{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T15:04:04Z","timestamp":1781967844543,"version":"3.54.5"},"reference-count":46,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,7,7]],"date-time":"2020-07-07T00:00:00Z","timestamp":1594080000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001862","name":"Svenska Forskningsr\u00e5det Formas","doi-asserted-by":"publisher","award":["Project 2017-00946 and Project 2019-00288"],"award-info":[{"award-number":["Project 2017-00946 and Project 2019-00288"]}],"id":[{"id":"10.13039\/501100001862","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004359","name":"Vetenskapsr\u00e5det","doi-asserted-by":"publisher","award":["Project 2015-05919"],"award-info":[{"award-number":["Project 2015-05919"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014440","name":"Ministerio de Ciencia, Innovaci\u00f3n y Universidades","doi-asserted-by":"publisher","award":["Juan de la Cierva Incorporaci\u00f3n Postdoctoral Research Program (IJDC-2015-24380)"],"award-info":[{"award-number":["Juan de la Cierva Incorporaci\u00f3n Postdoctoral Research Program (IJDC-2015-24380)"]}],"id":[{"id":"10.13039\/100014440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002809","name":"Generalitat de Catalunya","doi-asserted-by":"publisher","award":["2018 FI_B 00236"],"award-info":[{"award-number":["2018 FI_B 00236"]}],"id":[{"id":"10.13039\/501100002809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Semen changes the gene expression in endometrial and oviductal tissues modulating important processes for reproduction. We tested the hypothesis that mating and\/or sperm-free seminal plasma deposition in the reproductive tract affect the expression of genes associated with sperm-lining epithelium interactions, ovulation, and pre-implantation effects (nerve growth factor, NGF; \u03b1\/\u03b2 hydrolase domain-containing protein 2, ABHD2; C-terminal tensin-like protein, CTEN or TNS4; and versican, VCAN) in the period 10\u201372 h post-mating. In Experiment 1, does (n = 9) were treated with gonadotropin-releasing hormone (GnRH) (control), GnRH-stimulated, and vaginally infused with sperm-free seminal plasma (SP-AI), or GnRH-stimulated and naturally mated (NM). In Experiment 2, does (n = 15) were GnRH-stimulated and naturally mated. Samples were retrieved from the internal reproductive tracts (cervix-to-infundibulum) 20 h post-treatment (Experiment 1) or sequentially collected at 10, 24, 36, 68, or 72 h post-mating (Experiment 2, 3 does\/period). All samples were processed for gene expression analysis by quantitative PCR. Data showed an upregulation of endometrial CTEN and NGF by NM, but not by SP-AI. The findings suggest that the NGF gene affects the reproductive tract of the doe during ovulation and beyond, influencing the maternal environment during early embryonic development.<\/jats:p>","DOI":"10.3390\/genes11070758","type":"journal-article","created":{"date-parts":[[2020,7,7]],"date-time":"2020-07-07T10:41:09Z","timestamp":1594118469000},"page":"758","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Semen Modulates the Expression of NGF, ABHD2, VCAN, and CTEN in the Reproductive Tract of Female Rabbits"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7524-2088","authenticated-orcid":false,"given":"Jaume","family":"Gardela","sequence":"first","affiliation":[{"name":"Division of Children\u2019s and Women Health (BKH), Obstetrics and Gynecology, Department of Biomedical and Clinical Sciences (BKV), Link\u00f6ping University, 58185 Link\u00f6ping, Sweden"},{"name":"Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Aut\u00f2noma de Barcelona, 08193 Bellaterra, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amaia","family":"Jauregi-Miguel","sequence":"additional","affiliation":[{"name":"Division of Molecular Medicine and Virology (MMV), Link\u00f6ping University, 58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6811-0191","authenticated-orcid":false,"given":"Cristina A.","family":"Martinez","sequence":"additional","affiliation":[{"name":"Division of Children\u2019s and Women Health (BKH), Obstetrics and Gynecology, Department of Biomedical and Clinical Sciences (BKV), Link\u00f6ping University, 58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5194-2124","authenticated-orcid":false,"given":"Heriberto","family":"Rodriguez-Martinez","sequence":"additional","affiliation":[{"name":"Division of Children\u2019s and Women Health (BKH), Obstetrics and Gynecology, Department of Biomedical and Clinical Sciences (BKV), Link\u00f6ping University, 58185 Link\u00f6ping, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manel","family":"Lopez-Bejar","sequence":"additional","affiliation":[{"name":"Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Aut\u00f2noma de Barcelona, 08193 Bellaterra, Spain"},{"name":"College of Veterinary Medicine, Western University of Health Sciences, Pomona, CA 91766, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0120-354X","authenticated-orcid":false,"given":"Manuel","family":"Alvarez-Rodriguez","sequence":"additional","affiliation":[{"name":"Division of Children\u2019s and Women Health (BKH), Obstetrics and Gynecology, Department of Biomedical and Clinical Sciences (BKV), Link\u00f6ping University, 58185 Link\u00f6ping, Sweden"},{"name":"Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Aut\u00f2noma de Barcelona, 08193 Bellaterra, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,7,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.meatsci.2018.08.003","article-title":"Rabbit meat in need of a hat-trick: From tradition to innovation (and back)","volume":"146","author":"Petracci","year":"2018","journal-title":"Meat Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1006\/frne.2000.0198","article-title":"Neuroendocrine regulation of GnRH release in induced ovulators","volume":"21","author":"Bakker","year":"2000","journal-title":"Front. Neuroendocrinol."},{"key":"ref_3","first-page":"R199","article-title":"New insights of the role of B-NGF in the ovulation mechanism of induced ovulating species","volume":"157","author":"Ratto","year":"2019","journal-title":"Reproduction"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1002\/mrd.22674","article-title":"The role of mating in oviduct biology","volume":"83","author":"Reuquen","year":"2016","journal-title":"Mol. Reprod. Dev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.livprodsci.2004.10.011","article-title":"Influence of constant long days on ejaculate parameters of rabbits reared under natural environment conditions of Mediterranean area","volume":"94","author":"Roca","year":"2005","journal-title":"Livest. Prod. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1530\/jrf.0.0380131","article-title":"Sperm transport in the female rabbit: The role of the cervix","volume":"38","author":"Morton","year":"1974","journal-title":"J. Reprod. Fertil."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1095\/biolreprod56.1.83","article-title":"Role of Direct Contact between Spermatozoa and Oviductal Epithelial Cells in Maintaining Rabbit Sperm Viability","volume":"56","author":"Nothnick","year":"1997","journal-title":"Biol. Reprod."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/s00441-015-2244-2","article-title":"Interactions of Gametes with the Female Reproductive Tract","volume":"363","author":"Suarez","year":"2016","journal-title":"Cell Tissue Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1095\/biolreprod19.1.101","article-title":"Sperm Transport in the Reproductive Tract of the Female Rabbit: I. The Rapid Transit Phase of Transport","volume":"19","author":"Overstreet","year":"1978","journal-title":"Biol. Reprod."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1095\/biolreprod19.1.115","article-title":"Sperm Transport in the Reproductive Tract of the Female Rabbit: II. The Sustained Phase of Transport","volume":"19","author":"Overstreet","year":"1978","journal-title":"Biol. Reprod."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.theriogenology.2015.11.025","article-title":"The ubiquitous hyaluronan: Functionally implicated in the oviduct?","volume":"86","author":"Tienthai","year":"2016","journal-title":"Theriogenology"},{"key":"ref_12","first-page":"266","article-title":"Proteoglycans of the extracellular matrix and growth control","volume":"189","author":"Kresse","year":"2001","journal-title":"Tissue"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.matbio.2016.12.001","article-title":"Provisional Matrix: A Role for Versican and Hyaluronan","volume":"60","author":"Wight","year":"2017","journal-title":"Matrix Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"35448","DOI":"10.1074\/jbc.M003387200","article-title":"Binding of a large chondroitin sulfate\/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44","volume":"275","author":"Kawashima","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1242\/jeb.9.4.403","article-title":"Fertilisation in the Rabbit","volume":"9","author":"Pincus","year":"1932","journal-title":"J. Exp. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1530\/jrf.0.0140477","article-title":"Survival of Capacitated Spermatozoa in the Oviduct of the Rabbit","volume":"14","author":"Dukelow","year":"1967","journal-title":"J. Reprod. Fert."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s00441-005-1127-3","article-title":"Seminal plasma and male factor signalling in the female reproductive tract","volume":"322","author":"Robertson","year":"2005","journal-title":"Cell Tissue Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1111\/j.1439-0531.2012.02097.x","article-title":"Sperm interaction with the female reproductive tract","volume":"47","author":"Druart","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Alvarez-Rodriguez, M., Atikuzzaman, M., Venhoranta, H., Wright, D., and Rodriguez-Martinez, H. (2019). Expression of immune regulatory genes in the porcine internal genital tract is differentially triggered by spermatozoa and seminal plasma. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20030513"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1154","DOI":"10.1126\/science.3306916","article-title":"The nerve growth factor 35 years later","volume":"237","year":"1987","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1111\/rda.12609","article-title":"Gene Expression and Localization of NGF and Its Cognate Receptors NTRK1 and NGFR in the Sex Organs of Male Rabbits","volume":"50","author":"Maranesi","year":"2015","journal-title":"Reprod. Domest. Anim."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1080\/1828051X.2017.1382315","article-title":"\u03b2-nerve growth factor identification in male rabbit genital tract and seminal plasma and its role in ovulation induction in rabbit does","volume":"17","author":"Masdeu","year":"2018","journal-title":"Ital. J. Anim. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.anireprosci.2017.12.004","article-title":"Rabbit seminal plasma proteome: The importance of the genetic origin","volume":"189","author":"Vicente","year":"2018","journal-title":"Anim. Reprod. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1093\/biolre\/ioy041","article-title":"New insights on a NGF-mediated pathway to induce ovulation in rabbits (Oryctolagus cuniculus)","volume":"98","author":"Maranesi","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1126\/science.aad6887","article-title":"Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone","volume":"352","author":"Miller","year":"2016","journal-title":"Science"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-019-55834-z","article-title":"Release of Porcine Sperm from Oviduct Cells is Stimulated by Progesterone and Requires CatSper","volume":"9","author":"Machado","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Martinez, C.A., Alvarez-Rodriguez, M., Wright, D., and Rodriguez-Martinez, H. (2020). Does the pre-ovulatory pig oviduct rule sperm capacitation in vivo mediating transcriptomics of catsper channels?. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051840"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1530\/REP-18-0333","article-title":"Versican V1 in human endometrial epithelial cells promotes BeWo spheroid adhesion in vitro","volume":"157","author":"Miyazaki","year":"2019","journal-title":"Reproduction"},{"key":"ref_29","unstructured":"Alvarez-Rodriguez, M., Martinez, C., L\u00f3pez-B\u00e9jar, M., and Rodr\u00edguez-Martinez, H. (2019, January 19\u201322). Abstracts. Seminal Plasma Affects the Expression of the ABHD2 and VCAN Genes in the Sow Internal Genital Tract. Proceedings of the 23rd Annual Conference of the European Society for Domestic Animal Reproduction (ESDAR), St. Petersburg, Russia."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.biocel.2014.04.003","article-title":"C-terminal tensin-like (CTEN): A promising biomarker and target for cancer","volume":"51","author":"Lo","year":"2014","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e45","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_32","unstructured":"Team, R.C. (2020, January 01). Available online: https:\/\/www.r-project.org\/."},{"key":"ref_33","unstructured":"Pinheiro, J., Bates, D., DebRoy, S., Sarjar, D., and Team, R.C. (2020, January 01). Nlme: Linear and Nonlinear Mixed Effects Models. Available online: https:\/\/cran.r-project.org\/package=nlme."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/bimj.200810425","article-title":"Simultaneous Inference in General Parametric Models","volume":"50","author":"Hothorn","year":"2008","journal-title":"Biom. J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1071\/BI9530693","article-title":"Distribution of sperms in the genital tract of the female rabbit after coitus","volume":"6","author":"Braden","year":"1953","journal-title":"Aust. J. Biol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1016\/S0015-0282(16)37622-1","article-title":"Sperm transport and distribution in rabbit and cattle female tract","volume":"21","author":"Hafez","year":"1970","journal-title":"Fertil. Steril."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1186\/s12958-019-0533-4","article-title":"In vitro effect of nerve growth factor on the main traits of rabbit sperm","volume":"17","author":"Castellini","year":"2019","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Sanchez-Rodriguez, A., Paloma, A., Arias-Alvarez, M., Rebollar, P.G., Bautista, J.M., Lorenzo, P.L., and Garc\u00eda-Garc\u00eda, R.M. (2019). Recombinant rabbit beta nerve growth factor production and its biological effects on sperm and ovulation in rabbits. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0219780"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.theriogenology.2018.12.013","article-title":"Characterization of \u03b2-Nerve Growth Factor-TrkA system in male reproductive tract of rabbit and the relationship between \u03b2-NGF and testosterone levels with seminal quality during sexual maturation","volume":"126","author":"Bautista","year":"2019","journal-title":"Theriogenology"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Garcia-Garcia, R.M., Alvarez, M.A., Sanchez-Rodriguez, A., Lorenzo, P.L., and Rebollar, P.G. (2020). Role of Nerve Growth Factor in the Reproductive Physiology of Female Rabbits: A Review. Theriogenology.","DOI":"10.1016\/j.theriogenology.2020.01.070"},{"key":"ref_41","unstructured":"Garc\u00eda Garc\u00eda, R.M., Arias \u00c1lvarez, M., S\u00e1nchez Rodr\u00edguez, A., Garc\u00eda Rebollar, P., and Lorenzo, P.L. (2018, January 27\u201329). Abstracts. NGF systems is differentially expressed in the ovary, oviduct and uterus of rabbit does although independent of serum hormonal levels. Proceedings of the 22nd Annual Conference of the European Society for Domestic Animal Reproduction (ESDAR), C\u00f3rdoba, Spain."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/S0015-0282(16)34028-6","article-title":"A study of the transport of ova through the rabbit oviduct","volume":"12","author":"Greenwald","year":"1961","journal-title":"Fertil. Steril."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/s11259-009-9325-1","article-title":"Effect of nerve growth factor (NGF) on the development of preimplantation rabbit embryos in vitro","volume":"34","author":"Pei","year":"2010","journal-title":"Vet. Res. Commun."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3345","DOI":"10.4049\/jimmunol.1300825","article-title":"Nerve Growth Factor Downregulates Inflammatory Response in Human Monocytes through TrkA","volume":"192","author":"Prencipe","year":"2014","journal-title":"J. Immunol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1002\/mc.22034","article-title":"Up-regulated cten by FGF2 contributes to FGF2-mediated cell migration","volume":"53","author":"Hung","year":"2014","journal-title":"Mol. Carcinog."},{"key":"ref_46","first-page":"4217","article-title":"Bin Cten, a COOH-terminal tensin-like protein with prostate restricted expression, is down-regulated in prostate cancer","volume":"62","author":"Lo","year":"2002","journal-title":"Cancer Res."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/7\/758\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:48:28Z","timestamp":1760176108000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/7\/758"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,7]]},"references-count":46,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,7]]}},"alternative-id":["genes11070758"],"URL":"https:\/\/doi.org\/10.3390\/genes11070758","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,7]]}}}