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Macrophage-lineage TRAP+ cells recruit periosteum-derived cells for periosteal osteogenesis and regeneration
Bo Gao, … , Zhuojing Luo, Xu Cao
Bo Gao, … , Zhuojing Luo, Xu Cao
Published April 4, 2019
Citation Information: J Clin Invest. 2019;129(6):2578-2594. https://doi.org/10.1172/JCI98857.
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Research Article Bone biology Article has an altmetric score of 6

Macrophage-lineage TRAP+ cells recruit periosteum-derived cells for periosteal osteogenesis and regeneration

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Abstract

Cortical bones account for more than 80% of human bone mass. The periosteum, a thin tissue that covers almost the entire bone surface, is essential for bone formation and regeneration. However, its osteogenic and bone regenerative abilities are not well studied. In this study, we found that macrophage-lineage cells recruit periosteum-derived cells (PDCs) for cortical bone formation. Knockout of colony-stimulating factor-1 eliminated macrophage-lineage cells and resulted in loss of PDCs with impaired periosteal bone formation. Moreover, macrophage-lineage tartrate-resistant acid phosphatase–positive (TRAP+) cells induced transcriptional expression of periostin and recruitment of PDCs to the periosteal surface through secretion of PDGF-BB, where the recruited PDCs underwent osteoblast differentiation coupled with type H vessel formation. We also found that subsets of Nestin+ and LepR+CD45–Ter119–CD31– cells (LepR+ PDCs) possess multipotent and self-renewal abilities and contribute to cortical bone formation. Nestin+ PDCs are found primarily during bone development, whereas LepR+ PDCs are essential for bone homeostasis in adult mice. Importantly, conditional knockout of Pdgfr-β in LepR+ cells impaired periosteal bone formation and regeneration. These findings uncover the essential role of periosteal macrophage-lineage cells in regulating periosteum homeostasis and regeneration.

Authors

Bo Gao, Ruoxian Deng, Yu Chai, Hao Chen, Bo Hu, Xiao Wang, Shouan Zhu, Yong Cao, Shuangfei Ni, Mei Wan, Liu Yang, Zhuojing Luo, Xu Cao

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Figure 3

Deficiency in macrophage-lineage cells impairs cortical bone formation and periosteum homeostasis.

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Deficiency in macrophage-lineage cells impairs cortical bone formation a...
(A–C). Upper panels, representative images of coronal tibia diaphyseal periosteum sections from Csf1–/– mice and their control littermates (Csf1+/+) stained for TRAP and Nestin (A), TRAP and LepR (B), and periostin (C). Lower panels, high-power magnification images of the boxed area of the upper panels. (D–F) Quantification of TRAP+ mononuclear cells (D), Nestin+ cells and LepR+ cells (E), and periostin+ cells (F) in the inner layer of periosteum (no. cells/P.BS) and/or whole periosteum (no. cells/periosteum) (n = 5 mice/group). Dashed lines in A–C indicate the limit between periosteum and cortical bone. Scale bars: 100 μm (upper panels), 20 μm (lower panels). Data are presented as mean ± SEM. *P < 0.05; **P < 0.01. C, periosteal cortical bone; NS, not significant as determined by 2-tailed Student t test; P, periosteum.

Copyright © 2025 American Society for Clinical Investigation
ISSN: 0021-9738 (print), 1558-8238 (online)

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