{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T14:01:29Z","timestamp":1778594489546,"version":"3.51.4"},"reference-count":101,"publisher":"Oxford University Press (OUP)","issue":"10","license":[{"start":{"date-parts":[[2025,2,26]],"date-time":"2025-02-26T00:00:00Z","timestamp":1740528000000},"content-version":"vor","delay-in-days":1762,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Institutes of Health\/National Science Foundation","doi-asserted-by":"publisher","award":["1456940"],"award-info":[{"award-number":["1456940"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health\/Center for Evolutionary and Theoretical Immunology\/Centers of Biomedical Research Excellence","doi-asserted-by":"publisher","award":["P20GM103452"],"award-info":[{"award-number":["P20GM103452"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,5,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The adaptive immune system of all jawed vertebrates relies on the presence of B and T cell lymphocytes that aggregate in specific body sites to form primary and secondary lymphoid structures. Secondary lymphoid organs include organized MALT (O-MALT) such as the tonsils and Peyer patches. O-MALT became progressively organized during vertebrate evolution, and the TNF superfamily of genes has been identified as essential for the formation and maintenance of O-MALT and other secondary and tertiary lymphoid structures in mammals. Yet, the molecular drivers of O-MALT structures found in ectotherms and birds remain essentially unknown. In this study, we provide evidence that TNFSFs, such as lymphotoxins, are likely not a universal mechanism to maintain O-MALT structures in adulthood of teleost fish, sarcopterygian fish, or birds. Although a role for TNFSF2 (TNF-\u03b1) cannot be ruled out, transcriptomics suggest that maintenance of O-MALT in nonmammalian vertebrates relies on expression of diverse genes with shared biological functions in neuronal signaling. Importantly, we identify that expression of many genes with olfactory function is a unique feature of mammalian Peyer patches but not the O-MALT of birds or ectotherms. These results provide a new view of O-MALT evolution in vertebrates and indicate that different genes with shared biological functions may have driven the formation of these lymphoid structures by a process of convergent evolution.<\/jats:p>","DOI":"10.4049\/jimmunol.1901059","type":"journal-article","created":{"date-parts":[[2020,4,1]],"date-time":"2020-04-01T20:24:24Z","timestamp":1585772664000},"page":"2697-2711","source":"Crossref","is-referenced-by-count":20,"title":["Molecular Drivers of Lymphocyte Organization in Vertebrate Mucosal Surfaces: Revisiting the TNF Superfamily Hypothesis"],"prefix":"10.1093","volume":"204","author":[{"given":"Ryan D","family":"Heimroth","sequence":"first","affiliation":[{"name":"Center for Evolutionary and Theoretical Immunology, University of New Mexico , Albuquerque, NM 87131"},{"name":"Department of Biology, University of New Mexico , Albuquerque, NM 87131"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elisa","family":"Casadei","sequence":"additional","affiliation":[{"name":"Center for Evolutionary and Theoretical Immunology, University of New Mexico , Albuquerque, NM 87131"},{"name":"Department of Biology, University of New Mexico , Albuquerque, NM 87131"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Irene","family":"Salinas","sequence":"additional","affiliation":[{"name":"Center for Evolutionary and Theoretical Immunology, University of New Mexico , Albuquerque, NM 87131"},{"name":"Department of Biology, University of New Mexico , Albuquerque, NM 87131"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2020,5,15]]},"reference":[{"key":"2025030418555250700_r1","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1146\/annurev-cellbio-111315-125306","article-title":"Emergence and evolution of secondary lymphoid organs","volume":"32","author":"Neely","year":"2016","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2025030418555250700_r2","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1038\/s41577-018-0003-9","article-title":"A cold-blooded view of adaptive immunity","volume":"18","author":"Flajnik","year":"2018","journal-title":"Nat. Rev. Immunol."},{"key":"2025030418555250700_r3","first-page":"67","article-title":"Phylogeny of lower vertebrates and their immunological structures","volume":"248","author":"Zapata","year":"2000","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"2025030418555250700_r4","doi-asserted-by":"crossref","first-page":"2205","DOI":"10.4049\/jimmunol.0804324","article-title":"Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response","volume":"183","author":"Ruddle","year":"2009","journal-title":"J. Immunol."},{"key":"2025030418555250700_r5","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1016\/j.cub.2015.07.066","article-title":"African lungfish reveal the evolutionary origins of organized mucosal lymphoid tissue in vertebrates","volume":"25","author":"Tacchi","year":"2015","journal-title":"Curr. Biol."},{"key":"2025030418555250700_r6","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1016\/j.fsi.2019.08.044","article-title":"Visualization of CCL19-like transcripts in the ILT, thymus and head kidney of Atlantic salmon (Salmo salar L.)","volume":"93","author":"Bj\u00f8rgen","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"2025030418555250700_r7","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1111\/j.1469-7580.2008.00943.x","article-title":"Identification and characterization of a novel intraepithelial lymphoid tissue in the gills of Atlantic salmon","volume":"213","author":"Haugarvoll","year":"2008","journal-title":"J. Anat."},{"key":"2025030418555250700_r8","doi-asserted-by":"crossref","first-page":"3463","DOI":"10.4049\/jimmunol.1400797","article-title":"Transcriptional characterization of the T cell population within the salmonid interbranchial lymphoid tissue","volume":"193","author":"Aas","year":"2014","journal-title":"J. Immunol."},{"key":"2025030418555250700_r9","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.1002\/jmor.20403","article-title":"The interbranchial lymphoid tissue of Atlantic Salmon (Salmo salar L) extends as a diffuse mucosal lymphoid tissue throughout the trailing edge of the gill filament","volume":"276","author":"Dalum","year":"2015","journal-title":"J. Morphol."},{"key":"2025030418555250700_r10","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.fsi.2016.09.013","article-title":"Morphological and functional development of the interbranchial lymphoid tissue (ILT) in Atlantic salmon (Salmo salar L)","volume":"58","author":"Dalum","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"2025030418555250700_r11","doi-asserted-by":"crossref","first-page":"195","DOI":"10.3382\/ps.0580195","article-title":"Structure of the germinal centers in the chicken caecal tonsil: light and electron microscopic and autoradiographic studies","volume":"58","author":"Ol\u00e1h","year":"1979","journal-title":"Poult. Sci."},{"key":"2025030418555250700_r12","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/1742-9994-9-21","article-title":"Evidence of a true pharyngeal tonsil in birds: a novel lymphoid organ in Dromaius novaehollandiae and Struthio camelus (Palaeognathae)","volume":"9","author":"Crole","year":"2012","journal-title":"Front. Zool."},{"key":"2025030418555250700_r13","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.dci.2013.04.010","article-title":"Defense genes missing from the flight division","volume":"41","author":"Magor","year":"2013","journal-title":"Dev. Comp. Immunol."},{"key":"2025030418555250700_r14","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1292\/jvms.65.607","article-title":"Development of Peyer\u2019s patch and cecal tonsil in gut-associated lymphoid tissues in the chicken embryo","volume":"65","author":"Kajiwara","year":"2003","journal-title":"J. Vet. Med. Sci."},{"key":"2025030418555250700_r15","doi-asserted-by":"crossref","first-page":"2695","DOI":"10.4049\/jimmunol.1600799","article-title":"Characterization of lamprey BAFF-like gene: evolutionary implications","volume":"197","author":"Das","year":"2016","journal-title":"J. Immunol."},{"key":"2025030418555250700_r16","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S1074-7613(00)80588-9","article-title":"The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues","volume":"9","author":"F\u00fctterer","year":"1998","journal-title":"Immunity"},{"key":"2025030418555250700_r17","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/S1359-6101(03)00022-4","article-title":"Biological functions of tumor necrosis factor cytokines and their receptors","volume":"14","author":"Pfeffer","year":"2003","journal-title":"Cytokine Growth Factor Rev."},{"key":"2025030418555250700_r18","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1126\/science.8171322","article-title":"Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin","volume":"264","author":"De Togni","year":"1994","journal-title":"Science"},{"key":"2025030418555250700_r19","doi-asserted-by":"crossref","first-page":"1685","DOI":"10.4049\/jimmunol.155.4.1685","article-title":"Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness","volume":"155","author":"Banks","year":"1995","journal-title":"J. Immunol."},{"key":"2025030418555250700_r20","doi-asserted-by":"crossref","first-page":"6319","DOI":"10.1073\/pnas.94.12.6319","article-title":"Peyer\u2019s patch organogenesis is intact yet formation of B lymphocyte follicles is defective in peripheral lymphoid organs of mice deficient for tumor necrosis factor and its 55-kDa receptor","volume":"94","author":"Pasparakis","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030418555250700_r21","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1084\/jem.184.1.259","article-title":"Defective Peyer\u2019s patch organogenesis in mice lacking the 55-kD receptor for tumor necrosis factor","volume":"184","author":"Neumann","year":"1996","journal-title":"J. Exp. Med."},{"key":"2025030418555250700_r22","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1016\/j.dci.2011.03.031","article-title":"Origin and evolution of TNF and TNF receptor superfamilies","volume":"35","author":"Wiens","year":"2011","journal-title":"Dev. Comp. Immunol."},{"key":"2025030418555250700_r23","doi-asserted-by":"crossref","first-page":"1637","DOI":"10.1006\/rwei.1999.0418","volume-title":"Encyclopedia of Immunology.","author":"Cuff","year":"1998"},{"key":"2025030418555250700_r24","doi-asserted-by":"crossref","first-page":"4214","DOI":"10.1128\/MCB.01751-05","article-title":"Novel lymphotoxin alpha (LTalpha) knockout mice with unperturbed tumor necrosis factor expression: reassessing LTalpha biological functions","volume":"26","author":"Liepinsh","year":"2006","journal-title":"Mol. Cell. Biol."},{"key":"2025030418555250700_r25","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/S0002-9440(10)62239-0","article-title":"Lymphotoxin plays a crucial role in the development and function of nasal-associated lymphoid tissue through regulation of chemokines and peripheral node addressin","volume":"166","author":"Ying","year":"2005","journal-title":"Am. J. Pathol."},{"key":"2025030418555250700_r26","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.cytogfr.2014.02.001","article-title":"Lymphotoxin and TNF: how it all began-a tribute to the travelers","volume":"25","author":"Ruddle","year":"2014","journal-title":"Cytokine Growth Factor Rev."},{"key":"2025030418555250700_r27","doi-asserted-by":"crossref","first-page":"3456","DOI":"10.1182\/blood-2009-10-249177","article-title":"Cellular source and molecular form of TNF specify its distinct functions in organization of secondary lymphoid organs","volume":"116","author":"Tumanov","year":"2010","journal-title":"Blood"},{"key":"2025030418555250700_r28","doi-asserted-by":"crossref","first-page":"1585","DOI":"10.1084\/jem.186.9.1585","article-title":"Critical points of tumor necrosis factor action in central nervous system autoimmune inflammation defined by gene targeting","volume":"186","author":"K\u00f6rner","year":"1997","journal-title":"J. Exp. Med."},{"key":"2025030418555250700_r29","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1002\/eji.200526119","article-title":"Novel tumor necrosis factor-knockout mice that lack Peyer\u2019s patches","volume":"35","author":"Kuprash","year":"2005","journal-title":"Eur. J. Immunol."},{"key":"2025030418555250700_r30","doi-asserted-by":"crossref","first-page":"7955","DOI":"10.4049\/jimmunol.178.12.7955","article-title":"Early diversification of the TNF superfamily in teleosts: genomic characterization and expression analysis","volume":"178","author":"Glenney","year":"2007","journal-title":"J. Immunol."},{"key":"2025030418555250700_r31","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.it.2010.01.003","article-title":"B-cells need a proper house, whereas T-cells are happy in a cave: the dependence of lymphocytes on secondary lymphoid tissues during evolution","volume":"31","author":"Hofmann","year":"2010","journal-title":"Trends Immunol."},{"key":"2025030418555250700_r32","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1080\/03079457.2012.735359","article-title":"The long view: a bright past, a brighter future? Forty years of chicken immunology pre- and post-genome","volume":"41","author":"Kaiser","year":"2012","journal-title":"Avian Pathol."},{"key":"2025030418555250700_r33","volume-title":"SRA Knowledge Base.","author":"Sequence Read Archive Submissions Staff","year":"2011"},{"key":"2025030418555250700_r34","author":"Andrews","year":"2010"},{"key":"2025030418555250700_r35","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2025030418555250700_r36","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nbt.1883","article-title":"Full-length transcriptome assembly from RNA-seq data without a reference genome","volume":"29","author":"Grabherr","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"2025030418555250700_r37","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/nprot.2013.084","article-title":"De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis","volume":"8","author":"Haas","year":"2013","journal-title":"Nat. Protoc."},{"key":"2025030418555250700_r38","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2025030418555250700_r39","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The sequence alignment\/map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2025030418555250700_r40","doi-asserted-by":"crossref","first-page":"D754","DOI":"10.1093\/nar\/gkx1098","article-title":"Ensembl 2018","volume":"46","author":"Zerbino","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2025030418555250700_r41","doi-asserted-by":"crossref","first-page":"D279","DOI":"10.1093\/nar\/gkv1344","article-title":"The Pfam protein families database: towards a more sustainable future","volume":"44","author":"Finn","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"2025030418555250700_r42","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: improvements in performance and usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"2025030418555250700_r43","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"2025030418555250700_r44","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"2025030418555250700_r45","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-4939-6783-4_1","article-title":"Protein bioinformatics databases and resources","volume":"1558","author":"Chen","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"2025030418555250700_r46","author":"Oliveros","year":"2015"},{"key":"2025030418555250700_r47","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang D.","year":"2009","journal-title":"Nat. Protoc."},{"key":"2025030418555250700_r48","volume-title":"R: A Language and Environment for Statistical Computing.","author":"R Core Team","year":"2017"},{"key":"2025030418555250700_r49","article-title":"Peyer\u2019s patches: the immune sensors of the intestine","volume":"2010","author":"Jung","year":"2010","journal-title":"Int. J. Inflamm."},{"key":"2025030418555250700_r50","doi-asserted-by":"crossref","first-page":"50","DOI":"10.3844\/ajavsp.2007.50.54","article-title":"Histological study of the caecal tonsil in the cecum of 4- 6 months of age white leghorn chicks","volume":"2","author":"Rezaian","year":"2007","journal-title":"Am. J. Anim. Vet. Sci."},{"key":"2025030418555250700_r51","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1046\/j.1365-3083.2002.01116.x","article-title":"The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic cell immigration and T-cell zone formation during ontogeny of the spleen","volume":"56","author":"Rumfelt","year":"2002","journal-title":"Scand. J. Immunol."},{"key":"2025030418555250700_r52","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/S0968-0004(01)01995-8","article-title":"The molecular architecture of the TNF superfamily","volume":"27","author":"Bodmer","year":"2002","journal-title":"Trends Biochem. Sci."},{"key":"2025030418555250700_r53","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/S1471-4906(03)00166-2","article-title":"A co-evolution perspective of the TNFSF and TNFRSF families in the immune system","volume":"24","author":"Collette","year":"2003","journal-title":"Trends Immunol."},{"key":"2025030418555250700_r54","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1089\/jir.2005.25.467","article-title":"A genomic analysis of chicken cytokines and chemokines","volume":"25","author":"Kaiser","year":"2005","journal-title":"J. Interferon Cytokine Res."},{"key":"2025030418555250700_r55","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.1000475","article-title":"Multi-platform next-generation sequencing of the domestic Turkey (Meleagris gallopavo): genome assembly and analysis","volume":"8","author":"Dalloul","year":"2010","journal-title":"PLoS Biol."},{"key":"2025030418555250700_r56","doi-asserted-by":"crossref","DOI":"10.1128\/microbiolspec.MCHD-0007-2015","article-title":"Evolution of myeloid cells","author":"Barreda","year":"2016","journal-title":"Microbiol. Spectr."},{"key":"2025030418555250700_r57","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/S0168-9525(03)00056-8","article-title":"Predicting gene function by conserved co-expression","volume":"19","author":"van Noort","year":"2003","journal-title":"Trends Genet."},{"key":"2025030418555250700_r58","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1093\/protein\/12.2.85","article-title":"Twilight zone of protein sequence alignments","volume":"12","author":"Rost","year":"1999","journal-title":"Protein Eng."},{"key":"2025030418555250700_r59","doi-asserted-by":"crossref","first-page":"202","DOI":"10.4049\/jimmunol.1700900","article-title":"Original ligand for LT\u03b2R is LIGHT: insight into evolution of the LT\/LT \u03b2R system","volume":"201","author":"Maeda","year":"2018","journal-title":"J. Immunol."},{"key":"2025030418555250700_r60","doi-asserted-by":"crossref","first-page":"5475","DOI":"10.4049\/jimmunol.170.11.5475","article-title":"Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function","volume":"170","author":"Lorenz","year":"2003","journal-title":"J. Immunol."},{"key":"2025030418555250700_r61","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1038\/ni1330","article-title":"Lymphoid organ development: from ontogeny to neogenesis","volume":"7","author":"Drayton","year":"2006","journal-title":"Nat. Immunol."},{"key":"2025030418555250700_r62","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1146\/annurev-immunol-032713-120252","article-title":"Stromal cells in chronic inflammation and tertiary lymphoid organ formation","volume":"33","author":"Buckley","year":"2015","journal-title":"Annu. Rev. Immunol."},{"key":"2025030418555250700_r63","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1038\/nri2832","article-title":"New insights into the development of lymphoid tissues","volume":"10","author":"van de Pavert","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"2025030418555250700_r64","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3389\/fimmu.2017.00045","article-title":"High endothelial venules and other blood vessels: critical regulators of lymphoid organ development and function","volume":"8","author":"Ager","year":"2017","journal-title":"Front. Immunol."},{"key":"2025030418555250700_r65","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1016\/S0959-437X(00)00233-1","article-title":"Formation of Peyer\u2019s patches","volume":"11","author":"Finke","year":"2001","journal-title":"Curr. Opin. Genet. Dev."},{"key":"2025030418555250700_r66","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1038\/ni.1789","article-title":"Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation","volume":"10","author":"van de Pavert","year":"2009","journal-title":"Nat. Immunol."},{"key":"2025030418555250700_r67","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1365-2567.2005.02143.x","article-title":"The intriguing biology of the tumour necrosis factor\/tumour necrosis factor receptor superfamily: players, rules and the games","volume":"115","author":"Hehlgans","year":"2005","journal-title":"Immunology"},{"key":"2025030418555250700_r68","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.cytogfr.2013.12.007","article-title":"Lymphotoxin organizes contributions to host defense and metabolic illness from innate lymphoid cells","volume":"25","author":"Upadhyay","year":"2014","journal-title":"Cytokine Growth Factor Rev."},{"key":"2025030418555250700_r69","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1016\/j.it.2018.08.003","article-title":"A fresh view on lymph node organogenesis","volume":"39","author":"Onder","year":"2018","journal-title":"Trends Immunol."},{"key":"2025030418555250700_r70","doi-asserted-by":"crossref","first-page":"1997","DOI":"10.1084\/jem.186.12.1997","article-title":"Distinct roles of lymphotoxin \u03b1 and the type I tumor necrosis factor (TNF) receptor in the establishment of follicular dendritic cells from non-bone marrow-derived cells","volume":"186","author":"Matsumoto","year":"1997","journal-title":"J. Exp. Med."},{"key":"2025030418555250700_r71","doi-asserted-by":"crossref","first-page":"2173","DOI":"10.1182\/blood-2009-12-256065","article-title":"Lymphotoxin-alpha contributes to lymphangiogenesis","volume":"116","author":"Mounzer","year":"2010","journal-title":"Blood"},{"key":"2025030418555250700_r72","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/nri3406","article-title":"Lymphotoxin signalling in immune homeostasis and the control of microorganisms","volume":"13","author":"Upadhyay","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"2025030418555250700_r73","first-page":"139","article-title":"A Drosophila homolog of human proto-oncogene ret transiently expressed in embryonic neuronal precursor cells including neuroblasts and CNS cells","volume-title":"Mech. Dev.","author":"Sugaya","year":"1994"},{"key":"2025030418555250700_r74","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.05491.018","article-title":"The Ret receptor regulates sensory neuron dendrite growth and integrin mediated adhesion","author":"Soba","year":"2015","journal-title":"eLife."},{"key":"2025030418555250700_r75","doi-asserted-by":"crossref","first-page":"3029","DOI":"10.15252\/embj.201696247","article-title":"Ret receptor tyrosine kinase sustains proliferation and tissue maturation in intestinal epithelia","volume":"36","author":"Perea","year":"2017","journal-title":"EMBO J."},{"key":"2025030418555250700_r76","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1038\/nature18644","article-title":"Glial-cell-derived neuroregulators control type 3 innate lymphoid cells and gut defence","volume":"535","author":"Ibiza","year":"2016","journal-title":"Nature"},{"key":"2025030418555250700_r77","doi-asserted-by":"crossref","first-page":"2610","DOI":"10.4049\/jimmunol.0801141","article-title":"Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses","volume":"182","author":"Velaga","year":"2009","journal-title":"J. Immunol."},{"key":"2025030418555250700_r78","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0055224","article-title":"Loss of function of the mouse sharpin gene results in Peyer\u2019s patch regression","volume":"8","author":"Seymour","year":"2013","journal-title":"PLoS One"},{"key":"2025030418555250700_r79","doi-asserted-by":"crossref","first-page":"28372","DOI":"10.1074\/jbc.C200324200","article-title":"Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling","volume":"277","author":"Kanda","year":"2002","journal-title":"J. Biol. Chem."},{"key":"2025030418555250700_r80","doi-asserted-by":"crossref","first-page":"3009","DOI":"10.1093\/emboj\/cdf306","article-title":"Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway","volume":"21","author":"Igaki","year":"2002","journal-title":"EMBO J."},{"key":"2025030418555250700_r81","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1146\/annurev-animal-030117-014821","article-title":"The divergent genomes of teleosts","volume":"6","author":"Ravi","year":"2018","journal-title":"Annu. Rev. Anim. Biosci."},{"key":"2025030418555250700_r82","doi-asserted-by":"crossref","DOI":"10.1126\/sciimmunol.aau5265","article-title":"Single-cell transcriptional analysis reveals ILC-like cells in zebrafish","volume":"3","author":"Hern\u00e1ndez","year":"2018","journal-title":"Sci. Immunol."},{"key":"2025030418555250700_r83","doi-asserted-by":"crossref","first-page":"5959","DOI":"10.4049\/jimmunol.1301584","article-title":"Two types of TNF-\u03b1 exist in teleost fish: phylogeny, expression, and bioactivity analysis of type-II TNF-\u03b13 in rainbow trout Oncorhynchus mykiss","volume":"191","author":"Hong","year":"2013","journal-title":"J. Immunol."},{"key":"2025030418555250700_r84","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1111\/j.1469-7580.2007.00766.x","article-title":"Pyloric tonsil as a novel gut-associated lymphoepithelial organ of the chicken","volume":"211","author":"Nagy","year":"2007","journal-title":"J. Anat."},{"key":"2025030418555250700_r85","doi-asserted-by":"crossref","first-page":"16647","DOI":"10.1073\/pnas.0808800105","article-title":"Evolutionary redefinition of immunoglobulin light chain isotypes in tetrapods using molecular markers","volume":"105","author":"Das","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030418555250700_r86","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1093\/molbev\/msp212","article-title":"Analysis of the immunoglobulin light chain genes in zebra finch: evolutionary implications","volume":"27","author":"Das","year":"2010","journal-title":"Mol. Biol. Evol."},{"key":"2025030418555250700_r87","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s12862-018-1135-z","article-title":"The curious case of peroxiredoxin-5: what its absence in aves can tell us and how it can be used","volume":"18","author":"Pirson","year":"2018","journal-title":"BMC Evol. Biol."},{"key":"2025030418555250700_r88","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.jneuroim.2005.10.017","article-title":"Neural-immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems","volume":"172","author":"Wrona","year":"2006","journal-title":"J. Neuroimmunol."},{"key":"2025030418555250700_r89","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1003433","article-title":"Role of the nervous system in the control of proteostasis during innate immune activation: insights from C. elegans","volume":"9","author":"Aballay","year":"2013","journal-title":"PLoS Pathog."},{"key":"2025030418555250700_r90","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.immuni.2017.11.020","article-title":"Oxysterol sensing through the receptor GPR183 promotes the lymphoid-tissue-inducing function of innate lymphoid cells and colonic inflammation","volume":"48","author":"Emg\u00e5rd","year":"2018","journal-title":"Immunity"},{"key":"2025030418555250700_r91","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.jneuroim.2005.09.011","article-title":"The role of nicotinic acetylcholine receptors in lymphocyte development","volume":"171","author":"Skok","year":"2006","journal-title":"J. Neuroimmunol."},{"key":"2025030418555250700_r92","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0042959","article-title":"Different subtypes of GABA-A receptors are expressed in human, mouse and rat T lymphocytes","volume":"7","author":"Mendu","year":"2012","journal-title":"PLoS One"},{"key":"2025030418555250700_r93","doi-asserted-by":"crossref","first-page":"2156","DOI":"10.1073\/pnas.0308051100","article-title":"The mouse olfactory receptor gene family","volume":"101","author":"Godfrey","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030418555250700_r94","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1186\/1471-2164-7-121","article-title":"Widespread ectopic expression of olfactory receptor genes","volume":"7","author":"Feldmesser","year":"2006","journal-title":"BMC Genomics"},{"key":"2025030418555250700_r95","first-page":"1739","article-title":"Human olfactory receptors: novel cellular functions outside of the nose","volume-title":"Physiol. Rev.","author":"Ma\u00dfberg","year":"2018"},{"key":"2025030418555250700_r96","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1039\/C2MB25429H","article-title":"Non-traditional roles of G protein-coupled receptors in basic cell biology","volume":"9","author":"Zhang","year":"2013","journal-title":"Mol. Biosyst."},{"key":"2025030418555250700_r97","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/exd.13132","article-title":"Two olfactory receptors-OR2A4\/7 and OR51B5-differentially affect epidermal proliferation and differentiation","volume":"26","author":"Tsai","year":"2017","journal-title":"Exp. Dermatol."},{"key":"2025030418555250700_r98","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1189\/jlb.1A0914-425RR","article-title":"Odorants specifically modulate chemotaxis and tissue retention of CD4+ T cells via cyclic adenosine monophosphate induction","volume":"100","author":"Clark","year":"2016","journal-title":"J. Leukoc. Biol."},{"key":"2025030418555250700_r99","article-title":"Activation of olfactory receptors on mouse pulmonary macrophages promotes monocyte chemotactic protein-1 production","volume":"8","author":"Li","year":"2013","journal-title":"PLoS One"},{"key":"2025030418555250700_r100","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1007\/978-3-540-69828-9_12","article-title":"Bgee: integrating and comparing heterogeneous transcriptome data among species","volume":"5109","author":"Bastian","year":"2008","journal-title":"Lect. Notes Comput. Sci."},{"key":"2025030418555250700_r101","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1136\/gut.51.3.392","article-title":"Regression of Peyer\u2019s patches in G \u03b1 i2 deficient mice prior to colitis is associated with reduced expression of Bcl-2 and increased apoptosis","volume":"51","author":"\u00d6hman","year":"2002","journal-title":"Gut"}],"container-title":["The Journal of Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/204\/10\/2697\/61359335\/ji1901059.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/204\/10\/2697\/61359335\/ji1901059.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,4]],"date-time":"2025-03-04T20:52:35Z","timestamp":1741121555000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jimmunol\/article\/204\/10\/2697\/7943799"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5]]},"references-count":101,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2020,5,15]]}},"URL":"https:\/\/doi.org\/10.4049\/jimmunol.1901059","relation":{},"ISSN":["0022-1767","1550-6606"],"issn-type":[{"value":"0022-1767","type":"print"},{"value":"1550-6606","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,5]]},"published":{"date-parts":[[2020,5]]}}}