{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T03:05:55Z","timestamp":1790651155299,"version":"4.1.0"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,8,2]],"date-time":"2021-08-02T00:00:00Z","timestamp":1627862400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,8,2]],"date-time":"2021-08-02T00:00:00Z","timestamp":1627862400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>In the seminal plasma (n\u2009=\u2009118) and serum (n\u2009=\u200990) clusterin (CLU) the fucosylation and the expression of selected fucosyltransferases (FUTs) were analyzed. Samples from infertile men were divided into groups based on the results of the standard semen analysis: normozoospermic (N), teratozoospermic (T), asthenoteratozoospermic (AT) and oligoasthenoteratozoospermic (OAT). The CLU fucosylation was analyzed using lectin-ELISAs with biotinylated lectins specific to \u03b11,3-, \u03b11,2-linked antennary fucose, and \u03b11,6-linked core fucose (LTA, UEA, and LCA, respectively). The concentrations of FUT3 and FUT4, reflecting the expression of Le oligosaccharide structures, were measured using ELISA tests. The differences in serum CLU and FUT4 concentrations, and in the expression of core fucose and antennary fucose \u03b11,2-linked in CLU glycans between the N group and other groups examined suggest that the disturbances in sperm count, motility, and morphology are not the only cause of male infertility. Lack of similarities between levels of examined parameters in blood serum and seminal plasma may suggest the differences in mechanisms leading to glycoproteins glycosylation. It confirmed the observed differences in concentrations of seminal plasma CLU, FUT3, and FUT4 between the OAT group and N, T, AT groups, indicating that decreased sperm count may be related to these parameters expression. The serum CLU concentrations and expression of core fucose and fucose \u03b11,2-linked in CLU, seem to be good markers differentiating normozoospermic men from those with abnormal sperm parameters, which was not observed for seminal plasma.<\/jats:p>","DOI":"10.1038\/s41598-021-95288-w","type":"journal-article","created":{"date-parts":[[2021,8,2]],"date-time":"2021-08-02T10:03:01Z","timestamp":1627898581000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["The possible association of clusterin fucosylation changes with male fertility disorders"],"prefix":"10.1038","volume":"11","author":[{"given":"Ewa","family":"Janiszewska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Izabela","family":"Kokot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Iwona","family":"Gilowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ricardo","family":"Faundez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2948-4574","authenticated-orcid":false,"given":"Ewa Maria","family":"Kratz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,8,2]]},"reference":[{"key":"95288_CR1","doi-asserted-by":"crossref","unstructured":"Sun, H. et al. Global, regional, and national prevalence and disability-adjusted life-years for infertility in 195 countries and territories, 1990\u20132017: Results from a global burden of disease study, 2017. Aging (Albany NY). 11, 10952\u201310991 (2019).","DOI":"10.18632\/aging.102497"},{"key":"95288_CR2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1477-7827-13-1","volume":"13","author":"A Agarwal","year":"2015","unstructured":"Agarwal, A., Mulgund, A., Hamada, A. & Chyatte, M. R. A unique view on male infertility around the globe. Reprod. Biol. Endocrinol. 13, 1\u20139 (2015).","journal-title":"Reprod. Biol. Endocrinol."},{"key":"95288_CR3","first-page":"799","volume":"32","author":"L Bablok","year":"2011","unstructured":"Bablok, L. et al. Patterns of infertility in Poland: Multicenter study. Neuroendocrinol. Lett. 32, 799\u2013804 (2011).","journal-title":"Neuroendocrinol. Lett."},{"key":"95288_CR4","doi-asserted-by":"publisher","first-page":"1502","DOI":"10.1016\/j.fertnstert.2014.10.021","volume":"102","author":"C Wang","year":"2014","unstructured":"Wang, C. & Swerdloff, R. S. Limitations of semen analysis as a test of male fertility and anticipated needs from newer tests. Fertil. Steril. 102, 1502\u20131507 (2014).","journal-title":"Fertil. Steril."},{"key":"95288_CR5","doi-asserted-by":"publisher","first-page":"691","DOI":"10.1590\/S1807-59322011000400026","volume":"66","author":"SC Esteves","year":"2011","unstructured":"Esteves, S. C., Miyaoka, R. & Agarwal, A. An update on the clinical assessment of the infertile male. Clinics 66, 691\u2013700 (2011).","journal-title":"Clinics"},{"key":"95288_CR6","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.mcna.2010.08.030","volume":"95","author":"ZP Patel","year":"2011","unstructured":"Patel, Z. P. & Niederberger, C. S. Male factor assessment in infertility. Med. Clin. N. Am. 95, 223\u2013234 (2011).","journal-title":"Med. Clin. N. Am."},{"key":"95288_CR7","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1002\/prca.200700228","volume":"1","author":"MW Duncan","year":"2007","unstructured":"Duncan, M. W. & Thompson, H. S. Proteomics of semen and its constituents. Proteom. Clin. Appl. 1, 861\u2013875 (2007).","journal-title":"Proteom. Clin. Appl."},{"key":"95288_CR8","unstructured":"Kratz, E. M. & Achci\u0144ska, K. Mechanizmy molekularne w procesie zap\u0142odnienia: rola czynnika m\u0119skiego Molecular mechanisms of fertilization: the role of male factor. http:\/\/www.phmd.pl\/fulltxt.php?ICID=967076."},{"key":"95288_CR9","doi-asserted-by":"publisher","first-page":"10","DOI":"10.3109\/1354750X.2012.719035","volume":"18","author":"M Ferens-Sieczkowska","year":"2013","unstructured":"Ferens-Sieczkowska, M., Kowalska, B. & Kratz, E. M. Seminal plasma glycoproteins in male infertility and prostate diseases: Is there a chance for glyco-biomarkers?. Biomarkers 18, 10\u201322 (2013).","journal-title":"Biomarkers"},{"key":"95288_CR10","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1093\/humupd\/dmt046","volume":"20","author":"A Amaral","year":"2014","unstructured":"Amaral, A., Castillo, J., Ramalho-Santos, J. & Oliva, R. The combined human sperm proteome: Cellular pathways and implications for basic and clinical science. Hum. Reprod. Update 20, 40\u201362 (2014).","journal-title":"Hum. Reprod. Update"},{"key":"95288_CR11","doi-asserted-by":"crossref","unstructured":"Milardi, D. et al. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil. Steril. 97, 67 (2012).","DOI":"10.1016\/j.fertnstert.2011.10.013"},{"key":"95288_CR12","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1172\/JCI114594","volume":"85","author":"MK O\u2019Bryan","year":"1990","unstructured":"O\u2019Bryan, M. K. et al. Human seminal clusterin (SP-40-,40). Isolation and characterization. J. Clin. Investig. 85, 1477\u20131486 (1990).","journal-title":"J. Clin. Investig."},{"key":"95288_CR13","doi-asserted-by":"publisher","first-page":"7714","DOI":"10.1016\/S0021-9258(18)32238-5","volume":"258","author":"O Blaschuk","year":"1983","unstructured":"Blaschuk, O., Burdzy, K. & Fritz, I. B. Purification and characterization of a cell-aggregating factor (clusterin), the major glycoprotein in ram rete testis fluid. J. Biol. Chem. 258, 7714\u20137720 (1983).","journal-title":"J. Biol. Chem."},{"key":"95288_CR14","doi-asserted-by":"publisher","first-page":"11590","DOI":"10.1074\/jbc.M209233200","volume":"278","author":"KS Leskov","year":"2003","unstructured":"Leskov, K. S., Klokov, D. Y., Li, J., Kinsella, T. J. & Boothman, D. A. Synthesis and functional analyses of nuclear clusterin, a cell death protein. J. Biol. Chem. 278, 11590\u201311600 (2003).","journal-title":"J. Biol. Chem."},{"key":"95288_CR15","doi-asserted-by":"publisher","unstructured":"Naponelli, V. & Bettuzzi, S. Clusterin. In The Complement FactsBook: Second Edition 341\u2013349 (Elsevier, 2018). https:\/\/doi.org\/10.1016\/B978-0-12-810420-0.00032-8.","DOI":"10.1016\/B978-0-12-810420-0.00032-8"},{"key":"95288_CR16","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1038\/onc.2012.212","volume":"32","author":"N Li","year":"2013","unstructured":"Li, N., Zoubeidi, A., Beraldi, E. & Gleave, M. E. GRP78 regulates clusterin stability, retrotranslocation and mitochondrial localization under ER stress in prostate cancer. Oncogene 32, 1933\u20131942 (2013).","journal-title":"Oncogene"},{"key":"95288_CR17","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1002\/mrd.23340","volume":"87","author":"E Janiszewska","year":"2020","unstructured":"Janiszewska, E. & Kratz, E. M. Could the glycosylation analysis of seminal plasma clusterin become a novel male infertility biomarker?. Mol. Reprod. Dev. 87, 515\u2013524 (2020).","journal-title":"Mol. Reprod. Dev."},{"key":"95288_CR18","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1095\/biolreprod.107.060194","volume":"77","author":"Z Wang","year":"2007","unstructured":"Wang, Z., Widgren, E. E., Richardson, R. T. & O\u2019Rand, M. G. Characterization of an eppin protein complex from human semen and spermatozoa. Biol. Reprod. 77, 476\u2013484 (2007).","journal-title":"Biol. Reprod."},{"key":"95288_CR19","doi-asserted-by":"publisher","first-page":"514","DOI":"10.1159\/000351207","volume":"59","author":"IP Trougakos","year":"2013","unstructured":"Trougakos, I. P. The molecular chaperone apolipoprotein J\/Clusterin as a sensor of oxidative stress: Implications in therapeutic approaches\u2014A mini-review. Gerontology 59, 514\u2013523 (2013).","journal-title":"Gerontology"},{"key":"95288_CR20","doi-asserted-by":"publisher","first-page":"1545","DOI":"10.1093\/humrep\/dev113","volume":"30","author":"A Merlotti","year":"2015","unstructured":"Merlotti, A. et al. Fucosylated clusterin in semen promotes the uptake of stress-damaged proteins by dendritic cells via DC-SIGN. Hum. Reprod. 30, 1545\u20131556 (2015).","journal-title":"Hum. Reprod."},{"key":"95288_CR21","unstructured":"Varki, A. & Lowe, J. B. Chapter 6. Biological roles of glycans. Essentials Glycobiol. 1\u201314 (2009)."},{"key":"95288_CR22","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1373\/clinchem.2009.136333","volume":"56","author":"PM Drake","year":"2010","unstructured":"Drake, P. M. et al. Sweetening the pot: Adding glycosylation to the biomarker discovery equation. Clin. Chem. 56, 223\u2013236 (2010).","journal-title":"Clin. Chem."},{"key":"95288_CR23","doi-asserted-by":"publisher","first-page":"4411","DOI":"10.1021\/bi200346n","volume":"50","author":"A Larkin","year":"2011","unstructured":"Larkin, A. & Imperiali, B. The expanding horizons of asparagine-linked glycosylation. Biochemistry 50, 4411\u20134426 (2011).","journal-title":"Biochemistry"},{"key":"95288_CR24","doi-asserted-by":"crossref","unstructured":"Kratz, E. M., Faundez, R. & Ka\u0327tnik-Prastowska, I. Fucose and sialic acid expressions in human seminal fibronectin and \u03b1 1-acid glycoprotein associated with leukocytospermia of infertile men. Dis. Markers 31, 317\u2013325 (2011).","DOI":"10.1155\/2011\/914710"},{"key":"95288_CR25","doi-asserted-by":"publisher","first-page":"991","DOI":"10.1021\/acs.jproteome.5b01069","volume":"15","author":"M Saraswat","year":"2016","unstructured":"Saraswat, M. et al. N-glycoproteomics of human seminal plasma glycoproteins. J. Proteome Res. 15, 991\u20131001 (2016).","journal-title":"J. Proteome Res."},{"key":"95288_CR26","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1093\/glycob\/11.10.119R","volume":"11","author":"T De Vries","year":"2001","unstructured":"De Vries, T., Knegtel, R. M. A., Holmes, E. H. & Macher, B. A. Fucosyltransferases: Structure\/function studies. Glycobiology 11, 119\u2013128 (2001).","journal-title":"Glycobiology"},{"key":"95288_CR27","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1093\/glycob\/cwx034","volume":"27","author":"M Schneider","year":"2017","unstructured":"Schneider, M., Al-Shareffi, E. & Haltiwanger, R. S. Biological functions of fucose in mammals. Glycobiology 27, 601\u2013618 (2017).","journal-title":"Glycobiology"},{"key":"95288_CR28","doi-asserted-by":"publisher","first-page":"1885","DOI":"10.1021\/acs.jproteome.9b00818","volume":"19","author":"M Lastovickova","year":"2020","unstructured":"Lastovickova, M., Strouhalova, D. & Bobalova, J. Use of lectin-based affinity techniques in breast cancer glycoproteomics: A review. J. Proteome Res. 19, 1885\u20131899 (2020).","journal-title":"J. Proteome Res."},{"key":"95288_CR29","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1093\/glycob\/cwp016","volume":"19","author":"H Tateno","year":"2009","unstructured":"Tateno, H., Nakamura-Tsuruta, S. & Hirabayashi, J. Comparative analysis of core-fucose-binding lectins from Lens culinaris and Pisum sativum using frontal affinity chromatography. Glycobiology 19, 527\u2013536 (2009).","journal-title":"Glycobiology"},{"key":"95288_CR30","doi-asserted-by":"crossref","unstructured":"Bossuyt, X. Clinical performance characteristics of a laboratory test. A practical approach in the autoimmune laboratory. Autoimmun. Rev. 8, 543\u2013548 (2009).","DOI":"10.1016\/j.autrev.2009.01.013"},{"key":"95288_CR31","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1111\/and.12558","volume":"48","author":"T Fukuda","year":"2016","unstructured":"Fukuda, T., Miyake, H., Enatsu, N., Matsushita, K. & Fujisawa, M. Seminal level of clusterin in infertile men as a significant biomarker reflecting spermatogenesis. Andrologia 48, 1188\u20131194 (2016).","journal-title":"Andrologia"},{"key":"95288_CR32","doi-asserted-by":"publisher","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":"95288_CR33","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1242\/jcs.03258","volume":"120","author":"PCN Chiu","year":"2007","unstructured":"Chiu, P. C. N. et al. Glycodelin: A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding. J. Cell Sci. 120, 33\u201344 (2007).","journal-title":"J. Cell Sci."},{"key":"95288_CR34","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1002\/pros.10085","volume":"52","author":"DCW Poland","year":"2002","unstructured":"Poland, D. C. W. et al. High level of \u03b11-acid glycoprotein in human seminal plasma is associated with high branching and expression of Lewisa groups on its glycans: Supporting evidence for a prostatic origin. Prostate 52, 34\u201342 (2002).","journal-title":"Prostate"},{"key":"95288_CR35","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1071\/RD18124","volume":"31","author":"A Ka\u0142u\u017ca","year":"2019","unstructured":"Ka\u0142u\u017ca, A. et al. The content of immunomodulatory glycoepitopes in seminal plasma glycoproteins of fertile and infertile men. Reprod. Fertil. Dev. 31, 579\u2013589 (2019).","journal-title":"Reprod. Fertil. Dev."},{"key":"95288_CR36","doi-asserted-by":"publisher","first-page":"36593","DOI":"10.1074\/jbc.M705134200","volume":"282","author":"PC Pang","year":"2007","unstructured":"Pang, P. C. et al. Expression of bisecting type and Lewisx\/Lewisy terminated N-glycans on human sperm. J. Biol. Chem. 282, 36593\u201336602 (2007).","journal-title":"J. Biol. Chem."},{"key":"95288_CR37","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1093\/humrep\/des447","volume":"28","author":"GF Clark","year":"2013","unstructured":"Clark, G. F. The role of carbohydrate recognition during human sperm-egg binding. Hum. Reprod. 28, 566\u2013577 (2013).","journal-title":"Hum. Reprod."},{"key":"95288_CR38","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1074\/mcp.M111.008730","volume":"11","author":"GF Clark","year":"2012","unstructured":"Clark, G. F. et al. Tumor biomarker glycoproteins in the seminal plasma of healthy human males are endogenous ligands for DC-SIGN. Mol. Cell. Proteom. 11, 1\u201312 (2012).","journal-title":"Mol. Cell. Proteom."},{"key":"95288_CR39","doi-asserted-by":"publisher","first-page":"5299","DOI":"10.4049\/jimmunol.1101889","volume":"187","author":"J Sabatte","year":"2011","unstructured":"Sabatte, J. et al. Semen clusterin is a novel DC-SIGN ligand. J. Immunol. 187, 5299\u20135309 (2011).","journal-title":"J. Immunol."},{"key":"95288_CR40","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.1093\/humrep\/dem023","volume":"22","author":"ES Diaz","year":"2007","unstructured":"Diaz, E. S., Kong, M. & Morales, P. Effect of fibronectin on proteasome activity, acrosome reaction, tyrosine phosphorylation and intracellular calcium concentrations of human sperm. Hum. Reprod. 22, 1420\u20131430 (2007).","journal-title":"Hum. Reprod."},{"key":"95288_CR41","doi-asserted-by":"publisher","first-page":"274","DOI":"10.4103\/1008-682X.138187","volume":"17","author":"B Olejnik","year":"2015","unstructured":"Olejnik, B., Kratz, E. M., Zimmer, M. & Ferens-Sieczkowska, M. Glycoprotein fucosylation is increased in seminal plasma of subfertile men. Asian J. Androl. 17, 274\u2013280 (2015).","journal-title":"Asian J. Androl."},{"key":"95288_CR42","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1006\/jmbi.2000.4016","volume":"301","author":"R Loris","year":"2000","unstructured":"Loris, R. et al. Structural basis of carbohydrate recognition by lectin II from Ulex europaeus, a protein with a promiscuous carbohydrate-binding site. J. Mol. Biol. 301, 987\u20131002 (2000).","journal-title":"J. Mol. Biol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-95288-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-95288-w","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-95288-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T12:06:39Z","timestamp":1670069199000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-95288-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,2]]},"references-count":42,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["95288"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-95288-w","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,2]]},"assertion":[{"value":"12 June 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 July 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 August 2021","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":"15674"}}