Nat10-mediated N4-acetylcytidine modification enhances Nfatc1 translation to exacerbate osteoclastogenesis in postmenopausal osteoporosis

X Xiaoyi Mo (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) K Keyu Meng (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) B Bohan Xu (Department of Pathology, Nanfang Hospital, Southern Medical University) Z Zehui Li (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) S Shanwei Lan (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) Z Zhengda Ren (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) X Xin Xiang (Institute of Materials, China Academy of Engineering Physics) P Peiqian Zou (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) Z Zesen Chen (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) Z Zhongming Lai (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) X Xiang Ao (School of Biology and Biological Engineering, South China University of Technology) Z Zhongyuan Liu (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University) W Wanjing Shang B Bingyang Dai (Department of Biomedical Engineering, The Hong Kong Polytechnic University) L Li Luo (Department of Cardiac Surgery, The First Affiliated Hospital of Sun Yat-sen University) J Jiajia Xu (State Key Laboratory of Physical Chemistry of Solid Surfaces, iChEM, College of Chemistry and Chemical Engineering, Innovation Laboratory for Sciences and Technologies of Energy Materials of Fujian Province (IKKEM)) Z Zhizhang Wang (Department of Pathology, Nanfang Hospital, Southern Medical University) Z Zhongmin Zhang (Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University)

Abstract

Increased differentiation or activity of osteoclasts is the key pathogenic factor of postmenopausal osteoporosis (PMOP). N4‐acetylcytidine (ac4C) modification, catalyzed by Nat10, is a novel posttranscriptional mRNA modification related to many diseases. However, its impact on regulating osteoclast activation in PMOP remains uncertain. Here, we initially observed that Nat10-mediated ac4C positively correlates with osteoclast differentiation of monocytes and low bone mass in PMOP. The specific knockout of Nat10 in monocytes and remodelin, a Nat10 inhibitor, alleviates ovariectomized (OVX)-induced bone loss by downregulating osteoclast differentiation. Mechanistically, epitranscriptomic analyses reveal that the nuclear factor of activated T cells cytoplasmic 1 (Nfatc1) is the key downstream target of ac4C modification during osteoclast differentiation. Subsequently, translatomic results demonstrate that Nat10-mediated ac4C enhances the translation efficiency (TE) of Nfatc1, thereby inducing Nfatc1 expression and consequent osteoclast maturation. Cumulatively, these findings reveal the promotive role of Nat10 in osteoclast differentiation and PMOP from a novel field of RNA modifications and suggest that Nat10 can be a target of epigenetic therapy for preventing bone loss in PMOP.

Article Details

Volume / Issue Vol. 122, Issue 15
Published April 15, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (18)

X

Xiaoyi Mo

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

K

Keyu Meng

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

B

Bohan Xu

Department of Pathology, Nanfang Hospital, Southern Medical University

Z

Zehui Li

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

S

Shanwei Lan

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

Z

Zhengda Ren

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

X

Xin Xiang

Institute of Materials, China Academy of Engineering Physics

P

Peiqian Zou

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

Z

Zesen Chen

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

Z

Zhongming Lai

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

X

Xiang Ao

School of Biology and Biological Engineering, South China University of Technology

Z

Zhongyuan Liu

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University

W

Wanjing Shang

B

Bingyang Dai

Department of Biomedical Engineering, The Hong Kong Polytechnic University

L

Li Luo

Department of Cardiac Surgery, The First Affiliated Hospital of Sun Yat-sen University

J

Jiajia Xu

State Key Laboratory of Physical Chemistry of Solid Surfaces, iChEM, College of Chemistry and Chemical Engineering, Innovation Laboratory for Sciences and Technologies of Energy Materials of Fujian Province (IKKEM)

Z

Zhizhang Wang

Department of Pathology, Nanfang Hospital, Southern Medical University

Z

Zhongmin Zhang

Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University