{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T03:15:53Z","timestamp":1791170153552,"version":"4.1.0"},"reference-count":78,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,11,5]],"date-time":"2018-11-05T00:00:00Z","timestamp":1541376000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2018,11,5]],"date-time":"2018-11-05T00:00:00Z","timestamp":1541376000000},"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>\n                  <jats:p>\n                    Male fertility is the ability of sperm to fertilize the egg and sustain embryo development. Several factors determine the fertilizing capacity of mammalian sperm, including those intrinsic to sperm and components of the seminal plasma. The present study analyzed the seminal fluid proteome of\n                    <jats:italic>Bos taurus<\/jats:italic>\n                    and potential associations between proteins and fertility scores. Mass spectrometry coupled with nano HPLC allowed the identification of 1,159 proteins in the dairy bull seminal plasma. There were 50 and 29 seminal proteins more abundant in high (HF) low fertility (LF) bulls, respectively. Based on multivariate analysis, C-type natriuretic peptide, TIMP-2, BSP5 and sulfhydryl oxidase indicated relationship with HF bulls. Clusterin, tissue factor pathway inhibitor 2, galectin-3-binding protein and 5\u2032-nucleotidase were associated with LF bulls. Abundance of NAD(P)(+)-arginine ADP-ribosyltransferase, prosaposin and transmembrane protein 2 proteins had the highest positive correlations with fertility ranking. Quantities of vitamin D-binding protein, nucleotide exchange factor SIL1 and galectin-3-binding protein showed the highest negative correlations with fertility ranking. A fertility ranking score was calculated and the relationship with these proteins was significant (Spearman\u2019s rho\u2009=\u20090.94). The present findings represent a major and novel contribution to the study of bovine seminal proteins. Indicators of fertility can be used to improve reproductive biotechnologies.\n                  <\/jats:p>","DOI":"10.1038\/s41598-018-34152-w","type":"journal-article","created":{"date-parts":[[2018,10,30]],"date-time":"2018-10-30T07:00:43Z","timestamp":1540882843000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":103,"title":["Proteomic landscape of seminal plasma associated with dairy bull fertility"],"prefix":"10.1038","volume":"8","author":[{"given":"A. G. A.","family":"Viana","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. M. A.","family":"Martins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. H.","family":"Pontes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"W.","family":"Fontes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. S.","family":"Castro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C. A. O.","family":"Ricart","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2871-4430","authenticated-orcid":false,"given":"M. V.","family":"Sousa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A.","family":"Kaya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E.","family":"Topper","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E.","family":"Memili","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. A.","family":"Moura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,11,5]]},"reference":[{"key":"34152_CR1","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.anireprosci.2016.02.015","volume":"169","author":"A Kaya","year":"2016","unstructured":"Kaya, A. & Memili, E. Sperm macromolecules associated with bull fertility. Anim Reprod Sci. 169, 88\u201394 (2016).","journal-title":"Anim Reprod Sci."},{"key":"34152_CR2","doi-asserted-by":"publisher","first-page":"637","DOI":"10.3906\/vet-1404-76","volume":"38","author":"AM Parisi","year":"2014","unstructured":"Parisi, A. M., Thompson, S. K., Kaya, A. & Memili, E. Molecular, cellular, and physiological determinants of bull fertility. Turk J Vet Anim Sci. 38, 637\u2013642 (2014).","journal-title":"Turk J Vet Anim Sci."},{"issue":"3","key":"34152_CR3","doi-asserted-by":"publisher","first-page":"191","DOI":"10.21451\/1984-3143-AR884","volume":"13","author":"AA Moura","year":"2016","unstructured":"Moura, A. A. & Memili, E. Functional aspects of seminal plasma and sperm proteins and their potential as molecular markers of fertility. Anim Reprod. 13(3), 191\u2013199 (2016).","journal-title":"Anim Reprod."},{"key":"34152_CR4","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1002\/mrd.22202","volume":"80","author":"M Salehi","year":"2013","unstructured":"Salehi, M. et al. Correlation between human clusterin in seminal plasma with sperm protamine deficiency and DNA fragmentation. Mol Reprod Dev. 80, 718\u2013724 (2013).","journal-title":"Mol Reprod Dev."},{"key":"34152_CR5","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1016\/j.rbmo.2010.06.022","volume":"21","author":"JM Feugang","year":"2010","unstructured":"Feugang, J. M. et al. Transcriptome analysis of bull spermatozoa: implications for male fertility. Reprod Biomed Online. 21, 312\u2013324 (2010).","journal-title":"Reprod Biomed Online."},{"key":"34152_CR6","doi-asserted-by":"publisher","DOI":"10.1186\/1752-0509-2-19","volume":"2","author":"D Peddinti","year":"2008","unstructured":"Peddinti, D. et al. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with bull fertility. BMC Syst Biol. 2, 19 (2008).","journal-title":"BMC Syst Biol."},{"key":"34152_CR7","doi-asserted-by":"crossref","unstructured":"Velho, A. L. C. et al. Applications of metabolomics in reproductive biology. In: H Schatten & G. M. Constantinscu (Eds) Animal Models and Human Reproduction. Fisrt Edition. 509\u2013517 (2017).","DOI":"10.1002\/9781118881286.ch20"},{"key":"34152_CR8","doi-asserted-by":"publisher","first-page":"536","DOI":"10.2164\/jandrol.110.012583","volume":"33","author":"NS Juyena","year":"2012","unstructured":"Juyena, N. S. & Stelletta, C. Seminal plasma: an essential attribute to spermatozoa. J Androl. 33, 536\u2013551 (2012).","journal-title":"J Androl."},{"key":"34152_CR9","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1002\/bies.950160409","volume":"16","author":"J Aitken","year":"1994","unstructured":"Aitken, J. & Fisher, H. Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. Bioessays. 16, 259\u2013267 (1994).","journal-title":"Bioessays."},{"key":"34152_CR10","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/S0165-0378(01)00098-5","volume":"53","author":"P Manjunath","year":"2002","unstructured":"Manjunath, P. & Th\u00e9rien, I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol. 53, 109\u2013119 (2002).","journal-title":"J Reprod Immunol."},{"key":"34152_CR11","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1095\/biolreprod52.2.390","volume":"52","author":"MA Henault","year":"1995","unstructured":"Henault, M. A., Killian, G. J., Kavanaugh, J. F. & Griel, L. C. Effect of accessory sex gland fluid from bulls of differing fertilities on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes. Biol Reprod. 52, 390\u2013397 (1995).","journal-title":"Biol Reprod."},{"key":"34152_CR12","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1095\/biolreprod.106.052589","volume":"75","author":"Y Hao","year":"2006","unstructured":"Hao, Y. et al. Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol Reprod. 75, 726\u2013733 (2006).","journal-title":"Biol Reprod."},{"key":"34152_CR13","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1016\/j.theriogenology.2015.09.044","volume":"85","author":"P Rodr\u00edguez-Villamil","year":"2016","unstructured":"Rodr\u00edguez-Villamil, P. et al. Purification of binder of sperm protein 1 (BSP1) and its effects on bovine in vitro embryo development after fertilization with ejaculated and epididymal sperm. Theriogenology. 85, 540\u2013554 (2016).","journal-title":"Theriogenology."},{"key":"34152_CR14","doi-asserted-by":"publisher","first-page":"813","DOI":"10.2174\/0929866054864292","volume":"12","author":"TI Assump\u00e7\u00e3o","year":"2005","unstructured":"Assump\u00e7\u00e3o, T. I., Fontes, W., Sousa, M. V. & Ricart, C. A. O. Proteome analysis of Nelore bull (Bos taurus indicus) seminal plasma. Protein Pept Lett. 12, 813\u2013817 (2005).","journal-title":"Protein Pept Lett."},{"key":"34152_CR15","doi-asserted-by":"publisher","first-page":"534","DOI":"10.2164\/jandrol.05201","volume":"27","author":"AA Moura","year":"2006","unstructured":"Moura, A. A., Chapman, D. A., Koc, H. & Killian, G. J. Proteins of the cauda epididymal fluid associated with fertility of mature dairy bulls. J Androl. 27, 534\u2013541 (2006).","journal-title":"J Androl."},{"key":"34152_CR16","doi-asserted-by":"publisher","first-page":"5826","DOI":"10.1002\/pmic.200500830","volume":"6","author":"VC Kelly","year":"2006","unstructured":"Kelly, V. C. et al. Characterization of bovine seminal plasma by proteomics. Proteomics. 6, 5826\u20135833 (2006).","journal-title":"Proteomics."},{"key":"34152_CR17","first-page":"1","volume":"100","author":"B Westfalewicz","year":"2016","unstructured":"Westfalewicz, B. et al. Analysis of bull (Bos taurus) seminal vesicle fluid proteome in relation to seminal plasma proteome. J. Dairy Sci. 100, 1\u201317 (2016).","journal-title":"J. Dairy Sci."},{"key":"34152_CR18","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1007\/s00441-015-2320-7","volume":"363","author":"DT Carrell","year":"2016","unstructured":"Carrell, D. T., Aston, K. I., Oliva, R., Emery, B. R. & De Jonge, C. J. The \u201comics\u201d of human male infertility: integrating big data in a systems biology approach. Cell Tissue Res. 363, 295\u2013312 (2016).","journal-title":"Cell Tissue Res."},{"key":"34152_CR19","doi-asserted-by":"publisher","first-page":"206","DOI":"10.4103\/0974-1208.142485","volume":"7","author":"JAP Cadavid","year":"2014","unstructured":"Cadavid, J. A. P., Alvarez, A., Markert, U. R. & Maya, W. C. Differential protein expression in seminal plasma from fertile and infertile males. J Hum Reprod Sci. 7, 206\u2013211 (2014).","journal-title":"J Hum Reprod Sci."},{"key":"34152_CR20","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1016\/j.rbmo.2015.01.010","volume":"30","author":"E Giacomini","year":"2015","unstructured":"Giacomini, E. et al. Comparative analysis of the seminal plasma proteomes of oligoasthenozoospermic and normozoospermic men. Reprod Biomed Online. 30, 522\u2013531 (2015).","journal-title":"Reprod Biomed Online."},{"key":"34152_CR21","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1016\/j.theriogenology.2014.05.024","volume":"82","author":"V Gonz\u00e1lez-Cadavid","year":"2014","unstructured":"Gonz\u00e1lez-Cadavid, V. et al. Seminal plasma proteins of adult boars and correlations with sperm parameters. Theriogenology. 82, 697\u2013707 (2014).","journal-title":"Theriogenology."},{"key":"34152_CR22","doi-asserted-by":"publisher","first-page":"1202","DOI":"10.1095\/biolreprod49.6.1202","volume":"49","author":"GJ Killian","year":"1993","unstructured":"Killian, G. J., Chapman, D. A. & Rogowski, L. A. Fertility-associated proteins in Holstein bull seminal plasma. Biol Reprod. 49, 1202\u20131207 (1993).","journal-title":"Biol Reprod."},{"key":"34152_CR23","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.anireprosci.2006.03.012","volume":"98","author":"AA Moura","year":"2007","unstructured":"Moura, A. A., Chapman, D. A., Koc, H. & Killian, G. J. A comprehensive proteomic analysis of the accessory sex gland fluid from mature Holstein bulls. Anim Reprod Sci. 98, 169\u2013188 (2007).","journal-title":"Anim Reprod Sci."},{"key":"34152_CR24","doi-asserted-by":"publisher","first-page":"5308","DOI":"10.2527\/jas.2016-0811","volume":"94","author":"JP Rego","year":"2016","unstructured":"Rego, J. P. et al. Proteomic analysis of seminal plasma and sperm cells and their associations with semen freezbility in Guzerat bulls. J Anim Sci. 94, 5308\u20135320 (2016).","journal-title":"J Anim Sci."},{"key":"34152_CR25","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.anireprosci.2017.05.014","volume":"183","author":"EB Menezes","year":"2017","unstructured":"Menezes, E. B. et al. Proteomic analysis of seminal plasma from locally-adapted \u201cCurraleiro P\u00e9-Duro bulls\u201d (Bos taurus): identifying biomarkers involved in sperm physiology in endangered animals for conservation of biodiversity. Anim Reprod Sci. 183, 86\u2013101 (2017).","journal-title":"Anim Reprod Sci."},{"key":"34152_CR26","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1046\/j.1439-0531.2002.00343.x","volume":"37","author":"S Tanghe","year":"2002","unstructured":"Tanghe, S., Van Soom, A., Sterckx, V., Maes, D. & de Kruif, A. Assessment of different sperm quality parameters to predict in vitro fertility of bulls. Reprod Domest Anim. 37, 127\u2013132 (2002).","journal-title":"Reprod Domest Anim."},{"key":"34152_CR27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.anireprosci.2014.04.016","volume":"148","author":"JPA Rego","year":"2014","unstructured":"Rego, J. P. A. et al. Seminal plasma proteome of electro ejaculated Bos inducus bulls. Anim Rep Sci. 148, 1\u201317 (2014).","journal-title":"Anim Rep Sci."},{"key":"34152_CR28","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1095\/biolreprod.108.074088","volume":"80","author":"P Manjunath","year":"2009","unstructured":"Manjunath, P., Lefebvre, J., Jois, P. S., Fan, J. & Wright, M. W. New nomenclature for mammalian BSP genes. Biol Reprod. 80, 394\u2013397 (2009).","journal-title":"Biol Reprod."},{"key":"34152_CR29","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1016\/j.anireprosci.2007.11.027","volume":"105","author":"CAE Souza","year":"2008","unstructured":"Souza, C. A. E., Moura, A. A., Monaco, E. & Killian, G. J. Binding patterns of bovine seminal plasma proteins A1\/A2, 30 kDa and osteopon tin on ejaculated sperm before and after incubation with isthmic and ampullary oviductal fluid. Anim Reprod Sci. 105, 72\u201389 (2008).","journal-title":"Anim Reprod Sci."},{"key":"34152_CR30","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1095\/biolreprod61.3.590","volume":"61","author":"I Th\u00e9rien.","year":"1999","unstructured":"Th\u00e9rien, I., Moreau, R. & Manjunath, P. Bovine seminal plasma phopholipid binding proteins stimulate phospholipid efflux from epididymal sperm. Biol Reprod. 61, 590\u2013598 (1999).","journal-title":"Biol Reprod."},{"key":"34152_CR31","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/s00441-015-2244-2","volume":"363","author":"SS Suarez","year":"2016","unstructured":"Suarez, S. S. Mammalian sperm interactions with the female reproductive tract. Cell Tissue Res. 363, 185\u2013194 (2016).","journal-title":"Cell Tissue Res."},{"key":"34152_CR32","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1186\/s12861-014-0040-y","volume":"14","author":"D Bebbere","year":"2014","unstructured":"Bebbere, D. et al. Expression of maternally derived KHDC3, NLRP5, OOEP and TLE6is associated with oocyte developmental competence in the ovine species. BMC Dev Biol. 14, 40 (2014).","journal-title":"BMC Dev Biol."},{"key":"34152_CR33","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1016\/j.cardiores.2005.12.002","volume":"69","author":"H Nagase","year":"2006","unstructured":"Nagase, H., Visse, R. & Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular Res. 69, 562\u2013573 (2006).","journal-title":"Cardiovascular Res."},{"key":"34152_CR34","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1006\/dbio.2000.9825","volume":"225","author":"LM Correa","year":"2000","unstructured":"Correa, L. M., Cho, C., Myles, D. G. & Primakoff, P. A role for a TIMP-3-sensitive, Zn(2+)-dependent metalloprotease in mammalian gamete membrane fusion. Dev Biol. 225, 124\u2013134 (2000).","journal-title":"Dev Biol."},{"key":"34152_CR35","doi-asserted-by":"publisher","first-page":"458","DOI":"10.1002\/(SICI)1098-2795(199612)45:4<458::AID-MRD8>3.0.CO;2-Q","volume":"45","author":"KJ Leco","year":"1996","unstructured":"Leco, K. J., Edwards, D. R. & Schultz, G. A. Tissue inhibitor of metalloproteinases-3 is the major metalloproteinase inhibitor in the decidualizing murine uterus. Mol Reprod Dev. 45, 458\u2013465 (1996).","journal-title":"Mol Reprod Dev."},{"key":"34152_CR36","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1002\/1098-2795(200103)58:3<336::AID-MRD12>3.0.CO;2-Z","volume":"58","author":"TC McCauley","year":"2001","unstructured":"McCauley, T. C., Zhang, H. M., Bellin, M. E. & Ax, R. L. Identification of a heparin-binding protein in bovine seminal fluid as tissue inhibitor of metalloproteinases-2. Mol Reprod Dev. 58, 336\u2013341 (2001).","journal-title":"Mol Reprod Dev."},{"key":"34152_CR37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0065083","volume":"8","author":"H Alvarez-Gallardo","year":"2013","unstructured":"Alvarez-Gallardo, H. et al. Gamete therapeutics: recombinant protein adsorption by sperm for increasing fertility via artificial insemination. Plos One 8, 1\u20137 (2013).","journal-title":"Plos One."},{"issue":"4","key":"34152_CR38","first-page":"323","volume":"48","author":"C Am\u0103linei","year":"2007","unstructured":"Am\u0103linei, C., C\u0103runtu, I. & B\u0103lan, R. A. Biology of metalloproteinases. Rom J Morphol Embryol. 48(4), 323\u2013334 (2007).","journal-title":"Rom J Morphol Embryol."},{"issue":"1","key":"34152_CR39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1262\/jrd.18123","volume":"53","author":"K Hashizume","year":"2007","unstructured":"Hashizume, K. Analysis of utero-placental-specific molecules and their functions during implantation and placentation in the bovin. J Reprod Dev. 53(1), 1\u201311 (2007).","journal-title":"J Reprod Dev."},{"key":"34152_CR40","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1007\/978-3-540-68964-5_15","volume":"191","author":"LR Potter","year":"2009","unstructured":"Potter, L. R., Yoder, A. R., Flora, D. R., Antos, L. K. & Dickey, D. M. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb Exp Pharmacol. 191, 341\u2013366 (2009).","journal-title":"Handb Exp Pharmacol."},{"key":"34152_CR41","doi-asserted-by":"publisher","first-page":"2173","DOI":"10.1373\/clinchem.2005.053488","volume":"51","author":"SJ Nielsen","year":"2005","unstructured":"Nielsen, S. J. et al. Measurement of pro-C-type natriuretic peptide in plasma. Clin Chem. 51, 2173\u20132176 (2005).","journal-title":"Clin Chem."},{"key":"34152_CR42","doi-asserted-by":"publisher","first-page":"80","DOI":"10.4103\/1008-682X.154993","volume":"18","author":"H Xia","year":"2016","unstructured":"Xia, H. et al. Role of C type natriuretic peptide in the function of normal human sperm. Asian J Androl. 18, 80\u201384 (2016).","journal-title":"Asian J Androl."},{"key":"34152_CR43","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1038\/nature10897","volume":"484","author":"Y Cui","year":"2012","unstructured":"Cui, Y. et al. Role of corin in trophoblast invasion and uterine spiral artery remodelling in pregnancy. Nature. 484, 246\u2013250 (2012).","journal-title":"Nature."},{"key":"34152_CR44","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/0006-291X(79)91662-0","volume":"87","author":"MC Ostrowski","year":"1979","unstructured":"Ostrowski, M. C., Kistler, W. S. & Williams-Ashman, H. G. A flavoprotein responsible for the intense sulfhydryl oxidase activity of rat seminal vesicle secretion. Biochem Biophys Res Commun. 87, 171\u2013176 (1979).","journal-title":"Biochem Biophys Res Commun."},{"key":"34152_CR45","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/S0006-291X(75)80329-9","volume":"66","author":"TS Chang","year":"1975","unstructured":"Chang, T. S. & Morton, B. Epididymal sulfhydryl oxidase: a sperm-protective enzyme from the male reproductive tract. Biochem Biophys Res Commun. 66, 309\u2013315 (1975).","journal-title":"Biochem Biophys Res Commun."},{"key":"34152_CR46","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1095\/biolreprod39.1.141","volume":"39","author":"GA Cornwall","year":"1988","unstructured":"Cornwall, G. A., Vindivich, D., Tillman, S. & Chang, T. S. The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro. Biol Reprod. 39, 141\u2013155 (1988).","journal-title":"Biol Reprod."},{"key":"34152_CR47","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1007\/s00441-005-0043-x","volume":"323","author":"A Tury","year":"2006","unstructured":"Tury, A. et al. Cell-specific localization of the sulphydryl oxidase QSOX in rat peripheral tissues. Cell Tissue Res. 323, 91\u2013103 (2006).","journal-title":"Cell Tissue Res."},{"key":"34152_CR48","doi-asserted-by":"publisher","first-page":"2006","DOI":"10.1016\/j.jprot.2010.06.005","volume":"73","author":"AA Moura","year":"2010","unstructured":"Moura, A. A., Souza, C. E., Stanley, B. A., Chapman, D. A. & Killian, G. J. Proteomics of cauda epididymal fluid from mature Holstein bulls. J Proteomics. 73, 2006\u20132020 (2010).","journal-title":"J Proteomics."},{"key":"34152_CR49","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1002\/mrd.1080420311","volume":"42","author":"JG Alvarez","year":"1995","unstructured":"Alvarez, J. G. & Storey, B. T. Differential incorporation of fatty-acids into and peroxidative loss of fatty-acids from phospholipids of human spermatozoa. Mol Reprod Dev. 42, 334\u2013346 (1995).","journal-title":"Mol Reprod Dev."},{"key":"34152_CR50","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1095\/biolreprod32.1.145","volume":"32","author":"KJ Go","year":"1985","unstructured":"Go, K. J. & Wolf, D. P. Albumin-mediated changes in sperm sterol con-tent during capacitation. Biol Reprod. 32, 145\u2013153 (1985).","journal-title":"Biol Reprod."},{"key":"34152_CR51","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1002\/j.1939-4640.1983.tb00740.x","volume":"4","author":"CL Singleton","year":"1983","unstructured":"Singleton, C. L. & Killian, G. J. A study of phospholipase in albumin andits role in inducing the acrosome reaction of guinea pig spermatozoain vitro. J. Androl. 4, 150\u2013156 (1983).","journal-title":"J. Androl."},{"key":"34152_CR52","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.anireprosci.2009.02.007","volume":"116","author":"A Dhali","year":"2009","unstructured":"Dhali, A., Anchamparuthy, V. M., Butler, S. P., Pearson, R. E. & Gwazdauskas, F. C. In vitro development of bovine embryos cultured with stem cell factor or insulin-like growth factor-I following IVF with semen of two bulls having different field fertility. Animl Reprod Sci. 116, 188\u2013195 (2009).","journal-title":"Animl Reprod Sci."},{"key":"34152_CR53","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1095\/biolreprod66.4.1042","volume":"66","author":"RW Bailey","year":"2002","unstructured":"Bailey, R. W., Aronow, B., Harmony, J. A. & Griswold, M. D. Heat shock-initiated apoptosis is accelerated and removal of damaged cells is delayed in the testis of clusterin\/ApoJ knock-out mice. Biol Reprod. 66, 1042\u20131053 (2002).","journal-title":"Biol Reprod."},{"key":"34152_CR54","doi-asserted-by":"publisher","first-page":"6875","DOI":"10.1074\/jbc.274.11.6875","volume":"274","author":"DT Humphreys","year":"1999","unstructured":"Humphreys, D. T., Carver, J. A., Easterbrook-Smith, S. B. & Wilson, M. R. Clusterin has chaperone-like activity similar to that of small heat shock proteins. J Biol Chem. 274, 6875\u20136881 (1999).","journal-title":"J Biol Chem."},{"key":"34152_CR55","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/j.jprot.2013.02.027","volume":"82","author":"HA Shojaei Saadi","year":"2013","unstructured":"Shojaei Saadi, H. A. et al. Proteins associated with critical sperm functions and sperm head are differentally expressed in morphlogocally abnormal bovine sperm induced by scrotal insulation. J Proteomics. 82, 64\u201380 (2013).","journal-title":"J Proteomics."},{"key":"34152_CR56","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1002\/j.1939-4640.2001.tb02592.x","volume":"22","author":"NM Ibrahim","year":"2001","unstructured":"Ibrahim, N. M., Roman, O. J. E., Troedsson, M. H. & Crabo, B. G. Effect of scrotal insulation on clusterin-positive cells in ram semen and their relationship to semen quality. J Androl. 22, 863\u201377 (2001).","journal-title":"J Androl."},{"key":"34152_CR57","doi-asserted-by":"publisher","first-page":"1260","DOI":"10.1016\/j.juro.2012.06.012","volume":"188","author":"A Zalata","year":"2012","unstructured":"Zalata, A. et al. Seminal clusterin gene expression associated with seminal variables in fertile and infertile men. J Urol. 188, 1260\u20131264 (2012).","journal-title":"J Urol."},{"key":"34152_CR58","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1016\/j.theriogenology.2010.04.025","volume":"74","author":"S Novak","year":"2010","unstructured":"Novak, S. et al. Biomarkers of in vivo fertility in sperm and seminal plasma of fertile stallions. Theriogenology. 74, 956\u2013967 (2010).","journal-title":"Theriogenology."},{"key":"34152_CR59","doi-asserted-by":"publisher","first-page":"753","DOI":"10.1530\/REP-13-0220","volume":"147","author":"EA Santos","year":"2014","unstructured":"Santos, E. A. et al. Protein profile of the seminal plasma of collared peccaries (Pecari tajacu Linnaeus, 1758). Reproduction. 147, 753\u2013764 (2014).","journal-title":"Reproduction."},{"key":"34152_CR60","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.anireprosci.2015.09.003","volume":"162","author":"GB Boe-Hansen","year":"2015","unstructured":"Boe-Hansen, G. B. et al. Seminal plasma proteins and their relationship with percentage of morphologically normal sperm in 2-year-old Brahman (Bos indicus) bulls. Anim Reprod. 162, 20\u201330 (2015).","journal-title":"Anim Reprod."},{"key":"34152_CR61","doi-asserted-by":"publisher","first-page":"3353","DOI":"10.1073\/pnas.91.8.3353","volume":"91","author":"CA Sprecher","year":"1994","unstructured":"Sprecher, C. A., Kisiel, W., Mathewes, S. & Foster, D. C. Molecular cloning, expression, and partial characterization of a second human tissue-factor-pathway inhibitor. Proc Natl Acad Sci USA 91, 3353\u20133357 (1994).","journal-title":"Proc Natl Acad Sci USA"},{"key":"34152_CR62","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1093\/oxfordjournals.jbchem.a124648","volume":"116","author":"Y Miyagi","year":"1994","unstructured":"Miyagi, Y. et al. cDNA cloning and mRNA expression of a serine proteinase inhibitorsecreted by cancer cells: identification as placental protein 5 and tissue factor pathway inhibitor-2. J Biochem. 116, 939\u2013942 (1994).","journal-title":"J Biochem."},{"key":"34152_CR63","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1016\/S0143-4004(84)80021-1","volume":"5","author":"HT Salem","year":"1981","unstructured":"Salem, H. T., Menabawey, M., Seppala, M., Shaaban, M. M. & Chard, T. Human seminal plasma contains a wide range of trophoblast-\u2018specific\u2019 proteins. Placenta. 5, 413\u2013418 (1981).","journal-title":"Placenta."},{"key":"34152_CR64","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1016\/S0143-4004(84)80021-1","volume":"5","author":"HT Salem","year":"1984","unstructured":"Salem, H. T., Menabawey, M., Sepp\u00e4l\u00e4, M., Shaaban, M. M. & Chard, T. Human seminal plasma contains a wide range of trophoblast-\u2018specific\u2019 proteins. Placenta. 5, 413\u2013417 (1984).","journal-title":"Placenta."},{"issue":"2","key":"34152_CR65","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1111\/j.1439-0272.1992.tb02613.x","volume":"24","author":"WB Schill","year":"1992","unstructured":"Schill, W. B. & Miska, W. Possible effects of the kallikrein-kinin system on male reproductive functions. Andrologia. 24(2), 69\u201375 (1992).","journal-title":"Andrologia."},{"key":"34152_CR66","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1007\/BF00315912","volume":"101","author":"PJ Schiemann","year":"1994","unstructured":"Schiemann, P. J., Aliante, M., Wennemuth, G., Fini, C. & Aumiller, G. Distribution of endogenous and exogenous 5\u2032-nucleotidase on bovine spermatozoa. Histochemistry. 101, 253\u2013262 (1994).","journal-title":"Histochemistry."},{"key":"34152_CR67","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1002\/1098-2795(200012)57:4<384::AID-MRD11>3.0.CO;2-U","volume":"57","author":"SA Adeoya-Osiguwa","year":"2000","unstructured":"Adeoya-Osiguwa, S. A. & Fraser, L. R. Fertilization promoting peptide and adenosine, acting as first messengers, regulate cAMP production and consequent protein tyrosine phosphorylation in a capacitation-dependent manner. Mol Reprod Dev. 57, 384\u2013392 (2000).","journal-title":"Mol Reprod Dev."},{"key":"34152_CR68","first-page":"305","volume":"9","author":"A Krze\u015blak","year":"2004","unstructured":"Krze\u015blak, A. & Lipi\u0144ska, A. Galectin-3 as a multifunctional protein. Cell Mol Biol Lett. 9, 305\u2013328 (2004).","journal-title":"Cell Mol Biol Lett."},{"key":"34152_CR69","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1111\/aji.12273","volume":"72","author":"MR Kovak","year":"2014","unstructured":"Kovak, M. R., Saraswati, S., Schoen, D. J. & Diekman, A. B. Investigation of galectin-3 function in the reproductive tract by identification of binding ligands in human seminal plasma. Am J Reprod Immunol. 72, 403\u2013412 (2014).","journal-title":"Am J Reprod Immunol."},{"issue":"3-4","key":"34152_CR70","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1111\/j.1600-0897.1992.tb00742.x","volume":"27","author":"OA Vanderpuye","year":"1992","unstructured":"Vanderpuye, O. A., Labarrere, C. A. & McIntyre, J. A. The complement system in human reproduction. Am J Reprod Immunol. 27(3-4), 145\u201355 (1992).","journal-title":"Am J Reprod Immunol."},{"key":"34152_CR71","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1016\/j.fertnstert.2016.07.1101","volume":"106","author":"SA Robertson","year":"2016","unstructured":"Robertson, S. A. & Sharkey, D. J. Seminal fluid and fertility in women. Fertil Steril. 106, 511\u2013519 (2016).","journal-title":"Fertil Steril."},{"key":"34152_CR72","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1095\/biolreprod.114.125740","volume":"93","author":"JE Schjenken","year":"2015","unstructured":"Schjenken, J. E., Glynn, D. J., Sharkey, D. J. & Robertson, S. A. TLR4 signaling is a major mediator of the female tract response to seminal fluid in mice. Biol Reprod. 93, 68 (2015).","journal-title":"Biol Reprod."},{"key":"34152_CR73","doi-asserted-by":"publisher","first-page":"8080","DOI":"10.4049\/jimmunol.0804018","volume":"182","author":"LM Moldenhauer","year":"2009","unstructured":"Moldenhauer, L. M. et al. Cross-presentation of male seminal fluid antigens elicits T cell activation to initiate the female immune response to pregnancy. J Immunol. 182, 8080\u20138093 (2009).","journal-title":"J Immunol."},{"key":"34152_CR74","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1530\/REP-12-0399","volume":"146","author":"RV De Oliveira","year":"2013","unstructured":"De Oliveira, R. V. et al. Molecular morphology and function of bull spermatozoa linked to histones and associated with fertility. Reprod. 146, 263\u2013272 (2013).","journal-title":"Reprod."},{"key":"34152_CR75","first-page":"1","volume":"11","author":"S Arshid","year":"2017","unstructured":"Arshid, S. et al. High performance mass spectrometry based proteomics reveals enzyme and signaling pathway regulation in neutrophils during the early stage of surgical trauma. Proteomics Clin Appl. 11, 1\u20132 (2017a).","journal-title":"Proteomics Clin Appl."},{"key":"34152_CR76","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.jprot.2016.05.016","volume":"151","author":"S Arshid","year":"2017","unstructured":"Arshid, S. et al. Neutrophil proteomic analysis reveals the participation of antioxidant enzymes, motility and ribosomal proteins in the prevention of ischemic effects by preconditioning. J Proteomics. 151, 162\u2013173 (2017b).","journal-title":"J Proteomics."},{"key":"34152_CR77","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.jbiotec.2017.06.001","volume":"254","author":"HAR Gomes","year":"2017","unstructured":"Gomes, H. A. R. et al. Identification of multienzymatic complexes in the Clonostachys byssicola secretomes produced in response to different lignocellulosic carbon sources. J Biotechnol. 254, 51\u201358 (2017).","journal-title":"J Biotechnol."},{"key":"34152_CR78","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1111\/bju.13539","volume":"118","author":"MP Antoniassi","year":"2016","unstructured":"Antoniassi, M. P. et al. Analysis of the functional aspects and seminal plasma proteomic profile of sperm from smokers. BJU Int. 118, 814\u2013822 (2016).","journal-title":"BJU Int."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-34152-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-34152-w","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-34152-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,11]],"date-time":"2024-07-11T17:58:49Z","timestamp":1720720729000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-34152-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,11,5]]},"references-count":78,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["34152"],"URL":"https:\/\/doi.org\/10.1038\/s41598-018-34152-w","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,11,5]]},"assertion":[{"value":"14 February 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 September 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 November 2018","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":"16323"}}