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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2025,4,15]]},"abstract":"<jats:p>Increased differentiation or activity of osteoclasts is the key pathogenic factor of postmenopausal osteoporosis (PMOP). N4\u2010acetylcytidine (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.<\/jats:p>","DOI":"10.1073\/pnas.2423991122","type":"journal-article","created":{"date-parts":[[2025,4,7]],"date-time":"2025-04-07T15:01:45Z","timestamp":1744038105000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":20,"title":["Nat10-mediated N4-acetylcytidine modification enhances Nfatc1 translation to exacerbate osteoclastogenesis in postmenopausal osteoporosis"],"prefix":"10.1073","volume":"122","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5781-2534","authenticated-orcid":false,"given":"Xiaoyi","family":"Mo","sequence":"first","affiliation":[{"name":"Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University","place":["Guangzhou, 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Nanfang Hospital, Southern Medical University","place":["Guangzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zesen","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University","place":["Guangzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongming","family":"Lai","sequence":"additional","affiliation":[{"name":"Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University","place":["Guangzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiang","family":"Ao","sequence":"additional","affiliation":[{"name":"Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University","place":["Guangzhou, 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China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Luo","sequence":"additional","affiliation":[{"name":"Department of Cardiac Surgery, The First Affiliated Hospital of Sun Yat-sen University","place":["Guangzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajia","family":"Xu","sequence":"additional","affiliation":[{"name":"Division of Spine Surgery, Department of Orthopaedics, Nanfang Hospital, Southern Medical University","place":["Guangzhou, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4699-953X","authenticated-orcid":false,"given":"Zhizhang","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Pathology, Nanfang Hospital, Southern Medical University","place":["Guangzhou, China"]},{"name":"Department of Pathology, School of Basic Medical Sciences, Southern Medical University","place":["Guangzhou, 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Menopause 29, 335\u2013343 (2022).","journal-title":"Menopause"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(21)02646-5"},{"key":"e_1_3_4_5_2","article-title":"An integrated microcurrent delivery system facilitates human parathyroid hormone delivery for enhancing osteoanabolic effect","author":"Mo X.","year":"2024","unstructured":"X. Mo , An integrated microcurrent delivery system facilitates human parathyroid hormone delivery for enhancing osteoanabolic effect. Small Methods e2401144 (2024), 10.1002\/smtd.202401144.","journal-title":"Small Methods"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"1153585","DOI":"10.3389\/fgene.2023.1153585","article-title":"Comprehensive analysis of epigenetics mechanisms in osteoporosis","volume":"14","author":"Chen Y.","year":"2023","unstructured":"Y. Chen, Y. Sun, X. Xue, H. Ma, Comprehensive analysis of epigenetics mechanisms in osteoporosis. Front. 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Sci."},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","DOI":"10.1111\/cpr.13577","article-title":"NAT10-mediated ac(4)C modification promotes ectoderm differentiation of human embryonic stem cells via acetylating NR2F1 mRNA","volume":"57","author":"Ge J.","year":"2024","unstructured":"J. Ge, Z. Wang, J. Wu, NAT10-mediated ac(4)C modification promotes ectoderm differentiation of human embryonic stem cells via acetylating NR2F1 mRNA. Cell Prolif. 57, e13577 (2024).","journal-title":"Cell Prolif."},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"eadh9871","DOI":"10.1126\/sciadv.adh9871","article-title":"N-acetyltransferase NAT10 controls cell fates via connecting mRNA cytidine acetylation to chromatin signaling","volume":"10","author":"Hu Z.","year":"2024","unstructured":"Z. Hu , N-acetyltransferase NAT10 controls cell fates via connecting mRNA cytidine acetylation to chromatin signaling. Sci. Adv. 10, eadh9871 (2024).","journal-title":"Sci. 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Arango , Direct epitranscriptomic regulation of mammalian translation initiation through N4-acetylcytidine. Mol. Cell 82, 2912 (2022).","journal-title":"Mol. Cell"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/s10020-024-00788-w","article-title":"Recent advances of NFATc1 in rheumatoid arthritis-related bone destruction: Mechanisms and potential therapeutic targets","volume":"30","author":"Zheng H.","year":"2024","unstructured":"H. Zheng , Recent advances of NFATc1 in rheumatoid arthritis-related bone destruction: Mechanisms and potential therapeutic targets. Mol. Med. 30, 20 (2024).","journal-title":"Mol. 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Biophys."},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.omtn.2020.01.037","article-title":"The processing, gene regulation, biological functions, and clinical relevance of N4-acetylcytidine on RNA: A systematic review","volume":"20","author":"Jin G.","year":"2020","unstructured":"G. Jin, M. Xu, M. Zou, S. Duan, The processing, gene regulation, biological functions, and clinical relevance of N4-acetylcytidine on RNA: A systematic review. Mol. Ther. Nucleic Acids 20, 13\u201324 (2020).","journal-title":"Mol. Ther. Nucleic Acids"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"127789","DOI":"10.1016\/j.ijbiomac.2023.127789","article-title":"The emerging roles of ac4C acetylation \u201cwriter\u201d NAT10 in tumorigenesis: A comprehensive review","volume":"254","author":"Wang L.","year":"2024","unstructured":"L. Wang , The emerging roles of ac4C acetylation \u201cwriter\u201d NAT10 in tumorigenesis: A comprehensive review. Int. J. 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Alzheimers Dis. 90, 1659\u20131675 (2022).","journal-title":"J. Alzheimers Dis."},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bcp.2023.115628"},{"key":"e_1_3_4_38_2","first-page":"2464","article-title":"NAT1 promotes osteolytic metastasis in luminal breast cancer by regulating the bone metastatic niche via NF-kappaB\/IL-1B signaling pathway","volume":"10","author":"Zhao C.","year":"2020","unstructured":"C. Zhao , NAT1 promotes osteolytic metastasis in luminal breast cancer by regulating the bone metastatic niche via NF-kappaB\/IL-1B signaling pathway. Am. J. Cancer Res. 10, 2464\u20132479 (2020).","journal-title":"Am. J. Cancer Res."},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"2675","DOI":"10.2147\/OTT.S92275","article-title":"Associations of polymorphisms in NAT2 gene with risk and metastasis of osteosarcoma in young Chinese population","volume":"8","author":"Huang Z.","year":"2015","unstructured":"Z. Huang, L. Yuan, Z. Jiang, D. Wang, Associations of polymorphisms in NAT2 gene with risk and metastasis of osteosarcoma in young Chinese population. Onco. Targets Ther. 8, 2675\u20132680 (2015).","journal-title":"Onco. Targets Ther."},{"key":"e_1_3_4_40_2","first-page":"8833527","article-title":"NAT10 promotes osteogenic differentiation of mesenchymal stem cells by mediating N4-acetylcytidine modification of gremlin 1","volume":"2021","author":"Zhu Z.","year":"2021","unstructured":"Z. Zhu, X. Xing, S. Huang, Y. Tu, NAT10 promotes osteogenic differentiation of mesenchymal stem cells by mediating N4-acetylcytidine modification of gremlin 1. Stem. Cells Int. 2021, 8833527 (2021).","journal-title":"Stem. Cells Int."},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"6460","DOI":"10.1038\/s41598-017-06614-0","article-title":"Estrogen regulates bone turnover by targeting RANKL expression in bone lining cells","volume":"7","author":"Streicher C.","year":"2017","unstructured":"C. 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