Українська English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2017; 63(1): 95-104

MUSCLE FATIGUE: FACTORS OF DEVELOPMENT AND WAYS OF CORRECTION

T.Yu. Matvienko1, D.A. Zavodovskyi1, D.N. Nozdrenko1, I.V. Mishchenko2, O.P. Motuziuk2, K.I. Bogutska1, Yu.P. Sklyarov3, Yu.I. Prylutskyy1

  1. Taras Shevchenko National University of Kyiv; е-mail: prylut@ukr.net;
  2. Lesya Ukrainka Eastern European National University, Lutsk;
  3. O.O. Bogomolets National Medical University, Kyiv
DOI: https://doi.org/10.15407/fz63.01.095


Abstract

The data regarding the analysis of the physiological and biochemical mechanisms of muscle fatigue and ways to prevent it are summarized. The effect of the most common endogenous and exogenous antioxidants in the biochemical processes in muscle fatigue was analyzed. It is shown that biocompatible, non-toxic water-soluble C60 fullerenes, which possess powerful antioxidative properties, promise great prospects in the correction of skeletal muscle fatigue caused by the destructive action of free radicals.

Keywords: skeletal muscles; muscle fatigue; free radicals; C60 fullerene.

Full text: (PDF, in Ukrainian)

References

  1. Tipton MC. Exercise physiology: people and ideas. Amsterdam: Elsevier. 1993; 510 p. PubMedCentral
    2.  
  2. Mosso A. Fatigue (1904). Whitefish: Kessinger Publishing. 2008; 348 p.
    3.  
  3. Dittner AJ, Wessely SC, Brown RG. The assessment of fatigue: a practical guide for clinicians and researchers. J Psychosom Res. 2004; 56(2): 157-70. CrossRef  
  4. Boyas S, Guervel A. Neuromuscular fatigue in healthy muscle: underlying factors and adaptation mechanisms. Ann Phys Rehabil Med. 2011; 54(2): 88-108. CrossRef PubMed
    5.  
  5. Kostyukov AI, Day S, Hellstrom F, Radovanovic S, Ljubisavljevic M, Windhorst U, Johansson H. Fatiguerelated changes in electromyogram activity of cat gastrocnemius during frequency-modulated efferent stimulation. Neurosci. 2000; 97(4): 801-9. CrossRef  
  6. Kostyukov AI, Kalezic I, Serenko SG, Ljubisavljevic M, Windhorst U, Johansson H. Spreading of fatiguerelated effects from active to inactive parts in the medial gastrocnemius muscle of the cat. Eur J Appl Physiol. 2002; 86(4): 295-307. CrossRef PubMed
    7.  
  7. Ervilha UF, Farina D, Arendt-Nielsen L, Graven-Nielsen T. Experimental muscle pain changes motor control strategies in dynamic contractions. Exp Brain Res. 2005; 164(2): 215-24. CrossRef PubMed
    8.  
  8. Harris RC, Sale C. Beta-alanine supplementation in highintensity exercise. Med Sport Sci. 2012; 59: 1-17. CrossRef PubMed
    9.  
  9. Kalezic I, Bugaychenko LA, Kostyukov AI, Pilyavskii AI, Ljubisavljevic M, Windhorst U. Fatigue-related depression of the feline monosynaptic gastrocnemiussoleus reflex. J Physiol. 2004; 556(Pt1): 283-96. CrossRef PubMed PubMedCentral
    10.  
  10. Lehedza AV, Gorkovenko AV, Vereshchaka IV, Dornowski M, Kostyukov AI. Comparative analysis of electromyographic muscle activity of the human hand during cyclic turns of isometric effort vector of wrist in opposite directions. Fiziol Zh. 2015; 61(2): 3-14. CrossRef  
  11. Williams WO. Huxley's model of muscle contraction with compliance. J Elasticity. 2011; 105(1): 365-80. CrossRef  
  12. Cooke R. Modulation of the actomyosin interaction during fatigue of skeletal muscle. Muselé Nerve. 2007; 36(6): 756-77. CrossRef PubMed
    13.  
  13. Pate E, Bhimani M, Franks-Skiba K, Cooke R. Reduced effect of pH on skitined rabbit psoas muscle mechanics at high temperatures: implications for fatigue. J Physiol. 1995; 486(3): 689-94. CrossRef PubMed PubMedCentral
    14.  
  14. Debold EP, Beck SE, Warshaw DM. The effect of low pH on single skeletal muscle myosin mechanics and kinetics. Am J Physiol Cell Physiol. 2008; 295(1): 173-9. CrossRef PubMed PubMedCentral
    15.  
  15. Walter G, Vandenborne K, Elliott M, Leigh JS. In vivo ATP synthesis rates in single human muscles during high intensity exercise. J Physiol. 1999; 519(Pt3): 901-10. CrossRef PubMed PubMedCentral
    16.  
  16. Westerblad H, Allen DG, Lännergren J. Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci. 2002; 17: 17-21. PubMed
    17.  
  17. Dahlstedt AJ, Katz A, Westerblad H. Role of myoplasmic phosphate in contractile function of skeletal muscle: studies on creatine kinase-deficient mice. J Physiol. 2001; 533(2): 379-88. CrossRef PubMed PubMedCentral
    18.  
  18. Dahlstedt AJ, Katz A, Wieringa B, Westerblad H. Is creatine kinase responsible for fatigue? Studies of skeletal muscle deficient of creatine kinase. FASEB J. 2000; 14(7): 982-90. PubMed
    19.  
  19. Fryer MW, Owen VJ, Lamb GD, and Stephenson DG. Effects of creatine phosphate and Pi on Ca2+ movements and tension development in rat skinned skeletal muscle fibres. J Physiol. 1995; 482(1): 123-40. CrossRef PubMed PubMedCentral
    20.  
  20. Allen DG, Lännergren J, Westerblad H. Muscle cell function during prolonged activity: cellular mechanisms of fatigue. Exp Physiol. 1995; 80(4): 497-527. CrossRef PubMed
    21.  
  21. Ahern GP, Laver DR. ATP inhibition and rectification of a Ca2+-activated anion channel in sarcoplasmic reticulum of skeletal muscle. Biophys J. 1998; 74(5): 2335-51. CrossRef  
  22. Westerblad H, Bruton JD, Lännergren J. The effect of intracellular pH on contractile function of intact, single fibres of mouse muscle declines with increasing temperature. J Physiol. 1997; 500(Pt1): 193-204. CrossRef PubMed PubMedCentral
    23.  
  23. Wiseman RW, Beck TW, Chase PB. Effect of intracellular pH on force development depends on temperature in intact skeletal muscle from mouse. Am J Physiol Cell Physiol 1996; 271(3 Pt1): 878-86.
    24.  
  24. Bangsbo J, Madsen K, Kiens B, Richter EA. Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man. J Physiol. 1996; 495(Pt2): 587-96. CrossRef PubMed PubMedCentral
    25.  
  25. Nelson DL, Lehninger MC. Principles of biochemistry. New York: WH Freeman and company, 2008; 1158 p.
    26.  
  26. Greer F, Friars D, Graham TE. Comparison of caffeine and theophylline ingestion: exercise metabolism and endurance. J Appl Physiol. 2000; 89(5): 1837-44. PubMed
    27.  
  27. Barreiro E, Gea J, Di Falco M, Kriazhev L, James S, Hussain SN. Protein carbonyl formation in the diaphragm. Am J Respir Cell Mol Biol. 2005; 32(1): 9-17. CrossRef PubMed
    28.  
  28. Tsakiris S, Parthimos T, Parthimos N, Tsakiris T, Schulpis KH. The beneficial effect of L-cysteine supplementation on DNA oxidation induced by forced training. Pharmacol Res. 2006; 53(4): 386-90. CrossRef PubMed
    29.  
  29. Vasilaki A, Mansouri A, Remmen H, van der Meulen, JH, Larkin L, Richardson AG, McArdle A, Faulkner JA, Jackson MJ. Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell. 2006; 5(2): 109-17. CrossRef PubMed
    30.  
  30. Hasegawa A, Suzuki S, Matsumoto Y, Okubo T. In vivo fatiguing contraction of rat diaphragm produces hydroxyl radicals. Free Radic Biol Med. 1997; 22(1-2): 349-54. CrossRef  
  31. Stamler J, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev. 2001; 81(1): 209-37. PubMed
    32.  
  32. Abraham RZ, Miller CC, Reid MB. The contractile response to nitric oxide (NO) varies among skeletal muscle. Endothelium. 1995; 3: 108.
    33.  
  33. Nijs J, Meeus M, McGregor NR, Meeusen R, de Schutter G, van Hoof E, de Meirleir K. Chronic fatigue syndrome: exercise performance related to immune dysfunction. Med Sci Sports Exerc. 2005; 37(10): 1647-54. CrossRef PubMed
    34.  
  34. McIver K L, Evans C, Kraus RM, Ispas L, Sciotti VM, Hickner RC. NO-mediated alterations in skeletal muscle nutritive blood flow and lactate metabolism in fibromyalgia. Pain. 2005; 120(1-2): 161-9. CrossRef PubMed
    35.  
  35. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from mouse. J Physiol. 1998; 509(Pt2): 565-75. CrossRef PubMed PubMedCentral
    36.  
  36. Leeuwenburgh C, Hollander J, Leichtweis S, Griffiths M, Gore M, Ji LL. Adaptations of glutathione antioxidant system to endurance training are tissue and muscle fiber specific. Am J Physiol Regul Integr Comp Physiol. 1997; 272 (1 Pt2): 363-9.
    37.  
  37. Moopanar TR, Allen DG. Reactive oxygen species reduce myofibrillar calcium sensitivity in fatiguing mouse skeletal muscle at 37°C. J Physiol. 2005; 564(Pt1): 189-99. CrossRef PubMed PubMedCentral
    38.  
  38. Kanter M. Free radicals, exercise and antioxidant supplementation. Proc Nutr Soc. 1998; 57(1): 9-13. CrossRef PubMed
    39.  
  39. Ji LL. Exercise sport science reviews: Exercise and oxidative stress: Role of the cellular antioxidant systems. Exerc Sport Sci Rev. 1995; 23(1): 135-66. PubMed
    40.  
  40. Clanton TL, Zuo L, Klawitter P. Oxidants and skeletal muscle function: physiologic and pathophysiologic implications. Proc Soc Exp Biol Med. 1999; 222(3): 253-62. CrossRef PubMed
    41.  
  41. Ji LL. Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med. 2000; 222(3): 283-92. CrossRef  
  42. Katz A, Hernández A, Caballero DM, Briceno JF, Amezquita LV, Kosterina N, Bruton JD, Westerblad H. Effects of N-acetylcysteine on isolated mouse skeletal muscle: contractile properties, temperature dependence, and metabolism. Pflugers Arch. 2014; 466(3): 577-85. CrossRef PubMed
    43.  
  43. Trice I, Haymes EM. Effects of caffeine ingestion on exerciseinduced changes during high-intensity, intermittent exercise. Int J Sport Nutr. 1995; 5(1): 37-44. CrossRef PubMed
    44.  
  44. Pasman WJ, van Baak MA, Jeukendrup AE. The effect of different dosages of caffeine on endurance performance time. Int J Sports Med. 1995; 16(4): 225-30. CrossRef PubMed
    45.  
  45. Graham TE, Spriet LL. Metabolic, catecholamine, and exercise performance responses to various doses of caffeine. J Appl Physiol. 1995; 78(3): 867-4. PubMed
    46.  
  46. Mohr T, van Soeren M, Graham TE. Caffeine ingestion and metabolic responses of tetraplegic humans during electrical cycling. J Appl Physiol. 1998; 85(3): 979-85. PubMed
    47.  
  47. Cohen BS, Nelson AG, Prevost MC. Effects of caffeine ingestion on endurance racing in heat and humidity. Eur J Appl Physiol. 1996; 73(3-4): 358-63. CrossRef  
  48. Jackman M, Wendling P, Friars D. Metabolic, catecholamine, and endurance responses to caffeine during intense exercise. J Appl Physiol. 1996; 81(4): 1658-63. PubMed
    49.  
  49. Tarnopolsky MA, Cupido C. Caffeine potentiates low frequency skeletal muscle force in habitual and nonhabitual caffeine consumers. J Appl Physiol. 2000; 89(5): 1719-24. PubMed
    50.  
  50. Raguso CA, Coggan AR, Sidossis LS. Effect of theophylline on substratemetabolismduring exercise. Metabolism. 1996; 45(9): 1153-60. CrossRef  
  51. Graham TE, Helge JW, MacLean DA. Caffeine ingestion does not alter carbohydrate or fat metabolism in human skeletal muscle during exercise. J Physiol. 2000; 529(Pt3): 837-47. CrossRef PubMed PubMedCentral
    52.  
  52. Laurent D, Scheider KE, Prusaczyk WK. Effects of caffeine on muscle glycogen utilization and the neuroendocrine axis during exercise. J Clin Endocrinol Metab. 2000; 85(6): 2170-5. CrossRef  
  53. Chesley A, Howlett RA, Heigenhauser JF. Regulation of muscle glycogenolytic flux during intense aerobic exercise after caffeine ingestion. Am J Physiol. 1998; 275(2 Pt2): 596-603.
    54.  
  54. MacIntosh BR, Wright BM. Caffeine ingestion and performance of a 1500 meter swim. Can J Appl Physiol. 1995; 20(2): 168-77. CrossRef PubMed
    55.  
  55. Kalmar JM, Cafarelli E. Effects of caffeine on neuromuscular fatigue. J Appl Physiol. 1999; 87(2): 801-8. PubMed
    56.  
  56. Tullberg M, Alstergren PJ, Ernberg MM. Effects of lowpower laser exposure on masseter muscle pain and microcirculation. Pain. 2003; 105(1-2): 89-96. CrossRef  
  57. Silveira PC, Silva LA, Fraga DB, Freitas TP, Streck EL, Pinho R. Evaluation of mitochondrial respiratory chain activity in muscle healing by low-level laser therapy. J Photochem Photobiol B. 2009; 95(2): 89-92. CrossRef PubMed
    58.  
  58. Avni D, Levkovitz S, Maltz L, Oron U. Protection of skeletal muscles from ischemic injury: low-level laser therapy increases antioxidant activity. Photomed Laser Surg. 2005; 23(3): 273-7. CrossRef PubMed
    59.  
  59. Rizzi CF, Mauriz JL, Freitas Correa DS. Effects of lowlevel laser therapy (LLLT) on the nuclear factor (NF)- kappaB signaling pathway in traumatized muscle. Lasers Surg Med. 2006; 38(7): 704-13. CrossRef PubMed
    60.  
  60. Lopes-Martins RA, Marcos RL, Leonardo PS. Effect of low-level laser (Ga-Al-As 655 nm) on skeletal muscle fatigue induced by electrical stimulation in rats. J Appl Physiol. 2006; 101(1): 283-8. CrossRef PubMed
    61.  
  61. Leal Junior EC, Lopes-Martins RA, de Almeida P, Ramos L, Iversen VV, Bjordal JM. Effect of low-level laser therapy (GaAs 904 nm) in skeletal muscle fatigue and biochemical markers of muscle damage in rats. Eur J Appl Physiol. 2010; 108(6): 1083-8. CrossRef PubMed
    62.  
  62. Mach J, Midgley AW, Dank S, Grant R, Bentley DJ. The effect of antioxidant supplementation on fatigue during exercise: potential role for NAD+(H). Nutrients. 2010; 2(3): 319-29. CrossRef PubMed PubMedCentral
    63.  
  63. Prylutska SV, Grynyuk II, Matyshevska OP, Prylutskyy YuI, Ritter U, Scharff P. Anti-oxidant properties of C60 fullerenes in vitro. Fullerenes, Nanotubes, Carbon Nanostruct. 2008; 16(5-6): 698-705. CrossRef  
  64. Ritter U, Prylutskyy YuI, Evstigneev MP, Davidenko NA, Cherepanov VV, Senenko AI, Marchenko OA, Naumovets AG. Structural features of highly stable reproducible C60 fullerene aqueous colloid solution probed by various techniques. Fullerenes, Nanotubes, Carbon Nanostruct. 2015; 23(6): 530-4. CrossRef  
  65. Sun T, Xu Z. Radical scavenging activities of alpha-alanine C60 adduct. Bioorg Med Chem Lett. 2006; 16(14): 3731-4. CrossRef PubMed
    66.  
  66. Lai HS, Chen WJ, Chiang LY. Free radical scavenging activity of fullerenol on the ischemia-reperfusion intestine in dogs. World J Surg. 2000; 24(4): 450-4. CrossRef PubMed
    67.  
  67. Chen YW, Hwang KC, Yen CC, Lai YL. Fullerene derivatives protect against oxidative stress in RAW 264.7 cells and ischemia-reperfused lungs. Am J Physiol Regul Integr Comp Physiol. 2004; 287(1): 21-6. CrossRef PubMed
    68.  
  68. Lai YL, Murugan P, Hwang KC. Fullerene derivative attenuates ischemia-reperfusion-induced lung injury. Life Sci. 2003; 72(11): 1271-8. CrossRef  
  69. Cataldo F, Da Ros T. Medicinal chemistry and pharmacological potential of fullerenes and carbon nanotubes. Berlin: Springer. 2008; 408 p. CrossRef  
  70. Wilson SR. Biological aspects of fullerenes. Fullerenes: Chemistry, Physics and Technology. 2000; 437-65.
    71.  
  71. Andreichenko KS, Prylutska SV, Medynska KO, Bogutska KI, Nurishchenko NE, Prylutskyy YuI, Ritter U, Scharff P. Effect of fullerene C60 on ATPase activity and superprecipitation of skeletal muscle actomyosin. Ukr Biochem J. 2013; 85(2): 20-6. CrossRef  
  72. Ashcroft JM, Tsyboulski DA, Hartman KB. Fullerene C60 immunoconjugates: interaction of water-soluble C60 derivatives with the murine anti-gp240 melanoma antibody. Chem Commun. 2006; 28: 3004-6. CrossRef PubMed
    73.  
  73. Prylutska SV, Burlaka AP, Prylutskyy YuI. Pristine C60 fullerenes inhibit the rate of tumor growth and metastasis. Exp Oncol. 2011; 33(3): 162-4. PubMed
    74.  
  74. Prylutska SV, Burlaka AP, Klymenko PP. Using watersoluble C60 fullerenes in anticancer therapy. Cancer Nanotechnol. 2011; 2(1-6): 105-10. CrossRef PubMed PubMedCentral
    75.  
  75. Panchuk RR, Prylutska SV, Chumak VV, Skorokhyd NR, Lehka LV, Evstigneev MP, Prylutskyy YuI, Berger W, Heffeter P, Scharff P, Ritter U, Stoika RS. Application of C60 fullerene-doxorubicin complex for tumor cell treatment in vitro and in vivo. J Biomed Nanotechnol. 2015; 11(7): 1139-52. CrossRef PubMed
    76.  
  76. Halenova TI, Vareniuk IM, Roslova NM, Dzerzhynsky ME, Savchuk OM, Ostapchenko LI, Prylutskyy YuI, Ritter U, Scharff P. Hepatoprotective effect of orally applied water-soluble pristine C60 fullerene against CCl4-induced acute liver injury in rats. RSC Adv. 2016; 6(102): 100046-55. CrossRef  
  77. Mori T, Takada H, Ito S. Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology. 2006; 225(1): 48-54. CrossRef PubMed
    78.  
  78. Wang IC, Tai LA, Lee DD. C60 and water-soluble fullerene derivatives as antioxidants against radicals-initiated lipid peroxidation. J Med Chem. 1999; 42(22): 4614-20. CrossRef PubMed
    79.  
  79. Gharbi N, Pressac M, Hadchouel M. Fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett. 2005; 5(12): 2578-85. CrossRef PubMed
    80.  
  80. Xiao L, Takada H, Gan X, Miwa N. The water-soluble fullerene derivative «radicalsponge» exerts cytoprotective action against UV irradiation but not visible-lightcatalyzed cytotoxicity in human skin keratinocytes. Bioorg Med Chem Lett. 2006; 16(5): 1590-5. CrossRef PubMed
© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.