{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T06:03:09Z","timestamp":1778565789622,"version":"3.51.4"},"reference-count":75,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,3,25]],"date-time":"2021-03-25T00:00:00Z","timestamp":1616630400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>In jawed vertebrates, adaptive immune responses are enabled by T cells. Two lineages were characterized based on their T cell receptor (TcR) heterodimers, namely \u03b1\u03b2 or \u03b3\u03b4 peptide chains, which display an Ig domain-type sequence that is somatically rearranged. \u03b3\u03b4 T cells have been less extensively characterized than \u03b1\u03b2 and teleost fish, in particular, suffer from a severe scarcity of data. In this paper, we worked on the well-known model, the European sea bass Dicentrarchus labrax, to broaden the understanding of teleost \u03b3\u03b4-T cells. The T cell receptor chain (TR) \u03b3 transcript was expressed at a later developmental stage than TR\u03b2, suggesting a layered appearance of fish immune cells, and the thymus displayed statistically-significant higher mRNA levels than any other organ or lymphoid tissue investigated. The polyclonal antibody developed against the TR\u03b3 allowed the localization of TR\u03b3-expressing cells in lymphoid organs along the ontogeny. Cell positivity was investigated through flow cytometry and the highest percentage was found in peripheral blood leukocytes, followed by thymus, gut, gills, spleen and head kidney. Numerous TR\u03b3-expressing cells were localized in the gut mucosa, and the immunogold labelling revealed ultrastructural features that are typical of T cells. At last, microalgae-based diet formulations significantly modulated the abundance of TR\u03b3+ cells in the posterior intestine, hinting at a putative involvement in nutritional immunity. From a comparative immunological perspective, our results contribute to the comprehension of the diversity and functionalities of \u03b3\u03b4 T cells during the development of a commercially relevant marine teleost model.<\/jats:p>","DOI":"10.3390\/ijms22073376","type":"journal-article","created":{"date-parts":[[2021,3,25]],"date-time":"2021-03-25T14:51:12Z","timestamp":1616683872000},"page":"3376","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Molecular, Cellular and Functional Analysis of TR\u03b3 Chain along the European Sea Bass Dicentrarchus labrax Development"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4545-7229","authenticated-orcid":false,"given":"Andrea","family":"Miccoli","sequence":"first","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laura","family":"Guerra","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Valeria","family":"Pianese","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3225-0536","authenticated-orcid":false,"given":"Paolo Roberto","family":"Saraceni","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8045-5651","authenticated-orcid":false,"given":"Francesco","family":"Buonocore","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna Rita","family":"Taddei","sequence":"additional","affiliation":[{"name":"Section of Electron Microscopy, Great Equipment Center, University of Tuscia, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ana","family":"Couto","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Av. General Norton de Matos, 4450-208 Matosinhos, Portugal"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tania","family":"De Wolf","sequence":"additional","affiliation":[{"name":"INVE Aquaculture Research Center, 57016 Rosignano Solvay, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna Maria","family":"Fausto","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9730-9394","authenticated-orcid":false,"given":"Giuseppe","family":"Scapigliati","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6116-213X","authenticated-orcid":false,"given":"Simona","family":"Picchietti","sequence":"additional","affiliation":[{"name":"Department for Innovation in Biological, Agro-Food and Forest Systems, University of Tuscia, Largo dell\u2019Universit\u00e0, 01100 Viterbo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,3,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"17576","DOI":"10.1073\/pnas.1420936111","article-title":"Molecular Architecture of the A\u03b2 T Cell Receptor\u2013CD3 Complex","volume":"111","author":"Birnbaum","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1073\/pnas.91.3.1094","article-title":"Identification of T-Cell Receptor Alpha-Chain Genes in the Chicken","volume":"91","author":"Gobel","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s002510050198","article-title":"Structure and Diversity of the T-Cell Receptor \u03b1 Chain in the Mexican Axolotl","volume":"45","author":"Fellah","year":"1997","journal-title":"Immunogenetics"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"19991","DOI":"10.1073\/pnas.1010166107","article-title":"Identification of the Pre-T-Cell Receptor Chain in Nonmammalian Vertebrates Challenges the Structure-Function of the Molecule","volume":"107","author":"Smelty","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1016\/S0161-5890(98)00037-6","article-title":"T-Cell Receptors in Channel Catfish: Structure and Expression of TCR \u03b1 and \u03b2 Genes","volume":"35","author":"Wilson","year":"1998","journal-title":"Mol. Immunol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"9248","DOI":"10.1073\/pnas.91.20.9248","article-title":"T-Cell Receptor Gene Homologs Are Present in the Most Primitive Jawed Vertebrates","volume":"91","author":"Rast","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1006\/fsim.1999.0243","article-title":"Immunopurification of T-Cells from Sea Bass Dicentrarchus labrax (L.)","volume":"10","author":"Scapigliati","year":"2000","journal-title":"Fish Shellfish Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3081","DOI":"10.4049\/jimmunol.170.6.3081","article-title":"The Four TCR Genes of Teleost Fish: The CDNA and Genomic DNA Analysis of Japanese Flounder (Paralichthys olivaceus) TCR \u03b1-, \u03b2-, \u03b3-, and \u03b4-Chains","volume":"170","author":"Nam","year":"2003","journal-title":"J. Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.fsi.2007.12.007","article-title":"Molecular Cloning and Characterization of Common Carp (Cyprinus carpio L.) TCR\u03b3 and CD3\u03b3\/\u03b4 Chains","volume":"24","author":"Shang","year":"2008","journal-title":"Fish Shellfish Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Yazawa, R., Cooper, G.A., Beetz-Sargent, M., Robb, A., McKinnel, L., Davidson, W.S., and Koop, B.F. (2008). Functional Adaptive Diversity of the Atlantic Salmon T-Cell Receptor Gamma Locus. Mol. Immunol.","DOI":"10.1016\/j.molimm.2007.12.007"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Buonocore, F., Castro, R., Randelli, E., Lefranc, M.-P., Six, A., Kuhl, H., Reinhardt, R., Facchiano, A., Boudinot, P., and Scapigliati, G. (2012). Diversity, Molecular Characterization and Expression of T Cell Receptor \u03b3 in a Teleost Fish, the Sea Bass (Dicentrarchus labrax, L.). PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0047957"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1007\/s00251-014-0793-2","article-title":"Identification and Characterization of TCR\u03b3 and TCR\u03b4 Chains in Channel Catfish, Ictalurus punctatus","volume":"66","author":"Moulana","year":"2014","journal-title":"Immunogenetics"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1111\/jfd.12042","article-title":"Complementary DNA Sequences of the Constant Regions of T-Cell Antigen Receptors \u03b1, \u03b2 and \u03b3 in Mandarin Fish, Siniperca chuatsi Basilewsky, and Their Transcriptional Changes after Stimulation with Flavobacterium columnare","volume":"37","author":"Tian","year":"2014","journal-title":"J. Fish Dis."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Wan, F., Hu, C., Ma, J., Gao, K., Xiang, L., and Shao, J. (2017). Characterization of \u0393\u03b4 T Cells from Zebrafish Provides Insights into Their Important Role in Adaptive Humoral Immunity. Front. Immunol., 7.","DOI":"10.3389\/fimmu.2016.00675"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.fsi.2018.11.045","article-title":"Molecular Characterization and Expression Analysis of T Cell Receptor (TCR) \u03b3 and \u03b4 Genes in Dojo Loach (Misgurnus anguillicaudatus) in Response to Bacterial, Parasitic and Fungal Challenge","volume":"86","author":"Luo","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.fsi.2010.10.001","article-title":"Transcription of T Cell-Related Genes in Teleost Fish, and the European Sea Bass (Dicentrarchus labrax) as a Model","volume":"31","author":"Boschi","year":"2011","journal-title":"Fish Shellfish Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"329","DOI":"10.12717\/DR.2013.17.4.329","article-title":"Stage and Tissue Specific Expression of Four TCR Subunits in Olive Flounder (Paralichthys olivaceus)","volume":"17","author":"Lee","year":"2013","journal-title":"Dev. Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"James, K.D., Jenkinson, W.E., and Anderson, G. (2018). T-Cell Egress from the Thymus: Should I Stay or Should I Go?. J. Leukoc. Biol.","DOI":"10.1002\/JLB.1MR1217-496R"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.4049\/jimmunol.167.3.1325","article-title":"Heterogeneity of Channel Catfish CTL with Respect to Target Recognition and Cytotoxic Mechanisms Employed","volume":"167","author":"Zhou","year":"2001","journal-title":"J. Immunol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1146\/annurev.immunol.18.1.975","article-title":"\u0393\u03b4 Cells: A Right Time and a Right Place for a Conserved Third Way of Protection","volume":"18","author":"Hayday","year":"2000","journal-title":"Annu. Rev. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1038\/ni.2665","article-title":"Butyrophilin 3A1 Binds Phosphorylated Antigens and Stimulates Human \u0393\u03b4 T Cells","volume":"14","author":"Vavassori","year":"2013","journal-title":"Nat. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1038\/nm0798-764","article-title":"The \u0393\u03b4 T-Cell Bridge: Linking Innate and Acquired Immunity","volume":"4","author":"Mak","year":"1998","journal-title":"Nat. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fimmu.2018.00971","article-title":"Fish Lymphocytes: An Evolutionary Equivalent of Mammalian Innate-like Lymphocytes?","volume":"9","author":"Scapigliati","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.biotechadv.2006.11.002","article-title":"Micro-Algae as a Source of Protein","volume":"25","author":"Becker","year":"2007","journal-title":"Biotechnol. Adv."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Burnell, G., and Allan, G.L. (2009). New Technologies in Aquaculture: Improving Production Efficiency, Quality and Environmental Management, Woodhead Publishing.","DOI":"10.1533\/9781845696474"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Nakagawa, H., Sato, M., and Gatlin, D. (2007). Algae. Dietary Supplements for the Health and Quality of Cultured Fish, CABI Publishing.","DOI":"10.1079\/9781845931995.0000"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Dawood, M.A.O. (2020). Nutritional Immunity of Fish Intestines: Important Insights for Sustainable Aquaculture. Rev. Aquac., 1\u201322.","DOI":"10.1111\/raq.12492"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1007\/s10695-012-9670-9","article-title":"Enrichment of Gilthead Seabream (Sparus aurata L.) Diet with Microalgae: Effects on the Immune System","volume":"38","author":"Cerezuela","year":"2012","journal-title":"Fish Physiol. Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Picchietti, S., Buonocore, F., Guerra, L., Belardinelli, M.C., De Wolf, T., Couto, A., Fausto, A.M., Saraceni, P.R., Miccoli, A., and Scapigliati, G. (2021). Molecular and Cellular Characterization of European Sea Bass CD3\u03b5+ T Lymphocytes and Their Modulation by Microalgal Feed Supplementation. Cell Tissue Res.","DOI":"10.1007\/s00441-020-03347-x"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Gustafsson, K., Herrmann, T., and Dieli, F. (2020). Editorial: Understanding Gamma Delta T Cell Multifunctionality-Towards Immunotherapeutic Applications. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.00921"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/nrg2703","article-title":"Origin and Evolution of the Adaptive Immune System: Genetic Events and Selective Pressures","volume":"11","author":"Flajnik","year":"2010","journal-title":"Nat. Rev. Genet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1038\/nri2807","article-title":"The Origins of Vertebrate Adaptive Immunity","volume":"10","author":"Litman","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S1074-7613(00)80237-X","article-title":"A, \u0392, \u0393, and \u0394 T Cell Antigen Receptor Genes Arose Early in Vertebrate Phylogeny","volume":"6","author":"Rast","year":"1997","journal-title":"Immunity"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"9776","DOI":"10.1073\/pnas.0609106104","article-title":"A Unique T Cell Receptor Discovered in Marsupials","volume":"104","author":"Parra","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Parra, Z.E., Baker, M.L., Hathaway, J., Lopez, A.M., Trujillo, J., Sharp, A., and Miller, R.D. (2008). Comparative Genomic Analysis and Evolution of the T Cell Receptor Loci in the Opossum Monodelphis domestica. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-111"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5246","DOI":"10.4049\/jimmunol.1101113","article-title":"Platypus TCR \u03bc Provides Insight into the Origins and Evolution of a Uniquely Mammalian TCR Locus","volume":"187","author":"Wang","year":"2011","journal-title":"J. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"R1060","DOI":"10.1016\/j.cub.2014.09.070","article-title":"Re-Evaluation of the Immunological Big Bang","volume":"24","author":"Flajnik","year":"2014","journal-title":"Curr. Biol."},{"key":"ref_38","first-page":"219","article-title":"T cell antigen receptors","volume":"Volume 2","author":"Paul","year":"1982","journal-title":"Anticancer Research"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nri3384","article-title":"Six-of-the-Best: Unique Contributions of \u0393\u03b4 T Cells to Immunology","volume":"13","author":"Vantourout","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.immuni.2009.08.006","article-title":"\u0393\u03b4 T Cells and the Lymphoid Stress-Surveillance Response","volume":"31","author":"Hayday","year":"2009","journal-title":"Immunity"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/cmi.2012.44","article-title":"Defining the Nature of Human \u0393\u03b4 T Cells: A Biographical Sketch of the Highly Empathetic","volume":"10","author":"Kalyan","year":"2013","journal-title":"Cell. Mol. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"311","DOI":"10.4049\/jimmunol.1800934","article-title":"\u0393\u03b4 T Cell Update: Adaptate Orchestrators of Immune Surveillance","volume":"203","author":"Hayday","year":"2019","journal-title":"J. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Johnson, M.D., Witherden, D.A., and Havran, W.L. (2020). The Role of Tissue-Resident \u0393\u03b4 T Cells in Stress Surveillance and Tissue Maintenance. Cells, 9.","DOI":"10.3390\/cells9030686"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"486","DOI":"10.17221\/3294-VETMED","article-title":"Innate and Adaptive Immunity in Teleost Fish: A Review","volume":"56","author":"Uribe","year":"2011","journal-title":"Vet. Med. (Praha)"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/j.fsi.2005.02.003","article-title":"Development and Function of the Thymus in Teleosts","volume":"19","author":"Bowden","year":"2005","journal-title":"Fish Shellfish Immunol."},{"key":"ref_46","unstructured":"Argano, R. (1994). Histology of developing thymus in sea bass Dicentrarchus labrax (L.). Contributions to Animal Biology, Halocynthia Association."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1006\/fsim.1996.0047","article-title":"Immunocytochemical Detection of Thymocyte Antigenic Determinants in Developing Lymphoid Organs of Sea Bass Dicentrarchus labrax (L.)","volume":"6","author":"Abelli","year":"1996","journal-title":"Fish Shellfish Immunol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/S0145-305X(03)00103-4","article-title":"Development and Maturation of the Immune System in Zebrafish, Danio rerio: A Gene Expression Profiling, in Situ Hybridization and Immunological Study","volume":"28","author":"Lam","year":"2004","journal-title":"Dev. Comp. Immunol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.fsi.2009.04.003","article-title":"Lymphocyte Differentiation in Sea Bass Thymus: CD4 and CD8-\u03b1 Gene Expression Studies","volume":"27","author":"Picchietti","year":"2009","journal-title":"Fish Shellfish Immunol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.dci.2007.04.002","article-title":"Compartmentalisation of T Cells Expressing CD8\u03b1 and TCR\u03b2 in Developing Thymus of Sea Bass Dicentrarchus labrax (L.)","volume":"32","author":"Picchietti","year":"2008","journal-title":"Dev. Comp. Immunol."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Parker, M.E., and Ciofani, M. (2020). Regulation of \u0393\u03b4 T Cell Effector Diversification in the Thymus. Front. Immunol., 11.","DOI":"10.3389\/fimmu.2020.00042"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"154","DOI":"10.4049\/jimmunol.182.1.154","article-title":"TCR\u03bc Recombination and Transcription Relative to the Conventional TCR during Postnatal Development in Opossums","volume":"182","author":"Parra","year":"2009","journal-title":"J. Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.it.2017.01.007","article-title":"Thymic Determinants of \u0393\u03b4 T Cell Differentiation","volume":"38","author":"Sumaria","year":"2017","journal-title":"Trends Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.it.2012.11.004","article-title":"The Natural and the Inducible: Interleukin (IL)-17-Producing \u0393\u03b4 T Cells","volume":"34","author":"Chien","year":"2013","journal-title":"Trends Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/nri2820","article-title":"Determining \u03b3 \u03b4 versus \u03b1 \u03b2 T Cell Development","volume":"10","author":"Ciofani","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1126\/science.1103978","article-title":"Lymphotoxin-Mediated Regulation of \u0393\u03b4 Cell Differentiation by A\u03b2 T Cell Progenitors","volume":"307","author":"Pennington","year":"2005","journal-title":"Science"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"5940","DOI":"10.4049\/jimmunol.181.9.5940","article-title":"Identification of CD25 + \u0393\u03b4 T Cells As Fetal Thymus-Derived Naturally Occurring IL-17 Producers","volume":"181","author":"Shibata","year":"2008","journal-title":"J. Immunol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s41232-019-0095-z","article-title":"T Cell Receptor Signaling for \u0393\u03b4T Cell Development","volume":"39","author":"Muro","year":"2019","journal-title":"Inflamm. Regen."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.fsi.2014.11.012","article-title":"MHC II-\u03b2 Chain Gene Expression Studies Define the Regional Organization of the Thymus in the Developing Bony Fish Dicentrarchus labrax (L.)","volume":"42","author":"Picchietti","year":"2015","journal-title":"Fish Shellfish Immunol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1038\/nri2781","article-title":"\u03b3 \u03b4 T Cell Effector Functions: A Blend of Innate Programming and Acquired Plasticity","volume":"10","author":"Bonneville","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.immuni.2008.04.022","article-title":"Thymic Selection Determines \u0393\u03b4 T Cell Effector Fate: Antigen-Naive Cells Make Interleukin-17 and Antigen-Experienced Cells Make Interferon \u03b3","volume":"29","author":"Jensen","year":"2008","journal-title":"Immunity"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Khairallah, C., Chu, T.H., and Sheridan, B.S. (2018). Tissue Adaptations of Memory and Tissue-Resident Gamma Delta T Cells. Front. Immunol., 9.","DOI":"10.3389\/fimmu.2018.02636"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1006\/fsim.1996.0079","article-title":"Immunohistochemistry of Gut-Associated Lymphoid Tissue of the Sea Bass Dicentrarchus labrax (L.)","volume":"7","author":"Abelli","year":"1997","journal-title":"Fish Shellfish Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1007\/s004290050113","article-title":"Expression of Lymphocyte Antigenic Determinants in Developing Gut-Associated Lymphoid Tissue of the Sea Bass Dicentrarchus labrax (L.)","volume":"196","author":"Picchietti","year":"1997","journal-title":"Anat. Embryol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1016\/j.fsi.2010.12.006","article-title":"Intestinal T Cells of Dicentrarchus labrax (L.): Gene Expression and Functional Studies","volume":"30","author":"Picchietti","year":"2011","journal-title":"Fish Shellfish Immunol."},{"key":"ref_66","first-page":"391","article-title":"Intestinal Lamina Propria TcR\u03b3\u03b4+ Lymphocytes Selectively Express IL-10 and IL-17","volume":"20","author":"Asigbetse","year":"2010","journal-title":"J. Investig. Allergol. Clin. Immunol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.1365-2761.2007.00769.x","article-title":"Response to Soy: T-Cell-like Reactivity in the Intestine of Atlantic Salmon, Salmo Salar L.","volume":"30","author":"Lilleeng","year":"2007","journal-title":"J. Fish Dis."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/j.fsi.2008.10.008","article-title":"Early Treatment with Lactobacillus delbrueckii Strain Induces an Increase in Intestinal T-Cells and Granulocytes and Modulates Immune-Related Genes of Larval Dicentrarchus labrax (L.)","volume":"26","author":"Picchietti","year":"2009","journal-title":"Fish Shellfish Immunol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/jn\/138.1.1","article-title":"Bioactive Food Components That Enhance \u0393\u03b4 T Cell Function May Play a Role in Cancer Prevention","volume":"138","author":"Percival","year":"2008","journal-title":"J. Nutr."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Calduch-Giner, J.A., Sitj\u00e0-Bobadilla, A., and P\u00e9rez-S\u00e1nchez, J. (2016). Gene Expression Profiling Reveals Functional Specialization along the Intestinal Tract of a Carnivorous Teleostean Fish (Dicentrarchus labrax). Front. Physiol., 7.","DOI":"10.3389\/fphys.2016.00359"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1002\/1521-4141(200104)31:4<980::AID-IMMU980>3.0.CO;2-U","article-title":"An Accessory Role of TCR\u03b3\u03b4+ Cells in the Exacerbation of Inflammatory Bowel Disease in TCR\u03b1 Mutant Mice","volume":"31","author":"Shimada","year":"2001","journal-title":"Eur. J. Immunol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.1365-2249.1994.tb06610.x","article-title":"Predominance of T Cell Receptor V\u03b43 in Small Bowel Biopsies from Coeliac Disease Patients","volume":"98","author":"Falk","year":"1994","journal-title":"Clin. Exp. Immunol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2002","DOI":"10.1093\/nar\/29.9.e45","article-title":"A New Mathematical Model for Relative Quantification in Real-Time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Buonocore, F., Gerdol, M., Pallavicini, A., Stocchi, V., Randelli, E., Belardinelli, M.C., Miccoli, A., Saraceni, P.R., Secombes, C.J., and Scapigliati, G. (2020). Identification, Molecular Characterization and Functional Analysis of Interleukin (IL)-2 and IL-2like (IL-2L) Cytokines in Sea Bass (Dicentrarchus labrax L.). Cytokine, 126.","DOI":"10.1016\/j.cyto.2019.154898"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.fsi.2017.02.002","article-title":"Evolution of Lymphocytes. Immunoglobulin T of the Teleost Sea Bass (Dicentrarchus labrax): Quantitation of Gene Expressing and Immunoreactive Cells","volume":"63","author":"Picchietti","year":"2017","journal-title":"Fish Shellfish Immunol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/7\/3376\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:41:01Z","timestamp":1760161261000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/7\/3376"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,25]]},"references-count":75,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["ijms22073376"],"URL":"https:\/\/doi.org\/10.3390\/ijms22073376","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,25]]}}}