{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:27:52Z","timestamp":1790832472987,"version":"4.1.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1010667","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,7,14]],"date-time":"2022-07-14T00:00:00Z","timestamp":1657756800000}}],"reference-count":76,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2022,6,27]],"date-time":"2022-06-27T00:00:00Z","timestamp":1656288000000},"content-version":"vor","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":["32172805"],"award-info":[{"award-number":["32172805"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32172828"],"award-info":[{"award-number":["32172828"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31902262"],"award-info":[{"award-number":["31902262"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31872446"],"award-info":[{"award-number":["31872446"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Scientific and Technological Project of Jilin Province","award":["20210202041NC"],"award-info":[{"award-number":["20210202041NC"]}]},{"name":"Youth Science and Technology Talent Support Project of Jilin Province","award":["QT202015"],"award-info":[{"award-number":["QT202015"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Porcine hemagglutinating encephalomyelitis virus (PHEV) is a highly neurotropic coronavirus belonging to the genus\n                    <jats:italic>Betacoronavirus<\/jats:italic>\n                    . Similar to pathogenic coronaviruses to which humans are susceptible, such as SARS-CoV-2, PHEV is transmitted primarily through respiratory droplets and close contact, entering the central nervous system (CNS) from the peripheral nerves at the site of initial infection. However, the neuroinvasion route of PHEV are poorly understood. Here, we found that BALB\/c mice are susceptible to intranasal PHEV infection and showed distinct neurological manifestations. The behavioral study and histopathological examination revealed that PHEV attacks neurons in the CNS and causes significant smell and taste dysfunction in mice. By tracking neuroinvasion, we identified that PHEV invades the CNS via the olfactory nerve and trigeminal nerve located in the nasal cavity, and olfactory sensory neurons (OSNs) were susceptible to viral infection. Immunofluorescence staining and ultrastructural observations revealed that viral materials traveling along axons, suggesting axonal transport may engage in rapid viral transmission in the CNS. Moreover, viral replication in the olfactory system and CNS is associated with inflammatory and immune responses, tissue disorganization and dysfunction. Overall, we proposed that PHEV may serve as a potential prototype for elucidating the pathogenesis of coronavirus-associated neurological complications and olfactory and taste disorders.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1010667","type":"journal-article","created":{"date-parts":[[2022,6,27]],"date-time":"2022-06-27T13:37:44Z","timestamp":1656337064000},"page":"e1010667","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":25,"title":["PHEV infection: A promising model of betacoronavirus-associated neurological and olfactory dysfunction"],"prefix":"10.1371","volume":"18","author":[{"given":"Junchao","family":"Shi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zi","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rongyi","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yungang","family":"Lan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiyu","family":"Guan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rui","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenzhen","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huijun","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baofeng","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kui","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feng","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3254-1242","authenticated-orcid":true,"given":"Wenqi","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,6,27]]},"reference":[{"issue":"7798","key":"ppat.1010667.ref001","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/s41586-020-2012-7","article-title":"A pneumonia outbreak associated with a new coronavirus of probable bat origin","volume":"579","author":"P Zhou","year":"2020","journal-title":"Nature"},{"key":"ppat.1010667.ref002","article-title":"The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2","year":"2020","journal-title":"Nature microbiology"},{"issue":"9","key":"ppat.1010667.ref003","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1021\/acschemneuro.0c00172","article-title":"SARS-CoV-2: Olfaction, Brain Infection, and the Urgent Need for Clinical Samples Allowing Earlier Virus Detection","volume":"11","author":"R Butowt","year":"2020","journal-title":"ACS Chemical Neuroscience"},{"issue":"20","key":"ppat.1010667.ref004","doi-asserted-by":"crossref","first-page":"2089","DOI":"10.1001\/jama.2020.6771","article-title":"Alterations in Smell or Taste in Mildly Symptomatic Outpatients With SARS-CoV-2 Infection","volume":"323","author":"G Spinato","year":"2020","journal-title":"JAMA"},{"issue":"9","key":"ppat.1010667.ref005","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1016\/S1473-3099(20)30293-0","article-title":"Smell and taste dysfunction in patients with COVID-19","volume":"20","author":"MS Xydakis","year":"2020","journal-title":"The Lancet Infectious Diseases"},{"issue":"23","key":"ppat.1010667.ref006","doi-asserted-by":"crossref","first-page":"2268","DOI":"10.1056\/NEJMc2008597","article-title":"Neurologic Features in Severe SARS-CoV-2 Infection","volume":"382","author":"J Helms","year":"2020","journal-title":"N Engl J Med"},{"issue":"6","key":"ppat.1010667.ref007","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1001\/jamaneurol.2020.1127","article-title":"Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan","volume":"77","author":"L Mao","year":"2020","journal-title":"China. JAMA Neurol"},{"key":"ppat.1010667.ref008","article-title":"The neuroinvasiveness, neurotropism, and neurovirulence of SARS-CoV-2","author":"L Bauer","year":"2022","journal-title":"Trends in neurosciences"},{"issue":"7843","key":"ppat.1010667.ref009","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1038\/s41586-020-2943-z","article-title":"COVID-19 treatments and pathogenesis including anosmia in K18-hACE2 mice","volume":"589","author":"J Zheng","year":"2020","journal-title":"Nature"},{"issue":"596","key":"ppat.1010667.ref010","doi-asserted-by":"crossref","DOI":"10.1126\/scitranslmed.abf8396","article-title":"COVID-19-related anosmia is associated with viral persistence and inflammation in human olfactory epithelium and brain infection in hamsters","volume":"13","author":"GD de Melo","year":"2021","journal-title":"Science translational 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Microbiol"},{"key":"ppat.1010667.ref030","first-page":"92","article-title":"Ulk1 Governs Nerve Growth Factor\/TrkA Signaling by Mediating Rab5 GTPase Activation in Porcine Hemagglutinating Encephalomyelitis Virus-Induced Neurodegenerative Disorders","author":"Z Li","year":"2018","journal-title":"Journal of virology"},{"key":"ppat.1010667.ref031","doi-asserted-by":"crossref","first-page":"109015","DOI":"10.1016\/j.vetmic.2021.109015","article-title":"Porcine hemagglutinating encephalomyelitis virus induces atypical autophagy via opposite regulation of expression and nuclear translocation of transcription factor EB","volume":"255","author":"Z Wang","year":"2021","journal-title":"Veterinary microbiology"},{"issue":"1","key":"ppat.1010667.ref032","doi-asserted-by":"crossref","first-page":"e0169521","DOI":"10.1128\/JVI.01695-21","article-title":"The PERK\/PKR-eIF2alpha Pathway Negatively Regulates Porcine Hemagglutinating Encephalomyelitis Virus Replication by Attenuating Global Protein Translation and Facilitating Stress Granule Formation","volume":"96","author":"J Shi","year":"2022","journal-title":"Journal of virology"},{"issue":"12","key":"ppat.1010667.ref033","doi-asserted-by":"crossref","first-page":"5299","DOI":"10.1007\/s12035-020-02105-y","article-title":"An Experimental Model of Neurodegenerative Disease Based on Porcine Hemagglutinating Encephalomyelitis Virus-Related Lysosomal Abnormalities","volume":"57","author":"Y Lan","year":"2020","journal-title":"Mol Neurobiol"},{"key":"ppat.1010667.ref034","article-title":"Simple behavioral assessment of mouse olfaction","author":"M Yang","year":"2009","journal-title":"Curr Protoc Neurosci."},{"issue":"17","key":"ppat.1010667.ref035","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.00404-18","article-title":"Axonal Transport Enables Neuron-to-Neuron Propagation of Human Coronavirus OC43","volume":"92","author":"M Dube","year":"2018","journal-title":"Journal of 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Cancalon","year":"1982","journal-title":"Tissue Cell"},{"issue":"3","key":"ppat.1010667.ref039","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1002\/jemt.1070240302","article-title":"Morphological study of the effects of intranasal zinc sulfate irrigation on the mouse olfactory epithelium and olfactory bulb","volume":"24","author":"GD Burd","year":"1993","journal-title":"Microsc Res Tech"},{"issue":"3","key":"ppat.1010667.ref040","first-page":"226","article-title":"The effect of coronaviruses on olfaction: systematic review","volume":"59","author":"M Zugaj","year":"2021","journal-title":"Rhinology"},{"key":"ppat.1010667.ref041","article-title":"Corona Viruses and the Chemical Senses: Past, Present, and Future","author":"R Pellegrino","year":"2020","journal-title":"Chem Senses"},{"issue":"2","key":"ppat.1010667.ref042","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1097\/01.mlg.0000249922.37381.1e","article-title":"Identification of viruses in patients with postviral olfactory dysfunction","volume":"117","author":"M Suzuki","year":"2007","journal-title":"Laryngoscope"},{"key":"ppat.1010667.ref043","doi-asserted-by":"crossref","first-page":"386","DOI":"10.3389\/fncel.2018.00386","article-title":"Neurologic Alterations Due to Respiratory Virus Infections","volume":"12","author":"K Bohmwald","year":"2018","journal-title":"Frontiers in cellular neuroscience"},{"issue":"1","key":"ppat.1010667.ref044","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1038\/s41467-020-14626-0","article-title":"Influenza A viruses are transmitted via the air from the nasal respiratory epithelium of ferrets","volume":"11","author":"M Richard","year":"2020","journal-title":"Nature communications"},{"issue":"2","key":"ppat.1010667.ref045","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1038\/s41593-020-00758-5","article-title":"Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19","volume":"24","author":"J Meinhardt","year":"2021","journal-title":"Nat Neurosci"},{"issue":"1","key":"ppat.1010667.ref046","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1038\/s41392-021-00591-7","article-title":"The olfactory route is a potential way for SARS-CoV-2 to invade the central nervous system of rhesus monkeys","volume":"6","author":"L Jiao","year":"2021","journal-title":"Signal Transduct Target Ther"},{"issue":"4","key":"ppat.1010667.ref047","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1007\/s00401-012-1010-8","article-title":"Multiple routes of invasion of wild-type Clade 1 highly pathogenic avian influenza H5N1 virus into the central nervous system (CNS) after intranasal exposure in ferrets","volume":"124","author":"M Yamada","year":"2012","journal-title":"Acta neuropathologica"},{"issue":"7","key":"ppat.1010667.ref048","first-page":"e40308","article-title":"A new model for Hendra virus encephalitis in the mouse","volume":"7","author":"J Dups","year":"2012","journal-title":"PloS onePubMed Central PMCID"},{"key":"ppat.1010667.ref049","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1146\/annurev.cellbio.21.012804.093915","article-title":"Axonal wiring in the mouse olfactory system","volume":"22","author":"P. 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Sjolinder","year":"2010","journal-title":"PloS one"},{"key":"ppat.1010667.ref053","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1038\/srep00736","article-title":"Rapid Nipah virus entry into the central nervous system of hamsters via the olfactory route","volume":"2","author":"VJ Munster","year":"2012","journal-title":"Scientific reports"},{"issue":"2","key":"ppat.1010667.ref054","doi-asserted-by":"crossref","first-page":"e00025","DOI":"10.1128\/mBio.00025-14","article-title":"Burkholderia pseudomallei penetrates the brain via destruction of the olfactory and trigeminal nerves: implications for the pathogenesis of neurological melioidosis","volume":"5","author":"JA St John","year":"2014","journal-title":"mBio"},{"issue":"24","key":"ppat.1010667.ref055","doi-asserted-by":"crossref","first-page":"5932","DOI":"10.1016\/j.cell.2021.10.027","article-title":"Visualizing in deceased COVID-19 patients how SARS-CoV-2 attacks the respiratory and olfactory mucosae but spares the olfactory bulb","volume":"184","author":"M Khan","year":"2021","journal-title":"Cell"},{"issue":"7","key":"ppat.1010667.ref056","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/j.addr.2011.11.002","article-title":"Intranasal delivery of biologics to the central nervous system","volume":"64","author":"JJ Lochhead","year":"2012","journal-title":"Advanced drug delivery reviews"},{"key":"ppat.1010667.ref057","first-page":"eabd2985","article-title":"Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity","author":"L Cantuti-Castelvetri","year":"2020","journal-title":"Science"},{"issue":"6518","key":"ppat.1010667.ref058","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1126\/science.abd3072","article-title":"Neuropilin-1 is a host factor for SARS-CoV-2 infection","volume":"370","author":"JL Daly","year":"2020","journal-title":"Science"},{"issue":"1","key":"ppat.1010667.ref059","doi-asserted-by":"crossref","first-page":"e1009153","DOI":"10.1371\/journal.ppat.1009153","article-title":"The role of Neuropilin-1 in COVID-19","volume":"17","author":"BS Mayi","year":"2021","journal-title":"PLoS Pathog"},{"issue":"1","key":"ppat.1010667.ref060","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1038\/s41598-021-04622-9","article-title":"Recovery of anosmia in hamsters infected with SARS-CoV-2 is correlated with repair of the olfactory epithelium","volume":"12","author":"RA Reyna","year":"2022","journal-title":"Scientific reports"},{"issue":"1","key":"ppat.1010667.ref061","doi-asserted-by":"crossref","first-page":"4354","DOI":"10.1038\/s41467-021-24521-x","article-title":"SARS-CoV-2 infection induces the dedifferentiation of multiciliated cells and impairs mucociliary clearance","volume":"12","author":"R Robinot","year":"2021","journal-title":"Nature 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