TY - JOUR
T1 - TRPM7 kinase-mediated immunomodulation in macrophage plays a central role in magnesium ion-induced bone regeneration
AU - Qiao, Wei
AU - Wong, Karen H.M.
AU - Shen, Jie
AU - Wang, Wenhao
AU - Wu, Jun
AU - Li, Jinhua
AU - Lin, Zhengjie
AU - Chen, Zetao
AU - Matinlinna, Jukka P.
AU - Zheng, Yufeng
AU - Wu, Shuilin
AU - Liu, Xuanyong
AU - Lai, Keng Po
AU - Chen, Zhuofan
AU - Lam, Yun Wah
AU - Cheung, Kenneth M.C.
AU - Yeung, Kelvin W.K.
N1 - Funding Information:
We acknowledge HKU Li Ka Shing Faculty of Medicine Faculty Core Facility for providing a harmonious working environment. This work was financially supported by the National Key R&D Program of China (R&D#2018YFA0703100), General Research Fund of Hong Kong Research Grant Council (#17214516, #N_HKU725/16), Sanming Project of Medicine in Shenzhen Team of Excellence in Spinal Deformities and Spinal Degeneration Disease (SZSM201612055), Shenzhen Science and Technology Funds (JSGG20180507183242702), Hong Kong Innovation Technology Fund (ITS/287/17 and ITS/405/18), the Science and Technology Commission of Shanghai Municipality (No. 18410760600), International Partnership Program of Chinese Academy of Sciences (GJHZ1850), National Natural Science Foundation of China (81970975), and Guangdong Financial Fund for Hige-Caliber Hospital Construction (174-2018-XMZC-0001-03-2125/D-10). We thank Dr. Stuart Fraser, School of Medical Sciences, University of Sydney, Australia, and Prof. Cao Xu, Department of Orthopedics, School of Medicine, the Johns Hopkins University, for their useful comments.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/5/17
Y1 - 2021/5/17
N2 - Despite the widespread observations on the osteogenic effects of magnesium ion (Mg2+), the diverse roles of Mg2+ during bone healing have not been systematically dissected. Here, we reveal a previously unknown, biphasic mode of action of Mg2+ in bone repair. During the early inflammation phase, Mg2+ contributes to an upregulated expression of transient receptor potential cation channel member 7 (TRPM7), and a TRPM7-dependent influx of Mg2+ in the monocyte-macrophage lineage, resulting in the cleavage and nuclear accumulation of TRPM7-cleaved kinase fragments (M7CKs). This then triggers the phosphorylation of Histone H3 at serine 10, in a TRPM7-dependent manner at the promoters of inflammatory cytokines, leading to the formation of a pro-osteogenic immune microenvironment. In the later remodeling phase, however, the continued exposure of Mg2+ not only lead to the over-activation of NF-κB signaling in macrophages and increased number of osteoclastic-like cells but also decelerates bone maturation through the suppression of hydroxyapatite precipitation. Thus, the negative effects of Mg2+ on osteogenesis can override the initial pro-osteogenic benefits of Mg2+. Taken together, this study establishes a paradigm shift in the understanding of the diverse and multifaceted roles of Mg2+ in bone healing.
AB - Despite the widespread observations on the osteogenic effects of magnesium ion (Mg2+), the diverse roles of Mg2+ during bone healing have not been systematically dissected. Here, we reveal a previously unknown, biphasic mode of action of Mg2+ in bone repair. During the early inflammation phase, Mg2+ contributes to an upregulated expression of transient receptor potential cation channel member 7 (TRPM7), and a TRPM7-dependent influx of Mg2+ in the monocyte-macrophage lineage, resulting in the cleavage and nuclear accumulation of TRPM7-cleaved kinase fragments (M7CKs). This then triggers the phosphorylation of Histone H3 at serine 10, in a TRPM7-dependent manner at the promoters of inflammatory cytokines, leading to the formation of a pro-osteogenic immune microenvironment. In the later remodeling phase, however, the continued exposure of Mg2+ not only lead to the over-activation of NF-κB signaling in macrophages and increased number of osteoclastic-like cells but also decelerates bone maturation through the suppression of hydroxyapatite precipitation. Thus, the negative effects of Mg2+ on osteogenesis can override the initial pro-osteogenic benefits of Mg2+. Taken together, this study establishes a paradigm shift in the understanding of the diverse and multifaceted roles of Mg2+ in bone healing.
KW - magnesium ion (Mg2+)
KW - bone healing
KW - bone regeneration
UR - http://www.scopus.com/inward/record.url?scp=85106306570&partnerID=8YFLogxK
U2 - 10.1038/s41467-021-23005-2
DO - 10.1038/s41467-021-23005-2
M3 - Article
C2 - 34001887
AN - SCOPUS:85106306570
VL - 12
JO - Nature Communications
JF - Nature Communications
SN - 2041-1723
IS - 1
M1 - 2885
ER -