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Changes in biomarker levels and myofiber constitution in rat soleus muscle at different exercise intensities

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Abstract

Although exercise affects the function and structure of skeletal muscle, our knowledge regarding the biomedical alterations induced by different intensities of exercise is incomplete. Here we report on the changes in biomarker levels and myofiber constitution in the rat soleus muscle induced by exercise intensity. Male adult rats at 7 weeks of age were divided into 3 groups by exercise intensity, which was set based on the accumulated lactate levels in the blood using a treadmill: stationary control (0 m/min), aerobic exercise (15 m/min), and anaerobic exercise (25 m/min). The rats underwent 30 min/day treadmill training at different exercise intensities for 14 days. Immediately after the last training session, the soleus muscle was dissected out in order to measure the muscle biomarker levels and evaluate the changes in the myofibers. The mRNA expression of citrate synthase, glucose-6-phosphate dehydrogenase, and Myo D increased with aerobic exercise, while the mRNA expression of myosin heavy-chain I and Myo D increased in anaerobic exercise. These results suggest that muscle biomarkers can be used as parameters for the muscle adaptation process in aerobic/anaerobic exercise. Interestingly, by 14 days after the anaerobic exercise, the number of type II (fast-twitch) myofibers had decreased by about 20%. Furthermore, many macrophages and regenerated fibers were observed in addition to the injured fibers 14 days after the anaerobic exercise. Constitutional changes in myofibers due to damage incurred during anaerobic exercise are necessary for at least about 2 weeks. These results indicate that the changes in the biomarker levels and myofiber constitution by exercise intensity are extremely important for understanding the metabolic adaptations of skeletal muscle during physical exercise.

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Abbreviations

CS:

Citrate synthase

CK:

Creatine kinase

G6PD:

Glucose-6-phosphate dehydrogenase

References

  1. Husmann I, Soulet L, Gautron J, Martelly I, Barritault D (1996) Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev 7(3):249–258

    Article  CAS  PubMed  Google Scholar 

  2. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ishido M, Uda M, Masuhara M, Kami K (2006) Alterations of M-cadherin, neural cell adhesion molecule and beta-catenin expression in satellite cells during overload-induced skeletal muscle hypertrophy. Acta Physiol 187(3):407–418. https://doi.org/10.1111/j.1748-1716.2006.01577.x

    Article  CAS  Google Scholar 

  4. Ishido M, Kasuga N, Masuhara M (2008) Time Course Changes of the Expression of IGF-I, Phosphorylated Akt and Phosphorylated mTOR in Myofibers of the Early Stage of Functionally Overloaded Skeletal Muscle. Adv Exerc Sports Physiol 14(2):25–29

    Google Scholar 

  5. Halling JF, Ringholm S, Olesen J, Prats C, Pilegaard H (2017) Exercise training protects against aging-induced mitochondrial fragmentation in mouse skeletal muscle in a PGC-1α dependent manner. Exp Gerontol 96:1–6. https://doi.org/10.1016/j.exger.2017.05.020

    Article  CAS  PubMed  Google Scholar 

  6. Fridén J (1984) Changes in human skeletal muscle induced by long-term eccentric exercise. Cell Tissue Res 236(2):365–372

    Article  PubMed  Google Scholar 

  7. Kariya F, Yamauchi H, Kobayashi K, Narusawa M, Nakahara Y (2004) Effects of prolonged voluntary wheel-running on muscle structure and function in rat skeletal muscle. Eur J Appl Physiol 92(1–2):90–97. https://doi.org/10.1007/s00421-004-1061-1

    Article  PubMed  Google Scholar 

  8. Suzuki J (2016) Short-duration intermittent hypoxia enhances endurance capacity by improving muscle fatty acid metabolism in mice. Physiol Rep 4(7):e12744. https://doi.org/10.14814/phy2.12744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Suzuki J (2017) Endurance performance is enhanced by intermittent hyperbaric exposure via up-regulation of proteins involved in mitochondrial biogenesis in mice. Physiol Rep 5(15):e13349. https://doi.org/10.14814/phy2.13349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Siu PM, Donley DA, Bryner RW, Alway SE (2003) Citrate synthase expression and enzyme activity after endurance training in cardiac and skeletal muscles. J Appl Physiol 94(2):555–560. https://doi.org/10.1152/japplphysiol.00821.2002

    Article  CAS  PubMed  Google Scholar 

  11. Siu PM, Donley DA, Bryner RW, Alway SE (2004) Myogenin and oxidative enzyme gene expression levels are elevated in rat soleus muscles after endurance training. J Appl Physiol 97(1):277–285. https://doi.org/10.1152/japplphysiol.00534.2004

    Article  CAS  PubMed  Google Scholar 

  12. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ (2007) Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol 292(3):R1271–R1278. https://doi.org/10.1152/ajpregu.00472.2006

    Article  CAS  PubMed  Google Scholar 

  13. Lesmana R, Iwasaki T, Iizuka Y, Amano I, Shimokawa N, Koibuchi N (2016) The change in thyroid hormone signaling by altered training intensity in male rat skeletal muscle. Endocr J 63(8):727–738. https://doi.org/10.1507/endocrj.EJ16-0126

    Article  CAS  PubMed  Google Scholar 

  14. Hood DA, Irrcher I, Ljubicic V, Joseph AM (2006) Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209:2265–2275. https://doi.org/10.1242/jeb.02182

    Article  CAS  PubMed  Google Scholar 

  15. Soya H, Mukai A, Deocaris CC, Ohiwa N, Chang H, Nishijima T, Fujikawa T, Togashi K, Saito T (2007) Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci Res 58(4):341–348. https://doi.org/10.1016/j.neures.2007.04.004

    Article  CAS  PubMed  Google Scholar 

  16. Brooke MH, Kaiser KK (1970) Muscle fiber types: how many and what kind? Arch Neurol 23(4):369–379

    Article  CAS  PubMed  Google Scholar 

  17. Aparicio VA, Tassi M, Nebot E, Camiletti-Moirón D, Ortega E, Porres JM, Aranda P (2014) High-intensity exercise may compromise renal morphology in rats. Int J Sports Med 35(8):639–644. https://doi.org/10.1055/s-0033-1354383

    Article  CAS  PubMed  Google Scholar 

  18. Malaguti M, Angeloni C, Garatachea N, Baldini M, Leoncini E, Collado PS, Teti G, Falconi M, Gonzalez-Gallego J, Hrelia S (2009) Sulforaphane treatment protects skeletal muscle against damage induced by exhaustive exercise in rats. J Appl Physiol 107(4):1028–1036. https://doi.org/10.1152/japplphysiol.00293.2009

    Article  CAS  PubMed  Google Scholar 

  19. Koz M, Erbaş D, Bilgihan A, Aricioğlu A (1992) Effects of acute swimming exercise on muscle and erythrocyte malondialdehyde, serum myoglobin, and plasma ascorbic acid concentrations. Can J Physiol Pharmacol 70(10):1392–1395

    Article  CAS  PubMed  Google Scholar 

  20. Siu PM, Donley DA, Bryner RW, Alway SE (2004) Myogenin and oxidative enzyme gene expression levels are elevated in rat soleus muscles after endurance training. J Appl Physiol 97(1):277–285. https://doi.org/10.1152/japplphysiol.00534.2004

    Article  CAS  PubMed  Google Scholar 

  21. Lehmann M, Foster C, Gastmann U, Keizer H, Steinacker JM (1999) Definition, types, symptoms, findings, underlying mechanisms, and frequency of overtraining and overtraining syndrome. In: Lehmann M, Foster C, Gastmann U, Keizer H, Steinacker JM (eds) Overload, Performance Incompetence, and Regeneration in Sport. Springer, New York, pp 1–6

    Chapter  Google Scholar 

  22. Fry AC, Steinacker JM, Meeusen R (2005) Endocrinology of overtraining. In: Kraemer WJ, Rogol AD (eds) The Endocrine System in Sports and Exercise. Blackwell Publishing, Oxford, pp 578–599

    Chapter  Google Scholar 

  23. Fry RW, Morton AR, Keast D (1991) Overtraining in athletes. An update. Sports Med 12(1):32–65

    Article  CAS  PubMed  Google Scholar 

  24. Palacios G, Pedrero-Chamizo R, Palacios N, Maroto-Sánchez B, Aznar S, González-Gross M, EXERNET Study Group (2015) Biomarkers of physical activity and exercise. Nutr Hosp 31(Suppl 3):237–244

    PubMed  Google Scholar 

  25. Chiu D, Wang HH, Blumenthal MR (1976) Creatine phosphokinase release as a measure of tourniquet effect on skeletal muscle. Arch Surg 111(1):71–74

    Article  CAS  PubMed  Google Scholar 

  26. Seene T, Kaasik P, Alev K, Pehme A, Riso EM (2004) Composition and turnover of contractile proteins in volume-overtrained skeletal muscle. Int J Sports Med 25(6):438–445. https://doi.org/10.1055/s-2004-820935

    Article  CAS  PubMed  Google Scholar 

  27. Valberg SJ, Borgia L (2009) Muscle adaptations during growth and early training. In: Pagan JD (ed) Advances in equine nutrition IV. Kentucky Equine Research, Kentucky, pp 193–202

    Google Scholar 

  28. Lim CH, Gil JH, Quan H, Viet DH, Kim CK (2018) Effect of 8-week leucine supplementation and resistance exercise training on muscle hypertrophy and satellite cell activation in rats. Physiol Rep 6(12):e13725. https://doi.org/10.14814/phy2.13725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Spodaryk K, Miszta H, Dabrowski Z, Gawroński W (1989) Metabolism of red blood cells after short-term exercise in rats. Acta Physiol Pol 40(4):381–386

    CAS  PubMed  Google Scholar 

  30. Ohsawa I, Konno R, Masuzawa R, Kawano F (2018) Amount of daily exercise is an essential stimulation to alter the epigenome of skeletal muscle in rats. J Appl Physiol 125:1097. https://doi.org/10.1152/japplphysiol.00074.2018

    Article  CAS  PubMed  Google Scholar 

  31. Short KR, Vittone JL, Bigelow ML, Proctor DN, Coenen-Schimke JM, Rys P, Nair KS (2005) Changes in myosin heavy chain mRNA and protein expression in human skeletal muscle with age and endurance exercise training. J Appl Physiol 99(1):95–102. https://doi.org/10.1152/japplphysiol.00129.2005

    Article  CAS  PubMed  Google Scholar 

  32. Eigendorf J, May M, Friedrich J, Engeli S, Maassen N, Gros G, Meissner JD (2018) High intensity high volume interval training improves endurance performance and induces a nearly complete slow-to-fast fiber transformation on the mRNA level. Front Physiol 9:601. https://doi.org/10.3389/fphys.2018.00601

    Article  PubMed  PubMed Central  Google Scholar 

  33. Yoseph B, Soker S (2015) Redefining the satellite cell as the motor of skeletal muscle regeneration. J Sci Appl: Biomed 3(5):76–82

    Google Scholar 

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Acknowledgements

We would like to thank Drs. Hideaki Soya and Hiroshi Yorifuji for critical discussion and Drs. Lu Yu and Tsuyoshi Ichinose for technical assistance. This study was supported in part by a Grant-in-Aid for Challenging Exploratory Research (No. 24659449) and Grant-in-Aid for Scientific Research (No. 21390065) to N.K. and T.I. from the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT) and DIKTI-PUPT (2016) from Indonesian Ministry of Education to R.L. and R.F.

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  1. Reni Farenia and Ronny Lesmana contributed equally to this work.

Authors and Affiliations

  1. Department of Integrative Physiology, Gunma University Graduate School of Medicine, Gunma, 371-8511, Japan

    Reni Farenia, Ronny Lesmana, Toshiharu Iwasaki, Noriyuki Koibuchi & Noriaki Shimokawa

  2. Department of Basic Science, Physiology Division, Faculty of Medicine, Universitas Padjadjaran, Bandung, 45363, Indonesia

    Reni Farenia & Ronny Lesmana

  3. Central Laboratory, Universitas Padjadjaran, Bandung, 45363, Indonesia

    Ronny Lesmana

  4. Department of Nutrition, Takasaki University of Health and Welfare, Gunma, 370-0033, Japan

    Kaoru Uchida & Noriaki Shimokawa

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  1. Reni Farenia
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Correspondence to Noriaki Shimokawa.

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Farenia, R., Lesmana, R., Uchida, K. et al. Changes in biomarker levels and myofiber constitution in rat soleus muscle at different exercise intensities. Mol Cell Biochem 458, 79–87 (2019). https://doi.org/10.1007/s11010-019-03532-9

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