The integrative role of physical exercise and muscle satellite cells in remodeling muscle structure and function
Abstract
With the aging of the population and changes in lifestyle, sustaining muscular function has become essential for enhancing quality of life. Muscle satellite cells, as the principal source of regeneration for skeletal muscles, are essential for muscle growth, maintenance, and repair. Our review explores how physical exercise (PE) impacts the remodeling of muscle structure and function by modulating the activity of Muscle satellite cells (MuSCs), and further identifies the underlying implications of this process for the prevention and treatment of degenerative muscle diseases. By exploring current evidences on the interaction between MuSCs and PE, our review investigating the effect of PE on the activity, proliferation, and differentiation capabilities of MuSCs, and how these changes improve the enhancement of muscle mass and function. Evidences confirmed that PE can enhance the contribution of MuSCs to muscle fibers, particularly by boosting muscle adaptability through changes in muscle fiber type and size. PE-induced activation of MuSCs is linked not only to an increase in the number of muscle fibers but also with promoted endurance and strength performance of muscles. Besides, the positive effects of PE on MuSCs may vary with the form, intensity, and duration of PE. Additionally, PE plays a crucial role in the remodeling of muscle structure and function through the activation and proliferation of MuSCs, stressing the potential value of developing appropriate PE interventions in the prevention and treatment of muscle-related diseases, particularly among the elderly. Future research should further explore the specific effects of various types and intensities of PE on MuSCs activities to maximize exercise prescriptions for strengthening muscle health and function.
References
1. Masschelein E, D’Hulst G, Zvick J, et al. Exercise promotes satellite cell contribution to myofibers in a load-dependent manner. Skeletal Muscle. 2020; 10(1). doi: 10.1186/s13395-020-00237-2
2. Wang YX, Rudnicki MA. Satellite cells, the engines of muscle repair. Nature Reviews Molecular Cell Biology. 2011; 13(2). 127–133. doi: 10.1038/nrm3265
3. Snijders T, Nederveen JP, McKay BR, et al. Satellite cells in human skeletal muscle plasticity. Frontiers in Physiology. 2015; 6. doi: 10.3389/fphys.2015.00283
4. Fukada S ichiro, Higashimoto T, Kaneshige A. Differences in muscle satellite cell dynamics during muscle hypertrophy and regeneration. Skeletal Muscle. 2022; 12(1). doi: 10.1186/s13395-022-00300-0
5. Lu L, Mao L, Feng Y, et al. Effects of different exercise training modes on muscle strength and physical performance in older people with sarcopenia: a systematic review and meta-analysis. BMC Geriatrics. 2021; 21(1). doi: 10.1186/s12877-021-02642-8
6. Zhang Y, Zou L, Chen ST, et al. Effects and Moderators of Exercise on Sarcopenic Components in Sarcopenic Elderly: A Systematic Review and Meta-Analysis. Frontiers in Medicine. 2021; 8. doi: 10.3389/fmed.2021.649748
7. Morroni J, Benedetti A, Esposito L, et al. Injury-experienced satellite cells retain long-term enhanced regenerative capacity. Stem Cell Research & Therapy. 2023; 14(1). doi: 10.1186/s13287-023-03492-4
8. Dumont NA, Wang YX, Rudnicki MA. Intrinsic and extrinsic mechanisms regulating satellite cell function. Development. 2015; 142(9). doi: 10.1242/dev.114223
9. Sousa-Victor P, García-Prat L, Muñoz-Cánoves P. Control of satellite cell function in muscle regeneration and its disruption in ageing. Nature Reviews Molecular Cell Biology. 2021; 23(3). doi: 10.1038/s41580-021-00421-2
10. Campanario S, Ramírez-Pardo I, Hong X, et al. Assessing Autophagy in Muscle Stem Cells. Frontiers in Cell and Developmental Biology. 2021; 8. doi: 10.3389/fcell.2020.620409
11. Laumonier T, Menetrey J. Muscle injuries and strategies for improving their repair. Journal of Experimental Orthopaedics. 2016; 3(1). doi: 10.1186/s40634-016-0051-7
12. Mauro A. Satellite Cell Of Skeletal Muscle Fibers. The Journal of Cell Biology. 1961; 9(2). doi: 10.1083/jcb.9.2.493
13. Motohashi N, Asakura A. Muscle satellite cell heterogeneity and self-renewal. Frontiers in Cell and Developmental Biology. 2014; 2. doi: 10.3389/fcell.2014.00001
14. Scharner J, Zammit PS. The muscle satellite cell at 50: the formative years. Skeletal Muscle. 2011; 1(1). doi: 10.1186/2044-5040-1-28
15. Koike H, Manabe I, Oishi Y. Mechanisms of cooperative cell-cell interactions in skeletal muscle regeneration. Inflammation and Regeneration. 2022; 42(1). doi: 10.1186/s41232-022-00234-6
16. Kaczmarek A, Kaczmarek M, Ciałowicz M, et al. The Role of Satellite Cells in Skeletal Muscle Regeneration—The Effect of Exercise and Age. Biology. 2021; 10(10). doi: 10.3390/biology10101056
17. Karalaki M, Fili S, Philippou A, Koutsilieris M. Muscle Regeneration: Cellular and Molecular Events. In Vivo. 2009; 23(5): 779–796.
18. Zanou N, Gailly P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cellular and Molecular Life Sciences. 2013; 70(21). doi: 10.1007/s00018-013-1330-4
19. Cooper RN, Tajbakhsh S, Mouly V, et al. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. Journal of Cell Science. 1999; 112(17). doi: 10.1242/jcs.112.17.2895
20. Kong J, Mu Y, Zhu L, et al. Mechanism of satellite cell regulation and its role in ecological niche signaling during skeletal muscle regeneration. Chinese Journal of Tissue Engineering Research. 2024; 28(7).
21. Xie L, Yin A, Nichenko AS, et al. Transient HIF2A inhibition promotes satellite cell proliferation and muscle regeneration. Journal of Clinical Investigation. 2018; 128(6). doi: 10.1172/jci96208
22. Rodriguez-Outeiriño L, Hernandez-Torres F, Ramírez-de Acuña F, et al. Muscle Satellite Cell Heterogeneity: Does Embryonic Origin Matter? Frontiers in Cell and Developmental Biology. 2021; 9. doi: 10.3389/fcell.2021.750534
23. Arpke RW, Shams AS, Collins BC, et al. Preservation of satellite cell number and regenerative potential with age reveals locomotory muscle bias. Skeletal Muscle. 2021; 11(1). doi: 10.1186/s13395-021-00277-2
24. Cai Z, Liu D, Yang Y, et al. The role and therapeutic potential of stem cells in skeletal muscle in sarcopenia. Stem Cell Research & Therapy. 2022; 13(1). doi: 10.1186/s13287-022-02706-5
25. Purohit G, Dhawan J. Adult Muscle Stem Cells: Exploring the Links Between Systemic and Cellular Metabolism. Frontiers in Cell and Developmental Biology. 2019; 7. doi: 10.3389/fcell.2019.00312
26. Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skeletal Muscle. 2011; 1(1). doi: 10.1186/2044-5040-1-4
27. Galimov A, Merry TL, Luca E, et al. MicroRNA-29a in Adult Muscle Stem Cells Controls Skeletal Muscle Regeneration During Injury and Exercise Downstream of Fibroblast Growth Factor-2. Stem Cells. 2016; 34(3). doi: 10.1002/stem.2281
28. He B, Tang R hang, Weisleder N, et al. Enhancing Muscle Membrane Repair by Gene Delivery of MG53 Ameliorates Muscular Dystrophy and Heart Failure in δ-Sarcoglycan-deficient Hamsters. Molecular Therapy. 2012; 20(4). doi: 10.1038/mt.2012.5
29. Sudo T, Yokota T, Oritani K, et al. The Endothelial Antigen ESAM Monitors Hematopoietic Stem Cell Status between Quiescence and Self-Renewal. The Journal of Immunology. 2012; 189(1). doi: 10.4049/jimmunol.1200056
30. Fukada S ichiro. The roles of muscle stem cells in muscle injury, atrophy and hypertrophy. The Journal of Biochemistry. 2018; 163(5). doi: 10.1093/jb/mvy019
31. Sultan SHA, Dyer C, Knight RD. Notch Signaling Regulates Muscle Stem Cell Homeostasis and Regeneration in a Teleost Fish. Frontiers in Cell and Developmental Biology. 2021; 9. doi: 10.3389/fcell.2021.726281
32. Jones AE, Price FD, Le Grand F, et al. Wnt/β-catenin controls follistatin signalling to regulate satellite cell myogenic potential. Skeletal Muscle. 2015; 5(1). doi: 10.1186/s13395-015-0038-6
33. Cui S, Li L, Yu RT, et al. β-Catenin is essential for differentiation of primary myoblasts via cooperation with MyoD and α-catenin. Development. 2019; 146(6). doi: 10.1242/dev.167080
34. Tanaka S, Terada K, Nohno T. Canonical Wnt signaling is involved in switching from cell proliferation to myogenic differentiation of mouse myoblast cells. Journal of Molecular Signaling. 2011; 6. doi: 10.1186/1750-2187-6-12
35. Mouradian S, Cicciarello D, Lacoste N, et al. LSD1 controls a nuclear checkpoint in Wnt/β-Catenin signaling to regulate muscle stem cell self-renewal. Nucleic Acids Research. 2024; 52(7). doi: 10.1093/nar/gkae060
36. Yan X, Liu Z, Chen Y. Regulation of TGF-β signaling by Smad7. Acta Biochimica et Biophysica Sinica. 2009; 41(4). doi: 10.1093/abbs/gmp018
37. Blank U, Karlsson S. TGF-β signaling in the control of hematopoietic stem cells. Blood. 2015; 125(23). doi: 10.1182/blood-2014-12-618090
38. Han S, Cui C, Wang Y, et al. Knockdown of CSRP3 inhibits differentiation of chicken satellite cells by promoting TGF-β/Smad3 signaling. Gene. 2019; 707. doi: 10.1016/j.gene.2019.03.064
39. Zhu X, Lu J, Rao J, et al. Crosstalk between Interleukin-1 Receptor-Like 1 and Transforming Growth Factor-β Receptor Signaling Promotes Renal Fibrosis. The American Journal of Pathology. 2023; 193(8). doi: 10.1016/j.ajpath.2023.05.002
40. Yu JSL, Cui W. Proliferation, survival and metabolism: the role of PI3K/AKT/mTOR signalling in pluripotency and cell fate determination. Development. 2016; 143(17). doi: 10.1242/dev.137075
41. Nitulescu G, Van De Venter M, Nitulescu G, et al. The Akt pathway in oncology therapy and beyond (Review). International Journal of Oncology. 2018; 53(6). doi: 10.3892/ijo.2018.4597
42. Hein AL, Ouellette MM, Yan Y. Radiation-induced signaling pathways that promote cancer cell survival (Review). International Journal of Oncology. 2014; 45(5). doi: 10.3892/ijo.2014.2614
43. Chen X, Wan J, Yu B, et al. PIP5K1α promotes myogenic differentiation via AKT activation and calcium release. Stem Cell Research & Therapy. 2018; 9(1). doi: 10.1186/s13287-018-0770-z
44. Da Y, Mou Y, Wang M, et al. Mechanical stress promotes biological functions of C2C12 myoblasts by activating PI3K/AKT/mTOR signaling pathway. Molecular Medicine Reports. 2020; 21(1). doi: 10.3892/mmr.2019.10808
45. Guo Y, Pan W, Liu S, et al. ERK/MAPK signalling pathway and tumorigenesis (Review). Experimental and Therapeutic Medicine. 2020; 19(3). doi: 10.3892/etm.2020.8454
46. Leung SW, Lai JH, Wu JCC, et al. Neuroprotective Effects of Emodin against Ischemia/Reperfusion Injury through Activating ERK-1/2 Signaling Pathway. International Journal of Molecular Sciences. 2020; 21(8). doi: 10.3390/ijms21082899
47. Lu N, Malemud CJ. Extracellular Signal-Regulated Kinase: A Regulator of Cell Growth, Inflammation, Chondrocyte and Bone Cell Receptor-Mediated Gene Expression. International Journal of Molecular Sciences. 2019; 20(15). doi: 10.3390/ijms20153792
48. Arkun Y, Yasemi M. Dynamics and control of the ERK signaling pathway: Sensitivity, bistability, and oscillations. PLoS One. 2018; 13(4). doi: 10.1371/journal.pone.0195513
49. Fu X, Zhuang C le, Hu P. Regulation of muscle stem cell fate. Cell Regeneration. 2022; 11(1). doi: 10.1186/s13619-022-00142-7
50. Luo X, Zhang H, Cao X, et al. Endurance Exercise-Induced Fgf21 Promotes Skeletal Muscle Fiber Conversion through TGF-β1 and p38 MAPK Signaling Pathway. International Journal of Molecular Sciences. 2023; 24(14). doi: 10.3390/ijms241411401
51. Röckl KSC, Hirshman MF, Brandauer J, et al. Skeletal Muscle Adaptation to Exercise Training. Diabetes. 2007; 56(8). doi: 10.2337/db07-0255
52. Plotkin DL, Roberts MD, Haun CT, et al. Muscle Fiber Type Transitions with Exercise Training: Shifting Perspectives. Sports. 2021; 9(9). doi: 10.3390/sports9090127
53. Shadiow J, Miranda ER, Perkins RK, et al. Exercise-induced changes to the fiber type-specific redox state in human skeletal muscle are associated with aerobic capacity. Journal of Applied Physiology. 2023; 135(3). doi: 10.1152/japplphysiol.00662.2022
54. Verdijk LB, Gleeson BG, Jonkers RA, et al. Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J Gerontol A Biol Sci Med Sci. 2009; 64(3). doi: 10.1093/gerona/gln050
55. Ahmad SS, Ahmad K, Lee EJ, et al. Implications of Insulin-Like Growth Factor-1 in Skeletal Muscle and Various Diseases. Cells. 2020; 9(8). doi: 10.3390/cells9081773
56. Kong J, Xie Y, Chen S, et al. Blood flow restriction training interventions for sarcopenia in older adults: biological mechanisms and proposed application protocols. Chinese Journal of Tissue Engineering Research. 2024; 28(23).
57. Ato S, Tsushima D, Isono Y, et al. The Effect of Changing the Contraction Mode During Resistance Training on mTORC1 Signaling and Muscle Protein Synthesis. Frontiers in Physiology. 2019; 10. doi: 10.3389/fphys.2019.00406
58. Fernandes T, Soci Ú PR, Melo SFS, et al. Signaling pathways that mediate skeletal muscle hypertrophy: Effects of exercise training. In: Skeletal muscle-From Myogenesis to Clinical Relations. IntechOpen; 2012.
59. Venturaclapier R, Mettauer B, Bigard X. Beneficial effects of endurance training on cardiac and skeletal muscle energy metabolism in heart failure. Cardiovascular Research. 2007; 73(1). doi: 10.1016/j.cardiores.2006.09.003
60. Liang J, Zhang H, Zeng Z, et al. Lifelong Aerobic Exercise Alleviates Sarcopenia by Activating Autophagy and Inhibiting Protein Degradation via the AMPK/PGC-1α Signaling Pathway. Metabolites. 2021; 11(5). doi: 10.3390/metabo11050323
61. Konopka AR, Douglass MD, Kaminsky LA, et al. Molecular Adaptations to Aerobic Exercise Training in Skeletal Muscle of Older Women. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2010; 65A(11). doi: 10.1093/gerona/glq109
62. Liu C, Wu X, Vulugundam G, et al. Exercise Promotes Tissue Regeneration: Mechanisms Involved and Therapeutic Scope. Sports Medicine-Open. 2023; 9(1). doi: 10.1186/s40798-023-00573-9
63. Yoshida T, Delafontaine P. Mechanisms of IGF-1-Mediated Regulation of Skeletal Muscle Hypertrophy and Atrophy. Cells. 2020; 9(9). doi: 10.3390/cells9091970
64. Pang X, Zhang P, Chen X, et al. Ubiquitin-proteasome pathway in skeletal muscle atrophy. Frontiers in Physiology. 2023; 14. doi: 10.3389/fphys.2023.1289537
65. Xiao L, Liu J, Sun Z, et al. AMPK-dependent and -independent coordination of mitochondrial function and muscle fiber type by FNIP1. Trifunovic A, ed. PLOS Genetics. 2021; 17(3). doi: 10.1371/journal.pgen.1009488
66. Guo H, Kong J, Tian C. Role of mitochondrial autophagy-related receptor proteins and signaling pathways in the prevention and treatment of sarcopenia through exercise. Chinese Journal of Tissue Engineering Research. 2024; 28(27).
67. Mascher H, Tannerstedt J, Brink-Elfegoun T, et al. Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle. American Journal of Physiology-Endocrinology and Metabolism. 2008; 294(1). doi: 10.1152/ajpendo.00504.2007
68. Zhang L, Lang H, Ran L, et al. Long-term high loading intensity of aerobic exercise improves skeletal muscle performance via the gut microbiota-testosterone axis. Frontiers in Microbiology. 2022; 13. doi: 10.3389/fmicb.2022.1049469
69. Kong J, Li Z, Zhu L, et al. Comparison of blood flow restriction training and conventional resistance training for the improvement of sarcopenia in the older adults: A systematic review and meta-analysis. Sports Medicine and Health Science. 2022; 5(4). doi: 10.1016/j.smhs.2022.12.002
70. Li B, Feng L, Wu X, et al. Effects of different modes of exercise on skeletal muscle mass and function and IGF-1 signaling during early aging in mice. Journal of Experimental Biology. 2022; 225(21). doi: 10.1242/jeb.244650
71. Sorriento D, Di Vaia E, Iaccarino G. Physical Exercise: A Novel Tool to Protect Mitochondrial Health. Frontiers in Physiology. 2021; 12. doi: 10.3389/fphys.2021.660068
72. Hood DA, Irrcher I, Ljubicic V, et al. Coordination of metabolic plasticity in skeletal muscle. Journal of Experimental Biology. 2006; 209(12). doi: 10.1242/jeb.02182
73. Bernareggi A, Bosutti A, Massaria G, et al. The State of the Art of Piezo1 Channels in Skeletal Muscle Regeneration. International Journal of Molecular Sciences. 2022; 23(12). doi: 10.3390/ijms23126616
74. Zhang W, Liu Y, Zhang H. Extracellular matrix: an important regulator of cell functions and skeletal muscle development. Cell & Bioscience. 2021; 11(1). doi: 10.1186/s13578-021-00579-4
75. Vadlakonda L, Pasupuleti M, Pallu R. Role of PI3K-AKT-mTOR and Wnt Signaling Pathways in Transition of G1-S Phase of Cell Cycle in Cancer Cells. Frontiers in Oncology. 2013; 3. doi: 10.3389/fonc.2013.00085
76. Tóthová Z, Šemeláková M, Solárová Z, et al. The Role of PI3K/AKT and MAPK Signaling Pathways in Erythropoietin Signalization. International Journal of Molecular Sciences. 2021; 22(14). doi: 10.3390/ijms22147682
77. Long YC. AMP-activated protein kinase signaling in metabolic regulation. Journal of Clinical Investigation. 2006; 116(7). doi: 10.1172/jci29044
78. Hajj-Boutros G, Karelis AD, Cefis M, et al. Potential mechanisms involved in regulating muscle protein turnover after acute exercise: A brief review. Frontiers in Physiology. 2023; 13. doi: 10.3389/fphys.2022.1106425
79. Gugliuzza MV, Crist C. Muscle stem cell adaptations to cellular and environmental stress. Skeletal Muscle. 2022; 12(1). doi: 10.1186/s13395-022-00289-6
80. Joseph J, Doles JD. Disease-associated metabolic alterations that impact satellite cells and muscle regeneration: perspectives and therapeutic outlook. Nutrition & Metabolism. 2021; 18(1). doi: 10.1186/s12986-021-00565-0
81. Senesi P, Luzi L, Montesano A, et al. Betaine supplement enhances skeletal muscle differentiation in murine myoblasts via IGF-1 signaling activation. Journal of Translational Medicine. 2013; 11(1). doi: 10.1186/1479-5876-11-174
82. Tu H, Li YL. Inflammation balance in skeletal muscle damage and repair. Frontiers in Immunology. 2023; 14. doi: 10.3389/fimmu.2023.1133355
83. Johnson AL, Kamal M, Parise G. The Role of Supporting Cell Populations in Satellite Cell Mediated Muscle Repair. Cells. 2023; 12(15). doi: 10.3390/cells12151968
84. Burks TN, Cohn RD. Role of TGF-β signaling in inherited and acquired myopathies. Skeletal Muscle. 2011; 1(1). doi: 10.1186/2044-5040-1-19
85. Bonnet C, Brahmbhatt A, Deng SX, et al. Wnt signaling activation: targets and therapeutic opportunities for stem cell therapy and regenerative medicine. RSC Chemical Biology. 2021; 2(4). doi: 10.1039/d1cb00063b
86. Pang KT, Loo LSW, Chia S, et al. Insight into muscle stem cell regeneration and mechanobiology. Stem Cell Research & Therapy. 2023; 14(1). doi: 10.1186/s13287-023-03363-y
87. Roberts FL, Markby GR. New Insights into Molecular Mechanisms Mediating Adaptation to Exercise; A Review Focusing on Mitochondrial Biogenesis, Mitochondrial Function, Mitophagy and Autophagy. Cells. 2021; 10(10). doi: 10.3390/cells10102639
88. Xie Y, Kong J, Chen Y, et al. Biological mechanism of satellite cell aging in skeletal muscles and potential coping strategies. Chinese Journal of Tissue Engineering Research. 2024; 28(25).
89. Brocherie F, Goto K, Dupuy O, et al. Editorial: From Physiological Adaptations to Endurance Performance: It Is Time to Bridge the Gap. Frontiers in Sports and Active Living. 2021; 3. doi: 10.3389/fspor.2021.775654
90. Huo F, Liu Q, Liu H. Contribution of muscle satellite cells to sarcopenia. Frontiers in Physiology. 2022; 13. doi: 10.3389/fphys.2022.892749
91. Viecelli C, Ewald CY. The non-modifiable factors age, gender, and genetics influence resistance exercise. Frontiers in Aging. 2022; 3. doi: 10.3389/fragi.2022.1005848
92. Hiam D, Landen S, Jacques M, et al. Muscle miRNAs are influenced by sex at baseline and in response to exercise. BMC Biology. 2023; 21(1). doi: 10.1186/s12915-023-01755-3
93. O’Connor E, Mündel T, Barnes MJ. Nutritional Compounds to Improve Post-Exercise Recovery. Nutrients. 2022; 14(23). doi: 10.3390/nu14235069
94. Niu K, Guo H, Guo Y, et al. Royal Jelly Prevents the Progression of Sarcopenia in Aged Mice In Vivo and In Vitro. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2013; 68(12). doi: 10.1093/gerona/glt041
95. Okumura N, Toda T, Ozawa Y, et al. Royal Jelly Delays Motor Functional Impairment During Aging in Genetically Heterogeneous Male Mice. Nutrients. 2018; 10(9). doi: 10.3390/nu10091191
96. Docherty S, Harley R, McAuley JJ, et al. The effect of exercise on cytokines: implications for musculoskeletal health: a narrative review. BMC Sports Science, Medicine and Rehabilitation. 2022; 14(1). doi: 10.1186/s13102-022-00397-2
97. Kim HK, Konishi M, Takahashi M, et al. Effects of Acute Endurance Exercise Performed in the Morning and Evening on Inflammatory Cytokine and Metabolic Hormone Responses. Oster H, ed. PLOS ONE. 2015; 10(9). doi: 10.1371/journal.pone.0137567
98. Koveitypour Z, Panahi F, Vakilian M, et al. Signaling pathways involved in colorectal cancer progression. Cell & Bioscience. 2019; 9(1). doi: 10.1186/s13578-019-0361-4
99. Farooqi AA, Nayyab S, Martinelli C, et al. Regulation of Hippo, TGFβ/SMAD, Wnt/β-Catenin, JAK/STAT, and NOTCH by Long Non-Coding RNAs in Pancreatic Cancer. Frontiers in Oncology. 2021; 11. doi: 10.3389/fonc.2021.657965
100. Saadat S, Noureddini M, Mahjoubin-Tehran M, et al. Pivotal Role of TGF-β/Smad Signaling in Cardiac Fibrosis: Non-coding RNAs as Effectual Players. Frontiers in Cardiovascular Medicine. 2021; 7. doi: 10.3389/fcvm.2020.588347
101. Mirzoev TM. Mechanotransduction for Muscle Protein Synthesis via Mechanically Activated Ion Channels. Life. 2023; 13(2). doi: 10.3390/life13020341
102. Liu Z, Wang Q, Zhang J, et al. The Mechanotransduction Signaling Pathways in the Regulation of Osteogenesis. International Journal of Molecular Sciences. 2023; 24(18). doi: 10.3390/ijms241814326
103. van Ingen MJA, Kirby TJ. LINCing Nuclear Mechanobiology With Skeletal Muscle Mass and Function. Frontiers in Cell and Developmental Biology. 2021; 9. doi: 10.3389/fcell.2021.690577
104. Prieto-González P, Sedlacek J. Effects of Running-Specific Strength Training, Endurance Training, and Concurrent Training on Recreational Endurance Athletes’ Performance and Selected Anthropometric Parameters. International Journal of Environmental Research and Public Health. 2022; 19(17). doi: 10.3390/ijerph191710773
105. Roth SM, Martel GF, Ivey FM, et al. Skeletal Muscle Satellite Cell Characteristics in Young and Older Men and Women After Heavy Resistance Strength Training. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2001; 56(6). doi: 10.1093/gerona/56.6.b240
106. Fang J, Feng C, Chen W, et al. Redressing the interactions between stem cells and immune system in tissue regeneration. Biology Direct. 2021; 16(1). doi: 10.1186/s13062-021-00306-6
107. Wu J, Ding P, Wu H, et al. Sarcopenia: Molecular regulatory network for loss of muscle mass and function. Frontiers in Nutrition. 2023; 10. doi: 10.3389/fnut.2023.1037200
108. McMahon G, Morse CI, Winwood K, et al. Gender associated muscle-tendon adaptations to resistance training. PLOS ONE. 2018; 13(5). doi: 10.1371/journal.pone.0197852
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