{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T20:00:25Z","timestamp":1787169625161,"version":"build-2736575974"},"reference-count":108,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,2,2]],"date-time":"2024-02-02T00:00:00Z","timestamp":1706832000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1755197, 1950307, 1754872"],"award-info":[{"award-number":["1755197, 1950307, 1754872"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007543","name":"Grantov\u00e1 Agentura, Univerzita Karlova","doi-asserted-by":"publisher","award":["646119"],"award-info":[{"award-number":["646119"]}],"id":[{"id":"10.13039\/100007543","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007397","name":"Univerzita Karlova v Praze","doi-asserted-by":"publisher","award":["START\/SCI\/113 with reg. no. CZ.02.2.69\/0.0\/0.0\/19_073\/0016935"],"award-info":[{"award-number":["START\/SCI\/113 with reg. no. CZ.02.2.69\/0.0\/0.0\/19_073\/0016935"]}],"id":[{"id":"10.13039\/100007397","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001823","name":"Ministerstvo \u0160kolstv\u00ed, Ml\u00e1de\u017ee a T\u011blov\u00fdchovy","doi-asserted-by":"publisher","award":["e-INFRA CZ LM2018140 , 260684\/2023, INTER-ACTION grant no. LUAUS24184"],"award-info":[{"award-number":["e-INFRA CZ LM2018140 , 260684\/2023, INTER-ACTION grant no. LUAUS24184"]}],"id":[{"id":"10.13039\/501100001823","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:p>\n                    Pathogen adaptations during host-pathogen co-evolution can cause the host balance between immunity and immunopathology to rapidly shift. However, little is known in natural disease systems about the immunological pathways optimised through the trade-off between immunity and self-damage. The evolutionary interaction between the conjunctival bacterial infection\n                    <jats:italic>Mycoplasma gallisepticum<\/jats:italic>\n                    (MG) and its avian host, the house finch (\n                    <jats:italic>Haemorhous mexicanus<\/jats:italic>\n                    ), can provide insights into such adaptations in immune regulation. Here we use experimental infections to reveal immune variation in conjunctival tissue for house finches captured from four distinct populations differing in the length of their co-evolutionary histories with MG and their disease tolerance (defined as disease severity per pathogen load) in controlled infection studies. To differentiate contributions of host versus pathogen evolution, we compared house finch responses to one of two MG isolates: the original VA1994 isolate and a more evolutionarily derived one, VA2013. To identify differential gene expression involved in initiation of the immune response to MG, we performed 3\u2019-end transcriptomic sequencing (QuantSeq) of samples from the infection site, conjunctiva, collected 3-days post-infection. In response to MG, we observed an increase in general pro-inflammatory signalling, as well as T-cell activation and IL17 pathway differentiation, associated with a decrease in the IL12\/IL23 pathway signalling. The immune response was stronger in response to the evolutionarily derived MG isolate compared to the original one, consistent with known increases in MG virulence over time. The host populations differed namely in pre-activation immune gene expression, suggesting population-specific adaptations. Compared to other populations, finches from Virginia, which have the longest co-evolutionary history with MG, showed significantly higher expression of anti-inflammatory genes and Th1 mediators. This may explain the evolution of disease tolerance to MG infection in VA birds. We also show a potential modulating role of BCL10, a positive B- and T-cell regulator activating the NFKB signalling. Our results illuminate potential mechanisms of house finch adaptation to MG-induced immunopathology, contributing to understanding of the host evolutionary responses to pathogen-driven shifts in immunity-immunopathology trade-offs.\n                  <\/jats:p>","DOI":"10.3389\/fimmu.2024.1250818","type":"journal-article","created":{"date-parts":[[2024,2,1]],"date-time":"2024-02-01T23:40:21Z","timestamp":1706830821000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":10,"title":["Varying conjunctival immune response adaptations of house finch populations to a rapidly evolving bacterial pathogen"],"prefix":"10.3389","volume":"15","author":[{"given":"Nithya","family":"Kuttiyarthu Veetil","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amberleigh E.","family":"Henschen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dana M.","family":"Hawley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Balraj","family":"Melepat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rami A.","family":"Dalloul","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vladim\u00edr","family":"Bene\u0161","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James S.","family":"Adelman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michal","family":"Vinkler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,2,2]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1038\/ng1202-569","article-title":"Biological and biomedical implications of the co-evolution of pathogens and their hosts","volume":"32","author":"Woolhouse","year":"2002","journal-title":"Nat Genet"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1016\/0966-842X(94)90537-1","article-title":"The evolution of virulence","volume":"2","author":"Read","year":"1994","journal-title":"Trends Microbiol"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1701410114","article-title":"Emerging infectious diseases: A proactive approach","volume":"114","author":"Bloom","year":"2017","journal-title":"Proc Natl Acad Sci"},{"key":"B4","doi-asserted-by":"publisher","first-page":"20160167","DOI":"10.1098\/rstb.2016.0167","article-title":"One Health, emerging infectious diseases and wildlife: two decades of progress","volume":"372","author":"Cunningham","year":"2017","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001570","article-title":"Parallel patterns of increased virulence in a recently emerged wildlife pathogen","volume":"11","author":"Hawley","year":"2013","journal-title":"PloS Biol"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1126\/science.aao4806","article-title":"Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation","volume":"359","author":"Voyles","year":"2018","journal-title":"Science"},{"key":"B7","doi-asserted-by":"publisher","first-page":"20160044","DOI":"10.1098\/rstb.2016.0044","article-title":"Resistance in persisting bat populations after white-nose syndrome invasion","volume":"372","author":"Langwig","year":"2017","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1126\/science.aau7285","article-title":"Parallel adaptation of rabbit populations to myxoma virus","volume":"363","author":"Alves","year":"2019","journal-title":"Science"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ecolsys.36.102003.152622","article-title":"Evolutionary causes and consequences of immunopathology","volume":"36","author":"Graham","year":"2005","journal-title":"Annu Rev Ecol Evol Syst"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.68874","article-title":"Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm","volume":"10","author":"Seal","year":"2021","journal-title":"Elife"},{"key":"B11","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1006\/jtbi.1999.1009","article-title":"Three mechanisms of host resistance to microparasites\u2014avoidance, recovery and tolerance\u2014show different evolutionary dynamics","volume":"201","author":"Boots","year":"1999","journal-title":"J Theor Biol"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1126\/science.1148526","article-title":"Disentangling genetic variation for resistance and tolerance to infectious diseases in animals","volume":"318","author":"R\u00e5berg","year":"2007","journal-title":"Science"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2006.tb01173.x","article-title":"The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism","volume":"60","author":"Miller","year":"2006","journal-title":"Evolution"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1001006","article-title":"The coevolution of virulence: tolerance in perspective","volume":"6","author":"Little","year":"2010","journal-title":"PloS Pathog"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1093\/icb\/icz065","article-title":"What does tolerance mean for animal disease dynamics when pathology enhances transmission","volume":"59","author":"Henschen","year":"2019","journal-title":"Integr Comp Biol"},{"key":"B16","doi-asserted-by":"publisher","first-page":"20210362","DOI":"10.1098\/rsbl.2021.0362","article-title":"Disease tolerance alters host competence in a wild songbird","volume":"17","author":"Ruden","year":"2021","journal-title":"Biol Lett"},{"key":"B17","doi-asserted-by":"publisher","first-page":"20153115","DOI":"10.1098\/rspb.2015.3115","article-title":"Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations","volume":"283","author":"Savage","year":"2016","journal-title":"Proc R Soc B Biol Sci"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1007\/s10393-013-0899-2","article-title":"Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai \u2018i \u2018Amakihi (Hemignathus virens)","volume":"10","author":"Atkinson","year":"2013","journal-title":"EcoHealth"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1126\/science.abo3411","article-title":"Evolutionary gain and loss of a pathological immune response to parasitism","volume":"377","author":"Weber","year":"2022","journal-title":"Science"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1011408","article-title":"Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird","volume":"19","author":"Henschen","year":"2023","journal-title":"PloS Pathog"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1111\/jeb.14181","article-title":"Understanding the evolution of immune genes in jawed vertebrates","volume":"36","author":"Vinkler","year":"2023","journal-title":"J Evol Biol"},{"key":"B22","article-title":"Mycoplasma gallisepticum infection","volume-title":"Diseases of poultry","author":"Ley","year":"2008"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1002\/9781119371199.ch21","article-title":"Mycoplasmosis","author":"Ferguson-Noel","year":"2020","journal-title":"Dis Poult"},{"key":"B24","doi-asserted-by":"publisher","first-page":"480","DOI":"10.2307\/1592250","article-title":"Mycoplasma gallisepticum Isolated from House Finches (Carpodacus mexicanus) with Conjunctivitis","volume":"40","author":"Ley","year":"1996","journal-title":"Avian Dis"},{"key":"B25","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/j.actatropica.2005.01.009","article-title":"Dynamics of a novel pathogen in an avian host: Mycoplasmal conjunctivitis in house finches","volume":"94","author":"Dhondt","year":"2005","journal-title":"Acta Trop"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1111\/j.0021-8790.2004.00840.x","article-title":"Mycoplasma gallisepticum infection dynamics in a house finch population: seasonal variation in survival, encounter and transmission rate","volume":"73","author":"Faustino","year":"2004","journal-title":"J Anim Ecol"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.080551197","article-title":"Density-dependent decline of host abundance resulting from a new infectious disease","volume":"97","author":"Hochachka","year":"2000","journal-title":"Proc Natl Acad Sci"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1637\/11610-021317-Reg.1","article-title":"Detection of Mycoplasma gallisepticum in house finches (Haemorhous mexicanus) from Arizona","volume":"62","author":"Staley","year":"2018","journal-title":"Avian Dis"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.7589\/2015-09-244","article-title":"House Finch (Haemorhous mexicanus) Conjunctivitis, and Mycoplasma spp. Isolated from North American Wild Birds, 1994\u20132015","volume":"52","author":"Ley","year":"2016","journal-title":"J Wildl Dis"},{"key":"B30","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.vetmic.2011.08.003","article-title":"Pathogenicity and immunogenicity of three Mycoplasma gallisepticum isolates in house finches (Carpodacus mexicanus)","volume":"155","author":"Grodio","year":"2012","journal-title":"Vet Microbiol"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1111\/j.1420-9101.2010.02035.x","article-title":"Common garden experiment reveals pathogen isolate but no host genetic diversity effect on the dynamics of an emerging wildlife disease: Host genetic diversity and disease resistance","volume":"23","author":"Hawley","year":"2010","journal-title":"J Evol Biol"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1007\/s00114-004-0582-0","article-title":"Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch","volume":"92","author":"Hill","year":"2005","journal-title":"Naturwissenschaften"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1086\/670024","article-title":"House Finch Populations Differ in Early Inflammatory Signaling and Pathogen Tolerance at the Peak of Mycoplasma gallisepticum Infection","volume":"181","author":"Adelman","year":"2013","journal-title":"Am Nat"},{"key":"B34","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1128\/MMBR.62.4.1094-1156.1998","article-title":"Molecular biology and pathogenicity of mycoplasmas","volume":"62","author":"Razin","year":"1998","journal-title":"Microbiol Mol Biol Rev"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1097\/INF.0000000000000171","article-title":"Mycoplasma pneumoniae infections in childhood","volume":"33","author":"Atkinson","year":"2014","journal-title":"Pediatr Infect Dis J"},{"key":"B36","doi-asserted-by":"publisher","first-page":"220975","DOI":"10.1098\/rsos.220975","article-title":"High virulence is associated with pathogen spreadability in a songbird\u2013bacterial system","volume":"10","author":"Hawley","year":"2023","journal-title":"R Soc Open Sci"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.00013","article-title":"Differing house finch cytokine expression responses to original and evolved isolates of Mycoplasma gallisepticum","volume":"9","author":"Vinkler","year":"2018","journal-title":"Front Immunol"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1018580108","article-title":"Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird","volume":"108","author":"Bonneaud","year":"2011","journal-title":"Proc Natl Acad Sci"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2012.05551.x","article-title":"Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird","volume":"21","author":"Bonneaud","year":"2012","journal-title":"Mol Ecol"},{"key":"B40","first-page":"49","article-title":"Molt limits in North American passerines","volume":"22","author":"Pyle","year":"1997","journal-title":"North Am Bird Bander"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1126\/science.aao2140","article-title":"Incomplete host immunity favors the evolution of virulence in an emergent pathogen","volume":"359","author":"Fleming-Davies","year":"2018","journal-title":"Science"},{"key":"B42","doi-asserted-by":"publisher","first-page":"18895","DOI":"10.1038\/s41598-019-55434-x","article-title":"QuantSeq. 3\u2032 Sequencing combined with Salmon provides a fast, reliable approach for high throughput RNA expression analysis","volume":"9","author":"Corley","year":"2019","journal-title":"Sci Rep"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2020.562445","article-title":"A comparison of low read depth quantSeq 3\u2032 Sequencing to total RNA-seq in FUS mutant mice","volume":"11","author":"Jarvis","year":"2020","journal-title":"Front Genet"},{"key":"B44","doi-asserted-by":"publisher","first-page":"i","DOI":"10.1038\/nmeth.f.376","article-title":"QuantSeq 3\u2032 mRNA sequencing for RNA quantification","volume":"11","author":"Moll","year":"2014","journal-title":"Nat Methods"},{"key":"B45","doi-asserted-by":"publisher","first-page":"pdb","DOI":"10.1093\/nar\/gkaa942","article-title":"High-throughput illumina strand-specific RNA sequencing library preparation","author":"Zhong","year":"2011","journal-title":"Cold Spring Harb Protoc"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-018-5393-3","article-title":"A comparison between whole transcript and 3\u2019 RNA sequencing methods using Kapa and Lexogen library preparation methods","volume":"20","author":"Ma","year":"2019","journal-title":"BMC Genomics"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkaa942","article-title":"Ensembl 2021","volume":"49","author":"Howe","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btt656","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"B49","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/nar\/gkv007","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: an efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"Ritchie","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"B52","volume-title":"R: A language and environment for statistical computing","year":"2020"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btz931","article-title":"ShinyGO: a graphical gene-set enrichment tool for animals and plants","volume":"36","author":"Ge","year":"2020","journal-title":"Bioinformatics"},{"key":"B54","volume-title":"Avian immunology","author":"Kaspers","year":"2021"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0509592103","article-title":"Between-group analysis of microarray data","volume":"18","author":"Culhane","year":"2002","journal-title":"Bioinformatics"},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1016\/j.jointm.2022.01.001","article-title":"Mitochondrial ACOD1\/IRG1 in infection and sterile inflammation","volume":"2","author":"Wu","year":"2022","journal-title":"J Intensive Med"},{"key":"B57","doi-asserted-by":"publisher","DOI":"10.1007\/s10753-023-01910-6","article-title":"LIF aggravates pulpitis by promoting inflammatory response in macrophages","volume":"47","author":"Guo","year":"2024","journal-title":"Inflammation"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01172","article-title":"Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor","volume":"103","author":"Inagaki","year":"2006","journal-title":"Proc Natl Acad Sci"},{"key":"B59","doi-asserted-by":"publisher","first-page":"65","DOI":"10.2147\/OTT.S237162","article-title":"CXCL12 chemokine and its receptors as major players in the interactions between immune and nervous systems","volume":"8","author":"Guyon","year":"2014","journal-title":"Front Cell Neurosci"},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.1038\/s41423-020-0489-5","article-title":"ACOD1 in immunometabolism and disease","volume":"17","author":"Wu","year":"2020","journal-title":"Cell Mol Immunol"},{"key":"B61","doi-asserted-by":"publisher","first-page":"1172","DOI":"10.1128\/IAI.01356-12","article-title":"Interleukin-17D promotes pathogenicity during infection by suppressing CD8 T cell activity","volume":"10","author":"Lee","year":"2019","journal-title":"Front Immunol"},{"key":"B62","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.3389\/fimmu.2020.628804","article-title":"IFI30 is a novel immune-related target with predicting value of prognosis and treatment response in glioblastoma","volume":"13","author":"Zhu","year":"2020","journal-title":"OncoTargets Ther"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.3389\/fmolb.2021.745649","article-title":"Pan-cancer analysis of the associations of TGFBI expression with prognosis and immune characteristics","volume":"8","author":"Chen","year":"2021","journal-title":"Front Mol Biosci"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1016\/j.dci.2016.01.008","article-title":"Toll-like receptor 6 plays an important role in host innate resistance to Brucella abortus infection in mice","volume":"81","author":"de Almeida","year":"2013","journal-title":"Infect Immun"},{"key":"B65","doi-asserted-by":"publisher","first-page":"628804","DOI":"10.1016\/S0167-4889(01)00166-5","article-title":"Transcriptomic analysis of long-term protective immunity induced by vaccination with Mycoplasma gallisepticum strain ts-304","volume":"11","author":"Kulappu Arachchige","year":"2021","journal-title":"Front Immunol"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2022.111572","article-title":"Transcriptional profiling of the chicken tracheal response to virulent Mycoplasma gallisepticum strain Rlow","volume":"85","author":"Beaudet","year":"2017","journal-title":"Infect Immun"},{"key":"B67","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.dci.2016.01.008","article-title":"Roles of Toll-like receptors 2 and 6 in the inflammatory response to Mycoplasma gallisepticum infection in DF-1 cells and in chicken embryos","volume":"59","author":"Tian","year":"2016","journal-title":"Dev Comp Immunol"},{"key":"B68","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0167-4889(01)00166-5","article-title":"Multiple roles of the invariant chain in MHC class II function","volume":"1542","author":"Stumptner-Cuvelette","year":"2002","journal-title":"Biochim Biophys Acta BBA - Mol Cell Res"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2022.111572","article-title":"CD74 as a regulator of transcription in normal B cells","volume":"41","author":"David","year":"2022","journal-title":"Cell Rep"},{"key":"B70","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/S0092-8674(00)80957-5","article-title":"Interplay between soluble CD74 and macrophage-migration inhibitory factor drives tumor growth and influences patient survival in melanoma","volume":"13","author":"Fukuda","year":"2022","journal-title":"Cell Death Dis"},{"key":"B71","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.29.20127","article-title":"Chemokine and cytokine gene expression profiles in chickens inoculated with Mycoplasma gallisepticum strains Rlow or GT5","volume":"25","author":"Mohammed","year":"2007","journal-title":"Vaccine"},{"key":"B72","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.01539","article-title":"BCL10 \u2013 bridging CARDs to immune activation","volume":"9","author":"Gehring","year":"2018","journal-title":"Front Immunol"},{"key":"B73","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/s0092-8674(00)80957-5","article-title":"Bcl10 is involved in t (1; 14)(p22; q32) of MALT B cell lymphoma and mutated in multiple tumor types","volume":"96","author":"Willis","year":"1999","journal-title":"Cell"},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.786572","article-title":"c-E10 is a caspase-recruiting domain-containing protein that interacts with components of death receptors signaling pathway and activates nuclear factor-\u03baB","volume":"274","author":"Costanzo","year":"1999","journal-title":"J Biol Chem"},{"key":"B75","doi-asserted-by":"publisher","DOI":"10.1152\/physiolgenomics.00098.2006","article-title":"CIPER, a novel NF \u03baB-activating protein containing a caspase recruitment domain with homology to herpesvirus-2 protein E10","volume":"274","author":"Koseki","year":"1999","journal-title":"J Biol Chem"},{"key":"B76","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/S0092-8674(01)00189-1","article-title":"Bcl10 is a positive regulator of antigen receptor\u2013induced activation of NF-\u03ba B and neural tube closure","volume":"104","author":"Ruland","year":"2001","journal-title":"Cell"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0608388103","article-title":"Clinical and immunological features of human BCL10 deficiency","volume":"4732","author":"Garcia-Solis","year":"2021","journal-title":"Front Immunol"},{"key":"B78","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1111\/j.1600-065X.2008.00699.x","article-title":"Gene expression profiling of monocyte-derived macrophages following infection with Mycobacterium avium subspecies avium and Mycobacterium avium subspecies paratuberculosis","volume":"28","author":"Murphy","year":"2006","journal-title":"Physiol Genomics"},{"key":"B79","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jdermsci.2011.11.007","article-title":"The correlated expression of immune and energy metabolism related genes in the response to Salmonella enterica serovar Enteritidis inoculation in chicken","volume":"16","author":"Wang","year":"2020","journal-title":"BMC Vet Res"},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1016\/j.meegid.2013.12.004","article-title":"Bcl10 and Malt1 control lysophosphatidic acid-induced NF-\u03baB activation and cytokine production","volume":"104","author":"Klemm","year":"2007","journal-title":"Proc Natl Acad Sci"},{"key":"B81","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/s41385-022-00551-6","article-title":"The roles of IL-17A in inflammatory immune responses and host defense against pathogens","volume":"226","author":"Iwakura","year":"2008","journal-title":"Immunol Rev"},{"key":"B82","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1007\/BF02539415","article-title":"Chemokine receptors in the pathogenesis and therapy of psoriasis","volume":"65","author":"Mabuchi","year":"2012","journal-title":"J Dermatol Sci"},{"key":"B83","doi-asserted-by":"publisher","DOI":"10.1016\/j.meegid.2013.12.004","article-title":"A genome-wide association study identifies major loci affecting the immune response against infectious bronchitis virus in chicken","volume":"21","author":"Luo","year":"2014","journal-title":"Infect Genet Evol"},{"key":"B84","doi-asserted-by":"publisher","DOI":"10.1167\/iovs.63.12.13","article-title":"Mucosal immunology of the ocular surface","volume":"15","author":"de Paiva","year":"2022","journal-title":"Mucosal Immunol"},{"key":"B85","doi-asserted-by":"publisher","DOI":"10.1136\/gut.2010.233304","article-title":"\u03b1\/\u03b2-and \u03b3\/\u03b4-T cell-receptor-positive lymphocytes in healthy and inflamed human conjunctiva","volume":"234","author":"Bialasiewicz","year":"1996","journal-title":"Graefes Arch Clin Exp Ophthalmol"},{"key":"B86","doi-asserted-by":"publisher","first-page":"6077","DOI":"10.4049\/jimmunol.0803978","article-title":"Tissue resident memory T cells inhabit the deep human conjunctiva","volume":"12","author":"Arnous","year":"2022","journal-title":"Sci Rep"},{"key":"B87","doi-asserted-by":"publisher","DOI":"10.2741\/A845","article-title":"Conjunctiva resident \u03b3\u03b4 T cells expressed high level of IL-17A and promoted the severity of dry eye","volume":"63","author":"Li","year":"2022","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"B88","doi-asserted-by":"publisher","DOI":"10.12688\/f1000research.7010.1","article-title":"Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium","volume":"12","author":"Gaudet","year":"2011","journal-title":"Brief Bioinform"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.1016\/S1074-7613(00)00070-4","article-title":"FXR activation inhibits inflammation and preserves the intestinal barrier in IBD","volume":"60","author":"Wildenberg","year":"2011","journal-title":"Gut"},{"key":"B90","doi-asserted-by":"publisher","DOI":"10.1038\/nm.3895","article-title":"The bile acid receptor FXR is a modulator of intestinal innate immunity","volume":"183","author":"Vavassori","year":"2009","journal-title":"J Immunol"},{"key":"B91","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.173.3.1779","article-title":"Role of innate immunity in respiratory mycoplasma infection","volume":"7","author":"Hickman-Davis","year":"2002","journal-title":"Front Biosci-Landmark"},{"key":"B92","doi-asserted-by":"publisher","DOI":"10.12688\/f1000research.7010.1","article-title":"Regulation of IL-10 and IL-12 production and function in macrophages and dendritic cells","volume":"4","author":"Ma","year":"2015","journal-title":"F1000Research"},{"key":"B93","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.67.9.4435-4442.1999","article-title":"Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12","volume":"13","author":"Oppmann","year":"2000","journal-title":"Immunity"},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.1002\/eji.200636012","article-title":"IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases","volume":"21","author":"Teng","year":"2015","journal-title":"Nat Med"},{"key":"B95","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.173.3.1779","article-title":"ICOS expression by activated human th cells is enhanced by IL-12 and IL-23: increased ICOS expression enhances the effector function of both th1 and th2 cells","volume":"173","author":"Wassink","year":"2004","journal-title":"J Immunol"},{"key":"B96","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.747324","article-title":"Interleukin-7 biology and its effects on immune cells: mediator of generation, differentiation, survival, and homeostasis","volume":"12","author":"Chen","year":"2021","journal-title":"Front Immunol"},{"key":"B97","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2180-14-156","article-title":"A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice","volume":"67","author":"Li","year":"1999","journal-title":"Infect Immun"},{"key":"B98","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.919973","article-title":"Interleukin-10 derived from macrophages and\/or neutrophils regulates the inflammatory response to LPS but not the response to CpG DNA","volume":"36","author":"Siewe","year":"2006","journal-title":"Eur J Immunol"},{"key":"B99","doi-asserted-by":"publisher","DOI":"10.1186\/s13567-020-00777-x","article-title":"Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10","volume":"15","author":"Sun","year":"2009","journal-title":"Nat Med"},{"key":"B100","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.02148","article-title":"Resolution of a chronic viral infection after interleukin-10 receptor blockade","volume":"203","author":"Ejrnaes","year":"2006","journal-title":"J Exp Med"},{"key":"B101","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0278853","article-title":"Role of IL-17A and IL-10 in the antigen induced inflammation model by Mycoplasma pneumoniae","volume":"14","author":"Kurata","year":"2014","journal-title":"BMC Microbiol"},{"key":"B102","doi-asserted-by":"publisher","DOI":"10.1038\/nrg2484","article-title":"Interleukin-18 cytokine in immunity, inflammation, and autoimmunity: Biological role in induction, regulation, and treatment","volume":"4470","author":"Ihim","year":"2022","journal-title":"Front Immunol"},{"key":"B103","doi-asserted-by":"publisher","DOI":"10.1186\/s13567-020-00777-x","article-title":"Mycoplasma gallisepticum triggers immune damage in the chicken thymus by activating the TLR-2\/MyD88\/NF-\u03baB signaling pathway and NLRP3 inflammasome","volume":"51","author":"Chen","year":"2020","journal-title":"Vet Res"},{"key":"B104","doi-asserted-by":"publisher","first-page":"2148","DOI":"10.1098\/rsbl.2010.0020","article-title":"A double edged sword role of interleukin-22 in wound healing and tissue regeneration","volume":"11","author":"Arshad","year":"2020","journal-title":"Front Immunol"},{"key":"B105","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0278853","article-title":"The trehalose glycolipid C18Brar promotes antibody and T-cell immune responses to Mannheimia haemolytica and Mycoplasma ovipneumoniae whole cell antigens in sheep","volume":"18","author":"Gupta","year":"2023","journal-title":"PloS One"},{"key":"B106","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/nrg2484","article-title":"RNA-Seq: a revolutionary tool for transcriptomics","volume":"10","author":"Wang","year":"2009","journal-title":"Nat Rev Genet"},{"key":"B107","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1186\/s12864-021-07884-9","article-title":"Deploying new generation sequencing for the study of flesh color depletion in Atlantic Salmon (Salmo salar)","volume":"22","author":"Vo","year":"2021","journal-title":"BMC Genomics"},{"key":"B108","doi-asserted-by":"publisher","DOI":"10.1093\/bib\/bbr042","article-title":"Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics","volume":"6","author":"Bouwman","year":"2010","journal-title":"Biol Lett"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2024.1250818\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,1]],"date-time":"2024-02-01T23:40:35Z","timestamp":1706830835000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2024.1250818\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,2]]},"references-count":108,"alternative-id":["10.3389\/fimmu.2024.1250818"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2024.1250818","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,2]]},"article-number":"1250818"}}