{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,16]],"date-time":"2026-07-16T19:40:36Z","timestamp":1784230836612,"version":"3.55.0"},"reference-count":57,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2025,9,1]],"date-time":"2025-09-01T00:00:00Z","timestamp":1756684800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,9,1]],"date-time":"2025-09-01T00:00:00Z","timestamp":1756684800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,7,3]],"date-time":"2025-07-03T00:00:00Z","timestamp":1751500800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001826","name":"ZonMw","doi-asserted-by":"publisher","award":["10430072110008"],"award-info":[{"award-number":["10430072110008"]}],"id":[{"id":"10.13039\/501100001826","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000780","name":"European Commission","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000780","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003298","name":"Netherlands Institute for Health Services Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003298","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100016302","name":"Coalition for Epidemic Preparedness Innovations","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100016302","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010663","name":"European Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010663","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Current Opinion in Virology"],"published-print":{"date-parts":[[2025,9]]},"DOI":"10.1016\/j.coviro.2025.101476","type":"journal-article","created":{"date-parts":[[2025,7,22]],"date-time":"2025-07-22T17:58:11Z","timestamp":1753207091000},"page":"101476","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":7,"special_numbering":"C","title":["Human organoid models to study coronavirus infections of the respiratory tract"],"prefix":"10.1016","volume":"72","author":[{"given":"Merel R","family":"te Marvelde","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura LA","family":"van Dijk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark A","family":"Power","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie","family":"Rissmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rory D","family":"de Vries","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6221-2015","authenticated-orcid":false,"given":"Bart L","family":"Haagmans","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.coviro.2025.101476_bib1","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.virusres.2006.01.017","article-title":"Nidovirales: evolving the largest RNA virus genome","volume":"117","author":"Gorbalenya","year":"2006","journal-title":"Virus Res"},{"key":"10.1016\/j.coviro.2025.101476_bib2","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1016\/j.tim.2016.03.003","article-title":"Epidemiology, genetic recombination, and pathogenesis of coronaviruses","volume":"24","author":"Su","year":"2016","journal-title":"Trends Microbiol"},{"key":"10.1016\/j.coviro.2025.101476_bib3","doi-asserted-by":"crossref","first-page":"1967","DOI":"10.1056\/NEJMoa030747","article-title":"Identification of a novel coronavirus in patients with severe acute respiratory syndrome","volume":"348","author":"Drosten","year":"2003","journal-title":"N Engl J Med"},{"key":"10.1016\/j.coviro.2025.101476_bib4","doi-asserted-by":"crossref","first-page":"1814","DOI":"10.1056\/NEJMoa1211721","article-title":"Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia","volume":"367","author":"Zaki","year":"2012","journal-title":"N Engl J Med"},{"key":"10.1016\/j.coviro.2025.101476_bib5","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1056\/NEJMoa2001017","article-title":"A novel coronavirus from patients with pneumonia in China, 2019","volume":"382","author":"Zhu","year":"2020","journal-title":"N Engl J Med"},{"key":"10.1016\/j.coviro.2025.101476_bib6","doi-asserted-by":"crossref","DOI":"10.3390\/microorganisms11020445","article-title":"Evaluating the virology and evolution of seasonal human coronaviruses associated with the common cold in the COVID-19\u00a0era","volume":"11","author":"Harrison","year":"2023","journal-title":"Microorganisms"},{"key":"10.1016\/j.coviro.2025.101476_bib7","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/s41579-022-00713-0","article-title":"SARS-CoV-2 pathogenesis","volume":"20","author":"Lamers","year":"2022","journal-title":"Nat Rev Microbiol"},{"key":"10.1016\/j.coviro.2025.101476_bib8","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.66815","article-title":"Human airway cells prevent SARS-CoV-2 multibasic cleavage site cell culture adaptation","volume":"10","author":"Lamers","year":"2021","journal-title":"Elife"},{"key":"10.1016\/j.coviro.2025.101476_bib9","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1038\/s41586-020-2787-6","article-title":"Animal models for COVID-19","volume":"586","author":"Mu\u00f1oz-Fontela","year":"2020","journal-title":"Nature"},{"key":"10.1016\/j.coviro.2025.101476_bib10","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1091\/mbc.E19-03-0135","article-title":"Human organoids: a new dimension in cell biology","volume":"30","author":"Lehmann","year":"2019","journal-title":"Mol Biol Cell"},{"key":"10.1016\/j.coviro.2025.101476_bib11","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 cultures","volume":"146","author":"Ruiz Garc\u00eda","year":"2019","journal-title":"Development"},{"key":"10.1016\/j.coviro.2025.101476_bib12","doi-asserted-by":"crossref","DOI":"10.1016\/j.ejcb.2022.151231","article-title":"Cell function and identity revealed by comparative scRNA-seq analysis in human nasal, bronchial and epididymis epithelia","volume":"101","author":"Paranjapye","year":"2022","journal-title":"Eur J Cell Biol"},{"key":"10.1016\/j.coviro.2025.101476_bib13","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1007\/s004289900177","article-title":"Evidence of M cells as portals of entry for antigens in the nasopharyngeal lymphoid tissue of humans","volume":"436","author":"Fujimura","year":"2000","journal-title":"Virchows Arch"},{"key":"10.1016\/j.coviro.2025.101476_bib14","doi-asserted-by":"crossref","first-page":"1636","DOI":"10.1164\/rccm.201911-2199OC","article-title":"A single-cell atlas of the human healthy airways","volume":"202","author":"Deprez","year":"2020","journal-title":"Am J Respir Crit Care Med"},{"key":"10.1016\/j.coviro.2025.101476_bib15","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1242\/dmm.006031","article-title":"Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling","volume":"3","author":"Rock","year":"2010","journal-title":"Dis Model Mech"},{"key":"10.1016\/j.coviro.2025.101476_bib16","first-page":"332","article-title":"Cell number and cell characteristics of the normal human lung","volume":"126","author":"Crapo","year":"1982","journal-title":"Am Rev Respir Dis"},{"key":"10.1016\/j.coviro.2025.101476_bib17","doi-asserted-by":"crossref","DOI":"10.1242\/dmm.046920","article-title":"Pulmonary neuroendocrine cells: physiology, tissue homeostasis and disease","volume":"13","author":"Noguchi","year":"2020","journal-title":"Dis Model Mech"},{"key":"10.1016\/j.coviro.2025.101476_bib18","doi-asserted-by":"crossref","DOI":"10.3390\/ijms22147667","article-title":"The use of stem cell-derived organoids in disease modeling: an update","volume":"22","author":"Azar","year":"2021","journal-title":"Int J Mol Sci"},{"key":"10.1016\/j.coviro.2025.101476_bib19","doi-asserted-by":"crossref","DOI":"10.15252\/embj.2018100300","article-title":"Long-term expanding human airway organoids for disease modeling","volume":"38","author":"Sachs","year":"2019","journal-title":"EMBO J"},{"key":"10.1016\/j.coviro.2025.101476_bib20","doi-asserted-by":"crossref","DOI":"10.3390\/biomedicines11113034","article-title":"Alveolar type 2 epithelial cell organoids: focus on culture methods","volume":"11","author":"Jain","year":"2023","journal-title":"Biomedicines"},{"key":"10.1016\/j.coviro.2025.101476_bib21","doi-asserted-by":"crossref","DOI":"10.3390\/biom14010115","article-title":"Alveolar organoids in lung disease modeling","volume":"14","author":"Purev","year":"2024","journal-title":"Biomolecules"},{"key":"10.1016\/j.coviro.2025.101476_bib22","doi-asserted-by":"crossref","first-page":"3025","DOI":"10.1172\/JCI68782","article-title":"Type 2 alveolar cells are stem cells in adult lung","volume":"123","author":"Barkauskas","year":"2013","journal-title":"J Clin Invest"},{"key":"10.1016\/j.coviro.2025.101476_bib23","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1016\/j.stem.2020.10.005","article-title":"Human lung stem cell-based alveolospheres provide insights into SARS-CoV-2-mediated interferon responses and pneumocyte dysfunction","volume":"27","author":"Katsura","year":"2020","journal-title":"Cell Stem Cell"},{"key":"10.1016\/j.coviro.2025.101476_bib24","series-title":"Methods in Cell Biology","first-page":"115","article-title":"Chapter 6 - A method of generating alveolar organoids using human pluripotent stem cells","author":"Yamamoto","year":"2020"},{"key":"10.1016\/j.coviro.2025.101476_bib25","doi-asserted-by":"crossref","DOI":"10.15252\/embj.2020105912","article-title":"An organoid-derived bronchioalveolar model for SARS-CoV-2 infection of human alveolar type II-like cells","volume":"40","author":"Lamers","year":"2021","journal-title":"Embo J"},{"key":"10.1016\/j.coviro.2025.101476_bib26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/stmcls\/sxac074","article-title":"iPSC-derived airway epithelial cells: progress, promise, and challenges","volume":"41","author":"Yu","year":"2022","journal-title":"Stem Cells"},{"key":"10.1016\/j.coviro.2025.101476_bib27","doi-asserted-by":"crossref","DOI":"10.1186\/s13287-021-02172-5","article-title":"Lung organoids, useful tools for investigating epithelial repair after lung injury","volume":"12","author":"Kong","year":"2021","journal-title":"Stem Cell Res Ther"},{"key":"10.1016\/j.coviro.2025.101476_sbref28","doi-asserted-by":"crossref","DOI":"10.1016\/j.crtox.2024.100197","article-title":"iPSC-derived and patient-derived organoids: applications and challenges in scalability and reproducibility as pre-clinical models","volume":"7","author":"Heinzelmann","year":"2024","journal-title":"Curr Res Toxicol"},{"key":"10.1016\/j.coviro.2025.101476_bib29","doi-asserted-by":"crossref","first-page":"6081","DOI":"10.1128\/JVI.03368-12","article-title":"Isolation and characterization of current human coronavirus strains in primary human epithelial cell cultures reveal differences in target cell tropism","volume":"87","author":"Dijkman","year":"2013","journal-title":"J Virol"},{"key":"10.1016\/j.coviro.2025.101476_bib30","doi-asserted-by":"crossref","first-page":"285","DOI":"10.7883\/yoken.JJID.2020.776","article-title":"Isolation of human coronaviruses OC43, HKU1, NL63, and 229E in Yamagata, Japan, using primary human airway epithelium cells cultured by employing an air-liquid interface culture","volume":"74","author":"Komabayashi","year":"2021","journal-title":"Jpn J Infect Dis"},{"key":"10.1016\/j.coviro.2025.101476_bib31","doi-asserted-by":"crossref","first-page":"11255","DOI":"10.1128\/JVI.00947-10","article-title":"Culturing the unculturable: human coronavirus HKU1 infects, replicates, and produces progeny virions in human ciliated airway epithelial cell cultures","volume":"84","author":"Pyrc","year":"2010","journal-title":"J Virol"},{"key":"10.1016\/j.coviro.2025.101476_sbref32","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.cell.2022.11.030","article-title":"SARS-CoV-2 replication in airway epithelia requires motile cilia and microvillar reprogramming","volume":"186","author":"Wu","year":"2023","journal-title":"Cell"},{"key":"10.1016\/j.coviro.2025.101476_bib33","doi-asserted-by":"crossref","DOI":"10.1080\/22221751.2024.2327368","article-title":"Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses","volume":"13","author":"Gong","year":"2024","journal-title":"Emerg Microbes Infect"},{"key":"10.1016\/j.coviro.2025.101476_bib34","doi-asserted-by":"crossref","DOI":"10.1002\/jmv.29600","article-title":"Differential beta-coronavirus infection dynamics in human bronchial epithelial organoids","volume":"96","author":"Park","year":"2024","journal-title":"J Med Virol"},{"key":"10.1016\/j.coviro.2025.101476_bib35","article-title":"Resistance to SARS-CoV-2 infection in camelid nasal organoids is associated with lack of ACE2 expression","volume":"2","author":"Breugem","year":"2024","journal-title":"npj Virus"},{"key":"10.1016\/j.coviro.2025.101476_bib36","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1011571","article-title":"Glycosylated extracellular mucin domains protect against SARS-CoV-2 infection at the respiratory surface","volume":"19","author":"Chatterjee","year":"2023","journal-title":"PLoS Pathog"},{"key":"10.1016\/j.coviro.2025.101476_sbref37","article-title":"Human airway and nasal organoids reveal escalating replicative fitness of SARS-CoV-2 emerging variants","volume":"120","author":"Li","year":"2023","journal-title":"Proc Natl Acad Sci USA"},{"key":"10.1016\/j.coviro.2025.101476_bib38","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.stemcr.2023.01.011","article-title":"SARS-CoV-2 infection of airway organoids reveals conserved use of tetraspanin-8 by Ancestral, Delta, and Omicron variants","volume":"18","author":"Hysenaj","year":"2023","journal-title":"Stem Cell Rep"},{"key":"10.1016\/j.coviro.2025.101476_bib39","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/s41586-020-2901-9","article-title":"Identification of SARS-CoV-2 inhibitors using lung and colonic organoids","volume":"589","author":"Han","year":"2021","journal-title":"Nature"},{"key":"10.1016\/j.coviro.2025.101476_sbref40","doi-asserted-by":"crossref","DOI":"10.1002\/jmv.29579","article-title":"The use of human iPSC-derived alveolar organoids to explore SARS-CoV-2 variant infections and host responses","volume":"96","author":"Gandikota","year":"2024","journal-title":"J Med Virol"},{"key":"10.1016\/j.coviro.2025.101476_bib41","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-022-11700-z","article-title":"Apical-out airway organoids as a platform for studying viral infections and screening for antiviral drugs","volume":"12","author":"Stroulios","year":"2022","journal-title":"Sci Rep"},{"key":"10.1016\/j.coviro.2025.101476_bib42","doi-asserted-by":"crossref","DOI":"10.3390\/v15051166","article-title":"Apical-out human airway organoids modeling SARS-CoV-2 infection","volume":"15","author":"Chiu","year":"2023","journal-title":"Viruses"},{"key":"10.1016\/j.coviro.2025.101476_bib43","doi-asserted-by":"crossref","DOI":"10.1007\/s00018-024-05307-y","article-title":"Virus neutralization assays for human respiratory syncytial virus using airway organoids","volume":"81","author":"van Dijk","year":"2024","journal-title":"Cell Mol Life Sci"},{"key":"10.1016\/j.coviro.2025.101476_bib44","article-title":"Small molecule-directed differentiation of submerged-cultured human nasal airway epithelia for respiratory disease modelling","author":"Dreyer","year":"2024","journal-title":"Prepr bioRxiv"},{"key":"10.1016\/j.coviro.2025.101476_bib45","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1165\/rcmb.2013-0237OC","article-title":"Submersion and hypoxia inhibit ciliated cell differentiation in a notch-dependent manner","volume":"51","author":"Gerovac","year":"2014","journal-title":"Am J Respir Cell Mol Biol"},{"key":"10.1016\/j.coviro.2025.101476_bib46","doi-asserted-by":"crossref","DOI":"10.26508\/lsa.202201837","article-title":"The pro-inflammatory response to influenza A virus infection is fueled by endothelial cells","volume":"6","author":"Bauer","year":"2023","journal-title":"Life Sci Alliance"},{"key":"10.1016\/j.coviro.2025.101476_sbref47","doi-asserted-by":"crossref","DOI":"10.3389\/fbioe.2023.1212230","article-title":"Blood myeloid cells differentiate to lung resident cells and respond to pathogen stimuli in a 3D human tissue-engineered lung model","volume":"11","author":"Roe","year":"2023","journal-title":"Front Bioeng Biotechnol"},{"key":"10.1016\/j.coviro.2025.101476_bib48","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-017-08567-w","article-title":"Development of a primary human co-culture model of inflamed airway mucosa","volume":"7","author":"Yonker","year":"2017","journal-title":"Sci Rep"},{"key":"10.1016\/j.coviro.2025.101476_bib49","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2018.02514","article-title":"A co-culture model of PBMC and stem cell derived human nasal epithelium reveals rapid activation of NK and innate T cells upon influenza A virus infection of the nasal epithelium","volume":"9","author":"Luukkainen","year":"2018","journal-title":"Front Immunol"},{"key":"10.1016\/j.coviro.2025.101476_bib50","first-page":"369","article-title":"Give them vasculature and immune cells: how to fill the gap of organoids","volume":"212","author":"Yip","year":"2023","journal-title":"Cells Tissues Organs"},{"key":"10.1016\/j.coviro.2025.101476_bib51","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1128\/JVI.06348-11","article-title":"Human pulmonary microvascular endothelial cells support productive replication of highly pathogenic avian influenza viruses: possible involvement in the pathogenesis of human H5N1 virus infection","volume":"86","author":"Zeng","year":"2012","journal-title":"J Virol"},{"key":"10.1016\/j.coviro.2025.101476_bib52","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1038\/s41551-021-00718-9","article-title":"A human-airway-on-a-chip for the rapid identification of candidate antiviral therapeutics and prophylactics","volume":"5","author":"Si","year":"2021","journal-title":"Nat Biomed Eng"},{"key":"10.1016\/j.coviro.2025.101476_bib53","article-title":"Organoid modeling of lung-resident immune responses to SARS-CoV-2 infection","author":"Choi","year":"2023","journal-title":"Res Sq"},{"key":"10.1016\/j.coviro.2025.101476_sbref54","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/s41586-024-07791-5","article-title":"Human organoids with an autologous tissue-resident immune compartment","volume":"633","author":"Recaldin","year":"2024","journal-title":"Nature"},{"key":"10.1016\/j.coviro.2025.101476_bib55","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.67886","article-title":"A functional genetic toolbox for human tissue-derived organoids","volume":"10","author":"Sun","year":"2021","journal-title":"eLife"},{"key":"10.1016\/j.coviro.2025.101476_bib56","article-title":"Human apical-out nasal organoids reveal an essential role of matrix metalloproteinases in airway epithelial differentiation","volume":"15","author":"Li","year":"2024","journal-title":"Nat Commun"},{"key":"10.1016\/j.coviro.2025.101476_bib57","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-024-53791-4","article-title":"Live imaging of airway epithelium reveals that mucociliary clearance modulates SARS-CoV-2 spread","volume":"15","author":"Becker","year":"2024","journal-title":"Nat Commun"}],"container-title":["Current Opinion in Virology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1879625725000264?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1879625725000264?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,11,8]],"date-time":"2025-11-08T00:23:49Z","timestamp":1762561429000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1879625725000264"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,9]]},"references-count":57,"alternative-id":["S1879625725000264"],"URL":"https:\/\/doi.org\/10.1016\/j.coviro.2025.101476","relation":{},"ISSN":["1879-6257"],"issn-type":[{"value":"1879-6257","type":"print"}],"subject":[],"published":{"date-parts":[[2025,9]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Human organoid models to study coronavirus infections of the respiratory tract","name":"articletitle","label":"Article Title"},{"value":"Current Opinion in Virology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.coviro.2025.101476","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 The Author(s). Published by Elsevier B.V.","name":"copyright","label":"Copyright"}],"article-number":"101476"}}