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Here, we show that African swine fever virus (ASFV), one of most devastating pathogens to the worldwide swine industry, can reshape the autophagy\u2013lysosome axis by recruiting the critical lysosome membrane proteins (LAMP1 and LAMP2) to viral factories while inhibiting autophagic induction in macrophages. The screening of viral membrane proteins led to the identification of several ASFV membrane proteins, exemplified by viral protein pEP153R, that could significantly alter the subcellular localization of LAMP1\/2 when expressed alone in transfected cells. Further analysis showed that pEP153R was also a component of viral factories and could induce endoplasmic reticulum (ER) retention of LAMP1\/2, leading to the inhibition of the fusion of autophagosomes with lysosomes. Interestingly, the ASFV mutant lacking EP153R could still actively recruit LAMP into viral factories (VFs) and inhibit autophagic flux, indicating the existence of a functional redundancy of other viral proteins in the absence of pEP153R and highlighting the complexity of ASFV replication biology. Taken together, our results reveal novel information about the interplay of ASFV with the autophagy\u2013lysosome axis and a previously unrecognized function of ASFV protein pEP153R in regulating the cellular autophagic process.<\/jats:p>","DOI":"10.3390\/cimb46100667","type":"journal-article","created":{"date-parts":[[2024,10,7]],"date-time":"2024-10-07T08:35:23Z","timestamp":1728290123000},"page":"11236-11254","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Modulation of Autophagy\u2013Lysosome Axis by African Swine Fever Virus and Its Encoded Protein pEP153R"],"prefix":"10.3390","volume":"46","author":[{"given":"Si-Yu","family":"Bai","sequence":"first","affiliation":[{"name":"Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing 100094, China"},{"name":"National Key Laboratory of Veterinary Public Health 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100094, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-8680-5251","authenticated-orcid":false,"given":"Zhiying","family":"Cui","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, China Agricultural University, Beijing 100094, China"},{"name":"National Key Laboratory of Veterinary Public Health Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100094, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajun","family":"Wu","sequence":"additional","affiliation":[{"name":"China Animal Disease Control Center, Beijing 100125, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yajin","family":"Qu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Epidemiology of Ministry of Agriculture and Rural Affairs, College of Veterinary Medicine, 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