{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T03:08:18Z","timestamp":1790824098995,"version":"4.1.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1009041","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,5,11]],"date-time":"2021-05-11T00:00:00Z","timestamp":1620691200000}}],"reference-count":52,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2021,4,29]],"date-time":"2021-04-29T00:00:00Z","timestamp":1619654400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100015938","name":"Hillman Foundation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100015938","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Cystic Fibrosis Foundation Research Development Program to the University of Pittsburgh"},{"name":"Region V\u00e4stra G\u00f6taland, Sweden"},{"name":"Region V\u00e4stra G\u00f6taland, Sweden"},{"name":"Region V\u00e4stra G\u00f6taland, Sweden"},{"name":"Region V\u00e4stra G\u00f6taland, Sweden"},{"name":"University of Pittsburgh School of Medicine","award":["Dean\u2019s Faculty Advancement Award"],"award-info":[{"award-number":["Dean\u2019s Faculty Advancement Award"]}]},{"DOI":"10.13039\/100016300","name":"University of Pittsburgh Center for Research Computing","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100016300","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["P30CA047904"],"award-info":[{"award-number":["P30CA047904"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Epstein-Barr virus (EBV) is a ubiquitous \u03b3-herpesvirus with latent and lytic cycles. EBV replicates in the stratified epithelium but the nasopharynx is also composed of pseudostratified epithelium with distinct cell types. Latent infection is associated with nasopharyngeal carcinoma (NPC). Here, we show with nasopharyngeal conditionally reprogrammed cells cultured at the air-liquid interface that pseudostratified epithelial cells are susceptible to EBV infection. Donors varied in susceptibility to\n                    <jats:italic>de novo<\/jats:italic>\n                    EBV infection, but susceptible cultures also displayed differences with respect to pathogenesis. The cultures from one donor yielded lytic infection but cells from two other donors were positive for EBV-encoded EBERs and negative for other lytic infection markers. All cultures stained positive for the pseudostratified markers CK7, MUC5AC, \u03b1-tubulin in cilia, and the EBV epithelial cell receptor Ephrin receptor A2. To define EBV transcriptional programs by cell type and to elucidate latent\/lytic infection-differential changes, we performed single cell RNA-sequencing on one EBV-infected culture that resulted in alignment with many EBV transcripts. EBV transcripts represented a small portion of the total transcriptome (~0.17%). All cell types in the pseudostratified epithelium had detectable EBV transcripts with suprabasal cells showing the highest number of reads aligning to many EBV genes. Several restriction factors (\n                    <jats:italic>IRF1<\/jats:italic>\n                    ,\n                    <jats:italic>MX1<\/jats:italic>\n                    ,\n                    <jats:italic>STAT1<\/jats:italic>\n                    ,\n                    <jats:italic>C18orf25<\/jats:italic>\n                    ) known to limit lytic infection were expressed at lower levels in the lytic subcluster. A third of the differentially-expressed genes in NPC tumors compared to an uninfected pseudostratified ALI culture overlapped with the differentially-expressed genes in the latent subcluster. A third of these commonly perturbed genes were specific to EBV infection and changed in the same direction. Collectively, these findings suggest that the pseudostratified epithelium could harbor EBV infection and that the pseudostratified infection model mirrors many of the transcriptional changes imposed by EBV infection in NPC.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1009041","type":"journal-article","created":{"date-parts":[[2021,4,29]],"date-time":"2021-04-29T13:57:59Z","timestamp":1619704679000},"page":"e1009041","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":28,"title":["A primary nasopharyngeal three-dimensional air-liquid interface cell culture model of the pseudostratified epithelium reveals differential donor- and cell type-specific susceptibility to Epstein-Barr virus infection"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0389-986X","authenticated-orcid":true,"given":"Phillip","family":"Ziegler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yarong","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9365-3742","authenticated-orcid":true,"given":"Yulong","family":"Bai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanna","family":"Abrahamsson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8590-1195","authenticated-orcid":true,"given":"Alan","family":"B\u00e4ckerholm","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8993-8617","authenticated-orcid":true,"given":"Alex S.","family":"Reznik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony","family":"Green","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7599-0203","authenticated-orcid":true,"given":"John A.","family":"Moore","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6563-6606","authenticated-orcid":true,"given":"Stella E.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1417-2906","authenticated-orcid":true,"given":"Michael M.","family":"Myerburg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyun Jung","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1189-5092","authenticated-orcid":true,"given":"Ka-Wei","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9556-1745","authenticated-orcid":true,"given":"Kathy Ho Yen","family":"Shair","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,4,29]]},"reference":[{"issue":"12","key":"ppat.1009041.ref001","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1038\/nrc.2016.92","article-title":"Epstein-Barr virus: more than 50 years old and still providing surprises","volume":"16","author":"LS Young","year":"2016","journal-title":"Nature reviews Cancer"},{"key":"ppat.1009041.ref002","first-page":"339","article-title":"Nasopharyngeal Carcinoma: An Evolving Role for the Epstein-Barr Virus","volume":"390","author":"N Raab-Traub","year":"2015","journal-title":"Current topics in microbiology and immunology"},{"issue":"4","key":"ppat.1009041.ref003","article-title":"New Insights from Elucidating the Role of LMP1 in Nasopharyngeal Carcinoma","volume":"10","author":"KHY Shair","year":"2018","journal-title":"Cancers"},{"issue":"2","key":"ppat.1009041.ref004","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.semcancer.2012.02.004","article-title":"The biology of EBV infection in human epithelial cells","volume":"22","author":"SW Tsao","year":"2012","journal-title":"Seminars in cancer biology"},{"issue":"11","key":"ppat.1009041.ref005","first-page":"549","article-title":"Epstein-Barr virus infection and persistence in nasopharyngeal epithelial cells","volume":"33","author":"CM Tsang","year":"2014","journal-title":"Chin J 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Chan","year":"2000","journal-title":"Cancer research"},{"issue":"5","key":"ppat.1009041.ref009","article-title":"mSphere of Influence: 3-D Culture Models Influence Studies on Epstein-Barr Virus Molecular Pathogenesis in the Epithelium","volume":"5","author":"KHY Shair","year":"2020","journal-title":"mSphere"},{"issue":"4","key":"ppat.1009041.ref010","doi-asserted-by":"crossref","DOI":"10.1128\/mSphere.00152-18","article-title":"Air-Liquid Interface Method To Study Epstein-Barr Virus Pathogenesis in Nasopharyngeal Epithelial Cells","volume":"3","author":"EA Caves","year":"2018","journal-title":"mSphere"},{"issue":"1","key":"ppat.1009041.ref011","article-title":"The Long and Complicated Relationship between Epstein-Barr Virus and Epithelial Cells","volume":"91","author":"LM Hutt-Fletcher","year":"2017","journal-title":"Journal of 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virus infections","volume":"74","author":"J Webster-Cyriaque","year":"2000","journal-title":"Journal of virology"},{"issue":"22","key":"ppat.1009041.ref025","doi-asserted-by":"crossref","first-page":"8790","DOI":"10.1073\/pnas.87.22.8790","article-title":"Epstein-Barr virus small nuclear RNAs are not expressed in permissively infected cells in AIDS-associated leukoplakia","volume":"87","author":"K Gilligan","year":"1990","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"8","key":"ppat.1009041.ref026","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1002\/(SICI)1097-0142(19980415)82:8<1449::AID-CNCR3>3.0.CO;2-4","article-title":"Epstein-Barr virus detection in nasopharyngeal tissues of patients with suspected nasopharyngeal carcinoma","volume":"82","author":"ST Tsai","year":"1998","journal-title":"Cancer"},{"issue":"Pt 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Microbiol"},{"issue":"2","key":"ppat.1009041.ref030","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1038\/s41564-017-0080-8","article-title":"Ephrin receptor A2 is an epithelial cell receptor for Epstein-Barr virus entry","volume":"3","author":"H Zhang","year":"2018","journal-title":"Nat Microbiol"},{"issue":"5","key":"ppat.1009041.ref031","doi-asserted-by":"crossref","first-page":"340","DOI":"10.3109\/10520295.2010.502844","article-title":"A panel of antibodies for identifying squamous metaplasia in endobronchial biopsies from smokers","volume":"86","author":"J Merrifield","year":"2011","journal-title":"Biotech Histochem"},{"issue":"10","key":"ppat.1009041.ref032","doi-asserted-by":"crossref","first-page":"e1005195","DOI":"10.1371\/journal.ppat.1005195","article-title":"Differentiation-Dependent KLF4 Expression Promotes Lytic Epstein-Barr Virus Infection in Epithelial Cells","volume":"11","author":"DM Nawandar","year":"2015","journal-title":"PLoS pathogens"},{"issue":"11","key":"ppat.1009041.ref033","article-title":"Epstein-Barr Virus (EBV) Tegument Protein BGLF2 Suppresses Type I Interferon Signaling To Promote EBV Reactivation","volume":"94","author":"X Liu","year":"2020","journal-title":"Journal of virology"},{"issue":"1","key":"ppat.1009041.ref034","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.01342-18","article-title":"Going the Distance: Optimizing RNA-Seq Strategies for Transcriptomic Analysis of Complex Viral Genomes","volume":"93","author":"DP Depledge","year":"2019","journal-title":"Journal of virology"},{"key":"ppat.1009041.ref035","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.46339","article-title":"HSV-1 single-cell analysis reveals the activation of anti-viral and developmental programs in distinct sub-populations","volume":"8","author":"N Drayman","year":"2019","journal-title":"Elife"},{"issue":"1","key":"ppat.1009041.ref036","doi-asserted-by":"crossref","first-page":"4878","DOI":"10.1038\/s41467-019-12894-z","article-title":"Single-cell RNA-sequencing of herpes simplex virus 1-infected cells connects NRF2 activation to an antiviral program","volume":"10","author":"E Wyler","year":"2019","journal-title":"Nature communications"},{"key":"ppat.1009041.ref037","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.52168","article-title":"Single cell analysis reveals human cytomegalovirus drives latently infected cells towards an anergic-like monocyte state","volume":"9","author":"M Shnayder","year":"2020","journal-title":"Elife"},{"key":"ppat.1009041.ref038","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.62586","article-title":"Single-cell RNA-seq reveals transcriptomic heterogeneity mediated by host-pathogen dynamics in lymphoblastoid cell lines","volume":"10","author":"ED SoRelle","year":"2021","journal-title":"Elife"},{"issue":"11","key":"ppat.1009041.ref039","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1038\/s41422-020-00402-8","article-title":"Single-cell transcriptomic analysis defines the interplay between tumor cells, viral infection, and the microenvironment in nasopharyngeal carcinoma","volume":"30","author":"S Jin","year":"2020","journal-title":"Cell research"},{"issue":"1","key":"ppat.1009041.ref040","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1038\/s41467-021-21043-4","article-title":"Tumour heterogeneity and intercellular networks of nasopharyngeal carcinoma at single cell resolution","volume":"12","author":"Y Liu","year":"2021","journal-title":"Nature communications"},{"issue":"20","key":"ppat.1009041.ref041","doi-asserted-by":"crossref","DOI":"10.1242\/dev.177428","article-title":"Novel dynamics of human mucociliary differentiation revealed by single-cell RNA sequencing of nasal epithelial 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Siddiqi","year":"2019","journal-title":"Journal of virology"},{"key":"ppat.1009041.ref045","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.virol.2019.11.011","article-title":"Protein inhibitor of activated STAT1 (PIAS1) inhibits IRF8 activation of Epstein-Barr virus lytic gene expression","volume":"540","author":"K Zhang","year":"2020","journal-title":"Virology"},{"issue":"7","key":"ppat.1009041.ref046","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1002\/hed.25131","article-title":"Presence of lytic Epstein-Barr virus infection in nasopharyngeal carcinoma","volume":"40","author":"F Yu","year":"2018","journal-title":"Head & neck"},{"issue":"48","key":"ppat.1009041.ref047","doi-asserted-by":"crossref","first-page":"20464","DOI":"10.1073\/pnas.0907508106","article-title":"Fusion of epithelial cells by Epstein-Barr virus proteins is triggered by binding of viral glycoproteins gHgL to integrins alphavbeta6 or alphavbeta8","volume":"106","author":"LS Chesnokova","year":"2009","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"7","key":"ppat.1009041.ref048","doi-asserted-by":"crossref","first-page":"e1000496","DOI":"10.1371\/journal.ppat.1000496","article-title":"The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output","volume":"5","author":"V Hadinoto","year":"2009","journal-title":"PLoS pathogens"},{"issue":"1","key":"ppat.1009041.ref049","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1002\/jmv.24918","article-title":"Evaluation of nasal and nasopharyngeal swab collection for the detection of Epstein-Barr virus in nasopharyngeal carcinoma","volume":"90","author":"AE Coghill","year":"2018","journal-title":"Journal of medical virology"},{"issue":"3","key":"ppat.1009041.ref050","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1593\/neo.05625","article-title":"Epstein-Barr virus infection alters cellular signal 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