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PRRSV infects porcine alveolar macrophages (PAMs) and induces profound mitochondrial dysfunction, leading to the release of mitochondrial DNA (mtDNA). However, the mechanisms by which PRRSV-induced mitochondrial damage acts as a damage-associated molecular pattern (DAMP) to trigger inflammatory responses have not been fully elucidated. Here, we report that highly pathogenic PRRSV (HP-PRRSV) infection upregulates interleukin-1\u03b2 (IL-1\u03b2) messenger RNA (mRNA) expression and protein secretion in a dose- and time-dependent manner. Transmission electron microscopy revealed progressive mitochondrial swelling, cristae disorganization, and matrix loss during HP-PRRSV infection. Using RNAscope combined with MitoGreen staining, we discovered that mitochondrial double-stranded RNA (mtdsRNA), generated from bidirectional transcription of mitochondrial DNA, is released into the cytosol during PRRSV infection. In vitro, transcription-driven mtdsRNA or mtdsRNA isolated from PAMs directly activated the NLRP3 inflammasome, inducing caspase-1 cleavage and IL-1\u03b2 secretion. Mechanistically, the PRRSV-encoded nonstructural protein 11 (nsp11) inhibited NLRP3-dependent inflammatory responses by suppressing the oligomerization of the apoptosis-associated speck-like protein containing a caspase recruitment domain (CARD) (ASC), thereby constraining excessive inflammation and establishing a delicate balance between pro-inflammatory signaling and viral immune evasion. Collectively, our findings identify mtdsRNA as a previously unrecognized mitochondrial DAMP that links PRRSV-induced mitochondrial injury to NLRP3 inflammasome activation, while also revealing a counter-regulatory role for nsp11 in modulating inflammation.<\/jats:p>","DOI":"10.1186\/s13567-026-01854-3","type":"journal-article","created":{"date-parts":[[2026,10,11]],"date-time":"2026-10-11T08:01:26Z","timestamp":1791705686000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["PRRSV infection induces mitochondrial damage and releases mitochondrial dsRNA to activate the NLRP3-dependent inflammatory response"],"prefix":"10.1186","volume":"57","author":[{"given":"Jiangnan","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caihong","family":"Bi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liguo","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zengyu","family":"Shao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-0867-2058","authenticated-orcid":false,"given":"Changjiang","family":"Weng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-9864-1633","authenticated-orcid":false,"given":"Hongyang","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,10,11]]},"reference":[{"key":"1854_CR1","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1080\/01652176.1991.9694296","volume":"13","author":"G Wensvoort","year":"1991","unstructured":"Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F (1991) Mystery swine disease in The Netherlands: the isolation of Lelystad virus. 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