Kinetics of skeletal muscle regeneration after mild and severe muscle damage induced by electrically-evoked lengthening contractions
- PMID: 37534948
- DOI: 10.1096/fj.202201708RR
Kinetics of skeletal muscle regeneration after mild and severe muscle damage induced by electrically-evoked lengthening contractions
Abstract
Post-injury skeletal muscle regeneration requires interactions between myogenic and non-myogenic cells. Our knowledge on the regeneration process is mainly based on models using toxic, chemical, or physical (e.g., based on either muscle freezing or crushing) injury. Strikingly, the time course and magnitude of changes in the number of cells involved in muscle regeneration have been poorly described in relation to mild and severe muscle damage induced by electrically-evoked lengthening contractions. We investigated for the first time the kinetics and magnitude of changes in mononuclear cells in relation to the extent of muscle damage. Mild and severe injury were induced in vivo in the mouse gastrocnemius muscle by 1 and 30 electrically-evoked lengthening contractions, respectively. Several days after muscle damage, functional analysis of maximal torque production and histological investigations were performed to assess the related cellular changes. Torque recovery was faster after mild injury than after severe muscle damage. More necrotic and regenerating myofibers were observed after severe muscle damage as compared with mild injury, illustrating an association between functional and histological alterations. The kinetics of changes in muscle stem cells (total, proliferating, and differentiating), endothelial cells, fibro-adipogenic progenitors (FAPs), and macrophages in the regenerating muscle was similar in mild and severe models. However, the magnitude of changes in the number of differentiating muscle stem cells, hematopoietic cells, among which macrophages, and FAPs was higher in severe muscle damage. Collectively, our results show that the amount of myogenic and non-myogenic cells varies according to the extent of skeletal muscle injury to ensure efficient skeletal muscle regeneration while the kinetics of changes is independent of muscle tissue alterations. The possibility to experimentally modulate the extent of muscle damage will be useful to further investigate the cellular and molecular events involved in muscle regeneration.
Keywords: fibro-adipogenic progenitors; lengthening contraction; macrophages; muscle stem cells; skeletal muscle regeneration.
© 2023 Federation of American Societies for Experimental Biology.
Similar articles
-
Gli1 Defines a Subset of Fibro-adipogenic Progenitors that Promote Skeletal Muscle Regeneration With Less Fat Accumulation.J Bone Miner Res. 2021 Jun;36(6):1159-1173. doi: 10.1002/jbmr.4265. Epub 2021 Mar 2. J Bone Miner Res. 2021. PMID: 33529374 Free PMC article.
-
Icing after eccentric contraction-induced muscle damage perturbs the disappearance of necrotic muscle fibers and phenotypic dynamics of macrophages in mice.J Appl Physiol (1985). 2021 May 1;130(5):1410-1420. doi: 10.1152/japplphysiol.01069.2020. Epub 2021 Mar 25. J Appl Physiol (1985). 2021. PMID: 33764172
-
Head muscle fibro-adipogenic progenitors account for the tilted regeneration towards fibrosis.Biochem Biophys Res Commun. 2022 Jan 22;589:131-138. doi: 10.1016/j.bbrc.2021.12.009. Epub 2021 Dec 3. Biochem Biophys Res Commun. 2022. PMID: 34915407
-
Fibro-adipogenic progenitors in skeletal muscle homeostasis, regeneration and diseases.Open Biol. 2021 Dec;11(12):210110. doi: 10.1098/rsob.210110. Epub 2021 Dec 8. Open Biol. 2021. PMID: 34875199 Free PMC article. Review.
-
Signaling pathways regulating the fate of fibro/adipogenic progenitors (FAPs) in skeletal muscle regeneration and disease.FEBS J. 2022 Nov;289(21):6484-6517. doi: 10.1111/febs.16080. Epub 2021 Jul 6. FEBS J. 2022. PMID: 34143565 Review.
Cited by
-
Traumatic muscle injury.Nat Rev Dis Primers. 2023 Oct 19;9(1):56. doi: 10.1038/s41572-023-00469-8. Nat Rev Dis Primers. 2023. PMID: 37857686 Review.
-
Characterization of Skeletal Muscle Regeneration Revealed a Novel Growth Network Induced by Molecular Acupuncture-like Transfection.Biomolecules. 2024 Mar 19;14(3):363. doi: 10.3390/biom14030363. Biomolecules. 2024. PMID: 38540781 Free PMC article. Review.
References
REFERENCES
-
- Forcina L, Cosentino M, Musarò A. Mechanisms regulating muscle regeneration: insights into the interrelated and time-dependent phases of tissue healing. Cell. 2020;9:1297. doi:10.3390/cells9051297
-
- Panci G, Chazaud B. Inflammation during post-injury skeletal muscle regeneration. Semin Cell Dev Biol. 2021;119:32-38. doi:10.1016/j.semcdb.2021.05.031
-
- Dort J, Fabre P, Molina T, Dumont NA. Macrophages are key regulators of stem cells during skeletal muscle regeneration and diseases. Stem Cells Int. 2019;1-20. doi:10.1155/2019/4761427
-
- Hardy D, Besnard A, Latil M, et al. Comparative study of injury models for studying muscle regeneration in mice. PloS One. 2016;11:e0147198. doi:10.1371/journal.pone.0147198
-
- Baghdadi MB, Tajbakhsh S. Regulation and phylogeny of skeletal muscle regeneration. Dev Biol. 2018;433:200-209. doi:10.1016/j.ydbio.2017.07.026
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources