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Metabolic Profiling of Eccentric Exercise-Induced Muscle Damage in Human Urine

  • Jang, Hyun-Jun (College of Pharmacy, Dankook University) ;
  • Lee, Jung Dae (Division of Toxicology, College of Pharmacy, Sungkyunkwan University) ;
  • Jeon, Hyun-Sik (Department of Kinesiologic Medical Science, Graduate School, Dankook University) ;
  • Kim, Ah-Ram (Department of Kinesiologic Medical Science, Graduate School, Dankook University) ;
  • Kim, Suhkmann (Department of Chemistry and Chemistry Institute of Functional Materials, Pusan National University) ;
  • Lee, Ho-Seong (Department of Kinesiologic Medical Science, Graduate School, Dankook University) ;
  • Kim, Kyu-Bong (College of Pharmacy, Dankook University)
  • Received : 2018.01.30
  • Accepted : 2018.05.14
  • Published : 2018.07.15

Abstract

Skeletal muscle can be ultrastructurally damaged by eccentric exercise, and the damage causes metabolic disruption in muscle. This study aimed to determine changes in the metabolomic patterns in urine and metabolomic markers in muscle damage after eccentric exercise. Five men and 6 women aged 19~23 years performed 30 min of the bench step exercise at 70 steps per min at a determined step height of 110% of the lower leg length, and stepping frequency at 15 cycles per min. $^1H$ NMR spectral analysis was performed in urine collected from all participants before and after eccentric exercise-induced muscle damage conventionally determined using a visual analogue scale (VAS) and maximal voluntary contraction (MVC). Urinary metabolic profiles were built by multivariate analysis of principal component analysis (PCA) and orthogonal partial least square-discriminant analysis (OPLS-DA) using SIMCA-P. From the OPLS-DA, men and women were separated 2 hr after the eccentric exercise and the separated patterns were maintained or clarified until 96 hr after the eccentric exercise. Subsequently, urinary metabolic profiles showed distinct trajectory patterns between men and women. Finally, we found increased urinary metabolites (men: alanine, asparagine, citrate, creatine phosphate, ethanol, formate, glucose, glycine, histidine, and lactate; women: adenine) after the eccentric exercise. These results could contribute to understanding metabolic responses following eccentric exercise-induced muscle damage in humans.

Keywords

References

  1. Stauber, W.T. (1989) Eccentric action of muscles: physiology, injury, and adaptation. Exerc. Sport Sci. Rev., 17, 157-185.
  2. Brown, S., Day, S. and Donnelly, A. (1999) Indirect evidence of human skeletal muscle damage and collagen breakdown after eccentric muscle actions. J. Sports Sci., 17, 397-402. https://doi.org/10.1080/026404199365911
  3. Woledge, R.C., Curtin, N.A. and Homsher, E. (1985) Energetic aspects of muscle contraction. Monogr. Physiol. Soc., 41, 1-357.
  4. Bigland-Ritchie, B. and Woods, J.J. (1974) Integrated EMG and oxygen uptake during dynamic contractions of human muscles. J. Appl. Physiol., 36, 475-479. https://doi.org/10.1152/jappl.1974.36.4.475
  5. McCully, K.K. and Faulkner, J.A. (1986) Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J. Appl. Physiol., 61, 293-299. https://doi.org/10.1152/jappl.1986.61.1.293
  6. Tee, J.C., Bosch, A.N. and Lambert, M.I. (2007) Metabolic consequences of exercise-induced muscle damage. Sports Med., 37, 827-836. https://doi.org/10.2165/00007256-200737100-00001
  7. Byrne, C., Twist, C. and Eston, R. (2004) Neuromuscular function after exercise-induced muscle damage: theoretical and applied implications. Sports Med., 34, 49-69. https://doi.org/10.2165/00007256-200434010-00005
  8. Asp, S., Daugaard, J.R. and Richter, E.A. (1995) Eccentric exercise decreases glucose transporter GLUT4 protein in human skeletal muscle. J. Physiol., 482, 705-712. https://doi.org/10.1113/jphysiol.1995.sp020553
  9. Asp, S., Rohde, T. and Richter, E.A. (1997) Impaired muscle glycogen resynthesis after a marathon is not caused by decreased muscle GLUT-4 content. J. Appl. Physiol., 83, 1482-1485. https://doi.org/10.1152/jappl.1997.83.5.1482
  10. Asp, S., Daugaard, J.R., Kristiansen, S., Kiens, B., Richter, E.A. (1998) Exercise metabolism in human skeletal muscle exposed to prior eccentric exercise. J. Physiol., 509, 305-313. https://doi.org/10.1111/j.1469-7793.1998.305bo.x
  11. Asp, S., Daugaard, J.R., Rohde, T., Adamo, K. and Graham, T. (1999) Muscle glycogen accumulation after a marathon: roles of fiber type and pro- and macroglycogen. J. Appl. Physiol., 86, 474-478. https://doi.org/10.1152/jappl.1999.86.2.474
  12. Costill, D.L., Pascoe, D.D., Fink, W.J., Robergs, R.A., Barr, S.I. and Pearson, D. (1990) Impaired muscle glycogen resynthesis after eccentric exercise. J. Appl. Physiol., 69, 46-50. https://doi.org/10.1152/jappl.1990.69.1.46
  13. Evans, W.J., Meredith, C.N., Cannon, J.G., Dinarello, C.A., Frontera, W.R., Hughes, V.A., Jones, B.H. and Knuttgen, H.G. (1986) Metabolic changes following eccentric exercise in trained and untrained men. J. Appl. Physiol., 61, 1864-1868. https://doi.org/10.1152/jappl.1986.61.5.1864
  14. Kirwan, J.P., Hickner, R.C., Yarasheski, K.E., Kohrt, W.M., Wiethop, B.V. and Holloszy, J.O. (1992) Eccentric exercise induces transient insulin resistance in healthy individuals. J. Appl. Physiol., 72, 2197-2202.
  15. Nosaka, K. and Clarkson, P.M. (1995) Muscle damage following repeated bouts of high force eccentric exercise. Med. Sci. Sports Exerc., 27, 1263-1269.
  16. Selkow, N.M., Day, C., Liu, Z., Hart, J.M., Hertel, J. and Saliba, S.A. (2012) Microvascular perfusion and intramuscular temperature of the calf during cooling. Med. Sci. Sports Exerc., 44, 850-856. https://doi.org/10.1249/MSS.0b013e31823bced9
  17. Semark, A., Noakes, T.D., St Clair, G.A. and Lambert, M.I. (1999) The effect of a prophylactic dose of flurbiprofen on muscle soreness and sprinting performance in trained subjects. J. Sports Sci., 17, 197-203. https://doi.org/10.1080/026404199366091
  18. Sorichter, S., Puschendorf, B. and Mair, J. (1999) Skeletal muscle injury induced by eccentric muscle action: muscle proteins as markers of muscle fiber injury. Exerc. Immunol. Rev., 5, 5-21.
  19. Tuominen, J.A., Ebeling, P., Bourey, R., Koranyi, L., Lamminen, A., Rapola, J., Sane, T., Vuorinen-Markkola, H. and Koivisto, V.A. (1996) Postmarathon paradox: insulin resistance in the face of glycogen depletion. Am. J. Physiol., 270, E336-E343.
  20. Brancaccio, P., Lippi, G. and Maffulli, N. (2010) Biochemical markers of muscular damage. Clin. Chem. Lab. Med., 48, 757-767.
  21. Miles, M.P., Andring, J.M., Pearson, S.D., Gordon, L.K., Kasper, C., Depner, C.M. and Kidd, J.R. (2008) Diurnal variation, response to eccentric exercise, and association of inflammatory mediators with muscle damage variables. J. Appl. Physiol., 104, 451-458. https://doi.org/10.1152/japplphysiol.00572.2007
  22. Oosterom, D.L. and Betjes, M.G. (2006) Exertion-related abnormalities in the urine. Ned. Tijdschr. Geneeskd., 150, 606-610.
  23. Chung, Y.L., Rider, L.G., Bell, J.D., Summers, R.M., Zemel, L.S., Rennebohm, R.M., Passo, M.H., Hicks, J., Miller, F.W. and Scott, D.L. (2005) Juvenile dermatomyositis disease activity collaborative study G. Muscle metabolites, detected in urine by proton spectroscopy, correlate with disease damage in juvenile idiopathic inflammatory myopathies. Arthritis Rheum., 53, 565-570. https://doi.org/10.1002/art.21331
  24. Huerta-Alardin, A.L., Varon, J. and Marik, P.E. (2005) Bench-to-bedside review: rhabdomyolysis -- an overview for clinicians. Crit. Care, 9, 158-169. https://doi.org/10.1186/cc3221
  25. Khan, F.Y. (2009) Rhabdomyolysis: a review of the literature. Neth. J. Med., 67, 272-283.
  26. Duchen, M.R., Valdeolmillos, M., O'Neill, S.C. and Eisner, D.A. (1990) Effects of metabolic blockade on the regulation of intracellular calcium in dissociated mouse sensory neurones. J. Physiol., 424, 411-426. https://doi.org/10.1113/jphysiol.1990.sp018074
  27. Duncan, C.J. (1987) Role of calcium in triggering rapid ultrastructural damage in muscle: a study with chemically skinned fibres. J. Cell Sci., 87, 581-594.
  28. Armstrong, R.B., Warren, G.L. and Warren, J.A. (1991) Mechanisms of exercise-induced muscle fibre injury. Sports Med., 12, 184-207. https://doi.org/10.2165/00007256-199112030-00004
  29. Busch, W.A., Stromer, M.H., Goll, D.E. and Suzuki, A. (1972) $Ca^{2+}$-specific removal of Z lines from rabbit skeletal muscle. J. Cell Biol., 52, 367-381. https://doi.org/10.1083/jcb.52.2.367
  30. Baird, M.F., Graham, S.M., Baker, J.S. and Bickerstaff, G.F. (2012) Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J. Nutr. Metab., 2012, 960363.
  31. Barding, G.A., Jr., Salditos, R. and Larive, C.K. (2012) Quantitative NMR for bioanalysis and metabolomics. Anal. Bioanal. Chem., 404, 1165-1179. https://doi.org/10.1007/s00216-012-6188-z
  32. Jordan, K.W., Nordenstam, J., Lauwers, G.Y., Rothenberger, D.A., Alavi, K., Garwood, M. and Cheng, L.L. (2009) Metabolomic characterization of human rectal adenocarcinoma with intact tissue magnetic resonance spectroscopy. Dis. Colon. Rectum., 52, 520-525. https://doi.org/10.1007/DCR.0b013e31819c9a2c
  33. Ra, S.G., Maeda, S., Higashino, R., Imai, T. and Miyakawa, S. (2014) Metabolomics of salivary fatigue markers in soccer players after consecutive games. Appl. Physiol. Nutr. Metab., 39, 1120-1126. https://doi.org/10.1139/apnm-2013-0546
  34. Hicks, K.M., Onambele, G.L., Winwood, K. and Morse, C.I. (2016) Muscle damage following maximal eccentric knee extensions in males and females. PLoS ONE, 11, e0150848. https://doi.org/10.1371/journal.pone.0150848
  35. Newham, D.J., Jones, D.A. and Edwards, R.H. (1983) Large delayed plasma creatine kinase changes after stepping exercise. Muscle Nerve, 6, 380-385. https://doi.org/10.1002/mus.880060507
  36. Vissing, K., Overgaard, K., Nedergaard, A., Fredsted, A. and Schjerling, P. (2008) Effects of concentric and repeated eccentric exercise on muscle damage and calpain-calpastatin gene expression in human skeletal muscle. Eur. J. Appl. Physiol., 103, 323-332. https://doi.org/10.1007/s00421-008-0709-7
  37. Wilson, J.M., Kim, J.S., Lee, S.R., Rathmacher, J.A., Dalmau, B., Kingsley, J.D., Koch, H., Manninen, A.H., Saadat, R. and Panton, L.B. (2009) Acute and timing effects of beta-hydroxy-beta-methylbutyrate (HMB) on indirect markers of skeletal muscle damage. Nutr. Metab. (Lond), 6, 6. https://doi.org/10.1186/1743-7075-6-6
  38. Baroni, B.M., Leal Junior, E.C., De Marchi, T., Lopes, A.L., Salvador, M. and Vaz, M.A. (2010) Low level laser therapy before eccentric exercise reduces muscle damage markers in humans. Eur. J. Appl. Physiol., 110, 789-796. https://doi.org/10.1007/s00421-010-1562-z
  39. Selkow, N.M., Herman, D.C., Liu, Z., Hertel, J., Hart, J.M. and Saliba, S.A. (2015) Blood flow after exercise-induced muscle damage. J. Athl. Train, 50, 400-406. https://doi.org/10.4085/1062-6050-49.6.01
  40. Twist, C. and Eston, R.G. (2009) The effect of exercise-induced muscle damage on perceived exertion and cycling endurance performance. Eur. J. Appl. Physiol., 105, 559-567. https://doi.org/10.1007/s00421-008-0935-z
  41. Chen, T.C., Lin, K.Y., Chen, H.L., Lin, M.J. and Nosaka, K. (2011) Comparison in eccentric exercise-induced muscle damage among four limb muscles. Eur. J. Appl. Physiol., 111, 211-223. https://doi.org/10.1007/s00421-010-1648-7
  42. Penailillo, L., Blazevich, A., Numazawa, H. and Nosaka, K. (2015) Rate of force development as a measure of muscle damage. Scand. J. Med. Sci. Sports, 25, 417-427. https://doi.org/10.1111/sms.12241
  43. Clarkson, P.M. and Hubal, M.J. (2002) Exercise-induced muscle damage in humans. Am. J. Phys. Med. Rehabil., 81, S52-S69. https://doi.org/10.1097/00002060-200211001-00007
  44. Rinard, J., Clarkson, P.M., Smith, L.L. and Grossman, M. (2000) Response of males and females to high-force eccentric exercise. J. Sports Sci., 18, 229-236. https://doi.org/10.1080/026404100364965
  45. Ruoppolo, M., Scolamiero, E., Caterino, M., Mirisola, V., Franconi, F. and Campesi, I. (2015) Female and male human babies have distinct blood metabolomic patterns. Mol. Biosyst., 11, 2483-2492. https://doi.org/10.1039/C5MB00297D
  46. Tso, V.K., Sydora, B.C., Foshaug, R.R., Churchill, T.A., Doyle, J., Slupsky, C.M. and Fedorak, R.N. (2013) Metabolomic profiles are gender, disease and time specific in the interleukin-10 gene-deficient mouse model of inflammatory bowel disease. PLoS ONE, 8, e67654. https://doi.org/10.1371/journal.pone.0067654
  47. Dieli-Conwright, C.M., Spektor, T.M., Rice, J.C., Sattler, F.R. and Schroeder, E.T. (2009) Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J. Appl. Physiol., 107, 853-858. https://doi.org/10.1152/japplphysiol.00404.2009
  48. Saks, V. (2008) The phosphocreatine-creatine kinase system helps to shape muscle cells and keep them healthy and alive. J. Physiol., 586, 2817-2818. https://doi.org/10.1113/jphysiol.2008.155358
  49. Vigelso, A., Andersen, N.B. and Dela, F. (2014) The relationship between skeletal muscle mitochondrial citrate synthase activity and whole body oxygen uptake adaptations in response to exercise training. Int. J. Physiol. Pathophysiol. Pharmacol., 6, 84-101.
  50. Koopman, R., Ly, C.H. and Ryall, J.G. (2014) A metabolic link to skeletal muscle wasting and regeneration. Front Physiol., 5, 32.
  51. Powers, S.K. and Jackson, M.J. (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev., 88, 1243-1276. https://doi.org/10.1152/physrev.00031.2007
  52. Reid, M.B., Shoji, T., Moody, M.R. and Entman, M.L. (1992) Reactive oxygen in skeletal muscle. II. Extracellular release of free radicals. J. Appl. Physiol., 73, 1805-1809. https://doi.org/10.1152/jappl.1992.73.5.1805
  53. Son, D.O., Satsu, H. and Shimizu, M. (2005) Histidine inhibits oxidative stress- and TNF-alpha-induced interleukin-8 secretion in intestinal epithelial cells. FEBS Lett., 579, 4671-4677. https://doi.org/10.1016/j.febslet.2005.07.038
  54. Tidball, J.G. (2005) Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R345-R353. https://doi.org/10.1152/ajpregu.00454.2004
  55. Mangino, M.J., Murphy, M.K., Grabau, G.G. and Anderson, C.B. (1991) Protective effects of glycine during hypothermic renal ischemia-reperfusion injury. Am. J. Physiol., 261, F841-F848.
  56. Rush, G.F. and Ponsler, G.D. (1991) Cephaloridine-induced biochemical changes and cytotoxicity in suspensions of rabbit isolated proximal tubules. Toxicol. Appl. Pharmacol., 109, 314-326. https://doi.org/10.1016/0041-008X(91)90178-H
  57. Ascher, E., Hanson, J.N., Cheng, W., Hingorani, A. and Scheinman, M. (2001) Glycine preserves function and decreases necrosis in skeletal muscle undergoing ischemia and reperfusion injury. Surgery, 129, 231-235. https://doi.org/10.1067/msy.2001.112594
  58. Ham, D.J., Murphy, K.T., Chee, A., Lynch, G.S. and Koopman, R. (2014) Glycine administration attenuates skeletal muscle wasting in a mouse model of cancer cachexia. Clin. Nutr., 33, 448-458. https://doi.org/10.1016/j.clnu.2013.06.013
  59. Becker, A., Fritz-Wolf, K., Kabsch, W., Knappe, J., Schultz, S. and Volker Wagner, A.F. (1999) Structure and mechanism of the glycyl radical enzyme pyruvate formate-lyase. Nat. Struct. Biol., 6, 969-975. https://doi.org/10.1038/13341
  60. Dashko, S., Zhou, N., Compagno, C. and Piskur, J. (2014) Why, when, and how did yeast evolve alcoholic fermentation? FEMS Yeast Res., 14, 826-832. https://doi.org/10.1111/1567-1364.12161
  61. Doi, Y. and Ikegami, Y. (2014) Pyruvate formate-lyase is essential for fumarate-independent anaerobic glycerol utilizationin the Enterococcus faecalis strain W11. J. Bacteriol.,196, 2472-2480. https://doi.org/10.1128/JB.01512-14

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