{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,11]],"date-time":"2026-07-11T17:51:03Z","timestamp":1783792263060,"version":"3.55.0"},"reference-count":61,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,12,15]],"date-time":"2023-12-15T00:00:00Z","timestamp":1702598400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,12,15]],"date-time":"2023-12-15T00:00:00Z","timestamp":1702598400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Dynamic functional changes in the oviductal microenvironment are the prerequisite for the establishment of pregnancy. The objective of this study was to gain the first insights into oestrous cycle-dependent dynamics of polymorph nuclear neutrophils (PMN) and the mRNA abundance of selected genes and their correlations in the oviduct of living cows. Mini-cytobrush samples were taken from the oviducts of healthy heifers (n\u2009=\u20096) and cows (n\u2009=\u20097) during the follicular (FOL) and luteal phase (LUT) by transvaginal endoscopy. Total RNA was isolated from the samples and subjected to reverse transcription-quantitative PCR for selected pro-inflammatory factors, glycoproteins, and a metabolic marker. The percentage of PMN was determined by cytological examination. The mean PMN percentage was 2.8-fold greater during LUT than FOL. During LUT, significantly greater mRNA abundance of the pro-inflammatory factors<jats:italic>IL1B, CXCL1, CXCL3<\/jats:italic>, and<jats:italic>CXCL8<\/jats:italic>was observed. The<jats:italic>OVGP1<\/jats:italic>mRNA abundance was twice as high during FOL than in LUT. Pearson correlation, principal component analysis and heatmap analyses indicated characteristic functional patterns with strong correlations among investigated factors. Using this novel approach, we illustrate complex physiological dynamics and interactions of the mRNA expression of pro-inflammatory factors, mucins,<jats:italic>OVGP1<\/jats:italic>, and PMN in the oviduct during the oestrous cycle.<\/jats:p>","DOI":"10.1038\/s41598-023-49151-9","type":"journal-article","created":{"date-parts":[[2023,12,15]],"date-time":"2023-12-15T18:02:36Z","timestamp":1702663356000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["In vivo dynamics of pro-inflammatory factors, mucins, and polymorph nuclear neutrophils in the bovine oviduct during the follicular and luteal phase"],"prefix":"10.1038","volume":"13","author":[{"given":"L.","family":"Neubrand","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.","family":"Pothmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"U.","family":"Besenfelder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V.","family":"Havlicek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Gabler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Dolezal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C.","family":"Aurich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Drillich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"K.","family":"Wagener","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,12,15]]},"reference":[{"key":"49151_CR1","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1093\/biolre\/ioy083","volume":"99","author":"AM Gonella-Diaza","year":"2018","unstructured":"Gonella-Diaza, A. M. et al. Sex steroids drive the remodeling of oviductal extracellular matrix in cattle. Biol. Reprod. 99, 590\u2013599. https:\/\/doi.org\/10.1093\/biolre\/ioy083 (2018).","journal-title":"Biol. Reprod."},{"key":"49151_CR2","doi-asserted-by":"publisher","unstructured":"Gonz\u00e1lez Brusi, L. et al. A comparative view on the oviductal environment during the periconception period. Biomolecules. https:\/\/doi.org\/10.3390\/biom10121690 (2020).","DOI":"10.3390\/biom10121690"},{"key":"49151_CR3","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1111\/j.1439-0531.2012.02070.x","volume":"47","author":"U Besenfelder","year":"2012","unstructured":"Besenfelder, U., Havlicek, V. & Brem, G. Role of the oviduct in early embryo development. Reprod. Domest. Anim. 47, 156\u2013163. https:\/\/doi.org\/10.1111\/j.1439-0531.2012.02070.x (2012).","journal-title":"Reprod. Domest. Anim."},{"key":"49151_CR4","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1071\/rd11914","volume":"24","author":"MG Diskin","year":"2011","unstructured":"Diskin, M. G., Parr, M. H. & Morris, D. G. Embryo death in cattle: An update. Reprod. Fertil. Dev. 24, 244\u2013251. https:\/\/doi.org\/10.1071\/rd11914 (2011).","journal-title":"Reprod. Fertil. Dev."},{"key":"49151_CR5","doi-asserted-by":"publisher","first-page":"R1","DOI":"10.1530\/JOE-16-0302","volume":"232","author":"S Li","year":"2017","unstructured":"Li, S. & Winuthayanon, W. Oviduct: Roles in fertilization and early embryo development. J. Endocrinol. 232, R1\u2013R26. https:\/\/doi.org\/10.1530\/JOE-16-0302 (2017).","journal-title":"J. Endocrinol."},{"key":"49151_CR6","first-page":"67","volume":"24","author":"KE Leslie","year":"1983","unstructured":"Leslie, K. E. The events of normal and abnormal postpartum reproductive endocrinology and uterine involution in dairy cows: A review. Can. Vet. J. 24, 67\u201371 (1983).","journal-title":"Can. Vet. J."},{"key":"49151_CR7","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.anireprosci.2012.08.006","volume":"134","author":"D Salilew-Wondim","year":"2012","unstructured":"Salilew-Wondim, D., Schellander, K., Hoelker, M. & Tesfaye, D. Oviductal, endometrial and embryonic gene expression patterns as molecular clues for pregnancy establishment. Anim. Reprod. Sci. 134, 9\u201318. https:\/\/doi.org\/10.1016\/j.anireprosci.2012.08.006 (2012).","journal-title":"Anim. Reprod. Sci."},{"key":"49151_CR8","doi-asserted-by":"publisher","unstructured":"Binelli, M., Gonella-Diaza, A.M., Mesquita, F.S. & Membrive, C.M.B. Sex steroid-mediated control of oviductal function in cattle. Biology https:\/\/doi.org\/10.3390\/biology7010015 (2018).","DOI":"10.3390\/biology7010015"},{"key":"49151_CR9","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1071\/rd09120","volume":"22","author":"C Fischer","year":"2010","unstructured":"Fischer, C. et al. Selected pro-inflammatory factor transcripts in bovine endometrial epithelial cells are regulated during the oestrous cycle and elevated in case of subclinical or clinical endometritis. Reprod. Fertil. Dev. 22, 818\u2013829. https:\/\/doi.org\/10.1071\/rd09120 (2010).","journal-title":"Reprod. Fertil. Dev."},{"key":"49151_CR10","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1677\/jme.0.0320449","volume":"32","author":"S Bauersachs","year":"2004","unstructured":"Bauersachs, S. et al. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J. Mol. Endocrinol. 32, 449\u2013466. https:\/\/doi.org\/10.1677\/jme.0.0320449 (2004).","journal-title":"J. Mol. Endocrinol."},{"key":"49151_CR11","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1530\/rep.0.1230355","volume":"123","author":"WC Buhi","year":"2002","unstructured":"Buhi, W. C. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123, 355\u2013362. https:\/\/doi.org\/10.1530\/rep.0.1230355 (2002).","journal-title":"Reproduction"},{"key":"49151_CR12","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/s00418-021-02065-x","volume":"157","author":"Y Zhao","year":"2022","unstructured":"Zhao, Y., Vanderkooi, S. & Kan, F. W. K. The role of oviduct-specific glycoprotein (OVGP1) in modulating biological functions of gametes and embryos. Histochem. Cell Biol. 157, 371\u2013388. https:\/\/doi.org\/10.1007\/s00418-021-02065-x (2022).","journal-title":"Histochem. Cell Biol."},{"key":"49151_CR13","doi-asserted-by":"publisher","unstructured":"Danesh Mesgaran, S. et al. Different inflammatory responses of bovine oviductal epithelial cells in vitro to bacterial species with distinct pathogenicity characteristics and passage number. Theriogenology 106, 237\u2013246. https:\/\/doi.org\/10.1016\/j.theriogenology.2017.10.005 (2018).","DOI":"10.1016\/j.theriogenology.2017.10.005"},{"key":"49151_CR14","doi-asserted-by":"publisher","unstructured":"Danesh Mesgaran, S., Sharbati, J., Einspanier, R. & Gabler, C. mRNA expression pattern of selected candidate genes differs in bovine oviductal epithelial cells in vitro compared with the in vivo state and during cell culture passages. Reprod. Biol. Endocrinol. 14, 1\u201318. https:\/\/doi.org\/10.1186\/s12958-016-0176-7 (2016).","DOI":"10.1186\/s12958-016-0176-7"},{"key":"49151_CR15","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1095\/biolreprod.108.073874","volume":"81","author":"S K\u00f6lle","year":"2009","unstructured":"K\u00f6lle, S. et al. Ciliary transport, gamete interaction, and effects of the early embryo in the oviduct: Ex vivo analyses using a new digital videomicroscopic system in the cow. Biol. Reprod. 81, 267\u2013274. https:\/\/doi.org\/10.1095\/biolreprod.108.073874 (2009).","journal-title":"Biol. Reprod."},{"key":"49151_CR16","doi-asserted-by":"publisher","first-page":"768","DOI":"10.1016\/j.theriogenology.2009.07.003","volume":"73","author":"U Besenfelder","year":"2010","unstructured":"Besenfelder, U., Havlicek, V., Kuzmany, A. & Brem, G. Endoscopic approaches to manage in vitro and in vivo embryo development: Use of the bovine oviduct. Theriogenology 73, 768\u2013776. https:\/\/doi.org\/10.1016\/j.theriogenology.2009.07.003 (2010).","journal-title":"Theriogenology"},{"key":"49151_CR17","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1016\/S0093-691X(98)00179-4","volume":"50","author":"U Besenfelder","year":"1998","unstructured":"Besenfelder, U. & Brem, G. Tubal transfer of bovine embryos: A simple endoscopic method reducing long-term exposure of in vitro produced embryos. Theriogenology 50, 739\u2013745. https:\/\/doi.org\/10.1016\/S0093-691X(98)00179-4 (1998).","journal-title":"Theriogenology"},{"key":"49151_CR18","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1002\/mrd.1153","volume":"61","author":"D Rizos","year":"2002","unstructured":"Rizos, D., Ward, F., Duffy, P., Boland, M. P. & Lonergan, P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234\u2013248. https:\/\/doi.org\/10.1002\/mrd.1153 (2002).","journal-title":"Mol. Reprod. Dev."},{"key":"49151_CR19","doi-asserted-by":"publisher","first-page":"2348","DOI":"10.1093\/humrep\/dex286","volume":"32","author":"O T\u0161uiko","year":"2017","unstructured":"T\u0161uiko, O. et al. Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos. Hum. Reprod. 32, 2348\u20132357. https:\/\/doi.org\/10.1093\/humrep\/dex286 (2017).","journal-title":"Hum. Reprod."},{"key":"49151_CR20","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/j.theriogenology.2020.01.071","volume":"150","author":"AK Talukder","year":"2020","unstructured":"Talukder, A. K. et al. Roadmap to pregnancy in the first 7 days post-insemination in the cow: Immune crosstalk in the corpus luteum, oviduct, and uterus. Theriogenology 150, 313\u2013320. https:\/\/doi.org\/10.1016\/j.theriogenology.2020.01.071 (2020).","journal-title":"Theriogenology"},{"key":"49151_CR21","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1016\/S0093-691X(98)90604-5","volume":"49","author":"R Gilbert","year":"1998","unstructured":"Gilbert, R., Shin, S., Guard, C. & Erb, H. Incidence of endometritis and effects on reproductive performance of dairy cows. Theriogenology 49, 251. https:\/\/doi.org\/10.1016\/S0093-691X(98)90604-5 (1998).","journal-title":"Theriogenology"},{"key":"49151_CR22","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.theriogenology.2017.02.005","volume":"94","author":"K Wagener","year":"2017","unstructured":"Wagener, K., Gabler, C. & Drillich, M. A review of the ongoing discussion about definition, diagnosis and pathomechanism of subclinical endometritis in dairy cows. Theriogenology 94, 21\u201330. https:\/\/doi.org\/10.1016\/j.theriogenology.2017.02.005 (2017).","journal-title":"Theriogenology"},{"key":"49151_CR23","doi-asserted-by":"publisher","unstructured":"Owhor, L.E., Reese, S. & K\u00f6lle, S. Salpingitis impairs bovine tubal function and sperm-oviduct interaction. Sci. Rep. https:\/\/doi.org\/10.1038\/s41598-019-47431-x (2019).","DOI":"10.1038\/s41598-019-47431-x"},{"key":"49151_CR24","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1016\/j.theriogenology.2011.08.033","volume":"77","author":"M Drillich","year":"2012","unstructured":"Drillich, M. et al. Effects of polymorphonuclear neutrophile infiltration into the endometrial environment on embryonic development in superovulated cows. Theriogenology 77, 570\u2013578. https:\/\/doi.org\/10.1016\/j.theriogenology.2011.08.033 (2012).","journal-title":"Theriogenology"},{"key":"49151_CR25","doi-asserted-by":"publisher","unstructured":"Wagener, K., Drillich, M., Aurich, C. & Gabler, C. Endometrial inflammation at the time of insemination and its effect on subsequent fertility of dairy cows. Animals. https:\/\/doi.org\/10.3390\/ani11071858 (2021).","DOI":"10.3390\/ani11071858"},{"key":"49151_CR26","doi-asserted-by":"publisher","first-page":"835","DOI":"10.1002\/mrd.23164","volume":"86","author":"MS Yousef","year":"2019","unstructured":"Yousef, M. S., Abd-Elhafeez, H. H., Talukder, A. K. & Miyamoto, A. Ovulatory follicular fluid induces sperm phagocytosis by neutrophils, but oviductal fluid around oestrus suppresses its inflammatory effect in the buffalo oviduct in vitro. Mol. Reprod. Dev. 86, 835\u2013846. https:\/\/doi.org\/10.1002\/mrd.23164 (2019).","journal-title":"Mol. Reprod. Dev."},{"key":"49151_CR27","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1530\/REP-13-0375","volume":"147","author":"MA Marey","year":"2014","unstructured":"Marey, M. A. et al. Bovine oviduct epithelial cells downregulate phagocytosis of sperm by neutrophils: Prostaglandin E2 as a major physiological regulator. Reproduction 147, 211\u2013219. https:\/\/doi.org\/10.1530\/REP-13-0375 (2014).","journal-title":"Reproduction"},{"key":"49151_CR28","doi-asserted-by":"publisher","unstructured":"Yousef, M.S. et al. Sperm binding to oviduct epithelial cells enhances TGFB1 and IL10 expressions in epithelial cells aswell as neutrophils in vitro: Prostaglandin E2 as a main regulator of anti-inflammatory response in the bovine oviduct. PLoS ONE. https:\/\/doi.org\/10.1371\/journal.pone.0162309 (2016).","DOI":"10.1371\/journal.pone.0162309"},{"key":"49151_CR29","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/j.theriogenology.2016.12.013","volume":"90","author":"K Wagener","year":"2017","unstructured":"Wagener, K. et al. Endometrial mRNA expression of selected pro-inflammatory factors and mucins in repeat breeder cows with and without subclinical endometritis. Theriogenology 90, 237\u2013244. https:\/\/doi.org\/10.1016\/j.theriogenology.2016.12.013 (2017).","journal-title":"Theriogenology"},{"key":"49151_CR30","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1007\/s00441-017-2776-8","volume":"371","author":"B Petri","year":"2018","unstructured":"Petri, B. & Sanz, M. J. Neutrophil chemotaxis. Cell Tissue Res. 371, 425\u2013436. https:\/\/doi.org\/10.1007\/s00441-017-2776-8 (2018).","journal-title":"Cell Tissue Res."},{"key":"49151_CR31","doi-asserted-by":"publisher","first-page":"1406","DOI":"10.1095\/biolreprod59.6.1406","volume":"59","author":"FF Paula-Lopes","year":"1998","unstructured":"Paula-Lopes, F. F., de Moraes, A. A. S., Edwards, J. L., Justice, J. E. & Hansen, P. J. Regulation of preimplantation development of bovine embryos by interleukin-1\u03b21. Biol. Reprod. 59, 1406\u20131412. https:\/\/doi.org\/10.1095\/biolreprod59.6.1406 (1998).","journal-title":"Biol. Reprod."},{"key":"49151_CR32","doi-asserted-by":"publisher","unstructured":"Mah\u00e9, C. et al. The sperm-interacting proteome in the bovine isthmus and ampulla during the periovulatory period. J. Anim. Sci. Biotechnol. https:\/\/doi.org\/10.1186\/s40104-022-00811-2 (2023).","DOI":"10.1186\/s40104-022-00811-2"},{"key":"49151_CR33","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1002\/mrd.23352","volume":"87","author":"S K\u00f6lle","year":"2020","unstructured":"K\u00f6lle, S., Hughes, B. & Steele, H. Early embryo-maternal communication in the oviduct: A review. Mol. Reprod. Dev. 87, 650\u2013662. https:\/\/doi.org\/10.1002\/mrd.23352 (2020).","journal-title":"Mol. Reprod. Dev."},{"key":"49151_CR34","doi-asserted-by":"publisher","unstructured":"Anamthathmakula, P. & Winuthayanon, W. Prostaglandin-endoperoxide synthase 2 (PTGS2) in the oviduct: Roles in fertilization and early embryo development. Endocrinology. https:\/\/doi.org\/10.1210\/endocr\/bqab025 (2021).","DOI":"10.1210\/endocr\/bqab025"},{"key":"49151_CR35","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1095\/biolreprod.112.099051","volume":"87","author":"H Seo","year":"2012","unstructured":"Seo, H., Choi, Y., Shim, J., Choi, Y. & Ka, H. Regulatory mechanism for expression of IL1B receptors in the uterine endometrium and effects of IL1B on prostaglandin synthetic enzymes during the implantation period in pigs. Biol. Reprod. 87, 31. https:\/\/doi.org\/10.1095\/biolreprod.112.099051 (2012).","journal-title":"Biol. Reprod."},{"key":"49151_CR36","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1677\/JOE-08-0237","volume":"199","author":"M Tanikawa","year":"2008","unstructured":"Tanikawa, M. et al. Regulation of prostaglandin biosynthesis by interleukin-1 in cultured bovine endometrial cells. J. Endocrinol. 199, 425\u2013434. https:\/\/doi.org\/10.1677\/JOE-08-0237 (2008).","journal-title":"J. Endocrinol."},{"key":"49151_CR37","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1111\/j.8755-8920.2000.430304.x","volume":"43","author":"PN Rauk","year":"2000","unstructured":"Rauk, P. N. & Chiao, J.-P. Interleukin-1 stimulates human uterine prostaglandin production through induction of cyclooxygenase-2 expression. Am. J. Reprod. Immunol. 43, 152\u2013159. https:\/\/doi.org\/10.1111\/j.8755-8920.2000.430304.x (2000).","journal-title":"Am. J. Reprod. Immunol."},{"key":"49151_CR38","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1677\/joe.1.06761","volume":"191","author":"S Odau","year":"2006","unstructured":"Odau, S., Gabler, C., Holder, C. & Einspanier, R. Differential expression of cyclooxygenase 1 and cyclooxygenase 2 in the bovine oviduct. J. Endocrinol. 191, 263\u2013274. https:\/\/doi.org\/10.1677\/joe.1.06761 (2006).","journal-title":"J. Endocrinol."},{"key":"49151_CR39","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/S0378-4320(99)00021-4","volume":"56","author":"MPB Wijayagunawardane","year":"1999","unstructured":"Wijayagunawardane, M. P. B. et al. Effect of ovarian steroids and oxytocin on the production of prostaglandin E2, prostaglandin F(2\u03b1) and endothelin-1 from cow oviductal epithelial cell monolayers in vitro. Anim. Reprod. Sci. 56, 11\u201317. https:\/\/doi.org\/10.1016\/S0378-4320(99)00021-4 (1999).","journal-title":"Anim. Reprod. Sci."},{"key":"49151_CR40","doi-asserted-by":"publisher","unstructured":"Kasimanickam, R., Kasimanickam, V. & Kastelic, J.P. Mucin 1 and cytokines mRNA in endometrium of dairy cows with postpartum uterine disease or repeat breeding. Theriogenology 81, 952\u2013958. https:\/\/doi.org\/10.1016\/j.theriogenology.2014.01.018 (2014).","DOI":"10.1016\/j.theriogenology.2014.01.018"},{"key":"49151_CR41","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1530\/rep.1.00996","volume":"132","author":"S Bauersachs","year":"2006","unstructured":"Bauersachs, S. et al. Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 132, 319\u2013331. https:\/\/doi.org\/10.1530\/rep.1.00996 (2006).","journal-title":"Reproduction"},{"key":"49151_CR42","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1095\/biolreprod64.2.590","volume":"64","author":"M Meseguer","year":"2001","unstructured":"Meseguer, M. et al. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst 1. Biol. Reprod. 64, 590\u2013601. https:\/\/doi.org\/10.1095\/biolreprod64.2.590 (2001).","journal-title":"Biol. Reprod."},{"key":"49151_CR43","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1095\/biolreprod43.3.457","volume":"43","author":"ML Boice","year":"1990","unstructured":"Boice, M. L., Geisert, R. D., Blair, R. M. & Verhage, H. G. Identification and characterization of bovine oviductal glycoproteins synthesized at estrus. Biol. Reprod. 43, 457\u2013465. https:\/\/doi.org\/10.1095\/biolreprod43.3.457 (1990).","journal-title":"Biol. Reprod."},{"key":"49151_CR44","doi-asserted-by":"publisher","first-page":"1305","DOI":"10.1095\/biolreprod55.6.1305","volume":"55","author":"WC Buhi","year":"1996","unstructured":"Buhi, W. C., Alvarez, I. M., Choi, I., Cleaver, B. D. & Simmen, F. A. Molecular cloning and characterization of an estrogen-dependent porcine oviductal secretory glycoprotein1. Biol. Reprod. 55, 1305\u20131314. https:\/\/doi.org\/10.1095\/biolreprod55.6.1305 (1996).","journal-title":"Biol. Reprod."},{"key":"49151_CR45","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1530\/jrf.0.1120157","volume":"112","author":"H Abe","year":"1998","unstructured":"Abe, H., Satoh, T. & Hoshi, H. Primary modulation by oestradiol of the production of an oviduct-specific glycoprotein by the epithelial cells in the oviduct of newborn golden hamsters. J. Reprod. Fertil. 112, 157\u2013163. https:\/\/doi.org\/10.1530\/jrf.0.1120157 (1998).","journal-title":"J. Reprod. Fertil."},{"key":"49151_CR46","doi-asserted-by":"publisher","unstructured":"Ferraz, M. A. M. M. et al. An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming. Nat. Commun. https:\/\/doi.org\/10.1038\/s41467-018-07119-8 (2018).","DOI":"10.1038\/s41467-018-07119-8"},{"key":"49151_CR47","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1107\/S1744309109008537","volume":"65","author":"MM Hoque","year":"2009","unstructured":"Hoque, M. M. et al. Structure of D-3-hydroxybutyrate dehydrogenase prepared in the presence of the substrate D-3-hydroxybutyrate and NAD+. Acta Crystallogr. F 65, 331\u2013335. https:\/\/doi.org\/10.1107\/S1744309109008537 (2009).","journal-title":"Acta Crystallogr. F"},{"key":"49151_CR48","doi-asserted-by":"publisher","first-page":"758","DOI":"10.1016\/j.theriogenology.2009.07.004","volume":"73","author":"MA Velazquez","year":"2010","unstructured":"Velazquez, M. A. et al. Sampling techniques for oviductal and uterine luminal fluid in cattle. Theriogenology 73, 758\u2013767. https:\/\/doi.org\/10.1016\/j.theriogenology.2009.07.004 (2010).","journal-title":"Theriogenology"},{"key":"49151_CR49","doi-asserted-by":"publisher","first-page":"1021","DOI":"10.1071\/RD17389","volume":"30","author":"J Lamy","year":"2018","unstructured":"Lamy, J. et al. Metabolomic profiling of bovine oviductal fluid across the oestrous cycle using proton nuclear magnetic resonance spectroscopy. Reprod. Fertil. Dev. 30, 1021\u20131028. https:\/\/doi.org\/10.1071\/RD17389 (2018).","journal-title":"Reprod. Fertil. Dev."},{"key":"49151_CR50","doi-asserted-by":"publisher","first-page":"4135","DOI":"10.1038\/s41598-022-07929-3","volume":"12","author":"C Mahe","year":"2022","unstructured":"Mahe, C. et al. Spatiotemporal profiling of the bovine oviduct fluid proteome around the time of ovulation. Sci. Rep. 12, 4135. https:\/\/doi.org\/10.1038\/s41598-022-07929-3 (2022).","journal-title":"Sci. Rep."},{"key":"49151_CR51","doi-asserted-by":"publisher","first-page":"2618","DOI":"10.3168\/jds.2008-1795","volume":"92","author":"M Iwersen","year":"2009","unstructured":"Iwersen, M., Falkenberg, U., Voigtsberger, R., Forderung, D. & Heuwieser, W. Evaluation of an electronic cowside test to detect subclinical ketosis in dairy cows. J. Dairy Sci. 92, 2618\u20132624. https:\/\/doi.org\/10.3168\/jds.2008-1795 (2009).","journal-title":"J. Dairy Sci."},{"key":"49151_CR52","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1016\/j.theriogenology.2014.06.015","volume":"82","author":"I Prunner","year":"2014","unstructured":"Prunner, I., Wagener, K., Pothmann, H., Ehling-Schulz, M. & Drillich, M. Risk factors for uterine diseases on small- and medium-sized dairy farms determined by clinical, bacteriological, and cytological examinations. Theriogenology 82, 857\u2013865. https:\/\/doi.org\/10.1016\/j.theriogenology.2014.06.015 (2014).","journal-title":"Theriogenology"},{"key":"49151_CR53","doi-asserted-by":"publisher","first-page":"1516","DOI":"10.1016\/j.theriogenology.2005.08.021","volume":"65","author":"IM Sheldon","year":"2006","unstructured":"Sheldon, I. M., Lewis, G. S., LeBlanc, S. & Gilbert, R. O. Defining postpartum uterine disease in cattle. Theriogenology 65, 1516\u20131530. https:\/\/doi.org\/10.1016\/j.theriogenology.2005.08.021 (2006).","journal-title":"Theriogenology"},{"key":"49151_CR54","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.theriogenology.2019.04.009","volume":"132","author":"SM Papp","year":"2019","unstructured":"Papp, S. M. et al. A novel approach to study the bovine oviductal fluid proteome using transvaginal endoscopy. Theriogenology 132, 53\u201361. https:\/\/doi.org\/10.1016\/j.theriogenology.2019.04.009 (2019).","journal-title":"Theriogenology"},{"key":"49151_CR55","doi-asserted-by":"publisher","first-page":"1249","DOI":"10.1016\/j.theriogenology.2015.01.013","volume":"83","author":"H Pothmann","year":"2015","unstructured":"Pothmann, H. et al. The prevalence of subclinical endometritis and intrauterine infections in repeat breeder cows. Theriogenology 83, 1249\u20131253. https:\/\/doi.org\/10.1016\/j.theriogenology.2015.01.013 (2015).","journal-title":"Theriogenology"},{"key":"49151_CR56","doi-asserted-by":"crossref","unstructured":"Vandesompele, J. et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002).","DOI":"10.1186\/gb-2002-3-7-research0034"},{"key":"49151_CR57","doi-asserted-by":"publisher","first-page":"1686","DOI":"10.21105\/joss.01686","volume":"4","author":"H Wickham","year":"2019","unstructured":"Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686. https:\/\/doi.org\/10.21105\/joss.01686 (2019).","journal-title":"J. Open Source Softw."},{"key":"49151_CR58","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v067.i01","volume":"67","author":"D Bates","year":"2015","unstructured":"Bates, D., M\u00e4chler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1\u201348. https:\/\/doi.org\/10.18637\/jss.v067.i01 (2015).","journal-title":"J. Stat. Softw."},{"key":"49151_CR59","unstructured":"Wickham, H. Ggplot2: Elegant Graphics for Data Analysis (Springer\u2010Verlag, 2016). ISBN 978\u20103\u2010319\u201024277\u20104."},{"key":"49151_CR60","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","volume":"57","author":"Y Benjamini","year":"1995","unstructured":"Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B Met. 57, 289\u2013300 (1995).","journal-title":"J. R. Stat. Soc. B Met."},{"key":"49151_CR61","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1071\/RD14219","volume":"28","author":"MA G\u00e4rtner","year":"2016","unstructured":"G\u00e4rtner, M. A. et al. Increased mRNA expression of selected pro-inflammatory factors in inflamed bovine endometrium in vivo as well as in endometrial epithelial cells exposed to Bacillus pumilus in vitro. Reprod. Fertil. Dev. 28, 982\u2013994. https:\/\/doi.org\/10.1071\/RD14219 (2016).","journal-title":"Reprod. Fertil. Dev."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-49151-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-49151-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-49151-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,6]],"date-time":"2024-11-06T03:47:37Z","timestamp":1730864857000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-49151-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,15]]},"references-count":61,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["49151"],"URL":"https:\/\/doi.org\/10.1038\/s41598-023-49151-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,15]]},"assertion":[{"value":"15 September 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 December 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 December 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"22353"}}