{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,5]],"date-time":"2026-05-05T17:27:52Z","timestamp":1778002072098,"version":"3.51.4"},"reference-count":87,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,1,10]],"date-time":"2020-01-10T00:00:00Z","timestamp":1578614400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Estrogens are steroid hormones that affect a wide range of physiological functions. The effect of estrogens on male reproductive tissues and sperm cells through specific receptors is essential for sperm development, maturation, and function. Although estrogen receptors (ERs) have been studied in several mammalian species, including humans, they have not yet been described in bull spermatozoa and reproductive tissues. In this study, we analyzed the presence of all types of ERs (ESR1, ESR2, and GPER1) in bull testicular and epididymal tissues and epididymal and ejaculated spermatozoa, and we characterize them here for the first time. We observed different localizations of each type of ER in the sperm head by immunofluorescent microscopy. Additionally, using a selected polyclonal antibody, we found that each type of ER in bull sperm extracts had two isoforms with different molecular masses. The detailed detection of ERs is a prerequisite not only for understanding the effect of estrogen on all reproductive events but also for further studying the negative effect of environmental estrogens (endocrine disruptors) on processes that lead to fertilization.<\/jats:p>","DOI":"10.3390\/cells9010183","type":"journal-article","created":{"date-parts":[[2020,1,13]],"date-time":"2020-01-13T04:05:51Z","timestamp":1578888351000},"page":"183","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Missing Information from the Estrogen Receptor Puzzle: Where Are They Localized in Bull Reproductive Tissues and Spermatozoa?"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6617-6485","authenticated-orcid":false,"given":"Jana","family":"Antalikova","sequence":"first","affiliation":[{"name":"Laboratory of Reproductive Physiology, Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, 840 05 Bratislava, Slovakia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Petra","family":"Secova","sequence":"additional","affiliation":[{"name":"Laboratory of Reproductive Physiology, Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, 840 05 Bratislava, Slovakia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lubica","family":"Horovska","sequence":"additional","affiliation":[{"name":"Laboratory of Reproductive Physiology, Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, 840 05 Bratislava, Slovakia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Romana","family":"Krejcirova","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, 165 00 Prague 6, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6577-765X","authenticated-orcid":false,"given":"Ondrej","family":"Simonik","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, 165 00 Prague 6, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4714-6184","authenticated-orcid":false,"given":"Jana","family":"Jankovicova","sequence":"additional","affiliation":[{"name":"Laboratory of Reproductive Physiology, Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, 840 05 Bratislava, Slovakia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michaela","family":"Bartokova","sequence":"additional","affiliation":[{"name":"Laboratory of Reproductive Physiology, Institute of Animal Biochemistry and Genetics, Centre of Biosciences, Slovak Academy of Sciences, 840 05 Bratislava, Slovakia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lucie","family":"Tumova","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, 165 00 Prague 6, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pavla","family":"Manaskova-Postlerova","sequence":"additional","affiliation":[{"name":"Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, 165 00 Prague 6, Czech Republic"},{"name":"Laboratory of Reproductive Biology, Institute of Biotechnology CAS, v.v.i., BIOCEV, 252 50 Vestec, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,1,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1093\/humupd\/6.4.332","article-title":"Cellular and biochemical mechanisms by which environmental oestrogens influence reproductive function","volume":"6","author":"Rosselli","year":"2000","journal-title":"Hum. Reprod. Update"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/1477-7827-1-52","article-title":"Estrogen in the adult male reproductive tract: A review","volume":"1","author":"Hess","year":"2003","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Dostalova, P., Zatecka, E., and Dvorakova-Hortova, K. (2017). Of oestrogens and sperm: A review of the roles of oestrogens and oestrogen receptors in male reproduction. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18050904"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1093\/biolre\/ioy043","article-title":"Estrogen in the male: A historical perspective","volume":"99","author":"Hess","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_5","first-page":"289","article-title":"Estrogen and spermatogenesis","volume":"22","author":"Robertson","year":"2001","journal-title":"Endocr. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"7986","DOI":"10.1073\/pnas.96.14.7986","article-title":"Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene","volume":"96","author":"Robertson","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4796","DOI":"10.1210\/endo.137.11.8895349","article-title":"Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility","volume":"137","author":"Eddy","year":"1996","journal-title":"Endocrinology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1038\/37352","article-title":"A role for oestrogens in the male reproductive system","volume":"390","author":"Hess","year":"1997","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1670","DOI":"10.1210\/jcem.84.5.5670","article-title":"Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects","volume":"84","author":"Luconi","year":"1999","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1530\/REP-11-0326","article-title":"The slower the better: How sperm capacitation and acrosome reaction is modified in the presence of estrogens","volume":"143","author":"Sebkova","year":"2012","journal-title":"Reproduction"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1530\/REP-12-0472","article-title":"In vivo exposure to 17\u03b2-estradiol triggers premature sperm capacitation in cauda epididymis","volume":"145","author":"Ded","year":"2013","journal-title":"Reproduction"},{"key":"ref_12","first-page":"211","article-title":"Role of estradiol in the capacitation and acrosome reaction of hamster epididymal spermatozoa in the isolated uterus of mice incubated in vitro","volume":"43","author":"Bathla","year":"1999","journal-title":"Indian J. Physiol. Pharm."},{"key":"ref_13","first-page":"500","article-title":"Effects of estrogen on acrosome reaction and intracellular calcium in human spermatozoa and the possible mechanism concerned","volume":"36","author":"He","year":"2005","journal-title":"J. Sichuan Univ. Med Sci. Ed."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1093\/humrep\/deg037","article-title":"17\u03b2-Estradiol and environmental estrogens significantly affect mammalian sperm function","volume":"18","author":"Markoulaki","year":"2003","journal-title":"Hum. Reprod."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.canlet.2005.06.018","article-title":"Signaling regulation of genomic and nongenomic functions of estrogen receptors","volume":"238","author":"Acconcia","year":"2006","journal-title":"Cancer Lett."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"22278","DOI":"10.1074\/jbc.M611877200","article-title":"A conserved mechanism for steroid receptor translocation to the plasma membrane","volume":"282","author":"Pedram","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.tem.2009.06.009","article-title":"Plasma membrane estrogen receptors","volume":"20","author":"Levin","year":"2009","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1126\/science.1106943","article-title":"A transmembrane intracellular estrogen receptor mediates rapid cell signaling","volume":"307","author":"Revankar","year":"2005","journal-title":"Science"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5842","DOI":"10.1210\/en.2007-0436","article-title":"Expression of G protein-coupled receptor-30, a G protein-coupled membrane estrogen receptor, in oxytocin neurons of the rat paraventricular and supraoptic nuclei","volume":"148","author":"Sakamoto","year":"2007","journal-title":"Endocrinology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"5925","DOI":"10.1073\/pnas.93.12.5925","article-title":"Cloning of a novel receptor expressed in rat prostate and ovary","volume":"93","author":"Kuiper","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/0014-5793(96)00782-X","article-title":"ER\u03b2: Identification and characterization of a novel human estrogen receptor","volume":"392","author":"Mosselman","year":"1996","journal-title":"FEBS Lett."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3236","DOI":"10.1210\/en.2006-1605","article-title":"Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane","volume":"148","author":"Filardo","year":"2007","journal-title":"Endocrinology"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Kumar, R., Zakharov, M.N., Khan, S.H., Miki, R., Jang, H., Toraldo, G., Singh, R., Bhasin, S., and Jasuja, R. (2011). The dynamic structure of the estrogen receptor. J. Amino Acids, 2011.","DOI":"10.4061\/2011\/812540"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1210\/me.2009-0317","article-title":"Involvement of estrogen receptor variant ER-\u03b136, not GPR30, in nongenomic estrogen signaling","volume":"24","author":"Kang","year":"2010","journal-title":"Mol. Endocrinol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/S0024-3205(00)00669-X","article-title":"Steroid hormone-induced effects on membrane fluidity and their potential roles in non-genomic mechanisms","volume":"67","author":"Whiting","year":"2000","journal-title":"Life Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1210\/me.2004-0142","article-title":"Global uterine genomics in vivo: Microarray evaluation of the estrogen receptor \u03b1-growth factor cross-talk mechanism","volume":"19","author":"Collins","year":"2005","journal-title":"Mol. Endocrinol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5043","DOI":"10.1210\/en.2007-1593","article-title":"The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17\u03b2-estradiol on mouse spermatogonial GC-1 cell line","volume":"149","author":"Sirianni","year":"2008","journal-title":"Endocrinology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1002\/j.1939-4640.2002.tb02345.x","article-title":"Localization of androgen and estrogen receptors in adult male mouse reproductive tract","volume":"23","author":"Zhou","year":"2002","journal-title":"J. Androl."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1095\/biolreprod.107.063909","article-title":"17Beta-Estradiol Induces the Translocation of the Estrogen Receptors ESR1 and ESR2 to the Cell Membrane, MAPK3\/1 Phosphorylation and Proliferation of Cultured Immature Rat Sertoli Cells1","volume":"78","author":"Lucas","year":"2008","journal-title":"Biol. Reprod."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.ygcen.2012.07.004","article-title":"In vitro expression of androgen and estrogen receptors in prepubertal and adult rat epididymis","volume":"178","author":"Zaya","year":"2012","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/S0303-7207(01)00427-0","article-title":"Photoperiod-dependent capability of androgen aromatization and the role of estrogens in the bank vole testis visualized by means of immunohistochemistry","volume":"178","author":"Kotula","year":"2001","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.theriogenology.2012.02.018","article-title":"Detection of aromatase, androgen, and estrogen receptors in bank vole spermatozoa","volume":"78","author":"Hejmej","year":"2012","journal-title":"Theriogenology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1016\/j.theriogenology.2016.02.019","article-title":"Are aryl hydrocarbon receptor and G-protein\u2013coupled receptor 30 involved in the regulation of seasonal testis activity in photosensitive rodent\u2014the bank vole (Myodes glareolus)?","volume":"86","author":"Zarzycka","year":"2016","journal-title":"Theriogenology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/j.theriogenology.2005.12.013","article-title":"Immunolocalization of estrogen and androgen receptors and steroid concentrations in the stallion epididymis","volume":"66","author":"Parlevliet","year":"2006","journal-title":"Theriogenology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.anireprosci.2011.03.007","article-title":"Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri-and post-pubertal stallion testis","volume":"125","author":"Pearl","year":"2011","journal-title":"Anim. Reprod. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1093\/molehr\/7.6.497","article-title":"Localization of oestrogen receptors alpha and beta in human testis","volume":"7","author":"Weihua","year":"2001","journal-title":"Mol. Hum. Reprod."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1093\/molehr\/7.3.227","article-title":"Differential expression of oestrogen receptor \u03b1 and \u03b2 proteins in the testes and male reproductive system of human and non-human primates","volume":"7","author":"Saunders","year":"2001","journal-title":"Mol. Hum. Reprod."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/s00418-014-1216-z","article-title":"Expression pattern of estrogen receptors \u03b1 and \u03b2 and G-protein-coupled estrogen receptor 1 in the human testis","volume":"142","author":"Fietz","year":"2014","journal-title":"Histochem. Cell Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1186\/1477-7827-4-36","article-title":"Detection of estrogen receptors ER-alpha and ER-beta in human ejaculated immature spermatozoa with excess residual cytoplasm","volume":"4","author":"Rago","year":"2006","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.anireprosci.2011.08.008","article-title":"Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality","volume":"128","author":"Gunawan","year":"2011","journal-title":"Anim. Reprod. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/1477-7827-5-23","article-title":"Cytochrome P450arom, androgen and estrogen receptors in pig sperm","volume":"5","author":"Rago","year":"2007","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1002\/ar.a.20131","article-title":"Differential expression of estrogen receptors (ER\u03b1\/ER\u03b2) in testis of mature and immature pigs","volume":"281","author":"Rago","year":"2004","journal-title":"Anat. Rec. A Discov. Mol. Cell. Evol. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1530\/REP-06-0239","article-title":"Reduced endogenous estrogen delays epididymal development but has no effect on efferent duct morphology in boars","volume":"134","author":"Pearl","year":"2007","journal-title":"Reproduction"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.domaniend.2006.09.003","article-title":"Estrogen and androgen receptor expression in relation to steroid concentrations in the adult boar epididymis","volume":"33","author":"Pearl","year":"2007","journal-title":"Domest. Anim. Endocrinol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.ijbiomac.2018.05.015","article-title":"G protein-coupled estrogen receptor (GPER) in adult boar testes, epididymis and spermatozoa during epididymal maturation","volume":"116","author":"Rajmon","year":"2018","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/S1642-431X(12)60065-5","article-title":"Estrogens\u2013new players in spermatogenesis","volume":"11","author":"Carreau","year":"2011","journal-title":"Reprod. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.yexcr.2014.07.015","article-title":"Steroid receptors and their ligands: Effects on male gamete functions","volume":"328","author":"Aquila","year":"2014","journal-title":"Exp. Cell Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.mce.2016.03.024","article-title":"Differential roles of estrogen receptors, ESR1 and ESR2, in adult rat spermatogenesis","volume":"428","author":"Dumasia","year":"2016","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1080\/15592294.2017.1382786","article-title":"Estrogen, through estrogen receptor 1, regulates histone modifications and chromatin remodeling during spermatogenesis in adult rats","volume":"12","author":"Dumasia","year":"2017","journal-title":"Epigenetics"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"274","DOI":"10.2478\/sab-2018-0034","article-title":"Localization of Estrogen Receptors in Male Reproductive Tissues and Sperm Cells\u2013A Review","volume":"49","author":"Rajmon","year":"2018","journal-title":"SAB"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1007\/s004180100269","article-title":"Immunohistochemical localization of estrogen receptor-\u03b1 in sex ducts and gonads of newborn piglets","volume":"115","author":"Nielsen","year":"2001","journal-title":"Histochem. Cell Biol."},{"key":"ref_52","first-page":"5","article-title":"The role of estrogen in testis and the male reproductive tract: A review and species comparison","volume":"1","author":"Hess","year":"2004","journal-title":"Anim. Reprod."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Hess, R.A. (2002). The efferent ductules: Structure and functions. The Epididymis: From Molecules to Clinical Practice, Springer.","DOI":"10.1007\/978-1-4615-0679-9_4"},{"key":"ref_54","first-page":"1892","article-title":"Ductuli efferentes in the epididymis of boar, goat, ram, bull, and stallion","volume":"39","author":"Hemeida","year":"1978","journal-title":"Am. J. Vet. Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1095\/biolreprod.109.080366","article-title":"Epididymal hypo-osmolality induces abnormal sperm morphology and function in the estrogen receptor alpha knockout mouse","volume":"82","author":"Joseph","year":"2010","journal-title":"Biol. Reprod."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1101\/gad.367606","article-title":"Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes","volume":"20","author":"Gur","year":"2006","journal-title":"Genes Dev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1023\/A:1016549922439","article-title":"Estrogen receptor, calcium mobilization and rat sperm motility","volume":"237","author":"Saberwal","year":"2002","journal-title":"Mol. Cell. Biochem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/j.steroids.2004.05.013","article-title":"Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens","volume":"69","author":"Luconi","year":"2004","journal-title":"Steroids"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/1477-7827-8-87","article-title":"Effect of estrogens on boar sperm capacitation in vitro","volume":"8","author":"Ded","year":"2010","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_60","first-page":"4475","article-title":"Estrogen receptor-\u03b2 expression in human testicular germ cell tumors","volume":"9","author":"Pais","year":"2003","journal-title":"Clin. Cancer. Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1046\/j.1365-2605.2002.00350.x","article-title":"Evaluation of the acrosome reaction and viability in buffalo spermatozoa using two staining methods: The effects of heparin and calcium ionophore A23187","volume":"25","author":"Kitiyanant","year":"2002","journal-title":"Int. J. Androl."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1530\/REP-11-0310","article-title":"Sperm surface changes and physiological consequences induced by sperm handling and storage","volume":"142","author":"Leahy","year":"2011","journal-title":"Reproduction"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1095\/biolreprod.102.011056","article-title":"A differential mechanism is involved during heparin-and cryopreservation-induced capacitation of bovine spermatozoa","volume":"69","author":"Cormier","year":"2003","journal-title":"Biol. Reprod."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"45","DOI":"10.4141\/cjas94-007","article-title":"Cryopreservation alters the Ca2+ flux of bovine spermatozoa","volume":"74","author":"Bailey","year":"1994","journal-title":"Can. J. Anim. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1002\/j.1939-4640.1995.tb00526.x","article-title":"Cryopreservation extenders affect calcium flux in bovine spermatozoa during a temperature challenge","volume":"16","author":"Zhao","year":"1995","journal-title":"J. Androl."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1530\/REP-09-0134","article-title":"Ca2+-stores in sperm: Their identities and functions","volume":"138","author":"Costello","year":"2009","journal-title":"Reproduction"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1083\/jcb.200210057","article-title":"Phospholipase C\u03b44 is required for Ca2+ mobilization essential for acrosome reaction in sperm","volume":"161","author":"Fukami","year":"2003","journal-title":"J. Cell Biol."},{"key":"ref_68","first-page":"4204","article-title":"Receptor and centriole pathways of steroid action in normal and neoplastic cells","volume":"38","author":"Nenci","year":"1978","journal-title":"Cancer Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/0022-4731(82)90017-6","article-title":"Estrogens in seminal plasma of human and animal species: Identification and quantitative estimation by gas chromatography\u2014Mass spectrometry associated with stable isotope dilution","volume":"17","author":"Reiffsteck","year":"1982","journal-title":"J. Steroid Biochem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1530\/REP-17-0328","article-title":"Steroid hormones regulate sperm\u2013oviduct interactions in the bovine","volume":"154","author":"Lamy","year":"2017","journal-title":"Reproduction"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1530\/JOE-15-0001","article-title":"Steroid regulation of early postnatal development in the corpus epididymidis of pigs","volume":"225","author":"Katleba","year":"2015","journal-title":"J. Endocrinol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s12958-015-0042-z","article-title":"Immunolocalization of G protein-coupled estrogen receptor in the rat epididymis","volume":"13","author":"Pearl","year":"2015","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1038\/ncb0307-235","article-title":"[Ca 2+] i signalling in sperm\u2014making the most of what you\u2019ve got","volume":"9","author":"Publicover","year":"2007","journal-title":"Nat. Cell Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.ygcen.2016.05.022","article-title":"Implication of the estrogen receptors GPER, ESR1, ESR2 in post-testicular maturations of equine spermatozoa","volume":"233","author":"Gautier","year":"2016","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ygcen.2014.02.016","article-title":"Stallion spermatozoa: Putative target of estrogens; presence of the estrogen receptors ESR1, ESR2 and identification of the estrogen-membrane receptor GPER","volume":"200","author":"Arkoun","year":"2014","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Cornwall, G.A. (2014). Role of posttranslational protein modifications in epididymal sperm maturation and extracellular quality control. Posttranslational Protein Modifications in the Reproductive System, Springer.","DOI":"10.1007\/978-1-4939-0817-2_8"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1952","DOI":"10.1002\/pmic.201000662","article-title":"Purification and identification of sperm surface proteins and changes during epididymal maturation","volume":"11","author":"Belleannee","year":"2011","journal-title":"Proteomics"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/j.jsbmb.2008.03.006","article-title":"The ins and outs of GPR30: A transmembrane estrogen receptor","volume":"109","author":"Prossnitz","year":"2008","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2289","DOI":"10.1016\/j.bbamcr.2016.06.004","article-title":"Rapid steroid hormone actions via membrane receptors","volume":"1863","author":"Schwartz","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/j.bbrc.2005.08.226","article-title":"Identification, cloning, and expression of human estrogen receptor-\u03b136, a novel variant of human estrogen receptor-\u03b166","volume":"336","author":"Wang","year":"2005","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S0303-7207(99)00064-7","article-title":"Cloning of bovine estrogen receptor beta (ER\u03b2): Expression of novel deleted isoforms in reproductive tissues","volume":"152","author":"Walther","year":"1999","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/S0960-0760(02)00186-3","article-title":"Cloning of the novel isoform of the estrogen receptor beta cDNA (ER\u03b2 isoform M cDNA) from the human testicular cDNA library","volume":"82","author":"Shoda","year":"2002","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0014-5793(02)03015-6","article-title":"Estrogen receptor \u03b2: Potential functional significance of a variety of mRNA isoforms","volume":"524","author":"Lewandowski","year":"2002","journal-title":"Febs Lett."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.ygcen.2014.02.022","article-title":"Expression pattern of G protein-coupled receptor 30 in human seminiferous tubular cells","volume":"201","author":"Oliveira","year":"2014","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"R42","DOI":"10.1186\/gb-2009-10-4-r42","article-title":"A whole-genome assembly of the domestic cow, Bos taurus","volume":"10","author":"Zimin","year":"2009","journal-title":"Genome Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/nature01782","article-title":"The DNA sequence of human chromosome 7","volume":"424","author":"Hillier","year":"2003","journal-title":"Nature"},{"key":"ref_87","first-page":"307","article-title":"Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: Studies of ER\u03b1 and ER\u03b2 expressed in Chinese hamster ovary cells","volume":"13","author":"Razandi","year":"1999","journal-title":"Mol. Endocrinol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/1\/183\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:29:21Z","timestamp":1760362161000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/1\/183"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,10]]},"references-count":87,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["cells9010183"],"URL":"https:\/\/doi.org\/10.3390\/cells9010183","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,10]]}}}