{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,16]],"date-time":"2026-02-16T08:32:28Z","timestamp":1771230748745,"version":"3.50.1"},"reference-count":58,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,2,4]],"date-time":"2023-02-04T00:00:00Z","timestamp":1675468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Smithsonian Institution"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Key proteins transferred by epididymal extracellular vesicles (EVs) to the transiting sperm cells contribute to their centrosomal maturation and developmental potential. Although not reported in sperm cells yet, galectin-3-binding protein (LGALS3BP) is known to regulate centrosomal functions in somatic cells. Using the domestic cat model, the objectives of this study were to (1) detect the presence and characterize the transfer of LGALS3BP via EVs between the epididymis and the maturing sperm cells and (2) demonstrate the impact of LGALS3BP transfer on sperm fertilizing ability and developmental potential. Testicular tissues, epididymides, EVs, and spermatozoa were isolated from adult individuals. For the first time, this protein was detected in EVs secreted by the epididymal epithelium. The percentage of spermatozoa with LGALS3BP in the centrosome region increased as cells progressively incorporated EVs during the epididymal transit. When LGALS3BP was inhibited during in vitro fertilization with mature sperm cells, less fertilized oocytes and slower first cell cycles were observed. When the protein was inhibited in epididymal EVs prior to incubation with sperm cells, poor fertilization success further demonstrated the role of EVs in the transfer of LGALS3BP to the spermatozoa. The key roles of this protein could lead to new approaches to enhance or control fertility in clinical settings.<\/jats:p>","DOI":"10.3390\/ijms24043077","type":"journal-article","created":{"date-parts":[[2023,2,6]],"date-time":"2023-02-06T02:57:32Z","timestamp":1675652252000},"page":"3077","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Transfer of Galectin-3-Binding Protein via Epididymal Extracellular Vesicles Promotes Sperm Fertilizing Ability and Developmental Potential in the Domestic Cat Model"],"prefix":"10.3390","volume":"24","author":[{"given":"Tricia","family":"Rowlison","sequence":"first","affiliation":[{"name":"Smithsonian National Zoo and Conservation Biology Institute, Washington, DC 20008, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pierre","family":"Comizzoli","sequence":"additional","affiliation":[{"name":"Smithsonian National Zoo and Conservation Biology Institute, Washington, DC 20008, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"R27","DOI":"10.1530\/REP-13-0420","article-title":"New insights into epididymal function in relation to sperm maturation","volume":"147","author":"Dacheux","year":"2014","journal-title":"Reproduction"},{"key":"ref_2","unstructured":"De Jonge, C.J., and Barratt, C.L.R. The Sperm Cell: Production, Maturation, Fertilization, Regeneration, Cambridge University Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1262\/jrd.2016-028","article-title":"Roles of the reproductive tract in modifications of the sperm membrane surface","volume":"62","author":"Kuo","year":"2016","journal-title":"J. Reprod. Dev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1095\/biolreprod.106.051342","article-title":"Poor centrosomal function of cat testicular spermatozoa impairs embryo development in vitro after intracytoplasmic sperm injection","volume":"75","author":"Comizzoli","year":"2006","journal-title":"Biol. Reprod."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1111\/rda.12831","article-title":"Deciphering the mechanisms involving cenexin, ninein and centriolin in sperm maturation during epididymal transit in the domestic cat","volume":"52","author":"Rowlison","year":"2017","journal-title":"Reprod. Domes.t Anim."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"James, E.R., Carrell, D.T., Aston, K.I., Jenkins, T.G., Yeste, M., and Salas-Huetos, A. (2020). The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21155377"},{"key":"ref_7","first-page":"1","article-title":"Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis","volume":"89","author":"Calvo","year":"2013","journal-title":"Biol. Reprod."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"31794","DOI":"10.1038\/srep31794","article-title":"Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome","volume":"6","author":"Reilly","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"R209","DOI":"10.1530\/REP-18-0480","article-title":"The contribution of epididymosomes to the sperm small RNA profile","volume":"157","author":"Trigg","year":"2019","journal-title":"Reproduction"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1093\/humrep\/det088","article-title":"microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy","volume":"28","author":"Belleannee","year":"2013","journal-title":"Hum. Reprod."},{"key":"ref_11","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":"2005","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1002\/jemt.10312","article-title":"Contribution of epididymal secretory proteins for spermatozoa maturation","volume":"61","author":"Dacheux","year":"2003","journal-title":"Microsc. Res. Tech."},{"key":"ref_13","first-page":"1234","article-title":"The epididymis and its role on sperm quality and male fertility","volume":"14","author":"Lucca","year":"2018","journal-title":"Anim. Reprod. AR"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/BF00220971","article-title":"Ultrastructural observations suggesting merocrine secretion in the initial segment of the mammalian epididymis","volume":"184","author":"Nicander","year":"1977","journal-title":"Cell Tissue Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1095\/biolreprod.109.082438","article-title":"Characterization of Two Distinct Populations of Epididymosomes Collected in the Intraluminal Compartment of the Bovine Cauda Epididymis1","volume":"83","author":"Frenette","year":"2010","journal-title":"Biol. Reprod."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1111\/j.1745-7262.2007.00281.x","article-title":"Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit","volume":"9","author":"Sullivan","year":"2007","journal-title":"Asian J. Androl."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Zhou, W., Stanger, S.J., Anderson, A.L., Bernstein, I.R., De Iuliis, G.N., McCluskey, A., McLaughlin, E.A., Dun, M.D., and Nixon, B. (2019). Mechanisms of tethering and cargo transfer during epididymosome-sperm interactions. BMC Biol., 17.","DOI":"10.1186\/s12915-019-0653-5"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"S91","DOI":"10.1074\/mcp.RA118.000946","article-title":"Proteomic profiling of mouse epididymosomes reveals their contributions to post-testicular sperm maturation","volume":"18","author":"Nixon","year":"2019","journal-title":"Mol. Cell. Proteom."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/0040-8166(91)90008-H","article-title":"Release of cytoplasmic apical protrusions from principal cells of the cat epididymis, an electron microscopic study","volume":"23","author":"Morales","year":"1991","journal-title":"Tissue Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1002\/mrd.90023","article-title":"Nature\u2019s ingenuity: Bypassing the classical secretory route via apocrine secretion","volume":"63","author":"Hermo","year":"2002","journal-title":"Mol. Reprod. Dev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1439-0272.1995.tb02087.x","article-title":"Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis","volume":"27","author":"Fornes","year":"1995","journal-title":"Andrologia"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1002\/(SICI)1098-2795(199902)52:2<225::AID-MRD14>3.0.CO;2-M","article-title":"Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein","volume":"52","author":"Morales","year":"1999","journal-title":"Mol. Reprod. Dev. Inc. Gamete Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1093\/molehr\/gam051","article-title":"Region-specific gene expression profiling along the human epididymis","volume":"13","author":"Thimon","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1002\/mrd.1013","article-title":"Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface","volume":"59","author":"Frenette","year":"2001","journal-title":"Mol. Reprod. Dev."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2061","DOI":"10.1007\/s10815-021-02214-0","article-title":"Exposure to epididymal extracellular vesicles enhances immature sperm function and sustains vitality of cryopreserved spermatozoa in the domestic cat model","volume":"38","author":"Rowlison","year":"2021","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1007\/s10815-017-1083-3","article-title":"Key factors enhancing sperm fertilizing ability are transferred from the epididymis to the spermatozoa via epididymosomes in the domestic cat model","volume":"35","author":"Rowlison","year":"2018","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2090","DOI":"10.1074\/mcp.RA120.002251","article-title":"Novel Proteomic Profiling of Epididymal Extracellular Vesicles in the Domestic Cat Reveals Proteins Related to Sequential Sperm Maturation with Differences Observed between Normospermic and Teratospermic Individuals","volume":"19","author":"Rowlison","year":"2020","journal-title":"Mol. Cell. Proteom."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1038\/onc.2013.548","article-title":"LGALS3BP, lectin galactoside-binding soluble 3 binding protein, promotes oncogenic cellular events impeded by antibody intervention","volume":"34","author":"Stampolidis","year":"2015","journal-title":"Oncogene"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1531","DOI":"10.1038\/ncomms2517","article-title":"LGALS3BP regulates centriole biogenesis and centrosome hypertrophy in cancer cells","volume":"4","author":"Fogeron","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e1075643","DOI":"10.1080\/23723556.2015.1075643","article-title":"Regulation of the centrosome cycle","volume":"3","author":"Fujita","year":"2016","journal-title":"Mol. Cell. Oncol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1016\/0093-691X(89)90031-9","article-title":"Ultrastructure of the domestic tom cat (Felisdomestica) and tiger (Pantheratigrisaltaica) spermatozoa","volume":"31","author":"Schmehl","year":"1989","journal-title":"Theriogenology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3109\/01485019708988530","article-title":"Inheritance of sperm centrioles and centrosomes in bovine embryos","volume":"38","author":"Sathananthan","year":"1997","journal-title":"Arch. Androl."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1002\/(SICI)1097-0029(20000601)49:5<445::AID-JEMT6>3.0.CO;2-B","article-title":"Centrosome inheritance in sheep zygotes: Centrioles are contributed by the sperm","volume":"49","author":"Crozet","year":"2000","journal-title":"Microsc. Res. Tech."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1002\/ar.1091690203","article-title":"The fine structure of the neck of mammalian spermatozoa","volume":"169","author":"Zamboni","year":"1971","journal-title":"Anat. Rec."},{"key":"ref_35","unstructured":"Comizzoli, P., and Wildt, D.E. (2012). The Centrosome, Springer."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5384","DOI":"10.1073\/pnas.93.11.5384","article-title":"Phenotypic variations among paternal centrosomes expressed within the zygote as disparate microtubule lengths and sperm aster organization: Correlations between centrosome activity and developmental success","volume":"93","author":"Navara","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1006\/dbio.1994.1256","article-title":"The centrosome and its mode of inheritance: The reduction of the centrosome during gametogenesis and its restoration during fertilization","volume":"165","author":"Schatten","year":"1994","journal-title":"Dev. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1093\/molehr\/gap049","article-title":"The role of centrosomes in mammalian fertilization and its significance for ICSI","volume":"15","author":"Schatten","year":"2009","journal-title":"Mol. Hum. Reprod."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1038\/nrg1654","article-title":"Paternal contribution: New insights and future challenges","volume":"6","author":"Krawetz","year":"2005","journal-title":"Nat. Rev. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1530\/rep.1.00996","article-title":"Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity","volume":"132","author":"Bauersachs","year":"2006","journal-title":"Reproduction"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1530\/REP-18-0188","article-title":"Blastocyst-induced changes in the bovine endometrial transcriptome","volume":"156","author":"Passaro","year":"2018","journal-title":"Reproduction"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1093\/humrep\/deaa335","article-title":"Proteome of fluid from human ovarian small antral follicles reveals insights in folliculogenesis and oocyte maturation","volume":"36","author":"Pla","year":"2021","journal-title":"Hum. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zhang, P., Ni, X., Guo, Y., Guo, X., Wang, Y., Zhou, Z., Huo, R., and Sha, J. (2009). Proteomic-based identification of maternal proteins in mature mouse oocytes. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-348"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"17639","DOI":"10.1073\/pnas.1013185107","article-title":"Proteome of mouse oocytes at different developmental stages","volume":"107","author":"Wang","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1093\/molehr\/gax059","article-title":"Proteomic analysis of germinal vesicles in the domestic cat model reveals candidate nuclear proteins involved in oocyte competence acquisition","volume":"24","author":"Lee","year":"2018","journal-title":"Mol. Hum. Reprod. Basic Sci. Reprod. Med."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Candenas, L., and Chianese, R. (2020). Exosome composition and Seminal Plasma Proteome: A promising source of biomarkers of male infertility. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21197022"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1111\/j.2047-2927.2012.00059.x","article-title":"Comparative proteomic analysis coupled with conventional protein assay as a strategy to identify predictors of successful testicular sperm extraction in patients with non-obstructive azoospermia","volume":"1","author":"Freour","year":"2013","journal-title":"Andrology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1002\/aja.1001720406","article-title":"Maturation of spermatozoa in the epididymis of the Chinese hamster","volume":"172","author":"Yanagimachi","year":"1985","journal-title":"Am. J. Anat."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e475","DOI":"10.1111\/j.1365-2605.2011.01203.x","article-title":"Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis","volume":"34","author":"Girouard","year":"2011","journal-title":"Int. J. Androl."},{"key":"ref_50","unstructured":"Schade, S. (2017). Molecular and Functional Characterization of the Galectin-3-Binding Protein LGALS3BP in Cancer and Centrosome Biology. [Ph.D. Thesis, Free University of Berlin]."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1093\/humrep\/14.7.1811","article-title":"Acephalic spermatozoa and abnormal development of the head-neck attachment: A human syndrome of genetic origin","volume":"14","author":"Chemes","year":"1999","journal-title":"Hum. Reprod."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1093\/humupd\/dmg034","article-title":"Sperm pathology: A step beyond descriptive morphology. Origin, characterization and fertility potential of abnormal sperm phenotypes in infertile men","volume":"9","author":"Chemes","year":"2003","journal-title":"Hum. Reprod. Update"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1093\/humrep\/17.9.2344","article-title":"A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage","volume":"17","author":"Rawe","year":"2002","journal-title":"Hum. Reprod."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e2101066","DOI":"10.1002\/adbi.202101066","article-title":"The Knowns and Unknowns about Epididymal Extracellular Vesicles in Different Animal Species","volume":"6","author":"Rowlison","year":"2022","journal-title":"Adv. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1535750","DOI":"10.1080\/20013078.2018.1535750","article-title":"Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines","volume":"7","author":"Witwer","year":"2018","journal-title":"J. Extracell. Vesicles"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1111\/rda.12047","article-title":"Source of protein supplementation during in vitro culture does not affect the quality of resulting blastocysts in the domestic cat","volume":"47","author":"Nestle","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e1849","DOI":"10.7717\/peerj.1849","article-title":"Effective protein inhibition in intact mouse oocytes through peptide nanoparticle-mediated antibody transfection","volume":"4","author":"Li","year":"2016","journal-title":"PeerJ"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"670021","DOI":"10.3389\/fcell.2021.670021","article-title":"Oocyte Meiotic Competence in the Domestic Cat Model: Novel Roles for Nuclear Proteins BRD2 and NPM1","volume":"9","author":"Chavez","year":"2021","journal-title":"Front. Cell Dev. Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/4\/3077\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:24:15Z","timestamp":1760120655000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/4\/3077"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,4]]},"references-count":58,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["ijms24043077"],"URL":"https:\/\/doi.org\/10.3390\/ijms24043077","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,4]]}}}