https://doi.org/10.4081/ejtm.2024.13273
An aged-related structural study of DHPR tetrads in peripheral couplings of human skeletal muscle
Published: 29 October 2024
Abstract Views: 219
PDF: 67
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Among the numerous changes that occur in skeletal muscle during aging, the reduced regeneration potential after an injury is largely due to the impaired ability of satellite cells to proliferate and differentiate. Herein, using the freeze-fracture electron microscopy technique, we analyzed both the incidence and size of dihydropyridine receptors (DHPRs) tetrads (4 particles) in cultured myotubes from a young subject (28 years) after 9 days of differentiation and from an old subject (71 years) after 9 and 12 days of differentiation. Compared to young myotubes, at 9 days of differentiation old myotubes exhibited: i) a lower incidence and a smaller size of DHPR clusters and ii) a lower number of complete tetrads. At 12 days of differentiation values of incidence, size and number of complete tetrads in old myotubes were instead comparable with those of young myotubes at 9 days of differentiation. Collectively, these results indicate that in aged myotubes the synthesis process of the proteins involved in the excitation-contraction coupling mechanism, such as the DHPR, is somehow slowed, supporting previous studies evidence of a decrease in the differentiation potential of myotubes from elderly individuals.
Wiedmer P, Jung T, Castro JP, et al. Sarcopenia - Molecular mechanisms and open questions. Ageing Res Rev 2021;65:101200.
DOI: https://doi.org/10.1016/j.arr.2020.101200
Domingues-Faria C, Vasson MP, Goncalves-Mendes N, et al. Skeletal muscle regeneration and impact of aging and nutrition. Ageing Res Rev 2016;26:22-36.
DOI: https://doi.org/10.1016/j.arr.2015.12.004
Yamakawa H, Kusumoto D, Hashimoto H, Yuasa S. Stem cell aging in skeletal muscle regeneration and disease. Int J Mol Sci 2020;21:1830.
DOI: https://doi.org/10.3390/ijms21051830
Pietrangelo T, Puglielli C, Mancinelli R, et al. Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp Gerontol 2009;44:523-31.
DOI: https://doi.org/10.1016/j.exger.2009.05.002
Cade WT, Yarasheski KE. Metabolic and molecular aspects of sarcopenia. In: Runge MS, Patterson C (eds.), Principles of Molecular Medicine. Springer; 2006.
Tanabe T, Beam KG, Powell JA, Numa S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 1988;336:134–9.
DOI: https://doi.org/10.1038/336134a0
Adams BA, Tanabe T, Mikami A, et al. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature 1990;346:569-72.
DOI: https://doi.org/10.1038/346569a0
Rios E, Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 1987;325:717–20.
DOI: https://doi.org/10.1038/325717a0
Schneider MF, Chandler WK. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature 1973;242:244–6.
DOI: https://doi.org/10.1038/242244a0
Rios E, Ma JJ, Gonzalez A. The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle. J Muscle Res Cell Motil 1991;12:127–35.
DOI: https://doi.org/10.1007/BF01774031
Schneider MF. Control of calcium release in functioning skeletal muscle fibers. Annu Rev Physiol 1994;56:463–84.
DOI: https://doi.org/10.1146/annurev.ph.56.030194.002335
Franzini-Armstrong C. An updated view of the structural basis for dihydropyridine receptors-ryanodine receptors direct molecular interaction in skeletal muscle. Eur J Transl Myol 2024;34:12476.
DOI: https://doi.org/10.4081/ejtm.2024.12476
Franzini-Armstrong C. Studies of the triad: I. Structure of the junction in frog twitch fibers. J Cell Biol 1970;47:488–99.
DOI: https://doi.org/10.1083/jcb.47.2.488
Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 1988;107:2587–600.
DOI: https://doi.org/10.1083/jcb.107.6.2587
Franzini-Armstrong C. Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev Biol 1991;146:353-63.
DOI: https://doi.org/10.1016/0012-1606(91)90237-W
Takekura H, Sun X, Franzini-Armstrong C. Development of the excitation-contraction coupling apparatus in skeletal muscle: peripheral and internal calcium release units are formed sequentially. J Muscle Res Cell Motil 1994;15:102–18.
DOI: https://doi.org/10.1007/BF00130422
Takekura H, Bennett L, Tanabe T, et al. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys J 1994;67:793-803.
DOI: https://doi.org/10.1016/S0006-3495(94)80539-9
Protasi F, Franzini-Armstrong C, Allen PD. Role of ryanodine receptors in the assembly of calcium release units in skeletal muscle. J Cell Biol 1998;140:831–42.
DOI: https://doi.org/10.1083/jcb.140.4.831
Protasi F, Franzini-Armstrong C, Flucher BE. Coordinated incorporation of skeletal muscle dihydropyridine receptors and ryanodine receptors in peripheral couplings of BC3H1 cells. J Cell 1997;137:859–70.
DOI: https://doi.org/10.1083/jcb.137.4.859
Franzini-Armstrong C, Kish JW. Alternate disposition of tetrads in peripheral couplings of skeletal muscle. J Muscle Res Cell Motil 1995;16:319-24.
DOI: https://doi.org/10.1007/BF00121140
D Appelt 1, B Buenviaje, C Champ, C Franzini-Armstrong. Quantitation of 'junctional feet' content in two types of muscle fiber from hind limb muscles of the rat. Tissue Cell 1989;21:783-94.
DOI: https://doi.org/10.1016/0040-8166(89)90087-6
Franzini-Armstrong C. Freeze-fracture of frog slow tonic fibers. Structure of surface and internal membranes. Tissue Cell 1984;16:647-64.
DOI: https://doi.org/10.1016/0040-8166(84)90038-7
Takekura H, Shuman H, Franzini-Armstrong C. Differentiation of membrane systems during development of slow and fast skeletal muscle fibres in chicken. J Muscle Res Cell Motil 1993;14:633-45.
DOI: https://doi.org/10.1007/BF00141560
Fulle S, Di Donna S, Puglielli C, et al. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol 2005;40:189-97.
DOI: https://doi.org/10.1016/j.exger.2004.11.006
Protasi F. Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 2002;7:d650-8.
DOI: https://doi.org/10.2741/A801
Protasi F, Takekura H, Wang Y, et al. RYR1 and RYR3 have different roles in the assembly of calcium release units of skeletal muscle. Biophys J 2000;79:2494–508.
DOI: https://doi.org/10.1016/S0006-3495(00)76491-5
Renganathan M, Messi ML, Delbono O. Dihydropyridine receptor-ryanodine receptor uncoupling in aged skeletal muscle. J Membr Biol 1997;157:247–53.
DOI: https://doi.org/10.1007/s002329900233
Dayanidhi S, Lieber RL. Skeletal muscle satellite cells: Mediators of muscle growth during development and implications for developmental disorders. Muscle Nerve 2014;50:723-32.
DOI: https://doi.org/10.1002/mus.24441
Snijders T, Nederveen JP, McKay BR, et al. Satellite cells in human skeletal muscle plasticity. Front Physiol 2015;6:283.
DOI: https://doi.org/10.3389/fphys.2015.00283
Pallafacchina G, Blaauw B, Schiaffino S. Role of satellite cells in muscle growth and maintenance of muscle mass. Nutr Metab Cardiovasc Dis 2013;23:S12-8.
DOI: https://doi.org/10.1016/j.numecd.2012.02.002
Hawke TJ, Garry DJ. Myogenic satellite cells: Physiology to molecular biology. J Appl Physiol (1985) 2001;91:534-51. Erratum in: J Appl Physiol 2001;91:2414.
DOI: https://doi.org/10.1152/jappl.2001.91.2.534
Chen W, Datzkiw D, Rudnicki MA. Satellite cells in ageing: Use it or lose it. Open Biol 2020;10:200048.
DOI: https://doi.org/10.1098/rsob.200048
Alway SE, Myers MJ, Mohamed JS. Regulation of satellite cell function in sarcopenia. Front Aging Neurosci 2014;6:246.
DOI: https://doi.org/10.3389/fnagi.2014.00246
Sousa-Victor P, García-Prat L, Muñoz-Cánoves P. Control of satellite cell function in muscle regeneration and its disruption in ageing. Nat Rev Mol Cell Biol 2022;23:204-26.
DOI: https://doi.org/10.1038/s41580-021-00421-2
How to Cite
Pietrangelo, L., Mancinelli, R., Fulle, S., & Boncompagni, S. (2024). An aged-related structural study of DHPR tetrads in peripheral couplings of human skeletal muscle. European Journal of Translational Myology. https://doi.org/10.4081/ejtm.2024.13273
Copyright (c) 2024 the Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.