{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T22:06:41Z","timestamp":1790028401148,"version":"4.0.1"},"reference-count":63,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T00:00:00Z","timestamp":1741219200000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"European Union\u2019s Horizon 2020 and The Research Foundation\u2014Flanders","award":["860960"],"award-info":[{"award-number":["860960"]}]},{"name":"European Union\u2019s Horizon 2020 and The Research Foundation\u2014Flanders","award":["IBOF-23-005"],"award-info":[{"award-number":["IBOF-23-005"]}]}],"content-domain":{"domain":["rep.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2025,3,6]]},"abstract":"<jats:sec>\n                    <jats:title>In brief<\/jats:title>\n                    <jats:p>\n                      Bulls are selected for field fertility and semen quality, but traits such as polyspermy are not considered and can increase aneuploidy during\n                      <jats:italic>in vitro<\/jats:italic>\n                      embryo production. This study links bull-specific proteomic signatures to polyspermy and embryo quality, further refining bull selection criteria.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Abstract<\/jats:title>\n                    <jats:p>\n                      Male fertility plays a pivotal role in the success rates of\n                      <jats:italic>in vitro<\/jats:italic>\n                      embryo production. While livestock breeding programs rigorously select bulls according to their predicted field fertility, specific traits such as polyspermy rates are not routinely evaluated. Despite the known negative impact of polyspermy on embryo survival, the paternal factors involved remain unclear. In this study, we aimed to address this gap by evaluating the\n                      <jats:italic>in vitro<\/jats:italic>\n                      outcomes of four bulls, focusing on sperm motility, fertilization rates, polyspermy incidence, embryo development and quality. In addition, we analyzed the proteome profiles of sperm, 2\u20134 cell stage embryos and blastocysts derived from those bulls to identify potential molecular factors associated with male fertility. Bulls with comparable sperm motility parameters displayed varying\n                      <jats:italic>in vitro<\/jats:italic>\n                      fertilization outcomes. Notably, the bull with the highest polyspermy rate achieved blastocyst rates similar to those of bulls with lower polyspermy rates. The number of apoptotic cells in the blastocysts was bull-dependent. Proteomic analysis revealed bull-specific signatures in sperm and blastocysts, with no differences at the 2\u20134 cell stage. Differences in the sperm proteome suggested that bull-dependent penetration and polyspermy rates might be associated with the ability of the sperm to undergo capacitation and acrosomal reaction. At the blastocyst level, the bull with the highest polyspermy rates produced lower quality blastocysts due to imbalances in key proteins and pathways for embryo development. In conclusion, bulls with similar blastocyst rates may differ in polyspermy rates and resulting embryo quality underscoring the importance of careful bull selection for\n                      <jats:italic>in vitro<\/jats:italic>\n                      embryo production.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1530\/rep-24-0296","type":"journal-article","created":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T09:09:25Z","timestamp":1741252165000},"update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-11","source":"Crossref","is-referenced-by-count":6,"title":["Decoding bull fertility in vitro: a proteomics exploration from sperm to blastocyst"],"prefix":"10.1093","volume":"169","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3737-1473","authenticated-orcid":true,"given":"Andrea","family":"Fern\u00e1ndez-Montoro","sequence":"first","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emin","family":"Araftpoor","sequence":"additional","affiliation":[{"name":"VIB-UGent Center for Medical Biotechnology, VIB, Ghent, Belgium"},{"name":"Department of Biomolecular Medicine, Ghent University, Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tine","family":"De Coster","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Angel-Velez","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"},{"name":"Research Group in Animal Sciences \u2013 INCA-CES, Universidad CES, Medellin, Colombia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcel","family":"B\u00fchler","sequence":"additional","affiliation":[{"name":"VIB-UGent Center for Medical Biotechnology, VIB, Ghent, Belgium"},{"name":"Department of Biomolecular Medicine, Ghent University, Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"Hedia","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"},{"name":"Theriogenology Department, Cairo University, Giza, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kris","family":"Gevaert","sequence":"additional","affiliation":[{"name":"VIB-UGent Center for Medical Biotechnology, VIB, Ghent, Belgium"},{"name":"Department of Biomolecular Medicine, Ghent University, Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ann","family":"Van Soom","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7043-1007","authenticated-orcid":true,"given":"Krishna Chaitanya","family":"Pavani","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"},{"name":"Department for Reproductive Medicine, Ghent University Hospital, Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katrien","family":"Smits","sequence":"additional","affiliation":[{"name":"Reproductive Biology Unit, Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, Merelbeke, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","reference":[{"key":"bib1","series-title":"Reprod Fertil Dev","first-page":"395","article-title":"Assessment of sperm quality parameters of six bulls showing different abilities to promote embryo development in vitro","volume":"18","author":"Alomar M","year":"2006","unstructured":"Alomar M\n, \nMahieu J\n, \nVerhaeghe B\n, et al.\n 2006 Assessment of sperm quality parameters of six bulls showing different abilities to promote embryo development in vitro. Reprod Fertil Dev 18 395\u2013402. (https:\/\/doi.org\/10.1071\/RD05132)"},{"key":"bib2","series-title":"Anim Reprod Sci","first-page":"48","article-title":"Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls","volume":"107","author":"Alomar M","year":"2008","unstructured":"Alomar M\n, \nTasiaux H\n, \nRemacle S\n, et al.\n 2008 Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls. Anim Reprod Sci 107 48\u201361. (https:\/\/doi.org\/10.1016\/J.ANIREPROSCI.2007.06.009)"},{"key":"bib3","series-title":"Sci Rep","article-title":"Controlled spermatozoa-oocyte interaction improves embryo quality in sheep","volume":"11","author":"Anzalone DA","year":"2021","unstructured":"Anzalone DA\n, \nPalazzese L\n, \nCzernik M\n, et al.\n 2021 Controlled spermatozoa-oocyte interaction improves embryo quality in sheep. Sci Rep 11 22629. (https:\/\/doi.org\/10.1038\/S41598-021-02000-Z)"},{"key":"bib4","series-title":"Sci Rep","article-title":"Semen levels of matrix metalloproteinase (MMP) and tissue inhibitor of metalloproteinases (TIMP) protein families members in men with high and low sperm DNA fragmentation","volume":"9","author":"Belardin LB","year":"2019","unstructured":"Belardin LB\n, \nAntoniassi MP\n, \nCamargo M\n, et al.\n 2019 Semen levels of matrix metalloproteinase (MMP) and tissue inhibitor of metalloproteinases (TIMP) protein families members in men with high and low sperm DNA fragmentation. Sci Rep 9 903. (https:\/\/doi.org\/10.1038\/S41598-018-37122-4)"},{"key":"bib5","series-title":"Hum Reprod","first-page":"204","article-title":"Separating the chaff from the wheat: antibody-based removal of DNA-fragmented sperm","volume":"38","author":"Belardin LB","year":"2023","unstructured":"Belardin LB\n, \nAntoniassi MP\n, \nCamargo M\n, et al.\n 2023 Separating the chaff from the wheat: antibody-based removal of DNA-fragmented sperm. Hum Reprod 38 204\u2013215. (https:\/\/doi.org\/10.1093\/HUMREP\/DEAC260)"},{"key":"bib6","series-title":"Fertil Steril","first-page":"467","article-title":"Updates on preimplantation embryo research","volume":"120","author":"Bissiere S","year":"2023","unstructured":"Bissiere S\n, \nHernandez B\n, \nRubio C\n, et al.\n 2023 Updates on preimplantation embryo research. Fertil Steril 120 467\u2013472. (https:\/\/doi.org\/10.1016\/J.FERTNSTERT.2023.04.039)"},{"key":"bib7","series-title":"Nat Commun","article-title":"Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential","volume":"7","author":"Bolton H","year":"2016","unstructured":"Bolton H\n, \nGraham SJL\n, \nVan Der Aa N\n, et al.\n 2016 Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential. Nat Commun 7 11165. (https:\/\/doi.org\/10.1038\/NCOMMS11165)"},{"key":"bib8","series-title":"Nat Commun","article-title":"P53 and mTOR signalling determine fitness selection through cell competition during early mouse embryonic development","volume":"9","author":"Bowling S","year":"2018","unstructured":"Bowling S\n, \nDi Gregorio A\n, \nSancho M\n, et al.\n 2018 P53 and mTOR signalling determine fitness selection through cell competition during early mouse embryonic development. Nat Commun 9 1763. (https:\/\/doi.org\/10.1038\/S41467-018-04167-Y)"},{"key":"bib9","series-title":"Hum Reprod Update","first-page":"535","article-title":"The contribution of human sperm proteins to the development and epigenome of the preimplantation embryo","volume":"24","author":"Castillo J","year":"2018","unstructured":"Castillo J\n, \nJodar M\n & \nOliva R\n\n 2018 The contribution of human sperm proteins to the development and epigenome of the preimplantation embryo. Hum Reprod Update 24 535\u2013555. (https:\/\/doi.org\/10.1093\/HUMUPD\/DMY017)"},{"key":"bib10","series-title":"J Biol Chem","first-page":"5309","article-title":"Caltrin, the calcium transport regulatory peptide of spermatozoa, modulates acrosomal exocytosis in response to the egg\u2019s zona pellucida","volume":"268","author":"Clark EN","year":"1993","unstructured":"Clark EN\n, \nCorron ME\n & \nFlorman HM\n\n 1993 Caltrin, the calcium transport regulatory peptide of spermatozoa, modulates acrosomal exocytosis in response to the egg\u2019s zona pellucida. J Biol Chem 268 5309\u20135316. (https:\/\/doi.org\/10.1016\/S0021-9258(18)53534-1)"},{"key":"bib11","series-title":"Reproduction","first-page":"651","article-title":"Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos","volume":"131","author":"Corcoran D","year":"2006","unstructured":"Corcoran D\n, \nFair T\n, \nPark S\n, et al.\n 2006 Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Reproduction 131 651\u2013660. (https:\/\/doi.org\/10.1530\/REP.1.01015)"},{"key":"bib12","series-title":"Genome Biol","article-title":"Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts","volume":"23","author":"De Coster T","year":"2022","unstructured":"De Coster T\n, \nMasset H\n, \nT\u0161uiko O\n, et al.\n 2022 Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts. Genome Biol 23 201. (https:\/\/doi.org\/10.1186\/S13059-022-02763-2)"},{"key":"bib13","series-title":"Braz J Med Biol Res","first-page":"191","article-title":"Aspects of energetic substrate metabolism of in vitro and in vivo bovine embryos","volume":"48","author":"De Souza DK","year":"2015","unstructured":"De Souza DK\n, \nSalles LP\n, \nRosa e Silva AAM\n, et al.\n 2015 Aspects of energetic substrate metabolism of in vitro and in vivo bovine embryos. Braz J Med Biol Res 48 191\u2013197. (https:\/\/doi.org\/10.1590\/1414-431X20143744)"},{"key":"bib14","series-title":"Nat Methods","first-page":"41","article-title":"DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput","volume":"17","author":"Demichev V","year":"2020","unstructured":"Demichev V\n, \nMessner CB\n, \nVernardis SI\n, et al.\n 2020 DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput. Nat Methods 17 41\u201344. (https:\/\/doi.org\/10.1038\/S41592-019-0638-X)"},{"key":"bib15","series-title":"Nat Commun","article-title":"dia-PASEF data analysis using FragPipe and DIA-NN for deep proteomics of low sample amounts","volume":"13","author":"Demichev V","year":"2022","unstructured":"Demichev V\n, \nSzyrwiel L\n, \nYu F\n, et al.\n 2022 dia-PASEF data analysis using FragPipe and DIA-NN for deep proteomics of low sample amounts. Nat Commun 13 3944. (https:\/\/doi.org\/10.1038\/S41467-022-31492-0)"},{"key":"bib16","series-title":"Reprod Biol","article-title":"How to beat the bull: lycopene as a tool to improve in vitro fertilization efficiency in bulls with high polyspermy","volume":"24","author":"Fern\u00e1ndez-Montoro A","year":"2024","unstructured":"Fern\u00e1ndez-Montoro A\n, \nAngel-Velez D\n, \nCava-Cami B\n, et al.\n 2024 How to beat the bull: lycopene as a tool to improve in vitro fertilization efficiency in bulls with high polyspermy. Reprod Biol 24 100888. (https:\/\/doi.org\/10.1016\/J.REPBIO.2024.100888)"},{"key":"bib17","article-title":"Review: recent advances in bovine in vitro embryo production: reproductive biotechnology history and methods","author":"Ferr\u00e9 LB","year":"2019","unstructured":"Ferr\u00e9 LB\n, \nKjelland ME\n, \nStr\u00f8bech LB\n, et al.\n 2019 Review: recent advances in bovine in vitro embryo production: reproductive biotechnology history and methods. (https:\/\/doi.org\/10.1017\/S1751731119002775)"},{"key":"bib18","series-title":"Reprod Fertil Dev","first-page":"167","article-title":"Polyspermic penetration in porcine IVM-IVF systems","volume":"15","author":"Funahashi H","year":"2003","unstructured":"Funahashi H\n\n 2003 Polyspermic penetration in porcine IVM-IVF systems. Reprod Fertil Dev 15 167\u2013177. (https:\/\/doi.org\/10.1071\/RD02076)"},{"key":"bib19","series-title":"R package version 1.14.1. Bioconductor","article-title":"Quantitative features for mass spectrometry data","author":"Gatto L","year":"2024","unstructured":"Gatto L\n & \nVanderaa C\n\n 2024 Quantitative features for mass spectrometry data. R package version 1.14.1. Bioconductor. (https:\/\/bioconductor.org\/packages\/release\/bioc\/html\/QFeatures.html)"},{"key":"bib20","series-title":"Anim Reprod Sci","first-page":"201","article-title":"Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls","volume":"103","author":"Gillan L","year":"2008","unstructured":"Gillan L\n, \nKroetsch T\n, \nChis Maxwell WM\n, et al.\n 2008 Assessment of in vitro sperm characteristics in relation to fertility in dairy bulls. Anim Reprod Sci 103 201\u2013214. (https:\/\/doi.org\/10.1016\/J.ANIREPROSCI.2006.12.010)"},{"key":"bib21","series-title":"Anal Chem","first-page":"6278","article-title":"MSqRob takes the missing hurdle: uniting intensity- and count-based proteomics","volume":"92","author":"Goeminne LJE","year":"2020","unstructured":"Goeminne LJE\n, \nSticker A\n, \nMartens L\n, et al.\n 2020 MSqRob takes the missing hurdle: uniting intensity- and count-based proteomics. Anal Chem 92 6278\u20136287. (https:\/\/doi.org\/10.1021\/ACS.ANALCHEM.9B04375\/SUPPL_FILE\/AC9B04375_SI_006.XLSX)"},{"key":"bib22","series-title":"Sci Rep","first-page":"14661","article-title":"Protein signatures of seminal plasma from bulls with contrasting frozen-thawed sperm viability","volume":"10","author":"Gomes FP","year":"2020","unstructured":"Gomes FP\n, \nPark R\n, \nViana AG\n, et al.\n 2020 Protein signatures of seminal plasma from bulls with contrasting frozen-thawed sperm viability. Sci Rep 10 14661. (https:\/\/doi.org\/10.1038\/s41598-020-71015-9)"},{"key":"bib23","series-title":"Sci Rep","first-page":"1","article-title":"Characterization and functional roles of paternal RNAs in 2\u20134 cell bovine embryos","volume":"9","author":"Gross N","year":"2019","unstructured":"Gross N\n, \nStrillacci MG\n, \nPe\u00f1agaricano F\n, et al.\n 2019 Characterization and functional roles of paternal RNAs in 2\u20134 cell bovine embryos. Sci Rep 9 1\u20139. (https:\/\/doi.org\/10.1038\/s41598-019-55868-3)"},{"key":"bib24","series-title":"Theriogenology","first-page":"24","article-title":"The evolution of porcine embryo in vitro production","volume":"81","author":"Grupen CG","year":"2014","unstructured":"Grupen CG\n\n 2014 The evolution of porcine embryo in vitro production. Theriogenology 81 24\u201337. (https:\/\/doi.org\/10.1016\/J.THERIOGENOLOGY.2013.09.022)"},{"key":"bib25","series-title":"Biol Reprod","first-page":"1110","article-title":"Growth retardation of inner cell mass cells in polyspermic porcine embryos produced in vitro","volume":"60","author":"Han YM","year":"1999","unstructured":"Han YM\n, \nAbeydeera LR\n, \nKim JH\n, et al.\n 1999 Growth retardation of inner cell mass cells in polyspermic porcine embryos produced in vitro. Biol Reprod 60 1110\u20131113. (https:\/\/doi.org\/10.1095\/BIOLREPROD60.5.1110)"},{"key":"bib26","series-title":"Vet World","first-page":"593","article-title":"Comparative developmental competence of in vitro embryos recovered from Bali cattle with normal and poor sperm motility","volume":"17","author":"Hasbi H","year":"2024","unstructured":"Hasbi H\n, \nIskandar H\n, \nSonjaya H\n, et al.\n 2024 Comparative developmental competence of in vitro embryos recovered from Bali cattle with normal and poor sperm motility. Vet World 17 593\u2013601. (https:\/\/doi.org\/10.14202\/VETWORLD.2024.593-601)"},{"key":"bib27","series-title":"Reproduction","first-page":"R113","article-title":"Sperm and seminal plasma RNAs: what roles do they play beyond fertilization?","volume":"158","author":"Jodar M","year":"2019","unstructured":"Jodar M\n\n 2019 Sperm and seminal plasma RNAs: what roles do they play beyond fertilization? Reproduction 158 R113\u2013R123. (https:\/\/doi.org\/10.1530\/REP-18-0639)"},{"key":"bib28","series-title":"Anim Reprod Sci","first-page":"88","article-title":"Sperm macromolecules associated with bull fertility","volume":"169","author":"Kaya A","year":"2016","unstructured":"Kaya A\n & \nMemili E\n\n 2016 Sperm macromolecules associated with bull fertility. Anim Reprod Sci 169 88\u201394. (https:\/\/doi.org\/10.1016\/J.ANIREPROSCI.2016.02.015)"},{"key":"bib29","series-title":"Biochem J","first-page":"547","article-title":"Catalytic activity of bovine seminal ribonuclease is essential for its immunosuppressive and other biological activities","volume":"308","author":"Kim JS","year":"1995","unstructured":"Kim JS\n, \nSoucek J\n, \nMatousek J\n, et al.\n 1995 Catalytic activity of bovine seminal ribonuclease is essential for its immunosuppressive and other biological activities. Biochem J 308 547\u2013550. (https:\/\/doi.org\/10.1042\/BJ3080547)"},{"key":"bib30","series-title":"Anim Reprod Sci","first-page":"101","article-title":"Effects of in vitro fertilization conditions on preimplantation development and quality of pig embryos","volume":"90","author":"Koo DB","year":"2005","unstructured":"Koo DB\n, \nKim YJ\n, \nYu I\n, et al.\n 2005 Effects of in vitro fertilization conditions on preimplantation development and quality of pig embryos. Anim Reprod Sci 90 101\u2013110. (https:\/\/doi.org\/10.1016\/J.ANIREPROSCI.2005.01.005)"},{"key":"bib31","series-title":"Reprod Fertil Dev","first-page":"465","article-title":"Male-dependent variability of fertilization and embryo development in two bovine in vitro fertilization systems and the effects of casein phosphopeptides (CPPs)","volume":"9","author":"Kreysing U","year":"1997","unstructured":"Kreysing U\n, \nNagai T\n & \nNiemann H\n\n 1997 Male-dependent variability of fertilization and embryo development in two bovine in vitro fertilization systems and the effects of casein phosphopeptides (CPPs). Reprod Fertil Dev 9 465\u2013474. (https:\/\/doi.org\/10.1071\/R96097)"},{"key":"bib32","series-title":"BMC Genom","article-title":"Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos","volume":"18","author":"Kropp J","year":"2017","unstructured":"Kropp J\n, \nCarrillo JA\n, \nNamous H\n, et al.\n 2017 Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genom 18 280. (https:\/\/doi.org\/10.1186\/S12864-017-3673-Y)"},{"key":"bib33","series-title":"Sci Rep","first-page":"19408","article-title":"The mitochondrial respiration signature of the bovine blastocyst reflects both environmental conditions of development as well as embryo quality","volume":"13","author":"Kurzella J","year":"2023","unstructured":"Kurzella J\n, \nMiskel D\n, \nRings F\n, et al.\n 2023 The mitochondrial respiration signature of the bovine blastocyst reflects both environmental conditions of development as well as embryo quality. Sci Rep 13 19408. (https:\/\/doi.org\/10.1038\/s41598-023-45691-2)"},{"key":"bib34","series-title":"Nucleic Acids Res","first-page":"W199","article-title":"WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs","volume":"47","author":"Liao Y","year":"2019","unstructured":"Liao Y\n, \nWang J\n, \nJaehnig EJ\n, et al.\n 2019 WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res 47 W199\u2013W205. (https:\/\/doi.org\/10.1093\/NAR\/GKZ401)"},{"key":"bib35","series-title":"Reproduction","first-page":"337","article-title":"Sire modulates developmental kinetics and transcriptome of the bovine embryo","volume":"166","author":"Lockhart KN","year":"2023","unstructured":"Lockhart KN\n, \nDrum JN\n, \nBalboula AZ\n, et al.\n 2023 Sire modulates developmental kinetics and transcriptome of the bovine embryo. Reproduction 166 337\u2013348. (https:\/\/doi.org\/10.1530\/REP-23-0030\/VIDEO-2)"},{"key":"bib36","series-title":"Reproduction","first-page":"361","article-title":"Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization","volume":"102","author":"Long CR","year":"1994","unstructured":"Long CR\n, \nDamiani P\n, \nPinto-Correia C\n, et al.\n 1994 Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization. Reproduction 102 361\u2013369. (https:\/\/doi.org\/10.1530\/JRF.0.1020361)"},{"key":"bib37","series-title":"Reprod Nutr Dev","first-page":"259","article-title":"Evaluation of bull semen fertility by homologous in vitro fertilization tests","volume":"30","author":"Marquant-Le Guienne B","year":"1990","unstructured":"Marquant-Le Guienne B\n, \nHumblot P\n, \nThibier M\n, et al.\n 1990 Evaluation of bull semen fertility by homologous in vitro fertilization tests. Reprod Nutr Dev 30 259\u2013266. (https:\/\/doi.org\/10.1051\/rnd:19900212)"},{"key":"bib38","series-title":"Theriogenology","first-page":"503","article-title":"In vitro penetration assay of boar sperm fertility: effect of various factors on the penetrability of immature pig oocytes","volume":"46","author":"Mat\u00e1s C","year":"1996","unstructured":"Mat\u00e1s C\n, \nMart\u00ednez E\n, \nV\u00e1zquez JM\n, et al.\n 1996 In vitro penetration assay of boar sperm fertility: effect of various factors on the penetrability of immature pig oocytes. Theriogenology 46 503\u2013513. (https:\/\/doi.org\/10.1016\/0093-691X(96)00172-0)"},{"key":"bib39","series-title":"Expet Rev Proteonomics","first-page":"19","article-title":"Mapping the human sperm proteome \u2013 novel insights into reproductive research","volume":"20","author":"Miyazaki MA","year":"2023","unstructured":"Miyazaki MA\n, \nGuilharducci RL\n, \nIntasqui P\n, et al.\n 2023 Mapping the human sperm proteome \u2013 novel insights into reproductive research. Expet Rev Proteonomics 20 19\u201345. (https:\/\/doi.org\/10.1080\/14789450.2023.2210764)"},{"key":"bib40","series-title":"Anim Sci J","article-title":"Selection based on morphological features of porcine embryos produced by in vitro fertilization: timing of early cleavages and the effect of polyspermy","volume":"91","author":"Nguyen HT","year":"2020","unstructured":"Nguyen HT\n, \nDang-Nguyen TQ\n, \nSomfai T\n, et al.\n 2020 Selection based on morphological features of porcine embryos produced by in vitro fertilization: timing of early cleavages and the effect of polyspermy. Anim Sci J 91 e13401. (https:\/\/doi.org\/10.1111\/ASJ.13401)"},{"key":"bib41","series-title":"Theriogenology","first-page":"1375","article-title":"Variations in penetration rates in vitro of bovine follicular oocytes do not reflect conception rates after artificial insemination using frozen semen from different bulls","volume":"29","author":"Ohgoda O","year":"1988","unstructured":"Ohgoda O\n, \nNiwa K\n, \nYuhara M\n, et al.\n 1988 Variations in penetration rates in vitro of bovine follicular oocytes do not reflect conception rates after artificial insemination using frozen semen from different bulls. Theriogenology 29 1375\u20131381. (https:\/\/doi.org\/10.1016\/0093-691X(88)90018-0)"},{"key":"bib42","series-title":"BMC Syst Biol","first-page":"19","article-title":"Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility","volume":"2","author":"Peddinti D","year":"2008","unstructured":"Peddinti D\n, \nNanduri B\n, \nKaya A\n, et al.\n 2008 Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2 19. (https:\/\/doi.org\/10.1186\/1752-0509-2-19)"},{"key":"bib43","series-title":"2012 Statistics of Embryo Collection and Transfer in Domestic Farm Animals","author":"Perry G","year":"2013","unstructured":"Perry G\n\n 2013 2012 Statistics of Embryo Collection and Transfer in Domestic Farm Animals. International Embryo Transfer Society. (https:\/\/doi.org\/10.13140\/RG.2.2.24719.18086)"},{"key":"bib44","series-title":"Nat Cell Biol","first-page":"117","article-title":"Oct4 kinetics predict cell lineage patterning in the early mammalian embryo","volume":"13","author":"Plachta N","year":"2011","unstructured":"Plachta N\n, \nBollenbach T\n, \nPease S\n, et al.\n 2011 Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat Cell Biol 13 117\u2013123. (https:\/\/doi.org\/10.1038\/NCB2154)"},{"key":"bib45","series-title":"Int J Mol Sci","first-page":"3159","article-title":"Testis-specific isoform of Na\/K-ATPase (ATP1A4) interactome in raft and non-raft membrane fractions from capacitated bovine sperm","volume":"20","author":"Rajamanickam GD","year":"2019","unstructured":"Rajamanickam GD\n, \nKastelic JP\n & \nThundathil JC\n\n 2019 Testis-specific isoform of Na\/K-ATPase (ATP1A4) interactome in raft and non-raft membrane fractions from capacitated bovine sperm. Int J Mol Sci 20 3159. (https:\/\/doi.org\/10.3390\/IJMS20133159)"},{"key":"bib46","series-title":"Theriogenology","first-page":"751","article-title":"Effects of heparin, sperm concentration and bull variation on in vitro fertilization of bovine oocytes in a protein-free medium","volume":"43","author":"Saeki K","year":"1995","unstructured":"Saeki K\n, \nNagao Y\n, \nHoshi M\n, et al.\n 1995 Effects of heparin, sperm concentration and bull variation on in vitro fertilization of bovine oocytes in a protein-free medium. Theriogenology 43 751\u2013759. (https:\/\/doi.org\/10.1016\/0093-691X(95)00017-3)"},{"key":"bib47","series-title":"Hum Reprod","first-page":"1916","article-title":"The fate of the mosaic embryo: chromosomal constitution and development of day 4, 5 and 8 human embryos","volume":"25","author":"Santos MA","year":"2010","unstructured":"Santos MA\n, \nTeklenburg G\n, \nMacKlon NS\n, et al.\n 2010 The fate of the mosaic embryo: chromosomal constitution and development of day 4, 5 and 8 human embryos. Hum Reprod 25 1916\u20131926. (https:\/\/doi.org\/10.1093\/HUMREP\/DEQ139)"},{"key":"bib48","series-title":"Andrologia","article-title":"Comparative high-throughput analysis of sperm membrane proteins from crossbred bulls with contrasting fertility","volume":"54","author":"Saraf KK","year":"2022","unstructured":"Saraf KK\n, \nKumaresan A\n, \nArathi BP\n, et al.\n 2022 Comparative high-throughput analysis of sperm membrane proteins from crossbred bulls with contrasting fertility. Andrologia 54 e14451. (https:\/\/doi.org\/10.1111\/AND.14451)"},{"key":"bib49","series-title":"Reprod Domest Anim","first-page":"1090","article-title":"The influence of gamete co-incubation length on the in vitro fertility and sex ratio of bovine bulls with different penetration speed","volume":"46","author":"Sattar A","year":"2011","unstructured":"Sattar A\n, \nRubessa M\n, \nDi Francesco S\n, et al.\n 2011 The influence of gamete co-incubation length on the in vitro fertility and sex ratio of bovine bulls with different penetration speed. Reprod Domest Anim 46 1090\u20131097. (https:\/\/doi.org\/10.1111\/J.1439-0531.2011.01791.X)"},{"key":"bib50","series-title":"Reproduction","first-page":"433","article-title":"Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome","volume":"146","author":"Sim\u00f5es R","year":"2013","unstructured":"Sim\u00f5es R\n, \nFeitosa WB\n, \nSiqueira AFP\n, et al.\n 2013 Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome. Reproduction 146 433\u2013441. (https:\/\/doi.org\/10.1530\/REP-13-0123)"},{"key":"bib51","series-title":"Reproduction","first-page":"779","article-title":"The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg","volume":"142","author":"Snook RR","year":"2011","unstructured":"Snook RR\n, \nHosken DJ\n & \nKarr TL\n\n 2011 The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142 779\u2013792. (https:\/\/doi.org\/10.1530\/REP-11-0255)"},{"key":"bib52","series-title":"Microsc Res Tech","first-page":"327","article-title":"In vitro fertilization and polyspermy in the pig: factors affecting fertilization rates and cytoskeletal reorganization of the oocyte","volume":"61","author":"Suzuki H","year":"2003","unstructured":"Suzuki H\n, \nSaito Y\n, \nKagawa N\n, et al.\n 2003 In vitro fertilization and polyspermy in the pig: factors affecting fertilization rates and cytoskeletal reorganization of the oocyte. Microsc Res Tech 61 327\u2013334. (https:\/\/doi.org\/10.1002\/JEMT.10345)"},{"key":"bib53","series-title":"Hum Reprod Update","first-page":"395","article-title":"Contribution of semen to early embryo development: fertilization and beyond","volume":"29","author":"Vallet-Buisan M","year":"2023","unstructured":"Vallet-Buisan M\n, \nMecca R\n, \nJones C\n, et al.\n 2023 Contribution of semen to early embryo development: fertilization and beyond. Hum Reprod Update 29 395\u2013433. (https:\/\/doi.org\/10.1093\/HUMUPD\/DMAD006)"},{"key":"bib55","series-title":"Embryo Technology Newsl","first-page":"4","article-title":"2022 Statistics of embryo production and transfer in domestic farm animals","volume":"41","author":"Viana JH","year":"2023","unstructured":"Viana JH\n\n 2023 2022 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsl 41 4. (https:\/\/www.iets.org\/Portals\/0\/Documents\/Public\/Committees\/DRC\/IETS_Data_Retrieval_Report_2022.pdf)"},{"key":"bib54","series-title":"Sci Rep","article-title":"Proteomic landscape of seminal plasma associated with dairy bull fertility","volume":"8","author":"Viana AGA","year":"2018","unstructured":"Viana AGA\n, \nMartins AMA\n, \nPontes AH\n, et al.\n 2018 Proteomic landscape of seminal plasma associated with dairy bull fertility. Sci Rep 8 16323. (https:\/\/doi.org\/10.1038\/S41598-018-34152-W)"},{"key":"bib56","series-title":"Mol Reprod Dev","first-page":"308","article-title":"Morphologic comparison of ovulated and in vitro-matured porcine oocytes, with particular reference to polyspermy after in vitro fertilization","volume":"49","author":"Wang W-H","year":"1998","unstructured":"Wang W-H\n, \nAbeydeera LR\n, \nPrather RS\n, et al.\n 1998 Morphologic comparison of ovulated and in vitro-matured porcine oocytes, with particular reference to polyspermy after in vitro fertilization. Mol Reprod Dev 49 308\u2013316. (https:\/\/doi.org\/10.1002\/(SICI)1098-2795(199803)49:3)"},{"key":"bib57","series-title":"ggplot2: Elegant Graphics for Data Analysis","author":"Wickham H","year":"2016","unstructured":"Wickham H\n\n 2016 ggplot2: Elegant Graphics for Data Analysis. Springer. (https:\/\/doi.org\/10.1007\/978-3-319-24277-4)"},{"key":"bib58","series-title":"Anal Biochem","first-page":"228","article-title":"Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining","volume":"416","author":"Wydooghe E","year":"2011","unstructured":"Wydooghe E\n, \nVandaele L\n, \nBeek J\n, et al.\n 2011 Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal Biochem 416 228\u2013230. (https:\/\/doi.org\/10.1016\/J.AB.2011.05.033)"},{"key":"bib59","series-title":"Reprod Fertil Dev","first-page":"717","article-title":"Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture","volume":"26","author":"Wydooghe E","year":"2014","unstructured":"Wydooghe E\n, \nHeras S\n, \nDewulf J\n, et al.\n 2014 Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture. Reprod Fertil Dev 26 717\u2013724. (https:\/\/doi.org\/10.1071\/RD13043)"},{"key":"bib60","series-title":"Cell Tissue Res","first-page":"271","article-title":"Ultrastructural study of polyspermy during early embryo development in pigs, observed by scanning electron microscope and transmission electron microscope","volume":"303","author":"Xia P","year":"2001","unstructured":"Xia P\n, \nWang Z\n, \nYang Z\n, et al.\n 2001 Ultrastructural study of polyspermy during early embryo development in pigs, observed by scanning electron microscope and transmission electron microscope. Cell Tissue Res 303 271\u2013275. (https:\/\/doi.org\/10.1007\/S004410000315)"},{"key":"bib61","series-title":"Theriogenology","first-page":"745","article-title":"In vitro fertilization of in vitro matured pig oocytes: effects of boar and ejaculate fraction","volume":"45","author":"Xu X","year":"1996a","unstructured":"Xu X\n, \nDing J\n, \nSeth PC\n, et al.\n 1996a In vitro fertilization of in vitro matured pig oocytes: effects of boar and ejaculate fraction. Theriogenology 45 745\u2013755. (https:\/\/doi.org\/10.1016\/0093-691X(96)00004-0)"},{"key":"bib62","series-title":"Theriogenology","first-page":"1325","article-title":"Semen dilution for assessment of boar ejaculate quality in pig IVM and IVF systems","volume":"46","author":"Xu X","year":"1996b","unstructured":"Xu X\n, \nSeth PC\n, \nHarbison DS\n, et al.\n 1996b Semen dilution for assessment of boar ejaculate quality in pig IVM and IVF systems. Theriogenology 46 1325\u20131337. (https:\/\/doi.org\/10.1016\/S0093-691X(96)00313-5)"},{"key":"bib63","series-title":"Zygote","first-page":"371","article-title":"Fertility of mammalian spermatozoa: its development and relativity","volume":"2","author":"Yanagimachi R","year":"1994","unstructured":"Yanagimachi R\n\n 1994 Fertility of mammalian spermatozoa: its development and relativity. Zygote 2 371\u2013372. 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