{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T04:23:15Z","timestamp":1792210995448,"version":"4.4.0"},"reference-count":38,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2022,4,2]],"date-time":"2022-04-02T00:00:00Z","timestamp":1648857600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2022,4,2]],"date-time":"2022-04-02T00:00:00Z","timestamp":1648857600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["grant no. 81401194"],"award-info":[{"award-number":["grant no. 81401194"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Biol Rep"],"published-print":{"date-parts":[[2022,6]]},"DOI":"10.1007\/s11033-022-07316-1","type":"journal-article","created":{"date-parts":[[2022,4,2]],"date-time":"2022-04-02T16:08:48Z","timestamp":1648915728000},"page":"4673-4681","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Extracellular vesicles derived from human Sertoli cells: characterizations, proteomic analysis, and miRNA profiling"],"prefix":"10.1007","volume":"49","author":[{"given":"Xiao-Hui","family":"Tan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sheng-Ji","family":"Gu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Jie","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Peng","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang-Yang","family":"Gu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi-Ming","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xue-Song","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhong-Cheng","family":"Xin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sae Woong","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0422-846X","authenticated-orcid":false,"given":"Rui-Li","family":"Guan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Woong Jin","family":"Bae","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,4,2]]},"reference":[{"key":"7316_CR1","doi-asserted-by":"publisher","first-page":"6977","DOI":"10.1126\/science.aau6977","volume":"6478","author":"R Kalluri","year":"2020","unstructured":"Kalluri R, LeBleu VS (2020) The biology, function, and biomedical applications of exosomes. Science 6478:6977","journal-title":"Science"},{"key":"7316_CR2","doi-asserted-by":"publisher","first-page":"27066","DOI":"10.3402\/jev.v4.27066","volume":"1","author":"M Y\u00e1\u00f1ez-M\u00f3","year":"2015","unstructured":"Y\u00e1\u00f1ez-M\u00f3 M, Siljander PRM, Andreu Z et al (2015) Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 1:27066","journal-title":"J Extracell Vesicles"},{"key":"7316_CR3","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1111\/andr.12165","volume":"2","author":"LR Fran\u00e7a","year":"2016","unstructured":"Fran\u00e7a LR, Hess RA, Dufour JM, Hofmann MC, Griswold MD (2016) The Sertoli cell: one hundred fifty years of beauty and plasticity. Andrology 2:189\u2013212","journal-title":"Andrology"},{"key":"7316_CR4","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.semcdb.2014.02.011","volume":"1","author":"G Kaur","year":"2014","unstructured":"Kaur G, Thompson LA, Dufour JM (2014) Sertoli cells: immunological sentinels of spermatogenesis. Semin Cell Dev Biol 1:36\u201344","journal-title":"Semin Cell Dev Biol"},{"key":"7316_CR5","doi-asserted-by":"publisher","first-page":"5683","DOI":"10.1038\/s41467-020-19414-4","volume":"1","author":"L Zhao","year":"2020","unstructured":"Zhao L, Yao C, Xing X et al (2020) Single-cell analysis of developing and azoospermia human testicles reveals central role of Sertoli cells. Nat Commun 1:5683","journal-title":"Nat Commun"},{"key":"7316_CR6","doi-asserted-by":"publisher","first-page":"224","DOI":"10.3389\/fendo.2019.00224","volume":"10","author":"SB Meroni","year":"2019","unstructured":"Meroni SB, Galardo MN, Rindone G, Gorga A, Riera MF, Cigorraga SB (2019) Molecular mechanisms and signaling pathways involved in Sertoli cell proliferation. Front Endocrinol 10:224","journal-title":"Front Endocrinol"},{"key":"7316_CR7","doi-asserted-by":"publisher","first-page":"764","DOI":"10.1016\/j.stem.2020.12.004","volume":"4","author":"J Guo","year":"2021","unstructured":"Guo J, Sosa E, Chitiashvili T et al (2021) Single-cell analysis of the developing human testis reveals somatic niche cell specification and fetal germline stem cell establishment. Cell Stem Cell 4:764\u2013778","journal-title":"Cell Stem Cell"},{"key":"7316_CR8","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1186\/0717-6287-47-31","volume":"1","author":"P Urriola-Mu\u00f1oz","year":"2014","unstructured":"Urriola-Mu\u00f1oz P, Lizama C, Lagos-Cabr\u00e9 R, Reyes JG, Moreno RD (2014) Differential expression and localization of ADAM10 and ADAM17 during rat spermatogenesis suggest a role in germ cell differentiation. Biol Res 1:31","journal-title":"Biol Res"},{"key":"7316_CR9","doi-asserted-by":"publisher","first-page":"10903","DOI":"10.1073\/pnas.93.20.10903","volume":"20","author":"LS Huang","year":"1996","unstructured":"Huang LS, Voyiaziakis E, Chen HL, Rubin EM, Gordon JW (1996) A Novel functional role for apolipoprotein B in male infertility in heterozygous apolipoprotein B knockout mice. Proc Natl Acad Sci USA 20:10903\u201310907","journal-title":"Proc Natl Acad Sci USA"},{"key":"7316_CR10","doi-asserted-by":"publisher","first-page":"33742","DOI":"10.1074\/jbc.M404628200","volume":"32","author":"GW Okunade","year":"2004","unstructured":"Okunade GW, Miller ML, Pyne GJ et al (2004) Targeted ablation of plasma membrane Ca2+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. J Biol Chem 32:33742\u201333750","journal-title":"J Biol Chem"},{"key":"7316_CR11","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1093\/molehr\/gav041","volume":"10","author":"E Bromfield","year":"2015","unstructured":"Bromfield E, Aitken RJ, Nixon B (2015) Novel characterization of the HSPA2-stabilizing protein BAG6 in human spermatozoa. Mol Hum Reprod 10:755\u2013769","journal-title":"Mol Hum Reprod"},{"key":"7316_CR12","first-page":"1","volume":"3","author":"P Intasqui","year":"2018","unstructured":"Intasqui P, Agarwal A, Sharma R, Samanta L, Bertolla RP (2018) Towards the identification of reliable sperm biomarkers for male infertility: a sperm proteomic approach. Andrologia 3:1\u201310","journal-title":"Andrologia"},{"key":"7316_CR13","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1006\/excr.1993.1063","volume":"1","author":"M Nakamura","year":"1993","unstructured":"Nakamura M, Moriya M, Baba T et al (1993) An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res 1:101\u2013110","journal-title":"Exp Cell Res"},{"key":"7316_CR14","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1006\/geno.2000.6418","volume":"1","author":"ZA Jenkins","year":"2001","unstructured":"Jenkins ZA, H\u00e5\u00e5g PG, Johansson HE (2001) Human eIF5A2 on chromosome 3Q25-Q27 is a phylogenetically conserved vertebrate variant of eukaryotic translation initiation factor 5a with tissue-specific expression. Genomics 1:101\u2013109","journal-title":"Genomics"},{"key":"7316_CR15","first-page":"1","volume":"6","author":"E Testa","year":"2018","unstructured":"Testa E, Nardozi D, Antinozzi C et al (2018) H2AFX and MDC1 promote maintenance of genomic integrity in male germ cells. J Cell Sci 6:1\u201310","journal-title":"J Cell Sci"},{"key":"7316_CR16","doi-asserted-by":"publisher","first-page":"3483","DOI":"10.1242\/dev.106450","volume":"18","author":"BT Yuen","year":"2014","unstructured":"Yuen BT, Bush KM, Barrilleaux BL, Cotterman R, Knoepfler PS (2014) Histone H33 regulates dynamic chromatin states during spermatogenesis. Development 18:3483\u20133494","journal-title":"Development"},{"key":"7316_CR17","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1016\/j.rbmo.2015.07.010","volume":"5","author":"GD Yao","year":"2015","unstructured":"Yao GD, Shi SL, Song WY et al (2015) Role of PAFAH1B1 in human spermatogenesis, fertilization and early embryonic development. Reprod Biomed Online 5:613\u2013624","journal-title":"Reprod Biomed Online"},{"key":"7316_CR18","doi-asserted-by":"publisher","first-page":"141","DOI":"10.5603\/FHC.a2018.0019","volume":"3","author":"H Shi","year":"2018","unstructured":"Shi H, Liu J, Zhu P et al (2018) Expression of peroxiredoxins in the human testis, epididymis and spermatozoa and their role in preventing H2O2-induced damage to spermatozoa. Folia Histochem Cytobiol 3:141\u2013150","journal-title":"Folia Histochem Cytobiol"},{"key":"7316_CR19","first-page":"1","volume":"25","author":"TM Nguyen","year":"2017","unstructured":"Nguyen TM (2017) Impact of 5\u2019-amp-activated protein kinase on male gonad and spermatozoa functions. Front Cell Dev Biol 25:1\u201310","journal-title":"Front Cell Dev Biol"},{"key":"7316_CR20","doi-asserted-by":"publisher","first-page":"298","DOI":"10.4161\/spmg.1.4.18326","volume":"4","author":"YH Lin","year":"2011","unstructured":"Lin YH, Kuo YC, Chiang HS, Kuo PL (2011) The role of the septin family in spermiogenesis. Spermatogenesis 4:298\u2013302","journal-title":"Spermatogenesis"},{"key":"7316_CR21","doi-asserted-by":"publisher","first-page":"17991","DOI":"10.1038\/srep17991","volume":"5","author":"X Mu\u00f1oz","year":"2015","unstructured":"Mu\u00f1oz X, Mata A, Bassas L, Larriba S (2015) Altered miRNA signature of developing germ-cells in infertile patients relates to the severity of spermatogenic failure and persists in spermatozoa. Sci Rep 5:17991","journal-title":"Sci Rep"},{"key":"7316_CR22","doi-asserted-by":"publisher","first-page":"1028","DOI":"10.1111\/andr.12276","volume":"6","author":"A Salas-Huetos","year":"2016","unstructured":"Salas-Huetos A, Blanco J, Vidal F et al (2016) Spermatozoa from normozoospermic fertile and infertile individuals convey a distinct miRNA Cargo. Andrology 6:1028\u20131036","journal-title":"Andrology"},{"key":"7316_CR23","doi-asserted-by":"publisher","first-page":"1455","DOI":"10.1093\/humrep\/det088","volume":"6","author":"C Belleann\u00e9e","year":"2013","unstructured":"Belleann\u00e9e C, L\u00e9gar\u00e9 C, Calvo E, Thimon V, Sullivan R (2013) MicroRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy. Hum Reprod 6:1455\u20131467","journal-title":"Hum Reprod"},{"key":"7316_CR24","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.gene.2018.04.022","volume":"663","author":"R Zhou","year":"2018","unstructured":"Zhou R, Zhang Y, Du G et al (2018) Down-regulated let-7b-5p represses glycolysis metabolism by targeting AURKB in asthenozoospermia. Gene 663:83\u201387","journal-title":"Gene"},{"key":"7316_CR25","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1016\/j.fertnstert.2015.06.015","volume":"3","author":"A Salas-Huetos","year":"2015","unstructured":"Salas-Huetos A, Blanco J, Vidal F et al (2015) Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertil Steril 3:591\u2013601","journal-title":"Fertil Steril"},{"key":"7316_CR26","first-page":"7","volume":"13","author":"J Lian","year":"2009","unstructured":"Lian J, Zhang X, Tian H et al (2009) Altered microRNA expression in patients with non-obstructive azoospermia. Reprod Biol Endocrinol 13:7","journal-title":"Reprod Biol Endocrinol"},{"key":"7316_CR27","doi-asserted-by":"publisher","first-page":"1827","DOI":"10.1093\/humrep\/det099","volume":"7","author":"W Wu","year":"2013","unstructured":"Wu W, Qin Y, Li Z et al (2013) Genome-wide microRNA expression profiling in idiopathic non-obstructive azoospermia: significant up-regulation of mir-141, miR-429 and miR-7-1-3p. Hum Reprod 7:1827\u20131836","journal-title":"Hum Reprod"},{"key":"7316_CR28","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1093\/abbs\/gmp116","volume":"2","author":"J Zhang","year":"2010","unstructured":"Zhang J, Liu Q, Zhang W et al (2010) Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim Biophys Sin 2:145\u2013153","journal-title":"Acta Biochim Biophys Sin"},{"key":"7316_CR29","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.omtn.2017.09.007","volume":"9","author":"C Yao","year":"2017","unstructured":"Yao C, Yuan Q, Niu M et al (2017) Distinct expression profiles and novel targets of microRNAs in human spermatogonia, pachytene spermatocytes, and round spermatids between OA patients and NOA patients. Mol Ther Nucleic Acids 9:182\u2013194","journal-title":"Mol Ther Nucleic Acids"},{"key":"7316_CR30","doi-asserted-by":"publisher","first-page":"967","DOI":"10.1016\/j.clinbiochem.2013.11.009","volume":"10\u201311","author":"L Hu","year":"2014","unstructured":"Hu L, Wu C, Guo C, Li H, Xiong C (2014) Identification of microRNAs predominately derived from testis and epididymis in human seminal plasma. Clin Biochem 10\u201311:967\u2013972","journal-title":"Clin Biochem"},{"key":"7316_CR31","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1186\/s12958-018-0393-3","volume":"1","author":"D Tang","year":"2018","unstructured":"Tang D, Huang Z, He X et al (2018) Altered miRNA profile in testis of post-cryptorchidopexy patients with non-obstructive azoospermia. Reprod Biol Endocrinol 1:78","journal-title":"Reprod Biol Endocrinol"},{"key":"7316_CR32","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1210\/er.2014-1101","volume":"5","author":"DD Mruk","year":"2015","unstructured":"Mruk DD, Cheng CY (2015) The mammalian blood-testis barrier: its biology and regulation. Endocr Rev 5:564\u2013591","journal-title":"Endocr Rev"},{"key":"7316_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.mce.2018.04.001","volume":"476","author":"F Mancuso","year":"2018","unstructured":"Mancuso F, Calvitti M, Milardi D et al (2018) Testosterone and FSH modulate Sertoli cell extracellular secretion: proteomic analysis. Mol Cell Endocrinol 476:1\u20137","journal-title":"Mol Cell Endocrinol"},{"key":"7316_CR34","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1111\/andr.12714","volume":"1","author":"A Salas-Huetos","year":"2020","unstructured":"Salas-Huetos A, James ER, Aston KI, Carrell DT, Jenkins TG, Yeste M (2020) The role of miRNAs in male human reproduction: a systematic review. Andrology 1:7\u201326","journal-title":"Andrology"},{"key":"7316_CR35","doi-asserted-by":"publisher","first-page":"7290","DOI":"10.1093\/nar\/gku347","volume":"11","author":"L Vojtech","year":"2014","unstructured":"Vojtech L, Woo S, Hughes S et al (2014) Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res 11:7290\u20137304","journal-title":"Nucleic Acids Res"},{"key":"7316_CR36","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1002\/mrd.10323","volume":"1","author":"J Liu","year":"2003","unstructured":"Liu J, Schiltz JF, Ashar HR, Chada KK (2003) Hmga1 is required for normal sperm development. Mol Reprod Dev 1:81\u201389","journal-title":"Mol Reprod Dev"},{"key":"7316_CR37","first-page":"109","volume":"2","author":"HY Xu","year":"2019","unstructured":"Xu HY, Zhang HX, Xiao Z, Qiao J, Li R (2019) Regulation of anti-m\u00fcllerian hormone (AMH) in males and the associations of serum AMH with the disorders of male fertility. Asian J Androl 2:109\u2013114","journal-title":"Asian J Androl"},{"key":"7316_CR38","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1111\/j.2047-2927.2013.00070.x","volume":"3","author":"LF Bentson","year":"2013","unstructured":"Bentson LF, Agbor VA, Agbor LN et al (2013) New point mutation in golga3 causes multiple defects in spermatogenesis. Andrology 3:440\u2013450","journal-title":"Andrology"}],"container-title":["Molecular Biology Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11033-022-07316-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11033-022-07316-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11033-022-07316-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,8]],"date-time":"2022-07-08T08:41:56Z","timestamp":1657269716000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11033-022-07316-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,2]]},"references-count":38,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2022,6]]}},"alternative-id":["7316"],"URL":"https:\/\/doi.org\/10.1007\/s11033-022-07316-1","relation":{},"ISSN":["0301-4851","1573-4978"],"issn-type":[{"value":"0301-4851","type":"print"},{"value":"1573-4978","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,2]]},"assertion":[{"value":"9 January 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 March 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 April 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare that they have no conflicts of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}},{"value":"Ethical approval was waived since this article does not contain any studies with human participants or animals. Human Sertoli cells were commercially available and purchased from ScienCell Research Laboratories (Cat. No. 4520; Carlsbad, CA, USA).","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"All data generated or analyzed during this study are included in this published article and its supplementary information files, which are available on reasonable request. The microarray data have been available in the Gene Expression Omnibus (GEO) database () under the accession number GSE192696. Raw mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD030640.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Data availability"}}]}}