{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T15:54:08Z","timestamp":1780070048379,"version":"3.54.0"},"reference-count":54,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T00:00:00Z","timestamp":1611187200000},"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","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>Infectious bronchitis is a highly contagious, acute viral respiratory disease of chickens, regardless of the strain, and its infection may lead to considerable economic losses to the poultry industry. New nephropathogenic infectious bronchitis virus (NIBV) strains have increasingly emerged in recent years; hence, evaluating their infection-influenced immune function changes and the alteration of metabolite profiling is important. Initially, chickens were randomly distributed into two groups: the control group (Con) and the disease group (Dis). Here, the partial cytokines were examined, and the metabolome alterations of the bursa of Fabricius (BF) in NIBV infections in chickens were profiled by gas chromatography time-of-flight\/mass spectrometry (GC-TOF\/MS). The results revealed that the NIBV infection promotes the mRNA expression of inflammatory cytokines. Metabolic profile analysis indicated that clustering differed between the two groups and there were 75 significantly different metabolites detected between the two groups, suggesting that the host metabolism was significantly changed by NIBV infection. Notably, the following 12 metabolites were identified as the potential biomarkers: 3-phenyllactic acid, 2-deoxytetronic acid, aminomalonic acid, malonamide 5, uric acid, arachidonic acid, 2-methylglutaric acid, linoleic acid, ethanolamine, stearic acid, N-alpha-acetyl-<jats:sc>l<\/jats:sc>-ornithine, and O-acetylserine. Furthermore, the results of the correlation analysis showed that a strong correlation existed between metabolic biomarkers and inflammatory cytokines. Our results describe an immune and metabolic profile for the BF of chickens when infected with NIBV and provide new biomarkers of NIBV infection as potential targets and indicators of indicating therapeutic efficacy.<\/jats:p>","DOI":"10.3389\/fvets.2020.628270","type":"journal-article","created":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T05:44:16Z","timestamp":1611207856000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Nephropathogenic Infectious Bronchitis Virus Infection Altered the Metabolome Profile and Immune Function of the Bursa of Fabricius in Chicken"],"prefix":"10.3389","volume":"7","author":[{"given":"Jun","family":"Kuang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Puzhi","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Shi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yitian","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shupeng","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Changming","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guyue","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Zhuang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruiming","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guoliang","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoquan","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,1,21]]},"reference":[{"key":"B1","first-page":"161","article-title":"Role of a locally prepared bivalent inactivated infectious bronchitis virus (ibv) vaccine within vaccination program to control infectious bronchitis disease in layer chickens","volume":"8","author":"Salman","year":"2019","journal-title":"Int J Vet Sci."},{"key":"B2","first-page":"50","article-title":"Improved bivalent live and inactivated clone 30 and Infectious bronchitis virus vaccine","volume":"9","author":"Abd","year":"2020","journal-title":"Int J Vet Sci."},{"key":"B3","doi-asserted-by":"publisher","first-page":"470","DOI":"10.37422\/IJVS\/20.042","article-title":"Efficacy of live vaccines and specific prevention in chicken infectious bronchitis","volume":"9","author":"Javadov","year":"2020","journal-title":"Int J Vet Sci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.meegid.2010.09.002","article-title":"A 15-year analysis of molecular epidemiology of avian infectious bronchitis coronavirus in China","volume":"11","author":"Han","year":"2011","journal-title":"Infect Genet Evol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"4488","DOI":"10.3390\/v7082827","article-title":"Genetic characterization of the belgian nephropathogenic infectious bronchitis virus (NIBV) reference strain B1648","volume":"7","author":"Reddy","year":"2015","journal-title":"Viruses."},{"key":"B6","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1637\/7107","article-title":"Identification of a novel nephropathogenic infectious bronchitis virus in Israel","volume":"48","author":"Meir","year":"2004","journal-title":"Avian Dis."},{"key":"B7","doi-asserted-by":"publisher","first-page":"916","DOI":"10.1128\/JCM.43.2.916-918.2005","article-title":"Emergence of a nephropathogenic avian infectious bronchitis virus with a novel genotype in India","volume":"43","author":"Bayry","year":"2005","journal-title":"J Clin Microbiol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.vetmic.2010.12.015","article-title":"Isolation and molecular characterization of Sul\/01\/09 avian infectious bronchitis virus, indicates the emergence of a new genotype in the Middle East","volume":"150","author":"Mahmood","year":"2011","journal-title":"Vet Microbiol."},{"key":"B9","doi-asserted-by":"publisher","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":"B10","doi-asserted-by":"publisher","first-page":"3798","DOI":"10.1074\/jbc.M111.273854","article-title":"Identification and characterization of novel immunomodulatory bursal-derived pentapeptide-II (BPP-II)","volume":"287","author":"Feng","year":"2012","journal-title":"J Biol Chem."},{"key":"B11","doi-asserted-by":"publisher","first-page":"225","DOI":"10.3389\/fvets.2020.00225","article-title":"Mycoplasma gallisepticum infection impaired the structural integrity and immune function of bursa of fabricius in chicken: implication of oxidative stress and apoptosis","volume":"7","author":"Zhang","year":"2020","journal-title":"Front Vet Sci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1186\/s12864-018-5333-2","article-title":"Transcriptome profile in bursa of Fabricius reveals potential mode for stress-influenced immune function in chicken stress model","volume":"19","author":"Zhang","year":"2018","journal-title":"BMC Genomics."},{"key":"B13","doi-asserted-by":"publisher","first-page":"7137","DOI":"10.4049\/jimmunol.179.10.7137","article-title":"Extracellular branched-chain amino acids, especially valine, regulate maturation and function of monocyte-derived dendritic cells","volume":"179","author":"Kakazu","year":"2007","journal-title":"J Immunol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1016\/j.virol.2007.09.013","article-title":"Host responses are induced in feathers of chickens infected with Marek's disease virus","volume":"370","author":"Abdul-Careem","year":"2008","journal-title":"Virology."},{"key":"B15","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1017\/S1466252317000044","article-title":"Global distributions and strain diversity of avian infectious bronchitis virus: a review","volume":"18","author":"Bande","year":"2017","journal-title":"Anim Health Res Rev."},{"key":"B16","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.vetmic.2017.11.027","article-title":"Pathogenicity differences between QX-like and Mass-type infectious bronchitis viruses","volume":"213","author":"Cheng","year":"2018","journal-title":"Vet Microbiol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1186\/1743-422X-7-364","article-title":"Comparison of the expression of cytokine genes in the bursal tissues of the chickens following challenge with infectious bursal disease viruses of varying virulence","volume":"7","author":"Liu","year":"2010","journal-title":"Virol J."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1492","DOI":"10.3390\/ani10091492","article-title":"Effects of intermittent mild cold stimulation on mRNA expression of immunoglobulins, cytokines, and toll-like receptors in the small intestine of broilers","volume":"10","author":"Li","year":"2020","journal-title":"Animals (Basel)."},{"key":"B19","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.3390\/ani10091535","article-title":"Baicalin-copper complex modulates gut microbiota, inflammatory responses, and hormone secretion in DON-challenged piglets","volume":"10","author":"Zha","year":"2020","journal-title":"Animals (Basel)."},{"key":"B20","doi-asserted-by":"publisher","first-page":"8884","DOI":"10.1128\/jvi.74.19.8884-8892.2000","article-title":"Characteristics of bursal T lymphocytes induced by infectious bursal disease virus","volume":"74","author":"Kim","year":"2000","journal-title":"J Virol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.virusres.2005.04.014","article-title":"Infection and activation of bursal macrophages by virulent infectious bursal disease virus","volume":"113","author":"Khatri","year":"2005","journal-title":"Virus Res."},{"key":"B22","doi-asserted-by":"publisher","first-page":"451","DOI":"10.29261\/pakvetj\/2019.023","article-title":"Protective effect of probiotics in combination with vaccination on antibody response, biochemical and hematological indices in broilers","volume":"39","author":"Sarwar","year":"2019","journal-title":"Pak Vet J."},{"key":"B23","doi-asserted-by":"publisher","first-page":"E2320","DOI":"10.1073\/pnas.1720833115","article-title":"Role of glutathione metabolism in host defense against Borrelia burgdorferi infection","volume":"115","author":"Kerstholt","year":"2018","journal-title":"Proc Natl Acad Sci USA."},{"key":"B24","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1038\/nature08097","article-title":"Enhancing CD8 T-cell memory by modulating fatty acid metabolism","volume":"460","author":"Pearce","year":"2009","journal-title":"Nature."},{"key":"B25","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/nature10280","article-title":"Oxysterols direct immune cell migration via EBI2","volume":"475","author":"Hannedouche","year":"2011","journal-title":"Nature."},{"key":"B26","doi-asserted-by":"publisher","first-page":"4716","DOI":"10.1002\/pmic.200600106","article-title":"Metabolomics: current technologies and future trends","volume":"6","author":"Hollywood","year":"2006","journal-title":"Proteomics."},{"key":"B27","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1016\/j.trsl.2011.12.009","article-title":"Translational research in infectious disease: current paradigms and challenges ahead","volume":"159","author":"Fontana","year":"2012","journal-title":"Transl Res."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1016\/j.jprot.2011.10.027","article-title":"Recent and potential developments of biofluid analyses in metabolomics","volume":"75","author":"Zhang","year":"2012","journal-title":"J Proteomics."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1070","DOI":"10.3390\/v11111070","article-title":"A multi-omics study of chicken infected by nephropathogenic infectious bronchitis virus","volume":"11","author":"Xu","year":"2019","journal-title":"Viruses."},{"key":"B30","doi-asserted-by":"publisher","first-page":"423","DOI":"10.4142\/jvs.2015.16.4.423","article-title":"Elevated level of renal xanthine oxidase mRNA transcription after nephropathogenic infectious bronchitis virus infection in growing layers","volume":"16","author":"Lin","year":"2015","journal-title":"J Vet Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"944","DOI":"10.3389\/fphys.2018.00944","article-title":"Metabolomics responses of pearl oysters (Pinctada fucata martensii) fed a formulated diet indoors and cultured with natural diet outdoors","volume":"9","author":"Yang","year":"2018","journal-title":"Front Physiol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1002\/path.2417","article-title":"Distinctly different expression of cytokines and chemokines in the lungs of two H5N1 avian influenza patients","volume":"216","author":"Deng","year":"2008","journal-title":"J Pathol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1080\/03079450601028811","article-title":"Epidemiological and experimental evidence for immunodeficiency affecting avian infectious bronchitis","volume":"35","author":"Toro","year":"2006","journal-title":"Avian Pathol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1653","DOI":"10.3389\/fmicb.2016.01653","article-title":"Pathogenicity of a TW-like strain of infectious bronchitis virus and evaluation of the protection induced against it by a QX-like strain","volume":"7","author":"Yan","year":"2016","journal-title":"Front Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.abb.2003.12.008","article-title":"Redox events in interleukin-1 signaling","volume":"423","author":"Brigelius-Flohe","year":"2004","journal-title":"Arch Biochem Biophys."},{"key":"B36","doi-asserted-by":"publisher","first-page":"967","DOI":"10.1007\/s12192-015-0625-9","article-title":"Selenoproteins and heat shock proteins play important roles in immunosuppression in the bursa of Fabricius of chickens with selenium deficiency","volume":"20","author":"Khoso","year":"2015","journal-title":"Cell Stress Chaperones."},{"key":"B37","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/j.micpath.2017.08.023","article-title":"Astragalus polysaccharides enhance the immune response to avian infectious bronchitis virus vaccination in chickens","volume":"111","author":"Zhang","year":"2017","journal-title":"Microb Pathog."},{"key":"B38","doi-asserted-by":"publisher","first-page":"635","DOI":"10.3390\/v10110635","article-title":"The in ovo delivery of CpG oligonucleotides protects against infectious bronchitis with the recruitment of immune cells into the respiratory tract of chickens","volume":"10","author":"De Silva Senapathi","year":"2018","journal-title":"Viruses."},{"key":"B39","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1038\/nature05495","article-title":"Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus","volume":"445","author":"Kobasa","year":"2007","journal-title":"Nature."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.3201\/eid1707.101306","article-title":"Hantavirus pulmonary syndrome, United States, 1993-2009","volume":"17","author":"MacNeil","year":"2011","journal-title":"Emerg Infect Dis."},{"key":"B41","doi-asserted-by":"publisher","first-page":"24","DOI":"10.47278\/journal.abr\/2020.010","article-title":"Explore the potential STAT3 gene in broilers with ascites syndrome by bioinformatics analysis","volume":"2","author":"Li","year":"2020","journal-title":"Agrobiol Rec."},{"key":"B42","doi-asserted-by":"publisher","first-page":"e1002866","DOI":"10.1371\/journal.ppat.1002866","article-title":"Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection","volume":"8","author":"Delgado","year":"2012","journal-title":"PLoS Pathog."},{"key":"B43","doi-asserted-by":"publisher","first-page":"8873","DOI":"10.1038\/ncomms9873","article-title":"MYC-induced reprogramming of glutamine catabolism supports optimal virus replication","volume":"6","author":"Thai","year":"2015","journal-title":"Nat Commun."},{"key":"B44","doi-asserted-by":"publisher","first-page":"e64298","DOI":"10.1371\/journal.pone.0064298","article-title":"Nuclear magnetic resonance based profiling of biofluids reveals metabolic dysregulation in HIV-infected persons and those on anti-retroviral therapy","volume":"8","author":"Munshi","year":"2013","journal-title":"PLoS ONE."},{"key":"B45","doi-asserted-by":"publisher","first-page":"e0004449","DOI":"10.1371\/journal.pntd.0004449","article-title":"Metabolomics-based discovery of small molecule biomarkers in serum associated with dengue virus infections and disease outcomes","volume":"10","author":"Voge","year":"2016","journal-title":"PLoS Negl Trop Dis."},{"key":"B46","doi-asserted-by":"publisher","first-page":"a004820","DOI":"10.1101\/cshperspect.a004820","article-title":"Role of lipids in virus replication","volume":"3","author":"Lorizate","year":"2011","journal-title":"Cold Spring Harb Perspect Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1016\/j.tim.2011.03.007","article-title":"Multifaceted roles for lipids in viral infection","volume":"19","author":"Heaton","year":"2011","journal-title":"Trends Microbiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1074\/mcp.M112.019141","article-title":"Metabolomic analysis of key regulatory metabolites in hepatitis C virus-infected tree shrews","volume":"12","author":"Sun","year":"2013","journal-title":"Mol Cell Proteomics."},{"key":"B49","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1002\/bmc.3055","article-title":"Modified Jiu Wei Qiang Huo decoction improves dysfunctional metabolomics in influenza A pneumonia-infected mice","volume":"28","author":"Chen","year":"2014","journal-title":"Biomed Chromatogr."},{"key":"B50","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1186\/s12944-017-0437-2","article-title":"Serum lipid profile as a marker of liver impairment in hepatitis B Cirrhosis patients","volume":"16","author":"Arain","year":"2017","journal-title":"Lipids Health Dis."},{"key":"B51","doi-asserted-by":"publisher","first-page":"e1002124","DOI":"10.1371\/journal.ppat.1002124","article-title":"Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism","volume":"7","author":"Vastag","year":"2011","journal-title":"PLoS Pathog."},{"key":"B52","doi-asserted-by":"publisher","first-page":"40732","DOI":"10.1074\/jbc.M112.399899","article-title":"Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver","volume":"287","author":"Lanaspa","year":"2012","journal-title":"J Biol Chem."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1038\/labinvest.2014.98","article-title":"Uric acid induces fat accumulation via generation of endoplasmic reticulum stress and SREBP-1c activation in hepatocytes","volume":"94","author":"Choi","year":"2014","journal-title":"Lab Invest."},{"key":"B54","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1084\/jem.20151570","article-title":"Immunometabolism governs dendritic cell and macrophage function","volume":"213","author":"O'Neill","year":"2016","journal-title":"J Exp Med."}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2020.628270\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,21]],"date-time":"2021-01-21T05:44:20Z","timestamp":1611207860000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2020.628270\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,21]]},"references-count":54,"alternative-id":["10.3389\/fvets.2020.628270"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2020.628270","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,21]]},"article-number":"628270"}}