{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,12]],"date-time":"2026-11-12T13:36:33Z","timestamp":1794490593728,"version":"4.9.1"},"reference-count":49,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,11,22]],"date-time":"2023-11-22T00:00:00Z","timestamp":1700611200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p>Artificial insemination is a standard practice in the turkey breeder industry to ensure the production of fertile eggs. Even though hens are inseminated on a weekly basis, their fertility tends to decline after a few weeks of production. Avian species have a specialized structures called sperm storage tubules (SSTs), located in the uterovaginal junction (UVJ) of the oviduct. The ability of SSTs to store sperm is directly correlated with the fertility of the hen. The objective of the study was to examine changes in the transcriptome of the turkey hen\u2019s UVJ in response to the presence of sperm at three key stages of production. We hypothesized that repeated and prolonged exposure to sperm would alter the transcriptome of the UVJ. Samples were collected from virgin hens prior to the onset of lay, as well as from sham-inseminated (extender only) and semen-inseminated hens at early lay, peak lay, and late lay. Gene expression profiling of the UVJ was examined, and a differential expression analysis was conducted through pairwise comparisons between semen- and sham-inseminated groups at each production stage and across production stages. In the early laying stage, no significant gene expression changes were found between semen- and sham-inseminated groups. However, at peak lay, genes related to lipid biosynthesis, Wnt signaling, cell proliferation, and O-glycan biosynthesis were upregulated in the semen group, while the immune response and cytokine-cytokine receptor interaction were downregulated. In the late lay stage, the transcription pathway was upregulated in the semen group, whereas the translation pathway was downregulated. The local immune response that was suppressed during peak lay was increased at the late laying stage. In the semen-inseminated group, the UVJ exhibited advanced aging at the late laying stage, evidenced by reduced telomere maintenance and translation processes. The results from this study provide valuable insights into the alteration of the UVJ function in response to the presence of sperm at different stages of production and throughout the production cycle. Targeting the modulation of local immune response and addressing aging processes after peak production could potentially prevent or delay the decline in fertility of turkey breeder hens.<\/jats:p>","DOI":"10.3389\/fphys.2023.1275922","type":"journal-article","created":{"date-parts":[[2023,11,23]],"date-time":"2023-11-23T15:57:57Z","timestamp":1700755077000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Prolonged repeated inseminations trigger a local immune response and accelerate aging of the uterovaginal junction in turkey hens"],"prefix":"10.3389","volume":"14","author":[{"given":"Sunantha","family":"Kosonsiriluk","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kent M.","family":"Reed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sally L.","family":"Noll","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ben W.","family":"Wileman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marissa M.","family":"Studniski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kahina S.","family":"Boukherroub","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,11,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"202274","DOI":"10.1098\/rsos.202274","article-title":"Physiological factors influencing female fertility in birds","volume":"8","author":"Assersohn","year":"2021","journal-title":"R. Soc. Open Sci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1530\/REP-15-0253","article-title":"Mating induces the expression of immune- and pH-regulatory genes in the utero-vaginal junction containing mucosal sperm-storage tubuli of hens","volume":"150","author":"Atikuzzaman","year":"2015","journal-title":"Reproduction"},{"key":"B3","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1530\/jrf.0.0830873","article-title":"Turkey hen fertility and egg production after artificial insemination and multiple oviduct eversion during the pre-laying period","volume":"83","author":"Bakst","year":"1988","journal-title":"J. Reprod. Fertil."},{"key":"B4","doi-asserted-by":"publisher","first-page":"986","DOI":"10.3382\/ps.2009-00481","article-title":"Comparisons of sperm storage tubule distribution and number in 4 strains of mature broiler breeders and in Turkey hens before and after the onset of photostimulation","volume":"89","author":"Bakst","year":"2010","journal-title":"Poult. Sci."},{"key":"B5","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1111\/j.1095-8312.1992.tb00649.x","article-title":"Numbers and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study","volume":"45","author":"Birkhead","year":"1992","journal-title":"Biol. J. Linn. Soc."},{"key":"B6","doi-asserted-by":"publisher","first-page":"101704","DOI":"10.1016\/j.psj.2022.101704","article-title":"Transcriptome analysis of inseminated sperm storage tubules throughout the duration of fertility in the domestic Turkey, Meleagris gallopavo","volume":"101","author":"Brady","year":"2022","journal-title":"Poult. Sci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1095\/biolreprod43.2.271","article-title":"Quantification of spermatozoa in the sperm-storage tubules of Turkey hens and the relation to sperm numbers in the perivitelline layer of eggs","volume":"43","author":"Brillard","year":"1990","journal-title":"Biol. Reprod."},{"key":"B8","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1530\/jrf.0.1140111","article-title":"Physiological responses of hens divergently selected on the number of chicks obtained from a single insemination","volume":"114","author":"Brillard","year":"1998","journal-title":"J. Reprod. Fertil."},{"key":"B9","doi-asserted-by":"publisher","first-page":"2637","DOI":"10.1038\/s41598-022-06700-y","article-title":"Expression of genes and localization of enzymes involved in polyunsaturated fatty acid synthesis in rabbit testis and epididymis","volume":"12","author":"Castellini","year":"2022","journal-title":"Sci. Rep."},{"key":"B10","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1530\/rep.1.01177","article-title":"Expression of transforming growth factor-\u03b2 isoforms and their receptors in utero-vaginal junction of hen oviduct in presence or absence of resident sperm with reference to sperm storage","volume":"132","author":"Das","year":"2006","journal-title":"Reproduction"},{"key":"B11","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1530\/REP-08-0175","article-title":"Changes in the expression of interleukin-1beta and lipopolysaccharide-induced TNF factor in the oviduct of laying hens in response to artificial insemination","volume":"137","author":"Das","year":"2009","journal-title":"Reproduction"},{"key":"B12","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1262\/jrd.17027","article-title":"Changes in the localization of antigen presenting cells and T cells in the utero-vaginal junction after repeated artificial insemination in laying hens","volume":"51","author":"Das","year":"2005","journal-title":"J. Reprod. Dev."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1393392","DOI":"10.1155\/2022\/1393392","article-title":"Advanced practical strategies to enhance table egg production","volume":"2022","author":"El-Sabrout","year":"2022","journal-title":"Sci. (Cairo)"},{"key":"B14","doi-asserted-by":"publisher","first-page":"1539","DOI":"10.3382\/ps.2010-01159","article-title":"Oviductal expression of avidin, avidin-related protein-2, and progesterone receptor in Turkey hens in relation to sperm storage: effects of oviduct tissue type, sperm presence, and Turkey line","volume":"90","author":"Foye-Jackson","year":"2011","journal-title":"Poult. Sci."},{"key":"B15","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1186\/s12859-018-2486-6","article-title":"iDEP: an integrated web application for differential expression and pathway analysis of RNA-Seq data","volume":"19","author":"Ge","year":"2018","journal-title":"BMC Bioinforma."},{"key":"B16","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.mad.2017.04.003","article-title":"Alterations of the translation apparatus during aging and stress response","volume":"168","author":"Gonskikh","year":"2017","journal-title":"Mech. Ageing Dev."},{"key":"B17","doi-asserted-by":"publisher","first-page":"e0173696","DOI":"10.1371\/journal.pone.0173696","article-title":"Novel copy number variation of the TGF\u03b23 gene is associated with TGF\u03b23 gene expression and duration of fertility traits in hens","volume":"12","author":"Gu","year":"2017","journal-title":"PLoS One"},{"key":"B18","doi-asserted-by":"publisher","first-page":"1441","DOI":"10.1007\/s11250-019-01821-5","article-title":"Role of genome-wide mRNA-seq profiling in understanding the long-term sperm maintenance in the storage tubules of laying hens","volume":"51","author":"Han","year":"2019","journal-title":"Trop. Anim. Health Prod."},{"key":"B19","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1530\/jrf.0.0700025","article-title":"Carbonic anhydrase activity of the reproductive tract tissues of aged male fowls and its relationship to semen production","volume":"70","author":"Harris","year":"1984","journal-title":"J. Reprod. Fertil."},{"key":"B20","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1159\/000147853","article-title":"Localisation of carbonic anhydrase in the sperm storing regions of the domestic hen oviduct","volume":"156","author":"Holm","year":"1996","journal-title":"Acta Anat. (Basel)"},{"key":"B21","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1080\/713654906","article-title":"Carbonic anhydrase in the utero-vaginal junction of immature and mature ostriches","volume":"41","author":"Holm","year":"2000","journal-title":"Br. Poult. Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/s0378-4320(98)00142-0","article-title":"The effect of pH on the motility of spermatozoa from chicken, Turkey and quail","volume":"54","author":"Holm","year":"1998","journal-title":"Anim. Reprod. Sci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1111\/j.1439-0531.2011.01862.x","article-title":"Mechanisms of sperm storage in the female reproductive tract: an interspecies comparison","volume":"46","author":"Holt","year":"2011","journal-title":"Reproduction Domest. Animals"},{"key":"B24","doi-asserted-by":"publisher","first-page":"1334","DOI":"10.1016\/j.theriogenology.2015.12.020","article-title":"Expression of lipases and lipid receptors in sperm storage tubules and possible role of fatty acids in sperm survival in the hen oviduct","volume":"85","author":"Huang","year":"2016","journal-title":"Theriogenology"},{"key":"B25","doi-asserted-by":"publisher","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","year":"2009","journal-title":"Nat. Protoc."},{"key":"B26","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1186\/s12859-018-2190-6","article-title":"A computational approach to identify cellular heterogeneity and tissue-specific gene regulatory networks","volume":"19","author":"Jambusaria","year":"2018","journal-title":"BMC Bioinforma."},{"key":"B27","doi-asserted-by":"publisher","first-page":"D353-D361","DOI":"10.1093\/nar\/gkw1092","article-title":"KEGG: new perspectives on genomes, pathways, diseases and drugs","volume":"45","author":"Kanehisa","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"B28","doi-asserted-by":"publisher","first-page":"e9596","DOI":"10.15252\/msb.20209596","article-title":"Reduced proteasome activity in the aging brain results in ribosome stoichiometry loss and aggregation","volume":"16","author":"Kelmer Sacramento","year":"2020","journal-title":"Mol. Syst. Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"3302","DOI":"10.3390\/ani12233302","article-title":"Composition of fatty acids and localization of SREBP1 and ELOVL2 genes in cauda epididymides of Hu sheep with different fertility","volume":"12","author":"Liu","year":"2022","journal-title":"Animals"},{"key":"B30","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1830","DOI":"10.1093\/bioinformatics\/btt285","article-title":"Pathview: an R\/Bioconductor package for pathway-based data integration and visualization","volume":"29","author":"Luo","year":"2013","journal-title":"Bioinformatics"},{"key":"B32","doi-asserted-by":"publisher","first-page":"100543","DOI":"10.1016\/j.repbio.2021.100543","article-title":"Role of peroxisome proliferator-activated receptor gamma (PPAR\u03b3) in the regulation of fatty acid metabolism related gene expressions in testis of men with impaired spermatogenesis","volume":"21","author":"Olia Bagheri","year":"2021","journal-title":"Reprod. Biol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"970243","DOI":"10.3389\/fphys.2022.970243","article-title":"Transcriptome response of proliferating muscle satellite cells to thermal challenge in commercial Turkey","volume":"13","author":"Reed","year":"2022","journal-title":"Front. Physiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"205","DOI":"10.3382\/ps.2012-02536","article-title":"Sperm-egg interaction and fertility of Japanese breeder quails from 10 to 61 weeks","volume":"92","author":"Santos","year":"2013","journal-title":"Poult. Sci."},{"key":"B35","doi-asserted-by":"publisher","first-page":"W216","DOI":"10.1093\/nar\/gkac194","article-title":"DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update)","volume":"50","author":"Sherman","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"B36","doi-asserted-by":"publisher","first-page":"e1628","DOI":"10.1002\/wrna.1628","article-title":"Translational control in aging and neurodegeneration","volume":"12","author":"Skariah","year":"2021","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"B37","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1089\/107999001317205123","article-title":"Cytokines of birds: conserved functions\u2014a largely different look","volume":"21","author":"Staeheli","year":"2001","journal-title":"J. Interferon & Cytokine Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1038\/s41586-021-04295-4","article-title":"Ageing exacerbates ribosome pausing to disrupt cotranslational proteostasis","volume":"601","author":"Stein","year":"2022","journal-title":"Nature"},{"key":"B39","doi-asserted-by":"publisher","first-page":"2512","DOI":"10.18632\/aging.101922","article-title":"Impaired ribosome biogenesis: mechanisms and relevance to cancer and aging","volume":"11","author":"Turi","year":"2019","journal-title":"Aging (Albany NY)"},{"key":"B40","doi-asserted-by":"publisher","first-page":"995","DOI":"10.1038\/s41598-020-57839-5","article-title":"Differential expression and localisation of TGF-\u03b2 isoforms and receptors in the murine epididymis","volume":"10","author":"Voisin","year":"2020","journal-title":"Sci. Rep."},{"key":"B41","doi-asserted-by":"publisher","first-page":"29202","DOI":"10.1074\/jbc.M115.698597","article-title":"Normal fertility requires the expression of carbonic anhydrases II and IV in sperm","volume":"290","author":"Wandernoth","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B42","doi-asserted-by":"publisher","first-page":"e15061","DOI":"10.1371\/journal.pone.0015061","article-title":"Role of carbonic anhydrase IV in the bicarbonate-mediated activation of murine and human sperm","volume":"5","author":"Wandernoth","year":"2010","journal-title":"PLOS ONE"},{"key":"B43","doi-asserted-by":"publisher","first-page":"102624","DOI":"10.1016\/j.psj.2023.102624","article-title":"Transcriptome identification of genes associated with uterus-vagina junction epithelial folds formation in chicken hens","volume":"102","author":"Yang","year":"2023","journal-title":"Poult. Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"100892","DOI":"10.1016\/j.psj.2020.12.005","article-title":"Transcriptome analysis and identification of age-associated fertility decreased genes in hen uterovaginal junction","volume":"100","author":"Yang","year":"","journal-title":"Poult. Sci."},{"key":"B45","doi-asserted-by":"publisher","first-page":"101087","DOI":"10.1016\/j.psj.2021.101087","article-title":"Transcriptomic and metabolomic insights into the variety of sperm storage in oviduct of egg layers","volume":"100","author":"Yang","year":"","journal-title":"Poult. Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1016\/j.psj.2019.10.021","article-title":"Transcriptome analysis and identification of genes associated with chicken sperm storage duration","volume":"99","author":"Yang","year":"2020","journal-title":"Poult. Sci."},{"key":"B47","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1194\/jlr.M011346","article-title":"ELOVL2 controls the level of n-6 28:5 and 30:5 fatty acids in testis, a prerequisite for male fertility and sperm maturation in mice","volume":"52","author":"Zadravec","year":"2011","journal-title":"J. Lipid Res."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1209","DOI":"10.1093\/ps\/83.7.1209","article-title":"Localization of aquaporins in the sperm storage tubules in the Turkey oviduct","volume":"83","author":"Zaniboni","year":"2004","journal-title":"Poult. Sci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1097\/MCO.0000000000000254","article-title":"Desaturase and elongase limiting endogenous long chain polyunsaturated fatty acid biosynthesis","volume":"19","author":"Zhang","year":"2016","journal-title":"Curr. Opin. Clin. Nutr. Metab. Care"}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1275922\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,23]],"date-time":"2023-11-23T15:57:59Z","timestamp":1700755079000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1275922\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,22]]},"references-count":49,"alternative-id":["10.3389\/fphys.2023.1275922"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2023.1275922","relation":{"has-part":[{"id-type":"doi","id":"https:\/\/doi.org\/10.3389\/fphys.2023.1275922.s001","asserted-by":"subject"},{"id-type":"doi","id":"https:\/\/doi.org\/10.3389\/fphys.2023.1275922.s002","asserted-by":"subject"}]},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,22]]},"article-number":"1275922"}}