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Current Drug Metabolism

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ISSN (Print): 1389-2002
ISSN (Online): 1875-5453

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Mini-Review Article

Role of Exosomes in the Exchange of Spermatozoa after Leaving the Seminiferous Tubule: A Review

Author(s): Luming Wu, Yuan Ding, Shiqiang Han and Yiqing Wang*

Volume 21, Issue 5, 2020

Page: [330 - 338] Pages: 9

DOI: 10.2174/1389200221666200520091511

Price: $65

Abstract

Background: Exosomes are extracellular vesicles (EVs) released from cells upon fusion of an intermediate endocytic compartment with the plasma membrane. They refer to the intraluminal vesicles released from the fusion of multivesicular bodies with the plasma membrane. The contents and number of exosomes are related to diseases such as metabolic diseases, cancer and inflammatory diseases. Exosomes have been used in neurological research as a drug delivery tool and also as biomarkers for diseases. Recently, exosomes were observed in the seminal plasma of the one who is asthenozoospermia, which can affect sperm motility and capacitation.

Objective: The main objective of this review is to deeply discuss the role of exosomes in spermatozoa after leaving the seminiferous tubule.

Methods: We conducted an extensive search of the literature available on relationships between exosomes and exosomes in spermatozoa on the bibliographic database.

Conclusion: This review thoroughly discussed the role that exosomes play in the exchange of spermatozoa after leaving the seminiferous tubule and its potential as a drug delivery tool and biomarkers for diseases as well.

Keywords: Exosomes, spermatozoa, miRNA, proteins, epididymis, prostasomes.

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[1]
Kim, J.H.; Lee, J.; Park, J.; Gho, Y.S. Gram-negative and gram-positive bacterial extracellular vesicles. Semin. Cell Dev. Biol., 2015, 40, 97-104.
[http://dx.doi.org/10.1016/j.semcdb.2015.02.006] [PMID: 25704309]
[2]
Mantel, P.Y.; Marti, M. The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cell. Microbiol., 2014, 16(3), 344-354.
[http://dx.doi.org/10.1111/cmi.12259] [PMID: 24406102]
[3]
Cocucci, E.; Meldolesi, J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol., 2015, 25(6), 364-372.
[http://dx.doi.org/10.1016/j.tcb.2015.01.004] [PMID: 25683921]
[4]
Soung, Y.H.; Ford, S.; Zhang, V.; Chung, J. Exosomes in cancer diagnostics. Cancers (Basel), 2017, 9(1) E8
[http://dx.doi.org/10.3390/cancers9010008] [PMID: 28085080]
[5]
Zomer, A.; Vendrig, T.; Hopmans, E.S.; van Eijndhoven, M.; Middeldorp, J.M.; Pegtel, D.M. Exosomes: Fit to deliver small RNA. Commun. Integr. Biol., 2010, 3(5), 447-450.
[http://dx.doi.org/10.4161/cib.3.5.12339] [PMID: 21057637]
[6]
Colombo, M.; Moita, C.; van Niel, G.; Kowal, J.; Vigneron, J.; Benaroch, P.; Manel, N.; Moita, L.F.; Théry, C.; Raposo, G. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci., 2013, 126(Pt 24), 5553-5565.
[http://dx.doi.org/10.1242/jcs.128868] [PMID: 24105262]
[7]
Hessvik, N.P.; Llorente, A. Current knowledge on exosome biogenesis and release. Cell. Mol. Life Sci., 2018, 75(2), 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[8]
Tian, T.; Zhu, Y.L.; Zhou, Y.Y.; Liang, G.F.; Wang, Y.Y.; Hu, F.H.; Xiao, Z.D. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J. Biol. Chem., 2014, 289(32), 22258-22267.
[http://dx.doi.org/10.1074/jbc.M114.588046] [PMID: 24951588]
[9]
Fitzner, D.; Schnaars, M.; van Rossum, D.; Krishnamoorthy, G.; Dibaj, P.; Bakhti, M.; Regen, T.; Hanisch, U.K.; Simons, M. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci., 2011, 124(Pt 3), 447-458.
[http://dx.doi.org/10.1242/jcs.074088] [PMID: 21242314]
[10]
Feng, D.; Zhao, W.L.; Ye, Y.Y.; Bai, X.C.; Liu, R.Q.; Chang, L.F.; Zhou, Q.; Sui, S.F. Cellular internalization of exosomes occurs through phagocytosis. Traffic, 2010, 11(5), 675-687.
[http://dx.doi.org/10.1111/j.1600-0854.2010.01041.x] [PMID: 20136776]
[11]
Parolini, I.; Federici, C.; Raggi, C.; Lugini, L.; Palleschi, S.; De Milito, A.; Coscia, C.; Iessi, E.; Logozzi, M.; Molinari, A.; Colone, M.; Tatti, M.; Sargiacomo, M.; Fais, S. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem., 2009, 284(49), 34211-34222.
[http://dx.doi.org/10.1074/jbc.M109.041152] [PMID: 19801663]
[12]
Lötvall, J.; Hill, A.F.; Hochberg, F.; Buzás, E.I.; Di Vizio, D.; Gardiner, C.; Gho, Y.S.; Kurochkin, I.V.; Mathivanan, S.; Quesenberry, P.; Sahoo, S.; Tahara, H.; Wauben, M.H.; Witwer, K.W.; Théry, C. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles, 2014, 3, 26913.
[http://dx.doi.org/10.3402/jev.v3.26913] [PMID: 25536934]
[13]
Machtinger, R.; Laurent, L.C.; Baccarelli, A.A. Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum. Reprod. Update, 2016, 22(2), 182-193.
[PMID: 26663221]
[14]
Huang, X.; Yuan, T.; Tschannen, M.; Sun, Z.; Jacob, H.; Du, M.; Liang, M.; Dittmar, R.L.; Liu, Y.; Liang, M.; Kohli, M.; Thibodeau, S.N.; Boardman, L.; Wang, L. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics, 2013, 14, 319.
[http://dx.doi.org/10.1186/1471-2164-14-319] [PMID: 23663360]
[15]
Vojtech, L.; Woo, S.; Hughes, S.; Levy, C.; Ballweber, L.; Sauteraud, R.P.; Strobl, J.; Westerberg, K.; Gottardo, R.; Tewari, M.; Hladik, F. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res., 2014, 42(11), 7290-7304.
[http://dx.doi.org/10.1093/nar/gku347] [PMID: 24838567]
[16]
Théry, C.; Regnault, A.; Garin, J.; Wolfers, J.; Zitvogel, L.; Ricciardi-Castagnoli, P.; Raposo, G.; Amigorena, S. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J. Cell Biol., 1999, 147(3), 599-610.
[http://dx.doi.org/10.1083/jcb.147.3.599] [PMID: 10545503]
[17]
Yáñez-Mó, M.; Siljander, P.R.; Andreu, Z.; Zavec, A.B.; Borràs, F.E.; Buzas, E.I.; Buzas, K.; Casal, E.; Cappello, F.; Carvalho, J.; Colás, E.; Cordeiro-da Silva, A.; Fais, S.; Falcon-Perez, J.M.; Ghobrial, I.M.; Giebel, B.; Gimona, M.; Graner, M.; Gursel, I.; Gursel, M.; Heegaard, N.H.; Hendrix, A.; Kierulf, P.; Kokubun, K.; Kosanovic, M.; Kralj-Iglic, V.; Krämer-Albers, E.M.; Laitinen, S.; Lässer, C.; Lener, T.; Ligeti, E.; Linē, A.; Lipps, G.; Llorente, A.; Lötvall, J.; Manček-Keber, M.; Marcilla, A.; Mittelbrunn, M.; Nazarenko, I.; Nolte-’t Hoen, E.N.; Nyman, T.A.; O’Driscoll, L.; Olivan, M.; Oliveira, C.; Pállinger, É.; Del Portillo, H.A.; Reventós, J.; Rigau, M.; Rohde, E.; Sammar, M.; Sánchez-Madrid, F.; Santarém, N.; Schallmoser, K.; Ostenfeld, M.S.; Stoorvogel, W.; Stukelj, R.; Van der Grein, S.G.; Vasconcelos, M.H.; Wauben, M.H.; De Wever, O. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles, 2015, 4, 27066.
[http://dx.doi.org/10.3402/jev.v4.27066] [PMID: 25979354]
[18]
Brouwers, J.F.; Aalberts, M.; Jansen, J.W.; van Niel, G.; Wauben, M.H.; Stout, T.A.; Helms, J.B.; Stoorvogel, W. Distinct lipid compositions of two types of human prostasomes. Proteomics, 2013, 13(10-11), 1660-1666.
[http://dx.doi.org/10.1002/pmic.201200348] [PMID: 23404715]
[19]
Trajkovic, K.; Hsu, C.; Chiantia, S.; Rajendran, L.; Wenzel, D.; Wieland, F.; Schwille, P.; Brügger, B.; Simons, M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science, 2008, 319(5867), 1244-1247.
[http://dx.doi.org/10.1126/science.1153124] [PMID: 18309083]
[20]
Thakur, B.K.; Zhang, H.; Becker, A.; Matei, I.; Huang, Y.; Costa-Silva, B.; Zheng, Y.; Hoshino, A.; Brazier, H.; Xiang, J.; Williams, C.; Rodriguez-Barrueco, R.; Silva, J.M.; Zhang, W.; Hearn, S.; Elemento, O.; Paknejad, N.; Manova-Todorova, K.; Welte, K.; Bromberg, J.; Peinado, H.; Lyden, D. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res., 2014, 24(6), 766-769.
[http://dx.doi.org/10.1038/cr.2014.44] [PMID: 24710597]
[21]
Waldenström, A.; Gennebäck, N.; Hellman, U.; Ronquist, G. Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One, 2012, 7(4) e34653
[http://dx.doi.org/10.1371/journal.pone.0034653] [PMID: 22506041]
[22]
Guescini, M.; Genedani, S.; Stocchi, V.; Agnati, L.F. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J. Neural Transm. (Vienna), 2010, 117(1), 1-4.
[http://dx.doi.org/10.1007/s00702-009-0288-8] [PMID: 19680595]
[23]
Barile, L.; Vassalli, G. Exosomes: Therapy delivery tools and biomarkers of diseases. Pharmacol. Ther., 2017, 174, 63-78.
[http://dx.doi.org/10.1016/j.pharmthera.2017.02.020] [PMID: 28202367]
[24]
Aryani, A.; Denecke, B. Exosomes as a nanodelivery system: a key to the future of neuromedicine? Mol. Neurobiol., 2016, 53(2), 818-834.
[http://dx.doi.org/10.1007/s12035-014-9054-5] [PMID: 25502465]
[25]
Rao, P.S.S.; O’Connell, K.; Finnerty, T.K. Potential role of extracellular vesicles in the pathophysiology of drug addiction. Mol. Neurobiol., 2018, 55(8), 6906-6913.
[http://dx.doi.org/10.1007/s12035-018-0912-4] [PMID: 29363042]
[26]
Guo, L.; Guo, N. Exosomes: potent regulators of tumor malignancy and potential bio-tools in clinical application. Crit. Rev. Oncol. Hematol., 2015, 95(3), 346-358.
[http://dx.doi.org/10.1016/j.critrevonc.2015.04.002] [PMID: 25982702]
[27]
Takahashi, R.U.; Prieto-Vila, M.; Hironaka, A.; Ochiya, T. The role of extracellular vesicle microRNAs in cancer biology. Clin. Chem. Lab. Med., 2017, 55(5), 648-656.
[http://dx.doi.org/10.1515/cclm-2016-0708] [PMID: 28231055]
[28]
Rejraji, H.; Sion, B.; Prensier, G.; Carreras, M.; Motta, C.; Frenoux, J.M.; Vericel, E.; Grizard, G.; Vernet, P.; Drevet, J.R. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol. Reprod., 2006, 74(6), 1104-1113.
[http://dx.doi.org/10.1095/biolreprod.105.049304] [PMID: 16510839]
[29]
Höög, J.L.; Lötvall, J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J. Extracell. Vesicles, 2015, 4, 28680.
[http://dx.doi.org/10.3402/jev.v4.28680] [PMID: 26563734]
[30]
Murdica, V.; Giacomini, E.; Alteri, A.; Bartolacci, A.; Cermisoni, G. C.; Zarovni, N.; Papaleo, E.; Montorsi, F.; Salonia, A.; Vigano, P.; Vago, R. Seminal plasma of men with severe asthenozoospermia contain exosomes that affect spermatozoa motility and capacitation. Fertil Steril, 2019, 111(5), 897-908. e2
[http://dx.doi.org/10.1016/j.fertnstert.2019.01.030]
[31]
Sullivan, R.; Saez, F.; Girouard, J.; Frenette, G. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol. Dis., 2005, 35(1), 1-10.
[http://dx.doi.org/10.1016/j.bcmd.2005.03.005] [PMID: 15893944]
[32]
Neto, F.T.; Bach, P.V.; Najari, B.B.; Li, P.S.; Goldstein, M. Spermatogenesis in humans and its affecting factors. Semin. Cell Dev. Biol., 2016, 59, 10-26.
[http://dx.doi.org/10.1016/j.semcdb.2016.04.009] [PMID: 27143445]
[33]
Sullivan, R.; Saez, F. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction, 2013, 146(1), R21-R35.
[http://dx.doi.org/10.1530/REP-13-0058] [PMID: 23613619]
[34]
Owen, D.H.; Katz, D.F. A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J. Androl., 2005, 26(4), 459-469.
[http://dx.doi.org/10.2164/jandrol.04104] [PMID: 15955884]
[35]
Sisti, G.; Kanninen, T.T.; Witkin, S.S. Maternal immunity and pregnancy outcome: focus on preconception and autophagy. Genes Immun., 2016, 17(1), 1-7.
[http://dx.doi.org/10.1038/gene.2015.57] [PMID: 26656449]
[36]
Robertson, S.A.; Sharkey, D.J. The role of semen in induction of maternal immune tolerance to pregnancy. Semin. Immunol., 2001, 13(4), 243-254.
[http://dx.doi.org/10.1006/smim.2000.0320] [PMID: 11437632]
[37]
Ickowicz, D.; Finkelstein, M.; Breitbart, H. Mechanism of sperm capacitation and the acrosome reaction: role of protein kinases. Asian J. Androl., 2012, 14(6), 816-821.
[http://dx.doi.org/10.1038/aja.2012.81] [PMID: 23001443]
[38]
Fraser, L.R. Sperm capacitation and the acrosome reaction. Hum. Reprod., 1998, 13(Suppl. 1), 9-19.
[http://dx.doi.org/10.1093/humrep/13.suppl_1.9] [PMID: 9663766]
[39]
Zaneveld, L.J.; De Jonge, C.J.; Anderson, R.A.; Mack, S.R. Human sperm capacitation and the acrosome reaction. Hum. Reprod., 1991, 6(9), 1265-1274.
[http://dx.doi.org/10.1093/oxfordjournals.humrep.a137524] [PMID: 1752929]
[40]
Zhu, J.; Barratt, C.L.; Lippes, J.; Pacey, A.A.; Cooke, I.D. The sequential effects of human cervical mucus, oviductal fluid, and follicular fluid on sperm function. Fertil. Steril., 1994, 61(6), 1129-1135.
[http://dx.doi.org/10.1016/S0015-0282(16)56768-5] [PMID: 8194629]
[41]
Dacheux, J.L.; Belleannée, C.; Guyonnet, B.; Labas, V.; Teixeira-Gomes, A.P.; Ecroyd, H.; Druart, X.; Gatti, J.L.; Dacheux, F. The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Syst Biol Reprod Med, 2012, 58(4), 197-210.
[http://dx.doi.org/10.3109/19396368.2012.663233] [PMID: 22788532]
[42]
Belleannée, C.; Calvo, É.; Caballero, J.; Sullivan, R. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol. Reprod., 2013, 89(2), 30.
[http://dx.doi.org/10.1095/biolreprod.113.110486] [PMID: 23803555]
[43]
Fornés, M.W.; Barbieri, A.; Cavicchia, J.C. Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis. Andrologia, 1995, 27(1), 1-5.
[http://dx.doi.org/10.1111/j.1439-0272.1995.tb02087.x] [PMID: 7755184]
[44]
Rejraji, H.; Vernet, P.; Drevet, J.R. GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Mol. Reprod. Dev., 2002, 63(1), 96-103.
[http://dx.doi.org/10.1002/mrd.10136] [PMID: 12211066]
[45]
Gatti, J.L.; Métayer, S.; Belghazi, M.; Dacheux, F.; Dacheux, J.L. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod., 2005, 72(6), 1452-1465.
[http://dx.doi.org/10.1095/biolreprod.104.036426] [PMID: 15635128]
[46]
Thimon, V.; Frenette, G.; Saez, F.; Thabet, M.; Sullivan, R. Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum. Reprod., 2008, 23(8), 1698-1707.
[http://dx.doi.org/10.1093/humrep/den181] [PMID: 18482993]
[47]
Théry, C.; Ostrowski, M.; Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol., 2009, 9(8), 581-593.
[http://dx.doi.org/10.1038/nri2567] [PMID: 19498381]
[48]
Girouard, J.; Frenette, G.; Sullivan, R. Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int. J. Androl., 2011, 34(5 Pt 2), e475-e486.
[http://dx.doi.org/10.1111/j.1365-2605.2011.01203.x] [PMID: 21875428]
[49]
Frenette, G.; Lessard, C.; Sullivan, R. Polyol pathway along the bovine epididymis. Mol. Reprod. Dev., 2004, 69(4), 448-456.
[http://dx.doi.org/10.1002/mrd.20170] [PMID: 15457514]
[50]
Frenette, G.; Thabet, M.; Sullivan, R. Polyol pathway in human epididymis and semen. J. Androl., 2006, 27(2), 233-239.
[http://dx.doi.org/10.2164/jandrol.05108] [PMID: 16278369]
[51]
Vernet, P.; Aitken, R.J.; Drevet, J.R. Antioxidant strategies in the epididymis. Mol. Cell. Endocrinol., 2004, 216(1-2), 31-39.
[http://dx.doi.org/10.1016/j.mce.2003.10.069] [PMID: 15109742]
[52]
Kirchhoff, C.; Carballada, R.; Harms, B.; Kascheike, I. CD52 mRNA is modulated by androgens and temperature in epididymal cell cultures. Mol. Reprod. Dev., 2000, 56(1), 26-33.
[http://dx.doi.org/10.1002/(SICI)1098-2795(200005)56:1<26:AID-MRD4>3.0.CO;2-K] [PMID: 10737964]
[53]
Kirchhoff, C. CD52 is the ‘major maturation-associated’ sperm membrane antigen. Mol. Hum. Reprod., 1996, 2(1), 9-17.
[http://dx.doi.org/10.1093/molehr/2.1.9] [PMID: 9238651]
[54]
Kirchhoff, C.; Hale, G. Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Mol. Hum. Reprod., 1996, 2(3), 177-184.
[http://dx.doi.org/10.1093/molehr/2.3.177] [PMID: 9238677]
[55]
Yeung, C.H.; Schröter, S.; Wagenfeld, A.; Kirchhoff, C.; Kliesch, S.; Poser, D.; Weinbauer, G.F.; Nieschlag, E.; Cooper, T.G. Interaction of the human epididymal protein CD52 (HE5) with epididymal spermatozoa from men and cynomolgus monkeys. Mol. Reprod. Dev., 1997, 48(2), 267-275.
[http://dx.doi.org/10.1002/(SICI)1098-2795(199710)48:2<267:AID-MRD15>3.0.CO;2-V] [PMID: 9291477]
[56]
Moretti, E.; Collodel, G.; Salvatici, M.C.; Belmonte, G.; Signorini, C. New insights into sperm with total globozoospermia: Increased fatty acid oxidation and centrin1 alteration. Syst. Biol. Reprod. Med., 2019, 65(5), 390-399.
[http://dx.doi.org/10.1080/19396368.2019.1626934] [PMID: 31204846]
[57]
Vernet, P.; Faure, J.; Dufaure, J.P.; Drevet, J.R. Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase. Mol. Reprod. Dev., 1997, 47(1), 87-98.
[http://dx.doi.org/10.1002/(SICI)1098-2795(199705)47:1<87:AID-MRD12>3.0.CO;2-X] [PMID: 9110319]
[58]
Sutovsky, P.; Moreno, R.; Ramalho-Santos, J.; Dominko, T.; Thompson, W.E.; Schatten, G. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J. Cell Sci., 2001, 114(Pt 9), 1665-1675.
[PMID: 11309198]
[59]
Sutovsky, P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc. Res. Tech., 2003, 61(1), 88-102.
[http://dx.doi.org/10.1002/jemt.10319] [PMID: 12672125]
[60]
Bloom, B.R.; Bennett, B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science, 1966, 153(3731), 80-82.
[http://dx.doi.org/10.1126/science.153.3731.80] [PMID: 5938421]
[61]
Eickhoff, R.; Wilhelm, B.; Renneberg, H.; Wennemuth, G.; Bacher, M.; Linder, D.; Bucala, R.; Seitz, J.; Meinhardt, A. Purification and characterization of macrophage migration inhibitory factor as a secretory protein from rat epididymis: evidences for alternative release and transfer to spermatozoa. Mol. Med., 2001, 7(1), 27-35.
[http://dx.doi.org/10.1007/BF03401836] [PMID: 11474125]
[62]
Frenette, G.; Lessard, C.; Madore, E.; Fortier, M.A.; Sullivan, R. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol. Reprod., 2003, 69(5), 1586-1592.
[http://dx.doi.org/10.1095/biolreprod.103.019216] [PMID: 12826572]
[63]
Eickhoff, R.; Baldauf, C.; Koyro, H.W.; Wennemuth, G.; Suga, Y.; Seitz, J.; Henkel, R.; Meinhardt, A. Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Mol. Hum. Reprod., 2004, 10(8), 605-611.
[http://dx.doi.org/10.1093/molehr/gah075] [PMID: 15169922]
[64]
Meinhardt, A.; Bacher, M.; McFarlane, J.R.; Metz, C.N.; Seitz, J.; Hedger, M.P.; de Kretser, D.M.; Bucala, R. Macrophage migration inhibitory factor production by Leydig cells: evidence for a role in the regulation of testicular function. Endocrinology, 1996, 137(11), 5090-5095.
[http://dx.doi.org/10.1210/endo.137.11.8895383] [PMID: 8895383]
[65]
Shimizu, T.; Ohkawara, A.; Nishihira, J.; Sakamoto, W. Identification of macrophage migration inhibitory factor (MIF) in human skin and its immmunohistochemical localization. FEBS Lett., 1996, 381(3), 199-202.
[http://dx.doi.org/10.1016/0014-5793(96)00120-2] [PMID: 8601455]
[66]
Waeber, G.; Calandra, T.; Roduit, R.; Haefliger, J.A.; Bonny, C.; Thompson, N.; Thorens, B.; Temler, E.; Meinhardt, A.; Bacher, M.; Metz, C.N.; Nicod, P.; Bucala, R. Insulin secretion is regulated by the glucose-dependent production of islet beta cell macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. USA, 1997, 94(9), 4782-4787.
[http://dx.doi.org/10.1073/pnas.94.9.4782] [PMID: 9114069]
[67]
Yoshimoto, T.; Nishihira, J.; Tada, M.; Houkin, K.; Abe, H. Induction of macrophage migration inhibitory factor messenger ribonucleic acid in rat forebrain by reperfusion. Neurosurgery, 1997, 41(3), 648-653.
[PMID: 9310983]
[68]
Lolis, E.; Bucala, R. Crystal structure of macrophage migration inhibitory factor (MIF), a glucocorticoid-induced regulator of cytokine production, reveals a unique architecture. Proc. Assoc. Am. Physicians, 1996, 108(6), 415-419.
[PMID: 8956364]
[69]
Flieger, O.; Engling, A.; Bucala, R.; Lue, H.; Nickel, W.; Bernhagen, J. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett., 2003, 551(1-3), 78-86.
[http://dx.doi.org/10.1016/S0014-5793(03)00900-1] [PMID: 12965208]
[70]
Zhang, H.; Martin-DeLeon, P.A. Mouse Spam1 (PH-20) is a multifunctional protein: evidence for its expression in the female reproductive tract. Biol. Reprod., 2003, 69(2), 446-454.
[http://dx.doi.org/10.1095/biolreprod.102.013854] [PMID: 12672666]
[71]
Chen, H.; Griffiths, G.; Galileo, D.S.; Martin-DeLeon, P.A. Epididymal SPAM1 is a marker for sperm maturation in the mouse. Biol. Reprod., 2006, 74(5), 923-930.
[http://dx.doi.org/10.1095/biolreprod.105.048587] [PMID: 16436526]
[72]
Kimura, M.; Kim, E.; Kang, W.; Yamashita, M.; Saigo, M.; Yamazaki, T.; Nakanishi, T.; Kashiwabara, S.; Baba, T. Functional roles of mouse sperm hyaluronidases, HYAL5 and SPAM1, in fertilization. Biol. Reprod., 2009, 81(5), 939-947.
[http://dx.doi.org/10.1095/biolreprod.109.078816] [PMID: 19605784]
[73]
Belleannée, C. Extracellular microRNAs from the epididymis as potential mediators of cell-to-cell communication. Asian J. Androl., 2015, 17(5), 730-736.
[http://dx.doi.org/10.4103/1008-682X.155532] [PMID: 26178395]
[74]
Gillen, A.E.; Gosalia, N.; Leir, S.H.; Harris, A. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem. J., 2011, 438(1), 25-32.
[http://dx.doi.org/10.1042/BJ20110672] [PMID: 21689072]
[75]
Diao, R.; Fok, K.L.; Zhao, L.; Chen, H.; Tang, H.; Chen, J.; Zheng, A.; Zhang, X.; Gui, Y.; Chan, H.C.; Cai, Z. Decreased expression of cystic fibrosis transmembrane conductance regulator impairs sperm quality in aged men. Reproduction, 2013, 146(6), 637-645.
[http://dx.doi.org/10.1530/REP-13-0146] [PMID: 24077955]
[76]
Yeung, C.H.; Wang, K.; Cooper, T.G. Why are epididymal tumours so rare? Asian J. Androl., 2012, 14(3), 465-475.
[http://dx.doi.org/10.1038/aja.2012.20] [PMID: 22522502]
[77]
Jerczynski, O.; Lacroix-Pépin, N.; Boilard, E.; Calvo, E.; Bernet, A.; Fortier, M.A.; Björkgren, I.; Sipilä, P.; Belleannée, C. Role of dicer1-dependent factors in the paracrine regulation of epididymal gene expression. PLoS One, 2016, 11(10) e0163876
[http://dx.doi.org/10.1371/journal.pone.0163876] [PMID: 27695046]
[78]
Wang, Q.; Lee, I.; Ren, J.; Ajay, S.S.; Lee, Y.S.; Bao, X. Identification and functional characterization of tRNA-derived RNA fragments (tRFs) in respiratory syncytial virus infection. Mol. Ther., 2013, 21(2), 368-379.
[http://dx.doi.org/10.1038/mt.2012.237] [PMID: 23183536]
[79]
Lee, Y.S.; Shibata, Y.; Malhotra, A.; Dutta, A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev., 2009, 23(22), 2639-2649.
[http://dx.doi.org/10.1101/gad.1837609] [PMID: 19933153]
[80]
Peng, H.; Shi, J.; Zhang, Y.; Zhang, H.; Liao, S.; Li, W.; Lei, L.; Han, C.; Ning, L.; Cao, Y.; Zhou, Q.; Chen, Q.; Duan, E. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res., 2012, 22(11), 1609-1612.
[http://dx.doi.org/10.1038/cr.2012.141] [PMID: 23044802]
[81]
Sharma, U.; Conine, C.C.; Shea, J.M.; Boskovic, A.; Derr, A.G.; Bing, X.Y.; Belleannee, C.; Kucukural, A.; Serra, R.W.; Sun, F.; Song, L.; Carone, B.R.; Ricci, E.P.; Li, X.Z.; Fauquier, L.; Moore, M.J.; Sullivan, R.; Mello, C.C.; Garber, M.; Rando, O.J. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science, 2016, 351(6271), 391-396.
[http://dx.doi.org/10.1126/science.aad6780] [PMID: 26721685]
[82]
Ronquist, G.; Brody, I. The prostasome: its secretion and function in man. Biochim. Biophys. Acta, 1985, 822(2), 203-218.
[http://dx.doi.org/10.1016/0304-4157(85)90008-5] [PMID: 2992593]
[83]
Ronquist, G.; Brody, I.; Gottfries, A.; Stegmayr, B. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I. Andrologia, 1978, 10(4), 261-272.
[http://dx.doi.org/10.1111/j.1439-0272.1978.tb03030.x] [PMID: 152589]
[84]
Kravets, F.G.; Lee, J.; Singh, B.; Trocchia, A.; Pentyala, S.N.; Khan, S.A. Prostasomes: current concepts. Prostate, 2000, 43(3), 169-174.
[http://dx.doi.org/10.1002/(SICI)1097-0045(20000515)43:3<169:AID-PROS2>3.0.CO;2-D] [PMID: 10797491]
[85]
Saez, F.; Sullivan, R. Prostasomes, post-testicular sperm maturation and fertility. Front. Biosci., 2016, 21, 1464-1473.
[http://dx.doi.org/10.2741/4466] [PMID: 27100516]
[86]
Aalberts, M.; Stout, T.A.; Stoorvogel, W. Prostasomes: extracellular vesicles from the prostate. Reproduction, 2013, 147(1), R1-R14.
[http://dx.doi.org/10.1530/REP-13-0358] [PMID: 24149515]
[87]
Park, M.; Kang, K.W. Phosphatidylserine receptor-targeting therapies for the treatment of cancer. Arch. Pharm. Res., 2019, 42(7), 617-628.
[http://dx.doi.org/10.1007/s12272-019-01167-4] [PMID: 31172440]
[88]
Arienti, G.; Carlini, E.; Polci, A.; Cosmi, E.V.; Palmerini, C.A. Fatty acid pattern of human prostasome lipid. Arch. Biochem. Biophys., 1998, 358(2), 391-395.
[http://dx.doi.org/10.1006/abbi.1998.0876] [PMID: 9784255]
[89]
Carlini, E.; Palmerini, C.A.; Cosmi, E.V.; Arienti, G. Fusion of sperm with prostasomes: effects on membrane fluidity. Arch. Biochem. Biophys., 1997, 343(1), 6-12.
[http://dx.doi.org/10.1006/abbi.1997.9999] [PMID: 9210640]
[90]
Burden, H.P.; Holmes, C.H.; Persad, R.; Whittington, K. Prostasomes--their effects on human male reproduction and fertility. Hum. Reprod. Update, 2006, 12(3), 283-292.
[http://dx.doi.org/10.1093/humupd/dmi052] [PMID: 16373403]
[91]
Saez, F.; Frenette, G.; Sullivan, R. Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J. Androl., 2003, 24(2), 149-154.
[http://dx.doi.org/10.1002/j.1939-4640.2003.tb02653.x] [PMID: 12634297]
[92]
Salas-Huetos, A.; James, E.R.; Aston, K.I.; Carrell, D.T.; Jenkins, T.G.; Yeste, M. The role of miRNAs in male human reproduction: a systematic review. Andrology, 2020, 8(1), 7-26.
[PMID: 31578810]
[93]
Arienti, G.; Carlini, E.; Nicolucci, A.; Cosmi, E.V.; Santi, F.; Palmerini, C.A. The motility of human spermatozoa as influenced by prostasomes at various pH levels. Biol. Cell, 1999, 91(1), 51-54.
[http://dx.doi.org/10.1111/j.1768-322X.1999.tb01083.x] [PMID: 10321022]
[94]
Suarez, S.S.; Dai, X. Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome-reacted hamster sperm. Mol. Reprod. Dev., 1995, 42(3), 325-333.
[http://dx.doi.org/10.1002/mrd.1080420310] [PMID: 8579847]
[95]
Palmerini, C.A.; Carlini, E.; Nicolucci, A.; Arienti, G. Increase of human spermatozoa intracellular Ca2+ concentration after fusion with prostasomes. Cell Calcium, 1999, 25(4), 291-296.
[http://dx.doi.org/10.1054/ceca.1999.0031] [PMID: 10456226]
[96]
Park, K.H.; Kim, B.J.; Kang, J.; Nam, T.S.; Lim, J.M.; Kim, H.T.; Park, J.K.; Kim, Y.G.; Chae, S.W.; Kim, U.H. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci. Signal., 2011, 4(173), ra31.
[http://dx.doi.org/10.1126/scisignal.2001595] [PMID: 21586728]
[97]
Andrews, R.E.; Galileo, D.S.; Martin-DeLeon, P.A. Plasma membrane Ca2+-ATPase 4: interaction with constitutive nitric oxide synthases in human sperm and prostasomes which carry Ca2+/CaM-dependent serine kinase. Mol. Hum. Reprod., 2015, 21(11), 832-843.
[http://dx.doi.org/10.1093/molehr/gav049] [PMID: 26345709]
[98]
Knowles, R.G.; Moncada, S. Nitric oxide synthases in mammals. Biochem. J., 1994, 298(Pt 2), 249-258.
[http://dx.doi.org/10.1042/bj2980249] [PMID: 7510950]
[99]
Subirán, N.; Agirregoitia, E.; Valdivia, A.; Ochoa, C.; Casis, L.; Irazusta, J. Expression of enkephalin-degrading enzymes in human semen and implications for sperm motility. Fertil. Steril., 2008, 89(5)(Suppl.), 1571-1577.
[http://dx.doi.org/10.1016/j.fertnstert.2007.06.056] [PMID: 17953966]
[100]
Arienti, G.; Carlini, E.; Verdacchi, R.; Cosmi, E.V.; Palmerini, C.A. Prostasome to sperm transfer of CD13/aminopeptidase N (EC 3.4.11.2). Biochim. Biophys. Acta, 1997, 1336(3), 533-538.
[http://dx.doi.org/10.1016/S0304-4165(97)00071-8] [PMID: 9367181]
[101]
Flori, F.; Secciani, F.; Capone, A.; Paccagnini, E.; Caruso, S.; Ricci, M.G.; Focarelli, R. Menstrual cycle-related sialidase activity of the female cervical mucus is associated with exosome-like vesicles. Fertil. Steril., 2007, 88(4)(Suppl.), 1212-1219.
[http://dx.doi.org/10.1016/j.fertnstert.2007.01.209] [PMID: 17562335]
[102]
Li, H.; Huang, S.; Guo, C.; Guan, H.; Xiong, C. Cell-free seminal mRNA and microRNA exist in different forms. PLoS One, 2012, 7(4) e34566
[http://dx.doi.org/10.1371/journal.pone.0034566] [PMID: 22506029]
[103]
Ronquist, G.K.; Larsson, A.; Ronquist, G.; Isaksson, A.; Hreinsson, J.; Carlsson, L.; Stavreus-Evers, A. Prostasomal DNA characterization and transfer into human sperm. Mol. Reprod. Dev., 2011, 78(7), 467-476.
[http://dx.doi.org/10.1002/mrd.21327] [PMID: 21638509]
[104]
Ronquist, K.G.; Ronquist, G.; Carlsson, L.; Larsson, A. Human prostasomes contain chromosomal DNA. Prostate, 2009, 69(7), 737-743.
[http://dx.doi.org/10.1002/pros.20921] [PMID: 19143024]
[105]
Ronquist, G. Prostasomes: their characterisation: implications for human reproduction: prostasomes and human reproduction. Adv. Exp. Med. Biol., 2015, 868, 191-209.
[http://dx.doi.org/10.1007/978-3-319-18881-2_9] [PMID: 26178851]
[106]
Pons-Rejraji, H.; Artonne, C.; Sion, B.; Brugnon, F.; Canis, M.; Janny, L.; Grizard, G. Prostasomes: inhibitors of capacitation and modulators of cellular signalling in human sperm. Int. J. Androl., 2011, 34(6 Pt 1), 568-580.
[http://dx.doi.org/10.1111/j.1365-2605.2010.01116.x] [PMID: 21029115]
[107]
Cross, N.L.; Mahasreshti, P. Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch. Androl., 1997, 39(1), 39-44.
[http://dx.doi.org/10.3109/01485019708987900] [PMID: 9202832]
[108]
Bechoua, S.; Rieu, I.; Sion, B.; Grizard, G. Prostasomes as potential modulators of tyrosine phosphorylation in human spermatozoa. Syst Biol Reprod Med, 2011, 57(3), 139-148.
[http://dx.doi.org/10.3109/19396368.2010.549538] [PMID: 21332393]
[109]
Aalberts, M.; Sostaric, E.; Wubbolts, R.; Wauben, M.W.; Nolte-’t Hoen, E.N.; Gadella, B.M.; Stout, T.A.; Stoorvogel, W. Spermatozoa recruit prostasomes in response to capacitation induction. Biochim. Biophys. Acta, 2013, 1834(11), 2326-2335.
[http://dx.doi.org/10.1016/j.bbapap.2012.08.008] [PMID: 22940639]
[110]
Jin, M.; Fujiwara, E.; Kakiuchi, Y.; Okabe, M.; Satouh, Y.; Baba, S.A.; Chiba, K.; Hirohashi, N. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl. Acad. Sci. USA, 2011, 108(12), 4892-4896.
[http://dx.doi.org/10.1073/pnas.1018202108] [PMID: 21383182]
[111]
Palmerini, C.A.; Saccardi, C.; Carlini, E.; Fabiani, R.; Arienti, G. Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction. Fertil. Steril., 2003, 80(5), 1181-1184.
[http://dx.doi.org/10.1016/S0015-0282(03)02160-5] [PMID: 14607571]
[112]
Siciliano, L.; Marcianò, V.; Carpino, A. Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reprod. Biol. Endocrinol., 2008, 6, 5.
[http://dx.doi.org/10.1186/1477-7827-6-5] [PMID: 18234073]
[113]
Minelli, A.; Allegrucci, C.; Liguori, L.; Ronquist, G. Ecto-diadenosine polyphosphates hydrolase activity on human prostasomes. Prostate, 2002, 51(1), 1-9.
[http://dx.doi.org/10.1002/pros.10062] [PMID: 11920952]
[114]
Oliw, E.H.; Fabiani, R.; Johansson, L.; Ronquist, G. Arachidonic acid 15-lipoxygenase and traces of E prostaglandins in purified human prostasomes. J. Reprod. Fertil., 1993, 99(1), 195-199.
[http://dx.doi.org/10.1530/jrf.0.0990195] [PMID: 8283438]
[115]
Chutia, T.; Biswas, R.K.; Tamuli, M.K.; Deka, B.C.; Sinha, S.; Goswami, J.; Banik, S.; Kayastha, R.B. Effect of holding of semen and washing of seminal plasma on quality and fertility of Hampshire boar semen preserved at liquid state. Anim. Reprod. Sci., 2014, 145(3-4), 141-149.
[http://dx.doi.org/10.1016/j.anireprosci.2014.01.007] [PMID: 24559728]
[116]
Guo, H.; Chang, Z.; Zhang, Z.; Zhao, Y.; Jiang, X.; Yu, H.; Zhang, Y.; Zhao, R.; He, B. Extracellular ATPs produced in seminal plasma exosomes regulate boar sperm motility and mitochondrial metabolism. Theriogenology, 2019, 139, 113-120.
[http://dx.doi.org/10.1016/j.theriogenology.2019.08.003] [PMID: 31401476]

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