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Review
. 2024 Mar 4:15:1349253.
doi: 10.3389/fphys.2024.1349253. eCollection 2024.

The reciprocity of skeletal muscle and bone: an evolving view from mechanical coupling, secretory crosstalk to stem cell exchange

Hao Sui  1 , Jinfeng Dou  1 , Bing Shi  1 , Xu Cheng  1
Affiliations
Review

The reciprocity of skeletal muscle and bone: an evolving view from mechanical coupling, secretory crosstalk to stem cell exchange

Hao Sui et al. Front Physiol. .

Abstract

Introduction: Muscle and bone constitute the two main parts of the musculoskeletal system and generate an intricately coordinated motion system. The crosstalk between muscle and bone has been under investigation, leading to revolutionary perspectives in recent years. Method and results: In this review, the evolving concept of muscle-bone interaction from mechanical coupling, secretory crosstalk to stem cell exchange was explained in sequence. The theory of mechanical coupling stems from the observation that the development and maintenance of bone mass are largely dependent on muscle-derived mechanical loads, which was later proved by Wolff's law, Utah paradigm and Mechanostat hypothesis. Then bone and muscle are gradually recognized as endocrine organs, which can secrete various cytokines to modulate the tissue homeostasis and remodeling to each other. The latest view presented muscle-bone interaction in a more direct way: the resident mesenchymal stromal cell in the skeletal muscle, i.e., fibro-adipogenic progenitors (FAPs), could migrate to the bone injury site and contribute to bone regeneration. Emerging evidence even reveals the ectopic source of FAPs from tissue outside the musculoskeletal system, highlighting its dynamic property. Conclusion: FAPs have been established as the critical cell connecting muscle and bone, which provides a new modality to study inter-tissue communication. A comprehensive and integrated perspective of muscle and bone will facilitate in-depth research in the musculoskeletal system and promote novel therapeutic avenues in treating musculoskeletal disorders.

Keywords: bone regeneration; fibro-adipogenic progenitors; inter-tissue communication; muscular diseases; musculoskeletal system.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
A summary of the secretory crosstalk between muscle and bone.
FIGURE 2
FIGURE 2
An evolving view of bone-muscle interaction. (A) Muscle contraction generates a variety of motion-torque patterns at bone and enables the multidirectional movement of the musculoskeletal system. (B) Muscle and bone can both function as endocrine organs, which can secrete various cytokines to modulate the tissue homeostasis and remodeling to each other. (C) The resident mesenchymal stromal cell in the skeletal muscle, i.e., fibro-adipogenic progenitors (FAPs), could migrate to the bone injury site and contribute to bone regeneration.
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Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by National Natural Science Foundation of China (grant numbers 82001031, 81974147), Sichuan Provincial Health and Wellness Committee (grant 21PJ063).

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