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Despite the importance of piRNA for male fertility and a well-defined maturation process, the transcriptional machinery remains poorly understood. Here, we document that D1PAS1, an ATP-dependent RNA helicase, is critical for pachytene piRNA expression from multiple genomic loci and subsequent translocation into the cytoplasm to ensure mature piRNA biogenesis. Depletion of D1PAS1 in gene-edited mice results in the accumulation of R-loops in pachytene spermatocytes, leading to DNA-damage-induced apoptosis, disruption of piRNA biogenesis, spermatogenic arrest, and male infertility. Transcriptome, genome-wide R-loop profiling, and proteomic analyses document that D1PAS1 regulates pachytene piRNA transcript elongation and termination. D1PAS1 subsequently forms a complex with nuclear export components to ensure pachytene piRNA precursor translocation from the nucleus to the cytoplasm for processing into small non-coding RNAs. Thus, our study defines D1PAS1 as a specific transcription activator that promotes R-loop unwinding and is a critical factor in pachytene piRNA biogenesis.<\/jats:p>","DOI":"10.1093\/nar\/gkae712","type":"journal-article","created":{"date-parts":[[2024,8,20]],"date-time":"2024-08-20T11:02:55Z","timestamp":1724151775000},"page":"11973-11994","source":"Crossref","is-referenced-by-count":7,"title":["RNA helicase D1PAS1 resolves R-loops and forms a complex for mouse pachytene piRNA biogenesis required for male fertility"],"prefix":"10.1093","volume":"52","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4945-5674","authenticated-orcid":false,"given":"Heejin","family":"Choi","sequence":"first","affiliation":[{"name":"Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health , Bethesda , MD 20892,\u00a0","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1959-1117","authenticated-orcid":false,"given":"Lecong","family":"Zhou","sequence":"additional","affiliation":[{"name":"Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health , Bethesda , MD 20892,\u00a0","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yangu","family":"Zhao","sequence":"additional","affiliation":[{"name":"Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health , Bethesda , MD 20892,\u00a0","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7127-0871","authenticated-orcid":false,"given":"Jurrien","family":"Dean","sequence":"additional","affiliation":[{"name":"Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health , Bethesda , MD 20892,\u00a0","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,8,20]]},"reference":[{"key":"2024102814480484600_B1","first-page":"189","volume-title":"The Physiology of Reproduction","author":"Yanagimachi","year":"1994","edition":"2nd edn."},{"key":"2024102814480484600_B2","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1002\/aja.1000900202","article-title":"Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique","volume":"90","author":"Leblond","year":"1952","journal-title":"Am. 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