Extracellular vesicle cargo of the male reproductive tract and the paternal preconception environment

References

• Aalberts M, Sostaric E, Wubbolts R, Wauben MWM, Nolte-’T Hoen ENM, Gadella BM, Stout TAE, Stoorvogel W. 2013. Spermatozoa recruit prostasomes in response to capacitation induction. 1834(11):2326–2335. doi:10.1016/j.bbapap.2012.08.008.
   Google Scholar
• Aalberts M, van Dissel-emiliani FM, van Adrichem NP, van Wijnen M, Wauben MH, Stout TA, Stoorvogel W. 2012. Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod. 86(3):82. doi:10.1095/biolreprod.111.095760.
   PubMed Web of Science ®Google Scholar
• Abu-Halima M, Ludwig N, Hart M, Leidinger P, Backes C, Keller A, Hammadeh M, Meese E. 2016. Altered micro-ribonucleic acid expression profiles of extracellular microvesicles in the seminal plasma of patients with oligoasthenozoospermia. Fertil Steril. 106(5):1061–1069.e1063. doi:10.1016/j.fertnstert.2016.06.030.
   PubMed Web of Science ®Google Scholar
• Akers JC, Gonda D, Kim R, Carter BS, Chen CC. 2013. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 113(1):1–11. doi:10.1007/s11060-013-1084-8.
   PubMed Web of Science ®Google Scholar
• Babst M. 2011. MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol. 23(4):452–457. doi:10.1016/j.ceb.2011.04.008.
   PubMed Web of Science ®Google Scholar
• Bai R, Latifi Z, Kusama K, Nakamura K, Shimada M, Imakawa K. 2018. Induction of immune-related gene expression by seminal exosomes in the porcine endometrium. Biochem Biophys Res Commun. 495(1):1094–1101. doi:10.1016/j.bbrc.2017.11.100.
   PubMed Web of Science ®Google Scholar
• Barceló M, Mata A, Bassas L, Larriba S, Nicolau M. 2018. Exosomal microRNAs in seminal plasma are markers of the origin of azoospermia and can predict the presence of sperm in testicular tissue. Human Reprod (Oxford, England). 33. doi:10.1093/humrep/dey072.
   Google Scholar
• Bromfield JJ. 2014. Seminal fluid and reproduction: much more than previously thought. 31(6):627–636.
   Google Scholar
• Buck Louis GM, Sundaram R, Schisterman EF, Sweeney A, Lynch CD, Kim S, Maisog JM, Gore-Langton R, Eisenberg ML, Chen Z. 2014. Semen quality and time to pregnancy: the longitudinal investigation of fertility and the environment study. Fertil Steril. 101(2):453–462. doi:10.1016/j.fertnstert.2013.10.022.
   PubMed Web of Science ®Google Scholar
• Caballero JN, Frenette G, Belleannée C, Sullivan R. 2013. CD9-positive microvesicles mediate the transfer of molecules to bovine spermatozoa during epididymal maturation. PLOS ONE 8(6):e65364.
   Google Scholar
• Camargo M, Intasqui P, Bertolla RP. 2018. Understanding the seminal plasma proteome and its role in male fertility. Basic Clin Androl. 28:6. doi:10.1186/s12610-018-0071-5.
   PubMed Web of Science ®Google Scholar
• Chargaff E, West R. 1946. The biological significance of the thromboplastic protein of blood. J Biol Chem. 166(1):189–197.
   PubMed Web of Science ®Google Scholar
• Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, Feng G-H, Peng H, Zhang X, Zhang Y, et al. 2016. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 351(6271):397–400. doi:10.1126/science.aad7977.
   PubMed Web of Science ®Google Scholar
• Conine CC, Sun F, Song L, Rivera-Pérez JA, Rando OJ. 2018. Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. Dev Cell. 46(4):470–480.e473. doi:10.1016/j.devcel.2018.06.024.
   PubMed Web of Science ®Google Scholar
• D’Amours O, Frenette G, Bordeleau LJ, Allard N, Leclerc P, Blondin P, Sullivan R. 2012. Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biol Reprod. 87(4): 94-94. doi:10.1095/biolreprod.112.100990.
   Google Scholar
• Drabovich AP, Saraon P, Jarvi K, Diamandis EP. 2014. Seminal plasma as a diagnostic fluid for male reproductive system disorders. Nat Rev Urol. 11(5):278–288. doi:10.1038/nrurol.2014.74.
   PubMed Web of Science ®Google Scholar
• Du J, Shen J, Wang Y, Pan C, Pang W, Diao H, Dong W. 2016. Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget. 7(37):58832–58847. doi:10.18632/oncotarget.11315.
   PubMedGoogle Scholar
• Fabiani R, Johnsson L, Lundkvist Ö, Ronquist G. 1994. Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim-up medium. Hum Reprod. 9(8):1485–1489. doi:10.1093/oxfordjournals.humrep.a138735.
   PubMed Web of Science ®Google Scholar
• Frenette G, Lessard C, Sullivan R. 2002. Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. 67(1):308–313. doi:10.1095/biolreprod67.1.308.
   Google Scholar
• Friedler S, Ben-Ami I, Gidoni Y, Strassburger D, Kasterstein E, Maslansky B, Komarovsy D, Bern O, Ron-El R, Raziel A. 2013. Effect of seminal plasma application to the vaginal vault in in vitro fertilization or intracytoplasmic sperm injection treatment cycles-a double-blind, placebo-controlled, randomized study. J Assist Reprod Genet. 30(7):907–911. doi:10.1007/s10815-013-0033-y.
   PubMed Web of Science ®Google Scholar
• Hermo L, Oliveira RL, Smith CE, Au CE, Bergeron JJM. 2019. Dark side of the epididymis: tails of sperm maturation. Andrology. doi:10.1111/andr.12641
   PubMed Web of Science ®Google Scholar
• Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. 2005. Membrane microparticles: two sides of the coin. Physiology (Bethesda). 20:22–27. doi:10.1152/physiol.00029.2004.
   PubMed Web of Science ®Google Scholar
• Jansen FH, Krijgsveld J, van Rijswijk A, van den Bemd GJ, van den Berg MS, van Weerden WM, Willemsen R, Dekker LJ, Luider TM, Jenster G. 2009. Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol Cell Proteomics. 8(6):1192–1205. doi:10.1074/mcp.M800443-MCP200.
   PubMed Web of Science ®Google Scholar
• Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. 1987. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 262(19):9412–9420.
   PubMed Web of Science ®Google Scholar
• Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C. 2012. European association of urology guidelines on male fertility: the 2012 update. Eur Urol. 62(2):324–332. doi:10.1016/j.eururo.2012.04.048.
   PubMed Web of Science ®Google Scholar
• Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. 2010. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 285(23):17442–17452. doi:10.1074/jbc.M110.107821.
   PubMed Web of Science ®Google Scholar
• Levine H, Jorgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, Pinotti R, Swan SH. 2017. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 23(6):646–659.
   PubMed Web of Science ®Google Scholar
• Lu J, Li J, Liu S, Wang T, Ianni A, Bober E, Braun T, Xiang R, Yue S. 2017. Exosomal tetraspanins mediate cancer metastasis by altering host microenvironment. Oncotarget. 8(37):62803–62815. doi:10.18632/oncotarget.19119.
   PubMedGoogle Scholar
• Murdica V, Giacomini E, Alteri A, Bartolacci A, Cermisoni GC, Zarovni N, Papaleo E, Montorsi F, Salonia A, Viganò P, et al. 2019. Seminal plasma of men with severe asthenozoospermia contain exosomes that affect spermatozoa motility and capacitation. Fertil Steril. 111(5):897–908.e892. doi:10.1016/j.fertnstert.2019.01.030.
   PubMed Web of Science ®Google Scholar
• Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q. 2012. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci. 109(11):4146–4151. doi:10.1073/pnas.1200448109.
   PubMed Web of Science ®Google Scholar
• Nixon B, De Iuliis GN, Hart HM, Zhou W, Mathe A, Bernstein IR, Anderson AL, Stanger SJ, Skerrett-Byrne DA, Jamaluddin MFB, et al. 2019. Proteomic profiling of mouse epididymosomes reveals their contributions to post-testicular sperm maturation. Mol Cell Proteomics. 18(Supplement 1):S91–S108. doi:10.1074/mcp.RA118.000946.
   PubMedGoogle Scholar
• Nixon B, Stanger SJ, Mihalas BP, Reilly JN, Anderson AL, Tyagi S, Holt JE, McLaughlin EA. 2015. The MicroRNA signature of mouse spermatozoa is substantially modified during epididymal maturation1. Biol Reprod. 93(4): 91-91. doi:10.1095/biolreprod.115.132209.
   PubMed Web of Science ®Google Scholar
• Palmerini CA, Saccardi C, Carlini E, Fabiani R, Arienti G. 2003. Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction. Fertil Steril. 80(5):1181–1184. doi:10.1016/s0015-0282(03)02160-5.
   Google Scholar
• Panner Selvam MK, Agarwal A, Sharma R, Samanta L, Gupta S, Dias TR, Martins AD. 2019. Protein fingerprinting of seminal plasma reveals dysregulation of exosome-associated proteins in infertile men with unilateral varicocele. World J Men’s Health. doi:10.5534/wjmh.180108.
   Google Scholar
• Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT, Park JK, Kim YG, Chae SW, Kim UH. 2011. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 4(173):ra31. doi:10.1126/scisignal.2001595.
   PubMed Web of Science ®Google Scholar
• Pegtel DM, Gould SJ. 2019. Exosomes. Annu Rev Biochem. 88(1):487–514. doi:10.1146/annurev-biochem-013118-111902.
   PubMed Web of Science ®Google Scholar
• Piehl LL, Fischman ML, Hellman U, Cisale H, Miranda PV. 2013. Boar seminal plasma exosomes: effect on sperm function and protein identification by sequencing. Theriogenology. 79(7):1071–1082. doi:10.1016/j.theriogenology.2013.01.028.
   PubMed Web of Science ®Google Scholar
• Pols MS, Klumperman J. 2009. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 315(9):1584–1592. doi:10.1016/j.yexcr.2008.09.020.
   PubMed Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. 2013. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 200(4):373–383. doi:10.1083/jcb.201211138.
   PubMed Web of Science ®Google Scholar
• Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. 2006. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 20(5):847–856. doi:10.1038/sj.leu.2404132.
   PubMed Web of Science ®Google Scholar
• Reilly J, McLaughlin E, Stanger S, Anderson A, Hutcheon K, Church K, Mihalas B, Tyagi S, Holt J, Eamens A, et al. 2016. Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Sci Rep. 6. doi:10.1038/srep31794.
   Web of Science ®Google Scholar
• Ronquist G. (2015) Prostasomes: Their Characterisation: Implications for Human Reproduction. In: Bronson R. (eds) The Male Role in Pregnancy Loss and Embryo Implantation Failure. Advances in Experimental Medicine and Biology, vol 868. Springer, Cham. https://doi.org/10.1007/978-3-319-18881-2_9
   Google Scholar
• Ronquist G. 2015. Prostasomes: their characterisation: implications for human reproduction. Springer International Publishing; p. 191–209.
   Google Scholar
• Ronquist G, Brody I. 1984. The prostasome: its secretion and function in man. Biochimica et Biophysica Acta (BBA). 822(2):203–218. doi:10.1016/0304-4157(85)90008-5.
   Google Scholar
• Ronquist G, Brody I, Gottfries A, Stegmayr B. 1978. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part II. Andrologia. 10(6):427–433. doi:10.1111/j.1439-0272.1978.tb03064.x.
   PubMed Web of Science ®Google Scholar
• Samanta L, Parida R, Dias TR, Agarwal A. 2018. The enigmatic seminal plasma: a proteomics insight from ejaculation to fertilization. Reprod Biol Endocrinol. 16(1):41. doi:10.1186/s12958-018-0358-6.
   PubMedGoogle Scholar
• Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY, Belleannee C, Kucukural A, Serra RW, Sun F, et al. 2016. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science. 351(6271):391–396. doi:10.1126/science.aad6780.
   PubMed Web of Science ®Google Scholar
• Skog J, Würdinger T, Van Rijn S, Meijer DH, Gainche L, Curry WT, Carter BS, Krichevsky AM, Breakefield XO. 2008. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 10(12):1470–1476. doi:10.1038/ncb1800.
   PubMed Web of Science ®Google Scholar
• Sullivan R. 2015. Epididymosomes: a heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J Androl. 17(5):726–729.
   PubMed Web of Science ®Google Scholar
• Sullivan R, Saez F. 2013. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction. 146(1):R21–35. doi:10.1530/REP-13-0058.
   PubMed Web of Science ®Google Scholar
• Thery C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 9(8):581–593. doi:10.1038/nri2567.
   PubMed Web of Science ®Google Scholar
• Trams EG, Lauter CJ, Salem N Jr., Heine U. 1981. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim Biophys Acta. 645(1):63–70. doi:10.1016/0005-2736(81)90512-5.
   PubMed Web of Science ®Google Scholar
• Tremellen KP, Valbuena D, Landeras J, Ballesteros A, Martinez J, Mendoza S, Norman RJ, Robertson SA, Simon C. 2000. The effect of intercourse on pregnancy rates during assisted human reproduction. Hum Reprod. 15(12):2653–2658. doi:10.1093/humrep/15.12.2653.
   PubMed Web of Science ®Google Scholar
• Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 9(6):654–659. doi:10.1038/ncb1596.
   PubMed Web of Science ®Google Scholar
• Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, Strobl J, Westerberg K, Gottardo R, Tewari M, et al. 2014. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 42(11):7290–7304. doi:10.1093/nar/gku347.
   PubMed Web of Science ®Google Scholar
• Wu H, Hauser R, Krawetz SA, Pilsner JR. 2015. Environmental susceptibility of the sperm epigenome during windows of male germ cell development. Curr Environ Health Rep. doi:10.1007/s40572-015-0067-7
   PubMedGoogle Scholar
• Yanagimachi R, Kamiguchi Y, Mikamo K, Suzuki F, Yanagimachi H. 1985. Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat. 172(4):317–330. doi:10.1002/aja.1001720406.
   PubMedGoogle Scholar
• Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, et al. 2015. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4:27066. doi:10.3402/jev.v4.27066.
   PubMed Web of Science ®Google Scholar
• Yang C, Guo WB, Zhang WS, Bian J, Yang JK, Zhou QZ, Chen MK, Peng W, Qi T, Wang CY, et al. 2017. Comprehensive proteomics analysis of exosomes derived from human seminal plasma. Andrology. 5(5):1007–1015. doi:10.1111/andr.12412.
   PubMed Web of Science ®Google Scholar
• Yuan A, Farber E, Rapoport A, Tejada D, Deniskin R, Akhmedov N, Farber D. 2009. Transfer of MicroRNAs by embryonic stem cell microvesicles. PloS One. 4:e4722. doi:10.1371/journal.pone.0004722.
   PubMed Web of Science ®Google Scholar