{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T18:38:51Z","timestamp":1792607931560,"version":"4.5.0"},"reference-count":83,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T00:00:00Z","timestamp":1792540800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32402868"],"award-info":[{"award-number":["32402868"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Joint Funds of the National Natural Science Foundation of China","award":["U24A20449"],"award-info":[{"award-number":["U24A20449"]}]},{"name":"Postdoctoral Fellowship Program of CPSF","award":["GZB20240250"],"award-info":[{"award-number":["GZB20240250"]}]},{"name":"Hubei Provincial Natural Science Foundation","award":["2024AFE010"],"award-info":[{"award-number":["2024AFE010"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>Rabies virus (RABV), the prototypical lyssavirus, suppresses neuronal ferroptosis through lipid droplet (LD) biogenesis, which is a critical immune evasion strategy we previously identified. However, the mechanistic link between LD formation and ferroptosis regulation during RABV infection remains poorly defined. Here, we report that RABV upregulate Regulator of G Protein Signaling 4 (RGS4), a ferroptosis-associated regulator, and this induction is strictly dependent on triglyceride synthesis and subsequent LD formation. Functionally, genetic or pharmacological inhibition of RGS4 elevates ferroptosis susceptibility, thereby restricting viral replication. Mechanistically, RGS4 depletion reduces HERC2, impairing the assembly of branched K48\/K63 ubiquitin chains on NCOA4, which is essential for its proteasomal degradation, thereby enhancing NCOA4 stability. Stabilized NCOA4 promotes ferritinophagy, leading to degradation of ferritin heavy chain (FTH) and ultimately inducing ferroptosis. Critically, we identified that the lyssavirus matrix (M) protein directly counteracts this pathway: M protein inhibits RGS4 degradation via the Cys\/N-degron system through incomplete autophagy, stabilizing RGS4 to maintain HERC2 expression, promote NCOA4 ubiquitination, and attenuate ferritinophagy. This mechanism reduces ferroptosis susceptibility and enables viral replication. Our findings unveil a novel lyssavirus-specific regulatory axis, RGS4-HERC2-NCOA4-FTH, that modulates ferroptosis, highlighting the critical role of ferroptosis in lyssavirus infection and pathogenesis.<\/jats:p>","DOI":"10.1371\/journal.ppat.1014726","type":"journal-article","created":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T17:49:51Z","timestamp":1792604991000},"page":"e1014726","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Lyssavirus matrix protein stabilizes RGS4 to suppress ferroptosis via incomplete autophagy and iron metabolic reprogramming"],"prefix":"10.1371","volume":"22","author":[{"given":"Jianqing","family":"Zhao","sequence":"first","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pingping","family":"Chen","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meixin","family":"Sun","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chuan","family":"Liang","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhen F.","family":"Fu","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0569-8105","authenticated-orcid":true,"given":"Ling","family":"Zhao","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]},{"name":"Hubei Hongshan Laboratory","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming","family":"Zhou","sequence":"additional","affiliation":[{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["National Key Laboratory of Agricultural Microbiology"]},{"name":"Huazhong Agricultural University","place":["Wuhan, China"],"department":["Key Laboratory of Preventive Veterinary Medicine of Hubei Province, College of Veterinary Medicine"]},{"name":"Frontiers Science Center for Animal Breeding and Sustainable Production","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,10,21]]},"reference":[{"issue":"1","key":"ppat.1014726.ref001","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nrmicro2260","article-title":"The cell biology of rabies virus: using stealth to reach the brain","volume":"8","author":"MJ Schnell","year":"2010","journal-title":"Nat Rev Microbiol"},{"issue":"1","key":"ppat.1014726.ref002","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1146\/annurev-virology-100114-055157","article-title":"Everything You Always Wanted to Know About Rabies Virus (But Were Afraid to Ask)","volume":"2","author":"BM Davis","year":"2015","journal-title":"Annu Rev Virol"},{"key":"ppat.1014726.ref003","doi-asserted-by":"crossref","first-page":"17091","DOI":"10.1038\/nrdp.2017.91","article-title":"Rabies","volume":"3","author":"AR Fooks","year":"2017","journal-title":"Nat Rev Dis Primers"},{"issue":"4","key":"ppat.1014726.ref004","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1038\/nrmicro.2018.11","article-title":"The spread and evolution of rabies virus: conquering new frontiers","volume":"16","author":"CR Fisher","year":"2018","journal-title":"Nat Rev Microbiol"},{"issue":"2","key":"ppat.1014726.ref005","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.01473-21","article-title":"Lipid Droplets Are Beneficial for Rabies Virus Replication by Facilitating Viral Budding","volume":"96","author":"J Zhao","year":"2022","journal-title":"J Virol"},{"key":"ppat.1014726.ref006","article-title":"Metabolic regulatory nodes of the inflammasome and inflammatory cell death","author":"E Lee","year":"2026","journal-title":"Trends Immunol"},{"issue":"8","key":"ppat.1014726.ref007","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1038\/s41574-023-00845-0","article-title":"Lipid droplet biogenesis and functions in health and disease","volume":"19","author":"A Zadoorian","year":"2023","journal-title":"Nat Rev Endocrinol"},{"key":"ppat.1014726.ref008","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1146\/annurev-cellbio-100616-060608","article-title":"Lipid Droplet Biogenesis","volume":"33","author":"TC Walther","year":"2017","journal-title":"Annu Rev Cell Dev Biol"},{"issue":"7","key":"ppat.1014726.ref009","doi-asserted-by":"crossref","DOI":"10.1083\/jcb.202102136","article-title":"Lipid droplets in the nervous system","volume":"220","author":"I Ralhan","year":"2021","journal-title":"J Cell Biol"},{"issue":"7","key":"ppat.1014726.ref010","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1038\/s42255-025-01321-x","article-title":"Triglycerides are an important fuel reserve for synapse function in the brain","volume":"7","author":"M Kumar","year":"2025","journal-title":"Nat Metab"},{"key":"ppat.1014726.ref011","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.abb.2018.08.001","article-title":"Role of DGAT 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RGS4 confers receptor-selective inhibition of G protein signaling","volume":"273","author":"W Zeng","year":"1998","journal-title":"J Biol Chem"},{"issue":"14","key":"ppat.1014726.ref028","doi-asserted-by":"crossref","first-page":"2401","DOI":"10.1016\/j.cell.2022.06.003","article-title":"Ferroptosis turns 10: Emerging mechanisms, physiological functions, and therapeutic applications","volume":"185","author":"BR Stockwell","year":"2022","journal-title":"Cell"},{"key":"ppat.1014726.ref029","doi-asserted-by":"crossref","first-page":"5218","DOI":"10.1016\/j.csbj.2022.09.018","article-title":"Revealing a novel contributing landscape of ferroptosis-related genes in Parkinson\u2019s disease","volume":"20","author":"X Jian","year":"2022","journal-title":"Comput Struct Biotechnol J"},{"issue":"17","key":"ppat.1014726.ref030","doi-asserted-by":"crossref","first-page":"4781","DOI":"10.7150\/thno.25189","article-title":"RGS4 deficit in prefrontal cortex contributes to the behaviors related to schizophrenia via system xc--mediated glutamatergic dysfunction in mice","volume":"8","author":"M-W Huang","year":"2018","journal-title":"Theranostics"},{"issue":"1","key":"ppat.1014726.ref031","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s12964-020-00552-7","article-title":"Regulators of G-protein signaling, RGS2 and RGS4, inhibit protease-activated receptor 4-mediated signaling by forming a complex with the receptor and G\u03b1 in live cells","volume":"18","author":"Y Kim","year":"2020","journal-title":"Cell Commun Signal"},{"issue":"3","key":"ppat.1014726.ref032","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1046\/j.1471-4159.2000.0750934.x","article-title":"Activation of extracellular signal-regulated kinase (ERK) and Akt by human serotonin 5-HT(1B) receptors in transfected BE(2)-C neuroblastoma cells is inhibited by RGS4","volume":"75","author":"AM Leone","year":"2000","journal-title":"J Neurochem"},{"issue":"15","key":"ppat.1014726.ref033","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.aea3979","article-title":"Innate immune sensing of dietary alcohol ignites inflammation to drive alcohol-related disease","volume":"12","author":"Y Jang","year":"2026","journal-title":"Sci Adv"},{"issue":"3","key":"ppat.1014726.ref034","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.tcb.2022.07.005","article-title":"The Cys\/N-degron pathway in the ubiquitin-proteasome system and autophagy","volume":"33","author":"AJ Heo","year":"2023","journal-title":"Trends Cell Biol"},{"issue":"50","key":"ppat.1014726.ref035","article-title":"The N-terminal cysteine is a dual sensor of oxygen and oxidative stress","volume":"118","author":"AJ Heo","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"ppat.1014726.ref036","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1080\/15548627.2024.2338575","article-title":"The matrix protein of 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in myocardial ischemia-reperfusion injury","volume":"21","author":"S Xue","year":"2025","journal-title":"Autophagy"},{"key":"ppat.1014726.ref040","doi-asserted-by":"crossref","first-page":"1279655","DOI":"10.3389\/fmicb.2023.1279655","article-title":"The role of ferroptosis in virus infections","volume":"14","author":"J Wang","year":"2023","journal-title":"Front Microbiol"},{"key":"ppat.1014726.ref041","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.freeradbiomed.2023.05.004","article-title":"H1N1 influenza virus infection through NRF2-KEAP1-GCLC pathway induces ferroptosis in nasal mucosal epithelial cells","volume":"204","author":"C Liu","year":"2023","journal-title":"Free Radic Biol Med"},{"issue":"6","key":"ppat.1014726.ref042","doi-asserted-by":"crossref","first-page":"115783","DOI":"10.1016\/j.celrep.2025.115783","article-title":"Pexophagy-driven redox imbalance promotes virus-induced ferroptosis","volume":"44","author":"H Jiang","year":"2025","journal-title":"Cell Rep"},{"issue":"6","key":"ppat.1014726.ref043","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1038\/ncb3358","article-title":"The increasing complexity of the ubiquitin code","volume":"18","author":"R Yau","year":"2016","journal-title":"Nat Cell Biol"},{"issue":"7","key":"ppat.1014726.ref044","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.1716673115","article-title":"K63 ubiquitylation triggers proteasomal degradation by seeding branched ubiquitin chains","volume":"115","author":"F Ohtake","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5","key":"ppat.1014726.ref045","doi-asserted-by":"crossref","DOI":"10.1126\/sciadv.ade9585","article-title":"NRF2 controls iron homeostasis and ferroptosis through HERC2 and VAMP8","volume":"9","author":"A Anandhan","year":"2023","journal-title":"Sci 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Xia","year":"2021","journal-title":"Viruses"},{"issue":"1","key":"ppat.1014726.ref050","article-title":"Acyl-Coenzyme A Synthetase Long-Chain Family Member 4 Is Involved in Viral Replication Organelle Formation and Facilitates Virus Replication via Ferroptosis","volume":"13","author":"Y-A Kung","year":"2022","journal-title":"mBio"},{"issue":"9","key":"ppat.1014726.ref051","article-title":"Pseudorabies virus induces ferroptosis by disrupting iron homeostasis through activation of TfR1 and ferritinophagy","volume":"99","author":"Z Ma","year":"2025","journal-title":"J Virol"},{"issue":"1","key":"ppat.1014726.ref052","doi-asserted-by":"crossref","first-page":"2522877","DOI":"10.1080\/22221751.2025.2522877","article-title":"Monkeypox virus induces ferroptosis to facilitate viral replication and promotes inflammatory responses","volume":"14","author":"X Chuai","year":"2025","journal-title":"Emerg Microbes 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