ORIGINAL RESEARCH

Transcription factors in human skeletal muscle associated with single and regular strength exercises

Lednev EM1,2, Makhnovskii PA2, Vepkhvadze TF2, Sultanov RI1, Zhelankin AV1, Kanygina AV1, Popov DV1,2, Generozov EV1
About authors

1 Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical Biological Agency, Moscow, Russia

2 Institute for Biomedical Problems of the Russian Academy of Sciences, Moscow, Russia

Correspondence should be addressed: Egor M. Lednev
Khoroshevskoe shosse, 76A, Moscow, 123007, Russia moc.liamg@zuahdel

About paper

Funding: the study was supported financially by the Russian Science Foundation, Agreement № 21-15-00362 "Investigation of molecular genetic mechanisms of morphofunctional changes in human muscle fibers during high-intensity physical loads".

Author contribution: Lednev EM, Vepkhvadze TF — study design and conduct, muscle sampling; Makhnovskii PA, Sultanov RI and Kanygina AV — bioinformatic data analysis; Zhelankin AV, Lednev EM — laboratory research; Generozov EV, Popov DV — study design and conduct, data processing, article authoring.

Compliance with ethical standards: the study was approved by the Ethics Committee of the Lopukhin Federal Research and Clinical Center Of Physical-Chemical Medicine (Minutes № 202/06/01 of June 01, 2021). All participants signed the voluntary informed consent form.

Received: 2023-07-21 Accepted: 2023-09-01 Published online: 2023-09-27
|
  1. Vinogradova OL, Popov DV, Netreba AI, Cvirkun DV, Kurochkina NS, Bachinin AV, i dr. Optimizaciya processa fizicheskoj trenirovki: razrabotka novyx “shhadyashhix” podxodov k trenirovke silovyx vozmozhnostej, Fiziologiya cheloveka/"Human Physiol. 39 (2013) 71–85. Dostupno po ssylke: https://doi.org/10.7868/S0131164613050172. Russian.
  2. Solsona R, Pavlin L, Bernardi H., Sanchez AMJ. Molecular regulation of skeletal muscle growth and organelle biosynthesis: Practical recommendations for exercise training. Int J Mol Sci. 2021; 22: 1–31. Available from: https://doi.org/10.3390/ijms22052741.
  3. Mesquita PHC, Vann CG, Phillips SM, McKendry J, Young KC, Kavazis AN, et al. Skeletal muscle ribosome and mitochondrial biogenesis in response to different exercise training modalities. Front Physiol. 2021; 12. Available from: https://doi.org/10.3389/fphys.2021.725866.
  4. Gordon PM, Liu D, Sartor MA, IglayReger HB, Pistilli EE, Gutmann L, et al. Resistance exercise training influences skeletal muscle immune activation: a microarray analysis. J Appl Physiol. 2012: 112: 443–53. Available from: https://doi.org/10.1152/japplphysiol.00860.2011.
  5. Dickinson JM, D'Lugos AC, Naymik MA, Siniard AL, Wolfe AJ, Curtis DP, et al. Transcriptome response of human skeletal muscle to divergent exercise stimuli. J Appl Physiol. 2018; 124: 1529–40. Available from: https://doi.org/10.1152/japplphysiol.00014.2018.
  6. Damas F, Ugrinowitsch C, Libardi CA, Jannig PR, Hector AJ, Mcglory C, et al. Resistance training in young men induces muscle transcriptome-wide changes associated with muscle structure and metabolism refining the response to exercise-induced stress. Eur J Appl Physiol. 2018; 118: 2607–16. Available from: https://doi.org/10.1007/s00421-018-3984-y.
  7. Raue U, Trappe TA, Estrem ST, Qian HR, Helvering LM, Smith RC, et al. Transcriptome signature of resistance exercise adaptations: Mixed muscle and fiber type specific profiles in young and old adults. J Appl Physiol. 2012; 112: 1625–36. Available from: https://doi.org/10.1152/japplphysiol.00435.2011.
  8. Lundberg TR, Fernandez-Gonzalo R, Gustafsson T, Tesch PA. Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training. J Appl Physiol. 2013; 114: 81–89. Available from: https://doi.org/10.1152/japplphysiol.01013.2012.
  9. Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: Sex specific regulation. BMC Genomics. 2010; 11: 659. Available from: https://doi.org/10.1186/1471-2164-11-659.
  10. Nascimento EBM, Hangelbroek RWJ, GHooiveld GJEJ, Hoeks J, Van Marken Lichtenbelt WD, Hesselink MHC, et al. Comparative transcriptome analysis of human skeletal muscle in response to cold acclimation and exercise training in human volunteers. BMC Med Genomics. 2020; 13: 1–11. Available from: https://doi.org/10.1186/s12920-020-00784-z.
  11. Stepto NK, Coffey VG, Carey AL, Ponnampalam AP, Canny BJ, Powell D, et al. Global gene expression in skeletal muscle from well-trained strength and endurance athletes. Med Sci Sports Exerc. 2009; 41: 546–65. Available from: https://doi.org/10.1249/MSS.0b013e31818c6be9.
  12. Schoenfeld BJ, Grgic J, Ogborn D, Krieger JW. Strength and hypertrophy adaptations between low- vs. High-load resistance training: A systematic review and meta-analysis. J Strength Cond Res. 2017; 31: 3508–23. Available from: https://doi.org/10.1519/JSC.0000000000002200.
  13. Krieger JW. Single Vs. Multiple Sets of Resistance. J Strength Cond Res. 2010; 24: 1150–9. Available from: htpps://doi.org/10.1519/JSC.0b013e3181d4d36
  14. Schoenfeld BJ, Ogborn D, Krieger JW. Effects of Resistance Training Frequency on Measures of Muscle Hypertrophy: A Systematic Review and Meta-Analysis. Sport Med. 2016; 46: 1689–97. Available from: https://doi.org/10.1007/s40279-016-0543-8.
  15. Catoire M, Mensink M, Boekschoten MV, Hangelbroek R, Müller M, Schrauwen P, et al. Pronounced Effects of Acute Endurance Exercise on Gene Expression in Resting and Exercising Human Skeletal Muscle. PLoS One. 2012; 7. Available from: https://doi.org/10.1371/journal.pone.0051066.
  16. Schroder EA, Harfmann BD, Zhang X, Srikuea R, England JH, Hodge BA, et al. Intrinsic muscle clock is necessary for musculoskeletal health. J Physiol. 2015; 593: 5387–404. Available from: https://doi.org/10.1113/JP271436.
  17. Shanely AR, Zwetsloot KA, Travis Triplett N, Meaney MP, Farris GE, Nieman DC. Human skeletal muscle biopsy procedures using the modified Bergström technique. J Vis Exp. 2014; 1–8. Available from: https://doi.org/10.3791/51812.
  18. Makhnovskii PA, Gusev OA, Bokov RO, Gazizova GR, Vepkhvadze TF, Lysenko EA, et al. Alternative transcription start sites contribute to acute-stress-induced transcriptome response in human skeletal muscle. Hum Genomics. 2022; 16: 1–13. Available from: https://doi.org/10.1186/s40246-022-00399-8.
  19. Campos GER, Luecke TJ, Wendeln HK, Toma K, Hagerman FC, Murray TF et al. Muscular adaptations in response to three different resistance-training regimens: Specificity of repetition maximum training zones. Eur J Appl Physiol. 2002; 88: 50–60. Available from: https://doi.org/10.1007/s00421-002-0681-6.
  20. Yapici H, Gülü M, Yagin FH, Ugurlu D, Comertpay E, Eroglu O et al. The effect of 8-weeks of combined resistance training and chocolate milk consumption on maximal strength, muscle thickness, peak power and lean mass, untrained, university-aged males. Front Physiol. 2023; 14: 1–11. Available from: https://doi.org/10.3389/fphys.2023.1148494.
  21. Deane CS, Willis CRG, Phillips BE, Atherton PJ, Harries LW, Ames RM, et al. Transcriptomic meta-analysis of disuse muscle atrophy vs. resistance exercise-induced hypertrophy in young and older humans. J Cachexia Sarcopenia Muscle. 2021; 12: 629–45. Available from: https://doi.org/10.1002/jcsm.12706.
  22. Pillon NJ, Gabriel BM, Dollet L, Smith JAB, Sardón Puig L, Botella J, et al. Transcriptomic profiling of skeletal muscle adaptations to exercise and inactivity. Nat Commun. 2020; 11: 470. Available from: https://doi.org/10.1038/s41467-019-13869-w.
  23. Chapman MA, Arif M, Emanuelsson EB, Reitzner SM, Lindholm ME, Mardinoglu A, et al. Skeletal Muscle Transcriptomic Comparison between Long-Term Trained and Untrained Men and Women. Cell Rep. 2020; 31. Available from: https://doi.org/10.1016/j.celrep.2020.107808.
  24. Dzik KP, Grzywacz T, Łuszczyk M, Kujach S, Flis DJ, Kaczor JJ. Single bout of exercise triggers the increase of vitamin D blood concentration in adolescent trained boys: a pilot study. Sci Rep. 2022; 12: 1–10. Available from: https://doi.org/10.1038/s41598-022-05783-x.
  25. Rundqvist HC, Montelius A, Osterlund T, Norman B, Esbjornsson M, Jansson E. Acute sprint exercise transcriptome in human skeletal muscle. PLoS One. 2019; 14: 1–24. Available from: https://doi.org/10.1371/journal.pone.0223024.
  26. Makhnovskii PA, Bokov RO, Kolpakov FA, Popov DV. Transcriptomic signatures and upstream regulation in human skeletal muscle adapted to disuse and aerobic exercise. Int J Mol Sci. 2021; 22: 1–20. Available from: https://doi.org/10.3390/ijms22031208.
  27. Birdsey GM, Shah AV, Dufton N, Reynolds LE, Almagro LO, Yang Y et al. The endothelial transcription factor erg promotes vascular stability and growth through Wnt/β-catenin signaling. Dev Cell. 2015; 32: 82–96. Available from: https://doi.org/10.1016/j.devcel.2014.11.016.
  28. Sakuma K, Yamaguchi A. The functional role of calcineurin in hypertrophy, regeneration, and disorders of skeletal muscle. J Biomed Biotechnol. 2010; 2010. Available from: https://doi.org/10.1155/2010/721219.
  29. Hudson MB, Price SR. Calcineurin: A poorly understood regulator of muscle mass. Int J Biochem Cell Biol. 2013; 45: 2173–8. Available from: https://doi.org/10.1016/j.biocel.2013.06.029.
  30. Dunn SE, Burns JL, Michel RN. Calcineurin is required for skeletal muscle hypertrophy. J Biol Chem. 1999; 274: 21908–12. Available from: https://doi.org/10.1074/jbc.274.31.21908.
  31. Ehlers ML, Celona B, Black BL. NFATc1 controls skeletal muscle fiber type and is a negative regulator of MyoD activity. Cell Rep. 2014; 8: 1639–48. Available from: https://doi.org/10.1016/j.celrep.2014.08.035.NFATc1.
  32. Darby IA, Bisucci T, Raghoenath S, Olsson J, Muscat GEO, Koopman P. Sox18 is transiently expressed during angiogenesis in granulation tissue of skin wounds with an identical expression pattern to Flk-1 mRNA. Lab Investig. 2001; 81: 937–43. Available from: https://doi.org/10.1038/labinvest.3780304.
  33. Neyroud D, Nosacka RL, Callaway CS, Trevino JG, Hu H, Judge SM, et al. FoxP1 is a transcriptional repressor associated with cancer cachexia that induces skeletal muscle wasting and weakness. J Cachexia Sarcopenia Muscle. 2021; 12: 421–42. Available from: https://doi.org/10.1002/jcsm.12666.
  34. Wright WE, Li C, Zheng C, Tucker HO. FOXP1 Interacts with MyoD to Repress its Transcription and Myoblast Conversion. J Cell Signal. 2021; 2: 9–26.
  35. Kurosaka M, Ogura Y, Sato S, Kohda K, Funabashi T. Transcription factor signal transducer and activator of transcription 6 (STAT6) is an inhibitory factor for adult myogenesis. Skelet Muscle. 2021; 11: 1–14. Available from: https://doi.org/10.1186/s13395-021-00271-8.
  36. Yamaki T, Wu CL, Gustin M, Lim J, Jackman RW, Kandarian SC. Rel A/p65 is required for cytokine-induced myotube atrophy. Am J Physiol. Cell Physiol. 2012; 303: 135–43. Available from: https://doi.org/10.1152/ajpcell.00111.2012.
  37. Arensdorf AM, Diedrichs D, Rutkowski DT. Regulation of the transcriptome by ER stress: Non-canonical mechanisms and physiological consequences. Front Genet. 2013; 4: 1–16. Available from: https://doi.org/10.3389/fgene.2013.00256.
  38. Marafon BB, Pinto AP, Ropelle ER, de Moura LP, Cintra DE, Pauli JR, et al. Muscle endoplasmic reticulum stress in exercise. Acta Physiol. 2022; 235: e13799. Available from: https://doi.org/https://doi.org/10.1111/apha.13799.
  39. Møller AB, Vendelbo MH, Schjerling P, Couppé C, Møller N, Kjær M et al. Immobilization decreases foxo3a phosphorylation and increases autophagy-related gene and protein expression in human skeletal muscle. Front Physiol. 2019; 10: 1–14. Available from: https://doi.org/10.3389/fphys.2019.00736.
  40. Senf SM, Dodd SL, Judge AR. FOXO signaling is required for disuse muscle atrophy and is directly regulated by Hsp70. Am J Physiol. Cell Physiol. 2010; 298. Available from: https://doi.org/10.1152/ajpcell.00315.2009.
  41. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell. 2004; 117: 399–412. Available from: https://doi.org/10.1016/S0092-8674(04)00400-3.