Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow

Bone is an organ capable of perceiving external mechanical stress in real time and responding dynamically via mechanosensing proteins such as Piezo1 and YAP/TAZ. Upon sensing the mechano-signals, cells within the bone matrix collaborate to coordinate bone formation and resorption, while bone marrow...

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Main Authors: Shaotian Fu, Yahong Lu, Wenkun Sun, Wugui Chen, Chengshou Lin, An Qin
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Mechanobiology in Medicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2949907025000130
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author Shaotian Fu
Yahong Lu
Wenkun Sun
Wugui Chen
Chengshou Lin
An Qin
author_facet Shaotian Fu
Yahong Lu
Wenkun Sun
Wugui Chen
Chengshou Lin
An Qin
author_sort Shaotian Fu
collection DOAJ
description Bone is an organ capable of perceiving external mechanical stress in real time and responding dynamically via mechanosensing proteins such as Piezo1 and YAP/TAZ. Upon sensing the mechano-signals, cells within the bone matrix collaborate to coordinate bone formation and resorption, while bone marrow cells are also stimulated and mobilized. High-load exercise stimulates osteoblast differentiation and bone formation. However, the mechanism through which the low-load exercises affect bone homeostasis is still unclear. In this work, we established a long-term swimming training model to unload the mechanical stress in mice. Throughout the training model, we observed a significant loss in trabecular bone mass, as evidenced by microCT scanning and histological staining. Single-cell sequencing of the tibial bone marrow tissue revealed a significant increase in the percentage of bone marrow neutrophils, along with alterations in Integrins and the ERK1/2 signaling pathway. Notably, the changes in both Integrins and the ERK1/2 signaling pathway in macrophages were more pronounced than in other cell types, which suggests a mechanical adaptive response in these cells. Moreover, the involvement of Integrins is also critical for the crosstalk between monocyte precusors and macrophages during swimming. Together, this study provides a resource of the alterations of bone marrow cell gene expression profile after swimming and highlights the importance of Integrins and the ERK1/2 signaling pathway in the bone marrow microenvironment after swimming.
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publishDate 2025-06-01
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series Mechanobiology in Medicine
spelling doaj-art-a0e2f8539ab44b6a8805cb9f22af35ae2025-08-20T03:30:39ZengElsevierMechanobiology in Medicine2949-90702025-06-013210012510.1016/j.mbm.2025.100125Swimming induces bone loss via regulating mechanical sensing pathways in bone marrowShaotian Fu0Yahong Lu1Wenkun Sun2Wugui Chen3Chengshou Lin4An Qin5Shanghai Key Laboratory of Orthopedic Implants, Department of Orthopedics, Ninth People's Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, 200011, ChinaThe Fifth Affiliated Hospital of Wenzhou Medical University, Lishui Municipal Central Hospital, 289 Kuocang Road, Zhejiang, 323000, ChinaShanghai University of Medicine & Health Sciences, Shanghai, 201318, ChinaDepartment of Orthopaedics, Mindong Hospital Affiliated Fujian Medical University, Fujian, ChinaDepartment of Orthopaedics, Mindong Hospital Affiliated Fujian Medical University, Fujian, China; Corresponding author.Shanghai Key Laboratory of Orthopedic Implants, Department of Orthopedics, Ninth People's Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, 200011, China; Corresponding author.Bone is an organ capable of perceiving external mechanical stress in real time and responding dynamically via mechanosensing proteins such as Piezo1 and YAP/TAZ. Upon sensing the mechano-signals, cells within the bone matrix collaborate to coordinate bone formation and resorption, while bone marrow cells are also stimulated and mobilized. High-load exercise stimulates osteoblast differentiation and bone formation. However, the mechanism through which the low-load exercises affect bone homeostasis is still unclear. In this work, we established a long-term swimming training model to unload the mechanical stress in mice. Throughout the training model, we observed a significant loss in trabecular bone mass, as evidenced by microCT scanning and histological staining. Single-cell sequencing of the tibial bone marrow tissue revealed a significant increase in the percentage of bone marrow neutrophils, along with alterations in Integrins and the ERK1/2 signaling pathway. Notably, the changes in both Integrins and the ERK1/2 signaling pathway in macrophages were more pronounced than in other cell types, which suggests a mechanical adaptive response in these cells. Moreover, the involvement of Integrins is also critical for the crosstalk between monocyte precusors and macrophages during swimming. Together, this study provides a resource of the alterations of bone marrow cell gene expression profile after swimming and highlights the importance of Integrins and the ERK1/2 signaling pathway in the bone marrow microenvironment after swimming.http://www.sciencedirect.com/science/article/pii/S2949907025000130SwimmingMechanical stressMechanical sensingSingle-cell RNA sequencingOsteoprosis
spellingShingle Shaotian Fu
Yahong Lu
Wenkun Sun
Wugui Chen
Chengshou Lin
An Qin
Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
Mechanobiology in Medicine
Swimming
Mechanical stress
Mechanical sensing
Single-cell RNA sequencing
Osteoprosis
title Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
title_full Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
title_fullStr Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
title_full_unstemmed Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
title_short Swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
title_sort swimming induces bone loss via regulating mechanical sensing pathways in bone marrow
topic Swimming
Mechanical stress
Mechanical sensing
Single-cell RNA sequencing
Osteoprosis
url http://www.sciencedirect.com/science/article/pii/S2949907025000130
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AT wuguichen swimminginducesbonelossviaregulatingmechanicalsensingpathwaysinbonemarrow
AT chengshoulin swimminginducesbonelossviaregulatingmechanicalsensingpathwaysinbonemarrow
AT anqin swimminginducesbonelossviaregulatingmechanicalsensingpathwaysinbonemarrow