatographytime-of-flightmassspectrometrymetabolomicsapproachpre-post-marathonsamples31analyzedcomparedmetabolitesvaryingperturbationRESULTS:PrinciplecomponentanalysiscomparativegroupsnaturaldifferentiationduevariationtotalmetaboliteprofilesElevatedcarbohydratestricarboxylicacidcycleintermediatesketonesreducedaminovariousfuelsubstratesystemsAdditionallyelevatedodd-chainα-hydroxyutilizationα-oxidationalternativemechanismsAdaptationsgutmicrobe-associatedalsoobservedcorrelatedflexibilityCONCLUSION:resultsevidentplacesimmensestrainpathwaysleadingextensiveproteindegradationoxidativestressmammaliantargetrapamycincomplex1inhibitionunderstandingprovidenewinsightsoptimizingathleticdevelopingefficientnutritionregimensstrategiesimproverecoveryalteredhumanFuelsubstratesMarathonMetaboliteMetabolomicsSerum

Similar Articles

Cited By