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Here, we adapt oligonucleotide-mediated proximity-interactome mapping (O-MAP) to map genomic loci, RNAs, and proteins within discrete nuclear neighborhoods, using a cardiac-specific RNA factory organized around nascent\n                  <jats:italic>TTN<\/jats:italic>\n                  RNA as a model. We find that the\n                  <jats:italic>TTN<\/jats:italic>\n                  -associated microenvironment is embedded within a developmentally regulated hub of chromosomal interactions, including\n                  <jats:italic>cis-<\/jats:italic>\n                  interacting active domains and\n                  <jats:italic>trans<\/jats:italic>\n                  -interacting poised and repressed domains. In addition to chromatin contacts, the factory contains diverse RNAs in a pattern consistent with substantial post-transcriptional recruitment and is enriched for RNA-metabolic and chromatin-regulatory proteins. These include the splicing factor RBM20 and chromatin-scaffolding factor SAFB, which exert opposing effects on factory-associated gene expression. Disruption of factory architecture through loss of\n                  <jats:italic>TTN<\/jats:italic>\n                  RNA or RBM20 leads to widespread splicing defects and mislocalization of transcripts. Notably, many splicing defects caused by RBM20 loss are attenuated by\n                  <jats:italic>TTN<\/jats:italic>\n                  RNA depletion, indicating that\n                  <jats:italic>TTN\u2019s<\/jats:italic>\n                  unbound transcript exerts toxic gain-of-function effects on RNA metabolism in the absence of RBM20. Collectively, this work establishes O-MAP as a powerful approach for biochemically dissecting single-locus compartments and reveals how coding RNAs can influence nuclear architecture and gene regulation.\n                <\/jats:p>","DOI":"10.1101\/2024.11.05.622011","type":"posted-content","created":{"date-parts":[[2024,11,6]],"date-time":"2024-11-06T23:05:15Z","timestamp":1730934315000},"source":"Crossref","is-referenced-by-count":5,"title":["Nascent transcript O-MAP reveals the molecular architecture of an RBM20-regulated single-locus subnuclear compartment organized around the\n                  <i>TTN<\/i>\n                  RNA"],"prefix":"10.64898","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0266-6610","authenticated-orcid":false,"given":"Evan E.","family":"Kania","sequence":"first","affiliation":[{"name":"Department of Pharmacology, University of Washington, Seattle, WA, USA"},{"name":"Institute of Stem Cell and Regenerative Medicine, University of Washington, Seattle, 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