{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T14:29:02Z","timestamp":1792506542867,"version":"4.5.0"},"reference-count":50,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,2,11]],"date-time":"2021-02-11T00:00:00Z","timestamp":1613001600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31860715"],"award-info":[{"award-number":["31860715"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Guangxi Special Funding on Science and Technology Research","award":["AA17204057"],"award-info":[{"award-number":["AA17204057"]}]},{"name":"Guangxi Natural Science Foundation Grants","award":["2018GXNSFAA281009, 2019GXNSFAA245009"],"award-info":[{"award-number":["2018GXNSFAA281009, 2019GXNSFAA245009"]}]},{"name":"Nanning Scientific Research and Technology Development Project","award":["20182024-1"],"award-info":[{"award-number":["20182024-1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vaccines"],"abstract":"<jats:p>Infectious bronchitis virus (IBV) poses massive economic losses in the global poultry industry. Here, we firstly report the construction and immunogenicity comparison of virus-like particles (VLPs) carrying the S, M and E proteins (SME-VLPs); VLPs carrying the S and M proteins (SM-VLPs); and VLPs carrying the M and E proteins (ME-VLPs) from the dominant serotype representative strain GX-YL5 in China. The neutralizing antibody response induced by the SME-VLPs was similar to that induced by the inactivated oil vaccine (OEV) of GX-YL5, and higher than those induced by the SM-VLPs, ME-VLPs and commercial live vaccine H120. More importantly, the SME-VLPs elicited higher percentages of CD4+ and CD8+ T lymphocytes than the SM-VLPs, ME-VLPs and OEV of GX-YL5. Compared with the OEV of GX-YL5, higher levels of IL-4 and IFN-\u03b3 were also induced by the SME-VLPs. Moreover, the mucosal immune response (sIgA) induced by the SME-VLPs in the tear and oral swabs was comparable to that induced by the H120 vaccine and higher than that induced by the OEV of GX-YL5. In the challenge experiment, the SME-VLPs resulted in significantly lower viral RNA levels in the trachea and higher protection scores than the OEV of GX-YL5 and H120 vaccines, and induced comparable viral RNA levels in the kidneys, and tear and oral swabs to the OEV of GX-YL5. In summary, among the three VLPs, the SME-VLPs carrying the S, M and E proteins of IBV could stimulate the strongest humoral, cellular and mucosal immune responses and provide effective protection, indicating that it would be an attractive vaccine candidate for IB.<\/jats:p>","DOI":"10.3390\/vaccines9020146","type":"journal-article","created":{"date-parts":[[2021,2,12]],"date-time":"2021-02-12T18:46:31Z","timestamp":1613155591000},"page":"146","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Construction and Immunogenicity Comparison of Three Virus-Like Particles Carrying Different Combinations of Structural Proteins of Avian Coronavirus Infectious Bronchitis Virus"],"prefix":"10.3390","volume":"9","author":[{"given":"Yu","family":"Zhang","sequence":"first","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Yuan","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li-Hua","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Zhu","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lan-Ping","family":"Wei","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Sheng","family":"Fan","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chang-Run","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan-Jing","family":"Su","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian-Qi","family":"Liao","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Yong","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian-Chao","family":"Wei","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Wei","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mei-Lan","family":"Mo","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Guangxi University, Nanning 530004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,2,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1051\/vetres:2006055","article-title":"Coronavirus avian infectious bronchitis virus","volume":"38","author":"Cavanagh","year":"2007","journal-title":"Vet. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1080\/03079457.2012.680432","article-title":"The long view: 40 years of infectious bronchitis research","volume":"41","author":"Cook","year":"2012","journal-title":"Avian Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1080\/03079457.2020.1794237","article-title":"Diseases of poultry 14th edition","volume":"49","author":"McMullin","year":"2020","journal-title":"Avian Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/j.vetmic.2012.10.027","article-title":"Characterization of a recombinant coronavirus infectious bronchitis virus with distinct S1 subunits of spike and nucleocapsid genes and a 3\u2019 untranslated region","volume":"162","author":"Liu","year":"2013","journal-title":"Vet. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/j.virol.2016.08.030","article-title":"Polymorphisms in the S1 spike glycoprotein of Arkansas-type infectious bronchitis virus (IBV) show differential binding to host tissues and altered antigenicity","volume":"498","author":"Leyson","year":"2016","journal-title":"Virology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1080\/03079459208418816","article-title":"Location of the amino acid differences in the S1 spike glycoprotein subunit of closely related serotypes of infectious bronchitis virus","volume":"21","author":"Cavanagh","year":"1992","journal-title":"Avian Pathol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4967","DOI":"10.1128\/JVI.74.11.4967-4978.2000","article-title":"Assembly of the coronavirus envelope: Homotypic interactions between the M proteins","volume":"74","author":"Vennema","year":"2000","journal-title":"J. Virol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"9278","DOI":"10.1128\/jvi.71.12.9278-9284.1997","article-title":"Protein interactions during coronavirus assembly","volume":"71","author":"Nguyen","year":"1997","journal-title":"J. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.ppat.1002674","article-title":"A single polar residue and distinct membrane topologies impact the function of the infectious bronchitis coronavirus E protein","volume":"8","author":"Ruch","year":"2012","journal-title":"PLoS Pathog."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/978-0-387-33012-9_29","article-title":"Genetic and molecular biological analysis of protein-protein interactions in coronavirus assembly","volume":"581","author":"Masters","year":"2006","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"9084","DOI":"10.1128\/JVI.77.16.9084-9089.2003","article-title":"Recombinant avian infectious bronchitis virus expressing a heterologous spike gene demonstrates that the spike protein is a determinant of cell tropism","volume":"77","author":"Casais","year":"2003","journal-title":"J. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/0042-6822(87)90145-0","article-title":"Epitopes on the peplomer protein of infectious bronchitis virus strain M41 as defined by monoclonal antibodies","volume":"161","author":"Niesters","year":"1987","journal-title":"Virology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1556\/avet.52.2004.2.4","article-title":"A survey of the prevalence of infectious bronchitis virus type 4\/91 in Iran","volume":"52","author":"Shapouri","year":"2004","journal-title":"Acta Vet. Hung."},{"key":"ref_14","first-page":"293","article-title":"Rapid selection in chickens of subpopulations within ArkDPI-derived infectious bronchitis virus vaccines","volume":"37","author":"Toro","year":"2009","journal-title":"Avian Pathol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1016\/j.vaccine.2008.01.006","article-title":"Avian coronavirus infectious bronchitis attenuated live vaccines undergo selection of subpopulations and mutations following vaccination","volume":"26","author":"McKinley","year":"2008","journal-title":"Vaccine"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1576","DOI":"10.1016\/j.vaccine.2010.12.102","article-title":"Evaluation of recombinant fowlpox virus expressing infectious bronchitis virus S1 gene and chicken interferon-\u03b3 gene for immune protection against heterologous strains","volume":"29","author":"Shi","year":"2011","journal-title":"Vaccine"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.meegid.2015.03.034","article-title":"Serotype shift of a 793\/B genotype infectious bronchitis coronavirus by natural recombination","volume":"32","author":"Zhang","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1007\/s11262-016-1337-7","article-title":"Genome sequence and origin analyses of the recombinant novel IBV virulent isolate SAIBK2","volume":"52","author":"Wu","year":"2016","journal-title":"Virus Genes"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1637\/0005-2086(2002)046[0938:POCALA]2.0.CO;2","article-title":"Protection of chickens after live and inactivated virus vaccination against challenge with nephropathogenic infectious bronchitis virus PA\/Wolgemuth\/98","volume":"46","author":"Ladman","year":"2002","journal-title":"Avian Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1128\/CMR.00005-07","article-title":"Current status of veterinary vaccines","volume":"20","author":"Meeusen","year":"2007","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2015\/424860","article-title":"Progress and challenges toward the development of vaccines against avian infectious bronchitis","volume":"2015","author":"Bande","year":"2015","journal-title":"J. Immunol. Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3007","DOI":"10.3390\/v5123007","article-title":"Molecular characterization of major structural protein genes of avian coronavirus infectious bronchitis virus isolates in southern China","volume":"5","author":"Mo","year":"2013","journal-title":"Viruses"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1007\/s00705-013-1656-0","article-title":"Continuous evolution of avian infectious bronchitis virus resulting in different variants co-circulating in southern China","volume":"158","author":"Li","year":"2013","journal-title":"Arch. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"6576","DOI":"10.1038\/s41598-017-06987-2","article-title":"Epidemiology and characterization of avian infectious bronchitis virus strains circulating in southern China during the period from 2013\u20132015","volume":"7","author":"Feng","year":"2017","journal-title":"Sci. Rep. UK"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1007\/s00705-011-1206-6","article-title":"Serotype and genotype diversity of infectious bronchitis viruses isolated during 1985\u20132008 in Guangxi, China","volume":"157","author":"Li","year":"2012","journal-title":"Arch. Virol."},{"key":"ref_26","first-page":"162","article-title":"Genotypes and serotypes of avian infectious bronchitis viruses isolated during 2009\u20132011 in Guangxi, China","volume":"30","author":"Qin","year":"2014","journal-title":"Bing Du Xue Bao"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Fan, W., Tang, N., Dong, Z., Chen, J., Zhang, W., Zhao, C., He, Y., Li, M., Wang, C., and Wei, T. (2019). Genetic analysis of avian coronavirus infectious bronchitis virus in yellow chickens in southern China over the past decade: Revealing the changes of genetic diversity, dominant genotypes, and selection pressure. Viruses, 11.","DOI":"10.3390\/v11100898"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1292\/jvms.18-0249","article-title":"Immune protection conferred by three commonly used commercial live attenuated vaccines against the prevalent local strains of avian infectious bronchitis virus in southern China","volume":"80","author":"Fan","year":"2018","journal-title":"J. Vet. Med. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"531","DOI":"10.18388\/abp.2014_1875","article-title":"Virus-like particles as vaccine","volume":"61","author":"Chroboczek","year":"2014","journal-title":"Acta Biochim. Pol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.vaccine.2012.10.083","article-title":"Virus-like particles as a highly efficient vaccine platform: Diversity of targets and production systems and advances in clinical development","volume":"31","author":"Kushnir","year":"2012","journal-title":"Vaccine"},{"key":"ref_31","first-page":"287","article-title":"Bacterial carriers and virus-like-particles as antigen delivery devices: Role of dendritic cells in antigen presentation. Current drug targets","volume":"1","author":"Beyer","year":"2001","journal-title":"Infect. Disord."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1586\/erv.12.151","article-title":"Virus-like particles for the prevention of human papillomavirus-associated malignancies","volume":"12","author":"Wang","year":"2014","journal-title":"Expert Rev. Vaccines"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1111\/j.1365-2567.2010.03231.x","article-title":"Effect of mucosal and systemic immunization with virus-like particles of severe acute respiratory syndrome coronavirus in mice","volume":"130","author":"Lu","year":"2010","journal-title":"Immunology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"12686","DOI":"10.18632\/oncotarget.8475","article-title":"MERS-CoV virus-like particles produced in insect cells induce specific humoural and cellular imminity in rhesus macaques","volume":"8","author":"Wang","year":"2017","journal-title":"Oncotarget"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.jbiotec.2019.10.007","article-title":"Preparation of virus-like particle mimetic nanovesicles displaying the S protein of Middle East respiratory syndrome coronavirus using insect cells","volume":"306","author":"Kato","year":"2019","journal-title":"J. Biotechnol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1016\/j.bbrc.2004.04.111","article-title":"Assembly of human severe acute respiratory syndrome coronavirus-like particles","volume":"318","author":"Ho","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"11318","DOI":"10.1128\/JVI.01052-08","article-title":"The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles","volume":"82","author":"Siu","year":"2008","journal-title":"J. Virol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5524","DOI":"10.1016\/j.vaccine.2013.09.024","article-title":"Assembly and immunogenicity of coronavirus-like particles carrying infectious bronchitis virus M and S proteins","volume":"31","author":"Liu","year":"2013","journal-title":"Vaccine"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/s10529-015-1973-3","article-title":"Assembly and immunogenicity of baculovirus-derived infectious bronchitis virus\u2013like particles carrying membrane, envelope and the recombinant spike proteins","volume":"38","author":"Xu","year":"2016","journal-title":"Biotechnol. Lett."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"209","DOI":"10.4142\/jvs.2014.15.2.209","article-title":"Production and immunogenicity of chimeric virus-like particles containing the spike glycoprotein of infectious bronchitis virus","volume":"15","author":"Lv","year":"2014","journal-title":"J. Vet. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Wu, X., Zhai, X., Lai, Y., Zuo, L., Zhang, Y., Mei, X., Xiang, R., Kang, Z., Zhou, L., and Wang, H. (2019). Construction and immunogenicity of novel chimeric virus-like particles bearing antigens of infectious bronchitis virus and newcastle disease virus. Viruses, 11.","DOI":"10.3390\/v11030254"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Yuan, Y., Zhang, Z., He, Y., Fan, W., Dong, Z., Zhang, L., Sun, X., Song, L., Wei, T., and Mo, M. (2018). Protection against virulent infectious bronchitis virus challenge conferred by a recombinant baculovirus co-expressing S1 and N proteins. Viruses, 10.","DOI":"10.20944\/preprints201805.0165.v1"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zhu, W., Wen, Y., Lin, S., Chen, T., and Chen, H. (2020). Anti-influenza protective efficacy of a H6 virus-like particle in chickens. Vaccines, 8.","DOI":"10.3390\/vaccines8030465"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s12250-015-3696-y","article-title":"Responses of the Toll-like receptor and melanoma differentiation-associated protein 5 signaling pathways to avian infectious bronchitis virus infection in chicks","volume":"31","author":"He","year":"2016","journal-title":"Virol. Sin."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1080\/03079459994506","article-title":"Breadth of protection of the respiratory tract provided by different live-attenuated infectious bronchitis vaccines against challenge with infectious bronchitis viruses of heterologous serotypes","volume":"28","author":"Cook","year":"1999","journal-title":"Avian Pathol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1080\/03079457.2014.974504","article-title":"Factors influencing the outcome of infectious bronchitis vaccination and challenge experiments","volume":"43","author":"Cook","year":"2014","journal-title":"Avian Pathol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1126\/science.1217134","article-title":"Attenuated vaccines can recombine to form virulent field viruses","volume":"337","author":"Lee","year":"2012","journal-title":"Science"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6830","DOI":"10.1016\/j.vaccine.2006.06.040","article-title":"Safety and efficacy of an infectious bronchitis virus used for chicken embryo vaccination","volume":"24","author":"Tarpey","year":"2006","journal-title":"Vaccine"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/S0145-305X(99)00072-5","article-title":"Cytotoxic T lymphocytes are critical in the control of infectious bronchitis virus in poultry","volume":"24","author":"Collisson","year":"2000","journal-title":"Dev. Comp. Immunol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1016\/j.vaccine.2013.12.006","article-title":"BacMam virus-based surface display of the infectious bronchitis virus (IBV) S1 glycoprotein confers strong protection against virulent IBV challenge in chickens","volume":"32","author":"Zhang","year":"2014","journal-title":"Vaccine"}],"container-title":["Vaccines"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/2\/146\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:22:55Z","timestamp":1760160175000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-393X\/9\/2\/146"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,11]]},"references-count":50,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["vaccines9020146"],"URL":"https:\/\/doi.org\/10.3390\/vaccines9020146","relation":{},"ISSN":["2076-393X"],"issn-type":[{"value":"2076-393X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,11]]}}}