{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T02:35:06Z","timestamp":1760236506588,"version":"build-2065373602"},"reference-count":47,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,12,7]],"date-time":"2021-12-07T00:00:00Z","timestamp":1638835200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004569","name":"Ministry of Science and Higher Education","doi-asserted-by":"publisher","award":["010\/RID\/2018\/19"],"award-info":[{"award-number":["010\/RID\/2018\/19"]}],"id":[{"id":"10.13039\/501100004569","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"National Science Center","doi-asserted-by":"publisher","award":["2016\/21\/N\/NZ9\/02319"],"award-info":[{"award-number":["2016\/21\/N\/NZ9\/02319"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Epididymal maturation can be defined as a scope of changes occurring during epididymal transit that prepare spermatozoa to undergo capacitation. One of the most common post-translational modifications involved in the sperm maturation process and their ability to fertilise an oocyte is the phosphorylation of sperm proteins. The aim of this study was to compare tyrosine, serine, and threonine phosphorylation patterns of sperm proteins isolated from three subsequent segments of the stallion epididymis, during and out of the breeding season. Intensities of phosphorylation signals and phosphoproteins profiles varied in consecutive regions of the epididymis. However, significant differences in the phosphorylation status were demonstrated in case of endoplasmic reticulum chaperone BiP (75 and 32 kDa), protein disulfide-isomerase A3 (50 kDa), nesprin-1 (23 kDa), peroxiredoxin-5 (17 kDa), and protein bicaudal D homolog (15 kDa) for season x type of phosphorylated residues variables. Significant differences in the phosphorylation status were also demonstrated in case of endoplasmic reticulum chaperone BiP and albumin (61 kDa), protein disulfide-isomerase A3 (50 kDa), and protein bicaudal D homolog (15 kDa) for region x type of phosphorylated residues variables.<\/jats:p>","DOI":"10.3390\/ani11123487","type":"journal-article","created":{"date-parts":[[2021,12,7]],"date-time":"2021-12-07T09:52:29Z","timestamp":1638870749000},"page":"3487","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Influence of the Season and Region Factor on Phosphoproteome of Stallion Epididymal Sperm"],"prefix":"10.3390","volume":"11","author":[{"given":"Katarzyna","family":"Dyrda","sequence":"first","affiliation":[{"name":"Department of Animal Biochemistry and Biotechnology, Faculty of Animal Bioengineering, University of Warmia and Mazury in Olsztyn, M. Oczapowskiego 5, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6182-5095","authenticated-orcid":false,"given":"Aleksandra","family":"Orzo\u0142ek","sequence":"additional","affiliation":[{"name":"Department of Animal Biochemistry and Biotechnology, Faculty of Animal Bioengineering, University of Warmia and Mazury in Olsztyn, M. Oczapowskiego 5, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanna","family":"Ner-Kluza","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Neurobiology, Faculty of Materials Science and Ceramics, University of Science and Technology, A. Mickiewicza 30, 30-059 Krakow, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pawe\u0142","family":"Wysocki","sequence":"additional","affiliation":[{"name":"Department of Animal Biochemistry and Biotechnology, Faculty of Animal Bioengineering, University of Warmia and Mazury in Olsztyn, M. Oczapowskiego 5, 10-719 Olsztyn, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1111\/j.1745-7262.2007.00280.x","article-title":"Proteomic changes in mammalian spermatozoa during epididymal maturation","volume":"9","author":"Aitken","year":"2007","journal-title":"Asian J. Androl."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.dib.2014.08.008","article-title":"Data for chicken semen proteome and label free quantitative analyses displaying sperm quality biomarkers","volume":"1","author":"Labas","year":"2014","journal-title":"Data Brief"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1071\/RD05120","article-title":"Moving to the beat: A review of mammalian sperm motility regulation","volume":"18","author":"Turner","year":"2006","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1095\/biolreprod64.5.1545","article-title":"Impact of Epididymal Maturation on the Tyrosine Phosphorylation Patterns Exhibited by Rat Spermatozoa","volume":"64","author":"Lewis","year":"2001","journal-title":"Biol. Reprod."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1530\/rep.0.1250017","article-title":"Protein phosphorylation in mammalian spermatozoa","volume":"125","author":"Urner","year":"2003","journal-title":"Reproduction"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"103654","DOI":"10.1016\/j.jprot.2020.103654","article-title":"Human sperm phosphoproteome reveals differential phosphoprotein signatures that regulate human sperm motility","volume":"215","author":"Serrano","year":"2020","journal-title":"J. Proteom."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1080\/01485010701314032","article-title":"Role(s) of the serine\/threonine protein phosphatase 1 on mammalian sperm motility","volume":"53","author":"Han","year":"2007","journal-title":"Arch. Androl."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1093\/molehr\/gal085","article-title":"Evidence for the involvement of proline-directed serine\/threonine phosphorylation in sperm capacitation","volume":"12","author":"Jha","year":"2006","journal-title":"Mol. Hum. Reprod."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2075","DOI":"10.1126\/science.278.5346.2075","article-title":"Signaling through scaffold, anchoring, and adaptor proteins","volume":"278","author":"Pawson","year":"1997","journal-title":"Science"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1459","DOI":"10.1007\/s00726-014-1711-5","article-title":"PhosphoSVM: Prediction of phosphorylation sites by integrating various protein sequence attributes with a support vector machine","volume":"46","author":"Dou","year":"2014","journal-title":"Amino Acids"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1111\/joa.12016","article-title":"Stages and duration of the seminiferous epithelium cycle in the bat Sturnira lilium","volume":"222","author":"Morais","year":"2013","journal-title":"J. Anat."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/0093-691X(83)90087-0","article-title":"Seasonal changes in serum levels of FSH, LH and testosterone and in semen parameters in stallions","volume":"19","author":"Harris","year":"1983","journal-title":"Theriogenology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.anireprosci.2008.03.008","article-title":"Seasonal variations in the epididymis of the roe deer (Capreolus capreolus)","volume":"111","author":"Blottner","year":"2009","journal-title":"Anim. Reprod. Sci."},{"key":"ref_14","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_15","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0003-2697(76)80064-4","article-title":"Assay of proteins in the presence of interfering materials","volume":"70","author":"Bensadoun","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1912","DOI":"10.1126\/science.1075762","article-title":"The protein kinase complement of the human genome","volume":"298","author":"Manning","year":"2002","journal-title":"Science"},{"doi-asserted-by":"crossref","unstructured":"Tyanova, S., Cox, J., Olsen, J., Mann, M., and Frishman, D. (2013). Phosphorylation variation during the cell cycle scales with structural propensities of proteins. PLoS Comput. Biol., 9.","key":"ref_19","DOI":"10.1371\/journal.pcbi.1002842"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.cell.2006.09.026","article-title":"Global, in vivo, and site-specific phosphorylation dynamics in signaling networks","volume":"127","author":"Olsen","year":"2006","journal-title":"Cell"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1620","DOI":"10.1039\/c3mb25514j","article-title":"Regulation of protein\u2013protein binding by coupling between phosphorylation and intrinsic disorder: Analysis of human protein complexes","volume":"9","author":"Nishi","year":"2013","journal-title":"Mol. BioSyst."},{"key":"ref_22","first-page":"1","article-title":"Physicochemical mechanism of protein regulation by phosphorylation","volume":"270","author":"Nishi","year":"2014","journal-title":"Front. Genet."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/humrep\/deh040","article-title":"Human sperm subpopulations: Relationship between functional quality and protein tyrosine phosphorylation","volume":"19","author":"Buffone","year":"2004","journal-title":"Hum. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1007\/s00441-017-2705-x","article-title":"Evaluation of protein phosphorylation in bull sperm during their maturation in the epididymis","volume":"371","author":"Jankovicova","year":"2018","journal-title":"Cell Tissue Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1095\/biolreprod59.1.1","article-title":"Regulation of Protein Phosphorylation during Sperm Capacitation","volume":"59","author":"Visconti","year":"1998","journal-title":"Biol. Reprod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9905","DOI":"10.1074\/jbc.R110.173260","article-title":"The Giant Protein Titin: A regulatory node that integrates myocyte signaling pathways","volume":"286","author":"Kruger","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.fertnstert.2011.10.013","article-title":"Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men","volume":"97","author":"Milardi","year":"2012","journal-title":"Fertil. Steril."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2098","DOI":"10.1074\/jbc.REV118.002804","article-title":"The endoplasmic reticulum (ER) chaperone BiP is a master regulator of ER functions: Getting by with a little help from ERdj friends","volume":"294","author":"Pobre","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1083\/jcb.201112034","article-title":"Spectraplakins: Master orchestrators of cytoskeletal dynamics","volume":"197","author":"Suozzi","year":"2012","journal-title":"J. Cell Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.theriogenology.2018.06.021","article-title":"Identification of biomarker candidates for fertility in spermatozoa of crossbred bulls through comparative proteomics","volume":"119","author":"Aslam","year":"2018","journal-title":"Theriogenology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"732","DOI":"10.3390\/cells2040732","article-title":"Ubiquitination regulates the morphogenesis and function of sperm organelles","volume":"2","author":"Nakamura","year":"2013","journal-title":"Cells"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1095\/biolreprod.107.061275","article-title":"Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization","volume":"77","author":"Yi","year":"2007","journal-title":"Biol. Reprod."},{"doi-asserted-by":"crossref","unstructured":"Gob, E., Schmitt, J., Benavente, R., and Alsheimer, M. (2010). Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS ONE, 10.","key":"ref_33","DOI":"10.1371\/journal.pone.0012072"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1439-0531.2012.02024.x","article-title":"Distribution of PDIA3 transcript and protein in rat testis and sperm cells","volume":"48","author":"Zhao","year":"2013","journal-title":"Reprod. Domest. Anim."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1002\/jcp.10172","article-title":"Proteins of the PDI family: Unpredicted nonER locations and functions","volume":"193","author":"Turano","year":"2002","journal-title":"J. Cell. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1016\/j.devcel.2006.03.011","article-title":"A role for sperm surface protein disulfide isomerase activity in gamete fusion: Evidence for the participation of ERp57","volume":"10","author":"Ellerman","year":"2006","journal-title":"Dev. Cell"},{"doi-asserted-by":"crossref","unstructured":"Di Marzo, N., Chisci, E., and Giovannoni, R. (2018). The role of hydrogen peroxide in redox-dependent signaling homeostatic and pathological response inmammalian cells. Cells, 7.","key":"ref_37","DOI":"10.3390\/cells7100156"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"17174","DOI":"10.1038\/s41598-017-17488-7","article-title":"Peroxiredoxin activity is a major landmark of male fertility","volume":"7","author":"Ryu","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/s11010-013-1876-3","article-title":"Identification of peroxiredoxin-5 in bovine cauda epididymal sperm","volume":"387","author":"Nagdas","year":"2014","journal-title":"Mol. Cell. Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1038\/ncb891","article-title":"Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex","volume":"4","author":"Matanis","year":"2002","journal-title":"Nat. Cell Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1016\/j.ajhg.2013.04.018","article-title":"Mutations in BICD2 cause dominant congenital spinal muscular atrophy and hereditary spastic paraplegia","volume":"92","author":"Oates","year":"2013","journal-title":"Am. J. Hum. Genet."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"6016","DOI":"10.1073\/pnas.0711314105","article-title":"The mitotic kinesin CENP-E is a processive transport motor","volume":"105","author":"Yardimci","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"158","DOI":"10.3389\/fgene.2018.00158","article-title":"Intrinsic Disorder and Posttranslational Modifications: The Darker Side of the Biological Dark Matter","volume":"9","author":"Darling","year":"2018","journal-title":"Front. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1163\/15707563-17000124","article-title":"Seasonal changes in the protein profile and enzyme activity of the epididymal luminal fluid in the lizard, Eutropis carinata (Schneider, 1801)","volume":"68","author":"Medini","year":"2018","journal-title":"Anim. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"197","DOI":"10.3109\/19396368.2012.663233","article-title":"The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa","volume":"58","author":"Dasheux","year":"2012","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_46","first-page":"75","article-title":"Correlation between the proteins and protein profile(s) of different regions of epididymis and their contents in goat buck","volume":"29","author":"Cheema","year":"2011","journal-title":"Anim. Sci. Pap."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.anireprosci.2013.12.007","article-title":"Thiol-disulfide proteins of stallion epididymal spermatozoa","volume":"145","author":"Dias","year":"2014","journal-title":"Anim. Rep. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/12\/3487\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:42:43Z","timestamp":1760168563000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/12\/3487"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,7]]},"references-count":47,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["ani11123487"],"URL":"https:\/\/doi.org\/10.3390\/ani11123487","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2021,12,7]]}}}