Membrane-associated gamma-glutamyl transferase and alkaline phosphatase in the context of concanavalin A- and wheat germ agglutinin-reactive glycans mark seminal prostasome populations from normozoospermic and oligozoospermic men

References

• Carlsson L, Nilsson O, Larsson A, Stridsberg M, Sahlén G, Ronquist G. Characteristics of human prostasomes isolated from three different sources. Prostate. 2003;54:322–30. doi:10.1002/pros.10189
   PubMed Web of Science ®Google Scholar
• Sahlén G, Nilsson O, Larsson A, Carlsson L, Norlén BJ, Ronquist G. Secretions from seminal vesicles lack characteristic markers for prostasomes. Ups J Med Sci. 2010;115:107–12. doi:10.3109/03009730903366067
   PubMed Web of Science ®Google Scholar
• Ronquist G. Prostasomes are mediators of intercellular communication: from basic research to clinical implications. J Intern Med. 2012;271:400–13. doi:10.1111/j.1365-2796.2011.02487.x
   PubMed Web of Science ®Google Scholar
• Aalberts M, Stout TAE, Stoorvogel W. Prostasomes: extracellular vesicles from the prostate. Reproduction. 2014;147:R1–14. doi:10.1530/REP-13-0358
   PubMed Web of Science ®Google Scholar
• György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68:2667–88. doi:10.1007/s00018-011-0689-3
   PubMed Web of Science ®Google Scholar
• Kim D, Nishida H, An SY, Shetty AK, Bartosh TJ, Prockop DJ. Chromatographically isolated CD63 + CD81+ extracellular vesicles from mesenchymal stromal cells rescue cognitive impairments after TBI. Proc Natl Acad Sci USA. 2016;113:170–5. doi:10.1073/pnas.1522297113
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016;113:E968–77. doi:10.1073/pnas.1521230113
   PubMed Web of Science ®Google Scholar
• Gardiner C, Di Vizio D, Sahoo S, Théry C, Witwer KW, Wauben M, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles. 2016;5:32945. doi:10.3402/jev.v5.32945
   PubMed Web of Science ®Google Scholar
• Yáñez-Mó M, Siljander PRM, Andreu Z, Zavec AB, Borràs FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066. doi:10.3402/jev.v4.27066
   PubMed Web of Science ®Google Scholar
• Fais S, O’Driscoll L, Borras FE, Buzas E, Camussi G, Cappello F, et al. Evidence-based clinical use of nanoscale extracellular vesicles in nanomedicine. ACS Nano. 2016;10:3886–99. doi:10.1021/acsnano.5b08015
   PubMed Web of Science ®Google Scholar
• Kalra H, Drummen GPC, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. IJMS. 2016;17:170. doi:10.3390/ijms17020170
   Google Scholar
• Batista BS, Eng WS, Pilobello KT, Hendricks-Muñoz KD, Mahal LK. Identification of a conserved glycan signature for microvesicles. J Proteome Res. 2011;10:4624–33. doi:10.1021/pr200434y
   PubMed Web of Science ®Google Scholar
• Staubach S, Schadewaldt P, Wendel U, Nohroudi K, Hanisch FG. Differential glycomics of epithelial membrane glycoproteins from urinary exovesicles reveals shifts toward complex-type N-glycosylation in classical galactosemia. J Proteome Res. 2012;11:906–16. doi:10.1021/pr200711w
   PubMed Web of Science ®Google Scholar
• Gerlach JQ, Krüger A, Gallogly S, Hanley SA, Hogan MC, Ward CJ, et al. Surface glycosylation profiles of urine extracellular vesicles. PLoS One. 2013;8:e74801. doi:10.1371/journal.pone.0074801
   PubMed Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373–83. doi:10.1083/jcb.201211138
   PubMed Web of Science ®Google Scholar
• Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013;126:5553–65. doi:10.1242/jcs.128868
   PubMed Web of Science ®Google Scholar
• Liang Y, Eng WS, Colquhoun DR, Dinglasan RR, Graham DR, Mahal LK. Complex N-linked glycans serve as a determinant for exosome/microvesicle cargo recruitment. J Biol Chem. 2014;289:32526–37. doi:10.1074/jbc.M114.606269
   PubMed Web of Science ®Google Scholar
• Buzás EI, Tóth E, Sódar BW, Szabó-Taylor K. Molecular interactions at the surface of extracellular vesicles. Semin Immunopathol. 2018;40:453–64. doi:10.1007/s00281-018-0682-0
   PubMed Web of Science ®Google Scholar
• Lässer C, Jang SC, Lötvall J. Subpopulations of extracellular vesicles and their therapeutic potential. Mol Aspects Med. 2018;60:1–14. doi:10.1016/j.mam.2018.02.002
   PubMed Web of Science ®Google Scholar
• Milutinović B, Goč S, Mitić N, Kosanović M, Janković M. Surface glycans contribute to differences between seminal prostasomes from normozoospermic and oligozoospermic men. Ups J Med Sci. 2019;124:111–8. doi:10.1080/03009734.2019.1592266
   PubMed Web of Science ®Google Scholar
• Milutinovic B, Mitic N, Roncevic J, Goc S, Jankovic M. Glycome complexity of human seminal plasma high molecular mass components: evaluation of the contribution of acid-soluble glycoproteins/mucins and extracellular vesicles. Arch Biochem Biophys. 2016;609:20–30. doi:10.1016/j.abb.2016.09.005
   PubMed Web of Science ®Google Scholar
• Lilja H, Weiber H. γ-Glutamyltransferase bound to prostatic subcellular organelles and in free form in human seminal plasma. Scand J Clin Lab Invest. 1983;43:307–12. doi:10.3109/00365518309168262
   PubMed Web of Science ®Google Scholar
• Fabiani R. Functional and biochemical characteristics of human prostasomes. Ups J Med Sci. 1994;99:73–111. doi:10.3109/03009739409179353
   PubMedGoogle Scholar
• Fabiani R, Ronquist G. Association of some hydrolytic enzymes with the prostasome membrane and their differential responses to detergent and PIPLC treatment. Prostate. 1995;27b:95–101. doi:10.1002/pros.2990270206
   Google Scholar
• Mitić N, Kosanović M, Milutinović B, Goč S, Mladenović D, Grubiša I, et al. Nano-sized CA125 antigen glycocamouflage: mucin - extracellular vesicles alliance to watch? Arch Biochem Biophys. 2018;653:113–20. doi:10.1016/j.abb.2018.06.017
   PubMed Web of Science ®Google Scholar
• Kosanović M, Milutinović B, Goč S, Mitić N, Janković M. Ion-exchange chromatography purification of extracellular vesicles. Biotechniques. 2017;63:65–71. doi:10.2144/000114575
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–5. doi:10.1038/227680a0
   PubMed Web of Science ®Google Scholar
• Moremen KW, Tiemeyer M, Nairn AV. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol. 2012;13:448–62. doi:10.1038/nrm3383
   PubMed Web of Science ®Google Scholar
• Brockhausen I, Glycobiology protocols. Totowa, NJ: Humana Press; 2006.
   Google Scholar
• Ronquist G, Hedström M. Restoration of detergent-inactivated adenosine triphosphatase activity of human prostatic fluid with concanavalin A. Biochim Biophys Acta. 1977;483:483–6. doi:10.1016/0005-2744(77)90078-X
   PubMed Web of Science ®Google Scholar
• Sumi S, Arai K, Kitahara S, Yoshida K. Serial lectin affinity chromatography demonstrates altered asparagine-linked sugar-chain structures of prostate-specific antigen in human prostate carcinoma. J Chromatogr B Biomed Sci Appl. 1999;727:9–14. doi:10.1016/S0378-4347(99)00069-9
   PubMed Web of Science ®Google Scholar
• Cummings RD. Lectins as tools for glycoconjugate purification and characterization. In: Gabius H-J, Gabius S. Glycosciences: status and perspectives. London, UK: Chapman and Hall; 2008. 191–9.
   Google Scholar
• Tang W, Miura T, Nakata M, Kojima N, Mizuochi T. Binding specificities of lectins to immobilized glycoproteins and oligosaccharides differ from those of immobilized lectins to oligosaccharides. Acta Med Okayama. 1998;52:311–8. doi:10.18926/AMO/31309
   PubMed Web of Science ®Google Scholar
• Balaj L, Atai NA, Chen W, Mu D, Tannous BA, Breakefield XO, et al. Heparin affinity purification of extracellular vesicles. Sci Rep. 2015;5:10266. doi:10.1038/srep10266
   PubMed Web of Science ®Google Scholar
• Wang T, Turko IV. Proteomic toolbox to standardize the separation of extracellular vesicles and lipoprotein particles. J Proteome Res 2018;17:3107–13.
   Web of Science ®Google Scholar
• Dubois L, Ronquist KG, Ek B, Ronquist G, Larsson A. Proteomic profiling of detergent resistant membranes (lipid rafts) of prostasomes. Mol Cell Proteomics. 2015;14:3015–22. doi:10.1074/mcp.M114.047530
   PubMed Web of Science ®Google Scholar
• Witwer KW, Buzás EI, Bemis LT, Bora A, Lässer C, Lötvall J, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:20360. doi:10.3402/jev.v2i0.20360
   PubMedGoogle Scholar
• Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate. 2009;69:159–67. doi:10.1002/pros.20860
   PubMed Web of Science ®Google Scholar
• Brody I, Ronquist G, Gottfries A, Stegmayr B. Abnormal deficiency of both Mg2+ and Ca2+-dependent adenosine triphosphatase and secretory granules and vesicles in human seminal plasma. Scand J Urol Nephrol. 1981;15:85–90. doi:10.3109/00365598109179581
   PubMed Web of Science ®Google Scholar
• García-Rodríguez A, de la Casa M, Peinado H, Gosálvez J, Roy R. Human prostasomes from normozoospermic and non-normozoospermic men show a differential protein expression pattern. Andrology 2018;6:585–96. doi:10.1111/andr.12496
   PubMed Web of Science ®Google Scholar
• Verhoeven G, Steeno O. Evidence for the prostatic origin of gamma-glutamyltransferase activity in human semen. Andrologia. 1979;1:163–9. doi:10.1111/j.1439-0272.1979.tb02181.x
   Google Scholar
• Frierson HJ, Theodorescu D, Mills S, Hanigan M. Gamma-glutamyl transpeptidase in normal and neoplastic prostate glands. Mod Pathol 1997;10:1–6.
   PubMed Web of Science ®Google Scholar
• Whitfield JB. Gamma glutamyl transferase. Crit Rev Clin Lab Sci. 2001;38:263–355. doi:10.1080/20014091084227
   PubMed Web of Science ®Google Scholar