Extracellular vesicles: Roles in gamete maturation, fertilization and embryo implantation

Human Reproduction Update

Volumn 22, Issue 2, 2016, Pages 182-193

  Machtinger, Ronit ^a   Laurent, Louise C ^b   Baccarelli, Andrea A ^c  

^a SHEBA MEDICAL CENTER   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Embryo; Exosomes; Extracellular vesicles; Fertilization; Implantation; Oocyte; Ovarian follicle; Sperm

Indexed keywords

MICRORNA;

ACROSOME; ENDOMETRIUM; EXOSOME; FERTILIZATION; GAMETOGENESIS; HUMAN; NIDATION; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE; PARACRINE SIGNALING; POLYSPERMY; PRIORITY JOURNAL; REVIEW; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION; ANIMAL; CELL COMMUNICATION; CYTOLOGY; FEMALE; GENETICS; MALE; OOCYTE; OOCYTE DEVELOPMENT; PHYSIOLOGY; PREGNANCY; SPERM; SPERMATOGENESIS;

ANIMALS; CELL COMMUNICATION; EMBRYO IMPLANTATION; EXTRACELLULAR VESICLES; FEMALE; FERTILIZATION; HUMANS; MALE; OOCYTES; OOGENESIS; PREGNANCY; SEMEN; SPERMATOGENESIS;

EID: 84959914452     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmv055     Document Type: Review

References (142)

1. Aalberts M, Sostaric E, Wubbolts R, Wauben MWM, Nolte THENM, Gadella BM, Stout TAE, Stoorvogel W. Spermatozoa recruit prostasomes in response to capacitation induction. Biochim Biophys Acta 2013;1834:2326-2335.
2. Adashi EY. Endocrinology of the ovary. Hum Reprod 1994;9:815-827.
3. Aitken RJ, Nixon B. Sperm capacitation: a distant landscape glimpsed but unexplored. Mol Hum Reprod 2013;19:785-793.
4. Al-Dossary AA, Strehler EE, Martin-DeLeon PA. Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One 2013;8:e80181.
5. Arienti G, Carlini E, Palmerini CA. Fusion of human sperm to prostasomes at acidic p H. J Membr Biol 1997;155:89-94.
6. Arienti G, Carlini E, De Cosmo AM, Di Profio P, Palmerini CA. Prostasome-like particles in stallion semen. Biol Reprod 1998a; 59:309-313.
7. Arienti G, Carlini E, Polci A, Cosmi EV, Palmerini CA. Fatty acid pattern of human prostasome lipid. Arch Biochem Biophys 1998b; 358:391-395.
8. Arienti G, Carlini E, Nicolucci A, Cosmi EV, Santi F, PalmeriniCA. Themotility of human spermatozoa as influenced by prostasomes at various pH levels. Biol Cell 1999; 91:51-54.
9. Arvidson G, Ronquist G, Wikander G, Ojteg AC. Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering. Biochim Biophys Acta 1989;984:167-173.
10. Austin CR. The capacitation of the mammalian sperm. Nature 1952;170:326.
11. Barkalina N, Charalambous C, Jones C, Coward K. Nanotechnology in reproductive medicine: emerging applications of nanomaterials. Nanomedicine 2014;10: 921-938.
12. Barkalina N, Jones C,Wood MJ, Coward K. Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: learning fromnature. Hum Reprod Update. 2015;21:627-639.
13. Barraud-Lange V, Naud-Barriant N, Bomsel M,Wolf JP, Ziyyat A. Transfer of oocyte membrane fragments to fertilizing spermatozoa. FASEB J 2007;21:3446-3449.
14. Barraud-Lange V, Boissonnas CC, Serres C, Auer J, Schmitt A, Lefevre B, Wolf JP, Ziyyat A. Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of Cd9-deleted oocytes. Reproduction 2012;144:53-66.
15. Belleannee C, Calvo E, Caballero J, Sullivan R. Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biol Reprod 2013; 89:30.
16. Berube B, Sullivan R. Inhibition of in vivo fertilization by active immunization of male hamsters against a 26-kDa sperm glycoprotein. Biol Reprod 1994;51:1255-1263.
17. Bianchi E, Wright GJ. Izumo meets Juno: preventing polyspermy in fertilization. Cell Cycle 2014;13:2019-2020.
18. Bianchi E, Doe B, Goulding D, Wright GJ. Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 2014b; 508:483-487.
19. Boyer A, Goff AK, Boerboom D. WNT signaling in ovarian follicle biology and tumorigenesis. Trends Endocrinol Metab: TEM 2010;21:25-32.
20. Brower PT, Schultz RM. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 1982;90:144-153.
21. Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 1990;43:543-547.
22. Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE. Extracellular vesicles in luminal fluid of the ovine uterus. PLoS One 2014;9: e90913.
23. Caballero J, Frenette G, Sullivan R. Post testicular sperm maturational changes in the bull: important role of the epididymosomes and prostasomes. Vet Med Int 2011; 757194:1-13.
24. Campos VF, de Leon PM, Komninou ER, Dellagostin OA, Deschamps JC, Seixas FK, Collares T. NanoSMGT: transgene transmission into bovine embryos using halloysite clay nanotubes or nanopolymer to improve transfection efficiency. Theriogenology 2011;76:1552-1560.
25. Carlini E, Palmerini CA, Cosmi EV, Arienti G. Fusion of sperm with prostasomes: effects on membrane fluidity. Arch Biochem Biophys 1997;343:6-12.
26. Carlsson L, Pahlson C, Bergquist M, Ronquist G, Stridsberg M. Antibacterial activity of human prostasomes. Prostate 2000;44:279-286.
27. Carlsson L, Nilsson O, Larsson A, Stridsberg M, Sahlen G, Ronquist G. Characteristics of human prostasomes isolated from three different sources. Prostate 2003; 54:322-330.
28. Caselles AB, Miro-Moran A, Morullo Rodriguez A, Gallardo Bolanos JM, Ortega-Ferrusola C, Salido GM, Pena FJ, Tapia JA, Aparicio IM. Identification of apoptotic bodies in equine semen. Reprod Domest Anim 2014;49:254-262.
29. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951;168:697-698.
30. Chen H, Griffiths G, Galileo DS, Martin-DeLeon PA. Epididymal SPAM1 is a marker for sperm maturation in the mouse. Biol Reprod 2006;74:923-930.
31. Chesnel F, Wigglesworth K, Eppig JJ. Acquisition of meiotic competence by denuded mouse oocytes: participation of somatic-cell product(s) and cAMP. Dev Biol 1994; 161:285-295.
32. Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends in Cell Biology 2015;25:364-372.
33. Conti M, Hsieh M, Zamah AM, Oh JS. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol 2012;356:65-73.
34. Cooper TG. Epididymis and sperm function. Andrologia 1996;28:57-59.
35. Crescitelli R, Lasser C, Szabo TG, Kittel A, Eldh M, Dianzani I, Buzas EI, Lotvall J. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2013;2:20677.
36. Cuman C, Menkhorst E, Winship A, Van Sinderen M, Osianlis T, Rombauts LJ, Dimitriadis E. Fetal-maternal communication: the role of Notch signalling in embryo implantation. Reproduction 2014;147:R75-R86.
37. Dacheux JL, Belleannee C, Guyonnet B, Labas V, Teixeira-Gomes AP, Ecroyd H, Druart X, Gatti JL, Dacheux F. The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Systems Biol Reprod Medicine 2012;58:197-210.
38. da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM, Bouma GJ. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol Reprod 2012;86:71.
39. da Silveira JC, Carnevale EM, Winger QA, Bouma GJ. Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare. Reprod Biol Endocrinol 2014;12:44.
40. Denzer K, Kleijmeer MJ, Heijnen HF, StoorvogelW, Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000; 113:3365-3374.
41. Diez-Fraile A, Lammens T, Tilleman K, Witkowski W, Verhasselt B, De Sutter P, Benoit Y, Espeel M, D'Herde K. Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization. Hum Fertil 2014;17:90-98.
42. Dissen GA, Garcia-Rudaz C, Ojeda SR. Role of neurotrophic factors in early ovarian development. Semin Reprod Med 2009;27:24-31.
43. EL Andaloussi S, Mager I, Breakefield XO,Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013;12:347-357.
44. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001;122:829-838.
45. Eppig JJ, Chesnel F, Hirao Y, O'Brien MJ, Pendola FL, Watanabe S, Wigglesworth K. Oocyte control of granulosa cell development: how and why. Hum Reprod 1997; 12:127-132.
46. Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci USA 2002;99: 2890-2894.
47. Fabiani R, Ronquist G. Association of some hydrolytic enzymes with the prostasome membrane and their differential responses to detergent and PIPLC treatment. Prostate 1995;27:95-101.
48. Ferry L, Mermillod P, Massip A, Dessy F. Bovine embryos cultured in serum-poor oviduct-conditioned medium need cooperation to reach the blastocyst stage. Theriogenology 1994;42:445-453.
49. Fornes MW, Barbieri A, Cavicchia JC. Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis. Andrologia 1995; 27:1-5.
50. Fortune JE. Ovarian follicular growth and development in mammals. Biol Reprod 1994; 50:225-232.
51. Frenette G, Sullivan R. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 2001; 59:115-121.
52. Frenette G, Lessard C, Sullivan R. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 2002;67:308-313.
53. Frenette G, Lessard C, Madore E, Fortier MA, Sullivan R. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis. Biol Reprod 2003;69: 1586-1592.
54. Frenette G, Lessard C, Sullivan R. Polyol pathway along the bovine epididymis. Mol Reprod Dev 2004;69:448-456.
55. Frenette G, Thabet M, Sullivan R. Polyol pathway in human epididymis and semen. J Androl 2006a; 27:233-239.
56. Frenette G, Girouard J, Sullivan R. Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis. Biol Reprod 2006b; 75:885-890.
57. Frenette G, Girouard J, D'Amours O, Allard N, Tessier L, Sullivan R. Characterization of two distinct populations of epididymosomes collected in the intraluminal compartment of the bovine cauda epididymis. Biol Reprod 2010;83:473-480.
58. Gatti JL, Metayer S, Belghazi M, Dacheux F, Dacheux JL. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod 2005;72:1452-1465.
59. 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:e475-e486.
60. Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2013;2. doi: 10.3402/jev.v2i0.20389.
61. Griffiths GS, Galileo DS, Reese K, Martin-Deleon PA. Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Development 2008;75:1627-1636.
62. Gupta S, Primakoff P, Myles DG. Can the presence of wild-type oocytes during insemination rescue the fusion defect of CD9 null oocytes? Mol Reprod Dev 2009; 76:602.
63. Hamel M, Dufort I,Robert C, Gravel C, LeveilleMC,Leader A, SirardMA. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod 2008;23:1118-1127.
64. Hoelker M, Rings F, Lund Q, Ghanem N, PhatsaraC, Griese J, Schellander K, Tesfaye D. Effect of the microenvironment and embryo density on developmental characteristics and gene expression profile of bovine preimplantative embryos cultured in vitro. Reproduction 2009;137:415-425.
65. Huo LJ, Fan HY, Zhong ZS, Chen DY, Schatten H, Sun QY. Ubiquitin-proteasome pathway modulates mouse oocyte meiotic maturation and fertilization via regulation of MAPK cascade and cyclin B1 degradation. Mech Dev 2004;121: 1275-1287.
66. Ikawa M, Inoue N, Benham AM, Okabe M. Fertilization: a sperm's journey to and interaction with the oocyte. J Clin Invest 2010;120:984-994.
67. Inoue N, Ikawa M, Isotani A, Okabe M. The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 2005;434:234-238.
68. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N. Most fertilizing mouse spermatozoa begin their acrosomereaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 2011; 108:4892-4896.
69. Jones R. Sperm survival versus degradation in the Mammalian epididymis: a hypothesis. Biol Reprod 2004;71:1405-1411.
70. Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J,Weitz J, Chin L, Futreal A et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem 2014;289:3869-3875.
71. Kaji K,OdaS, Shikano T, OhnukiT, UematsuY, Sakagami J, Tada N, Miyazaki S, Kudo A. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 2000;24:279-282.
72. Katz-Jaffe MG, Schoolcraft WB, Gardner DK. Analysis of protein expression (secretome) by human and mouse preimplantation embryos. Fertil Steril 2006; 86:678-685.
73. Kim TS, Lee SH, Gang GT, Lee YS, Kim SU, Koo DB, Shin MY, Park CK, Lee DS. Exogenous DNA uptake of boar spermatozoa by a magnetic nanoparticle vector system. Reprod Domest Anim 2010;45:e201-e206.
74. Kim JH, Lee J, Park J, Gho YS. Gram-negative and Gram-positive bacterial extracellular vesicles. Seminars in Cell & Developmental Biology 2015;40:97-104.
75. 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;81:939-947.
76. Kirchhoff C, Pera I, Derr P, Yeung CH, Cooper T. The molecular biology of the sperm surface. Post-testicular membrane remodelling. Adv Exp Med Biol 1997; 424:221-232.
77. Knight PG, Glister C. Local roles of TGF-beta superfamily members in the control of ovarian follicle development. Anim Reprod Sci 2003;78:165-183.
78. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006; 132:191-206.
79. Kravets FG, Lee J, Singh B, Trocchia A, Pentyala SN, Khan SA. Prostasomes: Current concepts. Prostate 2000;43:169-174.
80. Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F, Pageaux JF, Kobayashi T, Salles JP, Perret B, Bonnerot C et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 2004;380:161-171.
81. Lei L, Jin S, Gonzalez G, Behringer RR,Woodruff TK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cell Endocrinol 2010;315:63-73.
82. Li J, Liu K, Liu Y, Xu Y, Zhang F, Yang H, Liu J, Pan T, Chen J, Wu M et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat Immunol 2013;14:793-803.
83. Lötvall J, Hill AF, Hochberg F, Buzás EI, Di Vizio D, Gardiner C, Gho YS, Kurochkin IV, Mathivanan S, Quesenberry P et al. 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; 22:26913.
84. Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, Takizawa T, Shigihara T, Goto T, Izumi A et al. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod 2009;81:717-729.
85. Madison MN, Roller RJ, Okeoma CM. Human semen contains exosomes with potent anti-HIV-1 activity. Retrovirology 2014;11:102.
86. Mantel PY, Marti M. The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cell Microbiology 2014;16:344-354.
87. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 2002;296:2178-2180.
88. Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X, Miyamoto K, Akutsu H, Kondo T, Takahashi Y et al. The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci USA 2008; 105:12921-12926.
89. Murchison EP, Stein P, Xuan Z, Pan H, ZhangMQ,Schultz RM, Hannon GJ. Critical roles for Dicer in the female germline. Genes Dev 2007;21:682-693.
90. Nagaraja AK, Andreu-Vieyra C, Franco HL, Ma L, Chen R, Han DY, Zhu H, Agno JE, Gunaratne PH, DeMayo FJ et al. Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol Endocrinol 2008;22:2336-2352.
91. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA. Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One 2013; 8:e58502.
92. Ohnami N, Nakamura A, Miyado M, Sato M, Kawano N, Yoshida K, Harada Y, Takezawa Y, Kanai S, Ono C et al. CD81 and CD9 work independently as extracellular components upon fusionof spermandoocyte. BiolOpen2012;1:640-647.
93. Oliveira DL, Nakayasu ES, Joffe LS, Guimaraes AJ, Sobreira TJ, Nosanchuk JD, Cordero RJ, Frases S, Casadevall A, Almeida IC et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One 2010;5:e11113.
94. 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;34:568-580.
95. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-383.
96. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006;20:847-856.
97. Record M, Subra C, Silvente-Poirot S, Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors. Biochem Pharmacol 2011;81:1171-1182.
98. Regente M, Corti-Monzon G, Maldonado AM, Pinedo M, Jorrin J, de la Canal L. Vesicular fractions of sunflower apoplastic fluids are associated with potential exosome marker proteins. FEBS Letters 2009;583:3363-3366.
99. Rejraji H, Vernet P, Drevet JR. GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. MolReprod Dev 2002;63:96-103.
100. Renneberg H, Konrad L, Dammshauser I, Seitz J, Aumuller G. Immunohistochemistry of prostasomes from human semen. Prostate 1997;30:98-106.
101. Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol 2009;7:40.
102. Rodgaard T, Heegaard PM, Callesen H. Non-invasive assessment of in-vitro embryo quality to improve transfer success. Reprod Biomed Online 2015;31:585-592.
103. RonquistG, Brody I. The prostasome: its secretion and function in man. Biochim Biophys Acta 1985;822:203-218.
104. RonquistG, Brody I, Gottfries A, Stegmayr B. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I. Andrologia 1978a; 10:261-272.
105. RonquistG, Brody I, Gottfries A, Stegmayr B. An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part II. Andrologia 1978b; 10:427-433.
106. Ronquist G, Carlsson L, Larsson A. Human prostasomes contain chromosomal DNA. Prostate 2009;69:737-743.
107. RonquistGK, Larsson A, Stavreus-Evers A, Ronquist G. Prostasomes are heterogeneous regarding size and appearance but affiliated to one DNA-containing exosome family. Prostate 2012;72:1736-1745.
108. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, Saffitz JE, Morgan BP. Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med 1993; 177:1409-1420.
109. Rosenbluth EM, Shelton DN,Wells LM, Sparks AET, Van Voorhis BJ. Human embryos secrete microRNAs into culture media-a potential biomarker for implantation. Fertil Steril 2014;101:1493-1500.
110. Runge KE, Evans JE,HeZY, Gupta S, McDonald KL, Stahlberg H, Primakoff P, MylesDG. Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 2007;304:317-325.
111. Saadeldin IM, Kim SJ, Choi YB, Lee BC. Improvement of cloned embryos development by co-culturing with parthenotes: a possible role of exosomes/microvesicles for embryos paracrine communication. Cell Reprogram 2014;16:223-234.
112. Saadeldin IM, Oh HJ, Lee BC. Embryonic-maternal cross-talk via exosomes: potential implications. Stem Cells Cloning Adv Appl 2015;8:103-107.
113. Saez F, Motta C, Boucher D, Grizard G. Antioxidant capacity of prostasomes in human semen. Mol Hum Rep 1998;4:667-672.
114. Saez F, Motta C, Boucher D, Grizard G. Prostasomes inhibit the NADPH oxidase activity of human neutrophils. Mol Hum Reprod 2000;6:883-891.
115. Saez F, Frenette G, Sullivan R. Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J Androl 2003;24:149-154.
116. Santonocito M, Vento M, Guglielmino MR, Battaglia R, Wahlgren J, Ragusa M, Barbagallo D, Borzi P, Rizzari S, Maugeri M et al. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil Steril 2014;102:1751-1761:e1751.
117. Senbon S, HiraoY, Miyano T. Interactions between the oocyte and surrounding somatic cells in follicular development: lessons from in vitro culture. J Reprod Dev 2003; 49:259-269.
118. Siciliano L, Marciano V, Carpino A. Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reprod Biol Endocrinol 2008;6:5.
119. Simpson RJ, Lim JW, Moritz RL, Mathivanan S. Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 2009;6:267-283.
120. Sohel MM, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C, Rings F, Uddin MJ, Spencer TE, Schellander K et al. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One 2013;8:e78505.
121. Subra C, Laulagnier K, Perret B, Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 2007;89:205-212.
122. Sullivan R, Saez F. Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction 2013;146:R21-R35.
123. 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; 35:1-10.
124. Sullivan R, Frenette G, Girouard J. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007;9:483-491.
125. Suzumori N, Burns KH, YanW, Matzuk MM. RFPL4 interacts with oocyte proteins of the ubiquitin-proteasome degradation pathway. Proc Natl Acad Sci USA 2003; 100:550-555.
126. Tanigawa M, Miyamoto K, Kobayashi S, Sato M, Akutsu H, Okabe M, Mekada E, Sakakibara K, Miyado M, Umezawa A et al. Possible involvement of CD81 in acrosome reaction of sperm in mice. Mol Reprod Dev 2008;75:150-155.
127. Tannetta D, Dragovic R, Alyahyaei Z, Southcombe J. Extracellular vesicles and reproduction-promotion of successful pregnancy. Cell Mol Immunol 2014; 11:548-563.
128. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009;9:581-593.
129. 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;23:1698-1707.
130. Traver S, Assou S, Scalici E, Haouzi D, Al-Edani T, Belloc S, Hamamah S. Cell-free nucleic acids as non-invasive biomarkers of gynecological cancers, ovarian, endometrial and obstetric disorders and fetal aneuploidy. Hum Reprod Update 2014;20:905-923.
131. Utleg AG, Yi EC, Xie T, Shannon P, White JT, Goodlett DR, Hood L, Lin B. Proteomic analysis of human prostasomes. Prostate 2003;56:150-161.
132. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659.
133. van der Grein SG, Nolte-'t Hoen EN. "Small Talk" in the innate immune system via RNA-containing extracellular vesicles. Front Immunol 2014;5:542.
134. Varela M, Spencer TE, Palmarini M, Arnaud F. Friendly viruses: the special relationship between endogenous retroviruses and their host. Ann N Y Acad Sci 2009; 1178:157-172.
135. Vernet P, Aitken RJ, Drevet JR. Antioxidant strategies in the epididymis. Mol Cell Endocrinol 2004;216:31-39.
136. Vojtech L,WooS, Hughes S, Levy C, Ballweber L, SauteraudRP, Strobl J,Westerberg K, Gottardo R, TewariMet al. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucl Acids Res 2014; 42:7290-7304.
137. Wright CF, Burton H. The use of cell-free fetal nucleic acids in maternal blood for non-invasive prenatal diagnosis. Hum Reprod Update 2009;15:139-151.
138. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 2003;278:10963-10972.
139. Xu YW,Wang B, Ding CH, Li T, Gu F, Zhou C. Differentially expressed micoRNAs in human oocytes. J Assist Reprod Genet 2011;28:559-566.
140. Yanagimachi R, Kamiguchi Y, Mikamo K, Suzuki F, Yanagimachi H. Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat 1985;172: 317-330.
141. Zhang H, Martin-DeLeon PA. Mouse Spam1 (PH-20) is a multifunctional protein: evidence for its expression in the female reproductive tract. Biol Reprod 2003; 69:446-454.
142. Zhang M, Ouyang H, Xia G. The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol Hum Reprod 2009;15:399-409.