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      <jats:title>Background<\/jats:title>\n                    <jats:p xml:lang=\"en\">\n                      Metabolic dysfunction\u2010associated steatohepatitis (MASH) is anticipated to become the leading cause of hepatocellular carcinoma (HCC). Accumulating evidence indicates that N6\u2010methyladenosine (m\n                      <jats:sup>6<\/jats:sup>\n                      A)\u2010modified circular RNAs (circRNAs) play key roles in tumor malignant progression. However, the precise molecular mechanisms by which circRNAs and their m\n                      <jats:sup>6<\/jats:sup>\n                      A modification regulatory networks respond to metabolic reprogramming, such as lipid overload stress, to drive malignant tumor progression in the context of MASH\u2010related HCC remain unclear. This study aimed to investigate the role and regulatory network of m\n                      <jats:sup>6<\/jats:sup>\n                      A\u2010modified circRNAs in MASH\u2010related HCC.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec xml:lang=\"en\">\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p xml:lang=\"en\">Epitranscriptomic microarray and in situ hybridization assays were used to validate circTACC3 expression in MASH\u2010related HCC specimens. Palmitic acid (PA) and oleic acid (OA) was applied to NAC\u2010organ assembled three\u2010dimensional\u2010organoid and HCC cell lines to imitate pathological lipid overload. The circTACC3\u2010paraspeckle interaction was studied utilizing fluorescence lifetime imaging microscopy\u2010Forster resonance energy transfer. An integrative analysis combining DNA\u2010RNA immunoprecipitation combined with chromatin isolation by RNA purification (DRIP\u2010ChIRP), \u03b3H2AX cleavage under target and tagmentation, and high\u2010throughput\/resolution chromosome conformation capture sequencing were used to study chromatin remodeling induced by circTACC3\u2010formed RNA\u2010DNA hybrids (R loops) at DNA double\u2010strand break (DSB) loci during lipid overload.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec xml:lang=\"en\">\n                    <jats:title>Results<\/jats:title>\n                    <jats:p xml:lang=\"en\">\n                      The most prevalent m\n                      <jats:sup>6<\/jats:sup>\n                      A\u2010modified circRNA in MASH\u2010related HCC, circTACC3, had a substantial impact on the intracellular lipid accumulation, growth, and environmental adaptive survival of tumor cells. Under lipid overload conditions, circTACC3 interacted directly with non\u2010POU domain\u2010containing octamer\u2010binding protein (NONO\/p54\n                      <jats:sup>nrb<\/jats:sup>\n                      ) to assemble intranuclear paraspeckle. This process was dependent on the m\n                      <jats:sup>6<\/jats:sup>\n                      A\u2010modification sites of circTACC3 and facilitated its nuclear retention. Using DRIP\u2010ChIRP\u2010sequencing, we demonstrated that circTACC3\u2010containing paraspeckles were recruited to DSB foci to form R loops (DSB\u2010circTACC3\u2010R loops). We discovered 4 highly enriched motifs of DSB\u2010circTACC3\u2010R loops. DSB\u2010circTACC3\u2010R loops further facilitated the contact and fusion of topologically associated domains (TADs) and selectively activated genes related to the malignant phenotype of MASH\u2010related HCC. Interestingly, circTACC3\u2010R loops exerted positive feedback control over the assembly of circTACC3 paraspeckle and clustering of TADs.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec xml:lang=\"en\">\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p xml:lang=\"en\">\n                      The m\n                      <jats:sup>6<\/jats:sup>\n                      A modification\u2010dependent circTACC3\u2010paraspeckle assembly results in the formation of R loops at DSB foci, leading to chromatin remodeling and the activation of genes involved in MASH\u2010related HCC malignant progression. This process identifies potential therapeutic targets.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1002\/cac2.70061","type":"journal-article","created":{"date-parts":[[2025,10,17]],"date-time":"2025-10-17T05:26:26Z","timestamp":1760678786000},"page":"1583-1610","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Intranuclear paraspeckle\u2010circular RNA TACC3 assembly forms RNA\u2010DNA hybrids to facilitate MASH\u2010related hepatocellular carcinoma growth in an m\n                    <sup>6<\/sup>\n                    A\u2010dependent manner"],"prefix":"10.34133","volume":"45","author":[{"given":"Jingbo","family":"Fu","sequence":"first","affiliation":[{"name":"Eastern Hepatobiliary Surgery Hospital","place":["Shanghai, P. R. China"]},{"name":"Second Military Medical University","place":["Shanghai, P. R. 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A multisociety Delphi consensus statement on new fatty liver disease nomenclature. J Hepatol. 2023;79((6)):1542\u201356.","journal-title":"J Hepatol"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41575-023-00754-7"},{"issue":"4","key":"e_1_3_2_5_2","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1016\/j.cgh.2018.05.057","article-title":"Nonalcoholic Steatohepatitis Is the Fastest Growing Cause of Hepatocellular Carcinoma in Liver Transplant Candidates","volume":"17","author":"Younossi Z","year":"2019","unstructured":"Younossi Z, Stepanova M, Ong JP, Jacobson IM, Bugianesi E, Duseja A, et\u00a0al. Nonalcoholic Steatohepatitis Is the Fastest Growing Cause of Hepatocellular Carcinoma in Liver Transplant Candidates. Clin Gastroenterol Hepatol. 2019;17((4)):748\u201355.e3.","journal-title":"Clin Gastroenterol Hepatol"},{"issue":"3","key":"e_1_3_2_6_2","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1053\/j.gastro.2021.06.008","article-title":"Evidence\u2010Based Management of Hepatocellular Carcinoma: Systematic Review and Meta\u2010analysis of Randomized Controlled Trials (2002\u20102020)","volume":"161","author":"Haber PK","year":"2021","unstructured":"Haber PK, Puigveh\u00ed M, Castet F, Lourdusamy V, Montal R, Tabrizian P, et\u00a0al. Evidence\u2010Based Management of Hepatocellular Carcinoma: Systematic Review and Meta\u2010analysis of Randomized Controlled Trials (2002\u20102020). Gastroenterology. 2021;161((3)):879\u201398.","journal-title":"Gastroenterology"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2022.06.003"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jhep.2017.11.014"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2022.04.021"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1002\/hep.30795"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.canlet.2024.216794"},{"issue":"1","key":"e_1_3_2_12_2","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1186\/s12943-020-01224-3","article-title":"The role of N6\u2010methyladenosine (m6A) modification in the regulation of circRNAs","volume":"19","author":"Zhang L","year":"2020","unstructured":"Zhang L, Hou C, Chen C, Guo Y, Yuan W, Yin D, et\u00a0al. The role of N6\u2010methyladenosine (m6A) modification in the regulation of circRNAs. 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