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While cardiomyocyte (CM) mutations are known triggers, the mechanisms initiating profibrotic signaling remain elusive. This study investigates the role of CM-derived exosomes and specific transfer RNA\u2013derived small RNAs (tsRNAs) in this pathogenic intercellular communication. Using a cTnIR193H knock-in mouse model, we observed pronounced CF prior to the onset of heart failure, without significant CM apoptosis. This primary fibrotic response was mediated by a paracrine mechanism, as conditioned medium from mutant CMs was sufficient to activate fibroblasts. Subsequent small RNA sequencing of CM-derived exosomes identified the tRNA-derived fragment 5\u2032tiRNA-GluCTC as a significantly enriched species. Functional studies established this RNA as a critical mediator, demonstrating that its overexpression exacerbated fibrotic responses in vitro and induced fibrotic remodeling in wild-type mice, while its inhibition via a cardiac-targeted Adeno-associated virus sponge attenuated fibroblast activation and alleviated fibrosis in RCM mice. Mechanistically, 5\u2032tiRNA-GluCTC is transferred to fibroblasts, directly targets the 3\u2032UTR of Foxq1 to repress its expression, and consequently activates the Smad3\/p-Smad3 signaling cascade. Collectively, these results delineate a 5\u2032tiRNA-GluCTC\/Foxq1\/Smad3 signaling axis that drives fibrosis in RCM, uncovering a previously uncharacterized signaling cascade with therapeutic potential.<\/jats:p>","DOI":"10.1042\/cs20251031","type":"journal-article","created":{"date-parts":[[2026,8,5]],"date-time":"2026-08-05T13:10:01Z","timestamp":1785935401000},"page":"1849-1872","update-policy":"https:\/\/doi.org\/10.1042\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["A novel tsRNA, 5\u2032tiRNA-GluCTC, mediates cardiomyocyte-fibroblast cross-talk to promote cardiac fibrosis in restrictive cardiomyopathy"],"prefix":"10.1042","volume":"140","author":[{"given":"Xiaohui","family":"Xu","sequence":"first","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoli","family":"Yan","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shan","family":"Huang","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maidina","family":"Aini","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lingjuan","family":"Liu","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajin","family":"Li","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jinpeng","family":"Zhang","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fujian","family":"Lu","sequence":"additional","affiliation":[{"name":"2Department of Cardiology, Zhongshan Hospital, Institutes of Biomedical Sciences, Fudan University, Shanghai Institute of Cardiovascular Diseases, Shanghai 200032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peng","family":"Gao","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key Cardiovascular Specialty, Chongqing Municipal Health Commission Key Laboratory of Children\u2019s Vital Organ Development and Diseases, Chongqing 401122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiewei","family":"Lv","sequence":"additional","affiliation":[{"name":"1Department of Cardiology, Children\u2019s Hospital of Chongqing Medical University, National Clinical Research Center for Children and Adolescents\u2019 Health and Diseases, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Key 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