{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T02:52:25Z","timestamp":1792637545509,"version":"4.5.0"},"reference-count":49,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2025,3,1]],"date-time":"2025-03-01T00:00:00Z","timestamp":1740787200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,3,1]],"date-time":"2025-03-01T00:00:00Z","timestamp":1740787200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2024,12,16]],"date-time":"2024-12-16T00:00:00Z","timestamp":1734307200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"German Research Foundation","doi-asserted-by":"publisher","award":["FOR5130"],"award-info":[{"award-number":["FOR5130"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100012065","name":"Houghton Trust","doi-asserted-by":"publisher","award":["HT\/SPRG\/23\/03"],"award-info":[{"award-number":["HT\/SPRG\/23\/03"]}],"id":[{"id":"10.13039\/100012065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Developmental Biology"],"published-print":{"date-parts":[[2025,3]]},"DOI":"10.1016\/j.ydbio.2024.12.006","type":"journal-article","created":{"date-parts":[[2024,12,16]],"date-time":"2024-12-16T02:48:42Z","timestamp":1734317322000},"page":"38-45","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":2,"special_numbering":"C","title":["The search to understand the development of the chicken immune system: Differences in expression of MHC class I loci and waves of thymocytes as evolutionary relics?"],"prefix":"10.1016","volume":"519","author":[{"given":"Samer","family":"Halabi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas","family":"Rocos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7216-8422","authenticated-orcid":false,"given":"Jim","family":"Kaufman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.ydbio.2024.12.006_bib1","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1146\/annurev-immunol-032712-095912","article-title":"The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules","volume":"31","author":"Adams","year":"2013","journal-title":"Annu. Rev. Immunol."},{"issue":"5","key":"10.1016\/j.ydbio.2024.12.006_bib2","doi-asserted-by":"crossref","first-page":"3324","DOI":"10.4049\/jimmunol.166.5.3324","article-title":"At least one class I gene in restriction fragment pattern-Y (Rfp-Y), the second MHC gene cluster in the chicken, is transcribed, polymorphic, and shows divergent specialization in antigen binding region","volume":"166","author":"Afanassieff","year":"2001","journal-title":"J. Immunol."},{"issue":"12","key":"10.1016\/j.ydbio.2024.12.006_bib3","doi-asserted-by":"crossref","DOI":"10.1016\/j.psj.2024.104295","article-title":"Sustainable poultry farming practices: a critical review of current strategies and future prospects","volume":"103","author":"Bist","year":"2024","journal-title":"Poultry Sci."},{"key":"10.1016\/j.ydbio.2024.12.006_bib4","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.05345","article-title":"Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding","volume":"4","author":"Chappell","year":"2015","journal-title":"Elife"},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib5","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1084\/jem.170.2.543","article-title":"Analysis of the first two waves of thymus homing stem cells and their T cell progeny in chick-quail chimeras","volume":"170","author":"Coltey","year":"1989","journal-title":"J. Exp. Med."},{"issue":"1","key":"10.1016\/j.ydbio.2024.12.006_bib6","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/0045-6039(87)90414-3","article-title":"Evidence for a cyclic renewal of lymphocyte precursor cells in the embryonic chick thymus","volume":"22","author":"Coltey","year":"1987","journal-title":"Cell Differ."},{"key":"10.1016\/j.ydbio.2024.12.006_bib7","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1038\/205143a0","article-title":"Delineation of the thymic and bursal lymphoid systems in the chicken","volume":"205","author":"Cooper","year":"1965","journal-title":"Nature"},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib8","article-title":"Casting a wider net: immunosurveillance by nonclassical MHC molecules","volume":"15","author":"D'Souza","year":"2019","journal-title":"PLoS Pathog."},{"issue":"10","key":"10.1016\/j.ydbio.2024.12.006_bib9","doi-asserted-by":"crossref","first-page":"2545","DOI":"10.1002\/eji.1830231025","article-title":"Migration patterns of thymus-derived gamma delta T cells during chicken development","volume":"23","author":"Dunon","year":"1993","journal-title":"Eur. J. Immunol."},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib10","first-page":"127","article-title":"Ontogenic appearance of MHC class I (B-F) antigens during chicken embryogenesis","volume":"1","author":"Dunon","year":"1990","journal-title":"Dev. Immunol."},{"issue":"4","key":"10.1016\/j.ydbio.2024.12.006_bib11","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1002\/j.1460-2075.1994.tb06323.x","article-title":"T cell migration during development: homing is not related to TCR V beta 1 repertoire selection","volume":"13","author":"Dunon","year":"1994","journal-title":"EMBO J."},{"issue":"35","key":"10.1016\/j.ydbio.2024.12.006_bib12","doi-asserted-by":"crossref","first-page":"14342","DOI":"10.1073\/pnas.1309840110","article-title":"Nonclassical MHC class I-dependent invariant T cells are evolutionarily conserved and prominent from early development in amphibians","volume":"110","author":"Edholm","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"17","key":"10.1016\/j.ydbio.2024.12.006_bib13","doi-asserted-by":"crossref","first-page":"E4023","DOI":"10.1073\/pnas.1722129115","article-title":"Distinct MHC class I-like interacting invariant T cell lineage at the forefront of mycobacterial immunity uncovered in Xenopus","volume":"115","author":"Edholm","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"8","key":"10.1016\/j.ydbio.2024.12.006_bib14","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1007\/s00251-016-0929-7","article-title":"Evolution of innate-like T cells and their selection by MHC class I-like molecules","volume":"68","author":"Edholm","year":"2016","journal-title":"Immunogenetics"},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib15","doi-asserted-by":"crossref","first-page":"576","DOI":"10.4049\/jimmunol.1500458","article-title":"Nonclassical MHC- restricted invariant v\u03b16 T cells are critical for efficient early innate antiviral immunity in the Amphibian Xenopus laevis","volume":"195","author":"Edholm","year":"2015","journal-title":"J. Immunol."},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib16","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/0167-5699(87)90240-4","article-title":"Changes in the immune system during metamorphosis of Xenopus","volume":"8","author":"Flajnik","year":"1987","journal-title":"Immunol. Today"},{"issue":"12","key":"10.1016\/j.ydbio.2024.12.006_bib17","doi-asserted-by":"crossref","first-page":"3891","DOI":"10.4049\/jimmunol.137.12.3891","article-title":"Major histocompatibility complex-encoded class I molecules are absent in immunologically competent Xenopus before metamorphosis","volume":"137","author":"Flajnik","year":"1986","journal-title":"J. Immunol."},{"key":"10.1016\/j.ydbio.2024.12.006_bib18","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2021.791081","article-title":"The chicken embryo model: a novel and relevant model for immune-based studies","volume":"12","author":"Garcia","year":"2021","journal-title":"Front. Immunol."},{"issue":"11","key":"10.1016\/j.ydbio.2024.12.006_bib19","doi-asserted-by":"crossref","first-page":"1114","DOI":"10.1038\/ni.3298","article-title":"The burgeoning family of unconventional T cells","volume":"16","author":"Godfrey","year":"2015","journal-title":"Nat. Immunol."},{"issue":"2\u20134","key":"10.1016\/j.ydbio.2024.12.006_bib20","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1159\/000213584","article-title":"Growth in amphibians","volume":"40","author":"Hota","year":"1994","journal-title":"Gerontology"},{"issue":"1","key":"10.1016\/j.ydbio.2024.12.006_bib21","doi-asserted-by":"crossref","first-page":"3769","DOI":"10.1038\/s41467-020-17557-y","article-title":"Butyrophilin-like proteins display combinatorial diversity in selecting and maintaining signature intraepithelial \u03b3\u03b4 T cell compartments","volume":"11","author":"Jandke","year":"2020","journal-title":"Nat. Commun."},{"issue":"8","key":"10.1016\/j.ydbio.2024.12.006_bib22","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1002\/eji.1830100809","article-title":"Lymphoid stem cell homing to the early thymic primordium of the avian embryo","volume":"10","author":"Jotereau","year":"1980","journal-title":"Eur. J. Immunol."},{"issue":"5","key":"10.1016\/j.ydbio.2024.12.006_bib23","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.it.2018.01.001","article-title":"Generalists and specialists: a new view of how MHC class I molecules fight infectious pathogens","volume":"39","author":"Kaufman","year":"2018","journal-title":"Trends Immunol."},{"key":"10.1016\/j.ydbio.2024.12.006_bib24","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1111\/j.1600-065X.1999.tb01385.x","article-title":"Gene organisation determines evolution of function in the chicken MHC","volume":"167","author":"Kaufman","year":"1999","journal-title":"Immunol. Rev."},{"issue":"6756","key":"10.1016\/j.ydbio.2024.12.006_bib25","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1038\/44856","article-title":"The chicken B locus is a minimal essential major histocompatibility complex","volume":"401","author":"Kaufman","year":"1999","journal-title":"Nature"},{"issue":"9","key":"10.1016\/j.ydbio.2024.12.006_bib26","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1007\/s00251-018-1066-2","article-title":"Two class I genes of the chicken MHC have different functions: BF1 is recognized by NK cells while BF2 is recognized by CTLs","volume":"70","author":"Kim","year":"2018","journal-title":"Immunogenetics"},{"issue":"149","key":"10.1016\/j.ydbio.2024.12.006_bib27","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/newbio246025b0","article-title":"Origin and renewal of lymphocytes in avian embryo thymuses studied in interspecific combinations","volume":"246","author":"LeDouarin","year":"1973","journal-title":"Nat. New Biol."},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib28","doi-asserted-by":"crossref","first-page":"375","DOI":"10.3382\/ps\/pev379","article-title":"Brief review of the chicken Major Histocompatibility Complex: the genes, their distribution on chromosome 16, and their contributions to disease resistance","volume":"95","author":"Miller","year":"2016","journal-title":"Poultry Sci."},{"issue":"6","key":"10.1016\/j.ydbio.2024.12.006_bib29","doi-asserted-by":"crossref","first-page":"2743","DOI":"10.1128\/JVI.02265-08","article-title":"HLA-B57\/B\u22175801 human immunodeficiency virus type 1 elite controllers select for rare gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte recognition","volume":"83","author":"Miura","year":"2009","journal-title":"J. Virol."},{"issue":"1","key":"10.1016\/j.ydbio.2024.12.006_bib30","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/imr.13181","article-title":"The layered development of mouse B and T cells","volume":"315","author":"Montecino-Rodriguez","year":"2023","journal-title":"Immunol. Rev."},{"key":"10.1016\/j.ydbio.2024.12.006_bib31","series-title":"Janeway's Immunobiology 10th Addition","author":"Murphy","year":"2022"},{"key":"10.1016\/j.ydbio.2024.12.006_bib32","doi-asserted-by":"crossref","first-page":"1468","DOI":"10.3389\/fimmu.2020.01468","article-title":"In and out of the bursa-the role of CXCR4 in chicken B cell development","volume":"11","author":"Nagy","year":"2020","journal-title":"Front. Immunol."},{"issue":"3","key":"10.1016\/j.ydbio.2024.12.006_bib33","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.dci.2013.03.007","article-title":"Retrospection to discovery of bursal function and recognition of avian dendritic cells; past and present","volume":"41","author":"Ol\u00e1h","year":"2013","journal-title":"Dev. Comp. Immunol."},{"issue":"10","key":"10.1016\/j.ydbio.2024.12.006_bib34","doi-asserted-by":"crossref","first-page":"696","DOI":"10.4049\/immunohorizons.2300081","article-title":"Larval T cells are functionally distinct from adult T cells in Xenopus laevis","volume":"7","author":"Paiola","year":"2023","journal-title":"Immunohorizons"},{"key":"10.1016\/j.ydbio.2024.12.006_bib35","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.coi.2017.03.013","article-title":"What chickens might tell us about the MHC class II system","volume":"46","author":"Parker","year":"2017","journal-title":"Curr. Opin. Immunol."},{"issue":"7","key":"10.1016\/j.ydbio.2024.12.006_bib36","doi-asserted-by":"crossref","first-page":"2322","DOI":"10.3382\/ps\/pey081","article-title":"In ovo applications in poultry: a review","volume":"97","author":"Peebles","year":"2018","journal-title":"Poultry Sci."},{"issue":"24","key":"10.1016\/j.ydbio.2024.12.006_bib37","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2121978119","article-title":"The biocultural origins and dispersal of domestic chickens","volume":"119","author":"Peters","year":"2022","journal-title":"Proc Natl Acad Sci U SA"},{"issue":"1\u20132","key":"10.1016\/j.ydbio.2024.12.006_bib38","first-page":"47","article-title":"Biology of the chicken MHC (B complex)","volume":"12","author":"Plachy","year":"1992","journal-title":"Crit. Rev. Immunol."},{"issue":"1\u20132","key":"10.1016\/j.ydbio.2024.12.006_bib39","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.dci.2005.06.018","article-title":"Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development","volume":"30","author":"Ratcliffe","year":"2006","journal-title":"Dev. Comp. Immunol."},{"issue":"2","key":"10.1016\/j.ydbio.2024.12.006_bib40","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.yexcr.2019.05.027","article-title":"The morphological basis of the development of the chick embryo immune system","volume":"381","author":"Ribatti","year":"2019","journal-title":"Exp. Cell Res."},{"issue":"5","key":"10.1016\/j.ydbio.2024.12.006_bib41","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1007\/s00251-023-01313-9","article-title":"The minor chicken class I gene BF1 is deleted between short imperfect direct repeats in the B14 and typical B15 major histocompatibility complex (MHC) haplotypes","volume":"75","author":"Rocos","year":"2023","journal-title":"Immunogenetics"},{"issue":"24","key":"10.1016\/j.ydbio.2024.12.006_bib42","doi-asserted-by":"crossref","first-page":"8668","DOI":"10.1073\/pnas.0409213102","article-title":"Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC","volume":"102","author":"Salomonsen","year":"2005","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"22","key":"10.1016\/j.ydbio.2024.12.006_bib43","doi-asserted-by":"crossref","first-page":"12382","DOI":"10.1128\/JVI.01543-07","article-title":"Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication","volume":"81","author":"Schneidewind","year":"2007","journal-title":"J. Virol."},{"issue":"9","key":"10.1016\/j.ydbio.2024.12.006_bib44","doi-asserted-by":"crossref","first-page":"5744","DOI":"10.4049\/jimmunol.178.9.5744","article-title":"Different evolutionary histories of the two classical class I genes BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens","volume":"178","author":"Shaw","year":"2007","journal-title":"J. Immunol."},{"issue":"8\u20139","key":"10.1016\/j.ydbio.2024.12.006_bib45","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1159\/000529376","article-title":"Fourth report on chicken genes and chromosomes 2022","volume":"162","author":"Smith","year":"2022","journal-title":"Cytogenet. Genome Res."},{"key":"10.1016\/j.ydbio.2024.12.006_bib46","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.molimm.2021.03.019","article-title":"Chickens as a simple system for scientific discovery: the example of the MHC","volume":"135","author":"Tregaskes","year":"2021","journal-title":"Mol. Immunol."},{"issue":"1","key":"10.1016\/j.ydbio.2024.12.006_bib47","doi-asserted-by":"crossref","first-page":"41","DOI":"10.4049\/jimmunol.142.1.41","article-title":"Precursor immigration and thymocyte succession during larval development and metamorphosis in Xenopus","volume":"142","author":"Turpen","year":"1989","journal-title":"J. Immunol."},{"issue":"5","key":"10.1016\/j.ydbio.2024.12.006_bib48","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1007\/s002510050368","article-title":"Wide tissue distribution of axolotl class II molecules occurs independently of thyroxin","volume":"47","author":"V\u00f6lk","year":"1998","journal-title":"Immunogenetics"},{"issue":"5","key":"10.1016\/j.ydbio.2024.12.006_bib49","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1073\/pnas.0507386103","article-title":"Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens","volume":"103","author":"Wallny","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A."}],"container-title":["Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160624002781?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160624002781?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T15:33:26Z","timestamp":1777390406000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0012160624002781"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3]]},"references-count":49,"alternative-id":["S0012160624002781"],"URL":"https:\/\/doi.org\/10.1016\/j.ydbio.2024.12.006","relation":{},"ISSN":["0012-1606"],"issn-type":[{"value":"0012-1606","type":"print"}],"subject":[],"published":{"date-parts":[[2025,3]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"The search to understand the development of the chicken immune system: Differences in expression of MHC class I loci and waves of thymocytes as evolutionary relics?","name":"articletitle","label":"Article Title"},{"value":"Developmental Biology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ydbio.2024.12.006","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2024 The Authors. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}