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Extracellular vesicles in mammalian reproduction: a review

Published online by Cambridge University Press:  02 June 2022

Erwin L. Muñoz Open the ORCID record for Erwin L. Muñoz [Opens in a new window] ,
Fernanda B. Fuentes Open the ORCID record for Fernanda B. Fuentes [Opens in a new window] ,
Ricardo N. Felmer Open the ORCID record for Ricardo N. Felmer [Opens in a new window] ,
Marc Yeste Open the ORCID record for Marc Yeste [Opens in a new window]  and
María E. Arias Open the ORCID record for María E. Arias [Opens in a new window]
Erwin L. Muñoz
Affiliation:
Laboratory of Reproduction, Centre of Excellence in Reproductive Biotechnology (CEBIOR), Universidad de La Frontera, Temuco, Chile Doctoral Program in Sciences, Major in Applied Cellular and Molecular Biology, Universidad de La Frontera, Temuco, Chile
Fernanda B. Fuentes
Affiliation:
Laboratory of Reproduction, Centre of Excellence in Reproductive Biotechnology (CEBIOR), Universidad de La Frontera, Temuco, Chile Doctoral Program in Sciences, Major in Applied Cellular and Molecular Biology, Universidad de La Frontera, Temuco, Chile
Ricardo N. Felmer
Affiliation:
Laboratory of Reproduction, Centre of Excellence in Reproductive Biotechnology (CEBIOR), Universidad de La Frontera, Temuco, Chile Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry Sciences, Universidad de La Frontera, Temuco, Chile
Marc Yeste
Affiliation:
Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, ES-17003 Girona, Spain
María E. Arias*
Affiliation:
Laboratory of Reproduction, Centre of Excellence in Reproductive Biotechnology (CEBIOR), Universidad de La Frontera, Temuco, Chile Department of Agricultural Production Faculty of Agriculture and Forestry, Universidad de La Frontera, Temuco, Chile
*
Author for correspondence: María Elena Arias Cea, Laboratory of Reproduction, Centre of Excellence in Reproductive Biotechnology, Department of Animal Production, Faculty of Agriculture and Forestry Sciences, Universidad de La Frontera, Montevideo 0870, P.O. Box 54-D, Temuco, Chile. Tel: +56 45 2596911. E-mail: mariaelena.arias@gmail.com
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Summary

Over the last decades, extracellular vesicles (EVs) have been found to be implicated in a complex universal mechanism of communication between different cell types. EVs are nanostructures of lipid nature that have an exosomal or ectosomal biogenesis, responsible for the intercellular transport of proteins, lipids, carbohydrates, nucleic acids, ions, among other molecules. The content of EVs can vary due to various factors such as hormonal stimuli, non-physiological conditions, metabolic state, etc. Once EVs reach their target cell, they can modulate processes such as gene expression, metabolism, response to external factors, and can even be associated with the delivery of molecules involved in epigenetic inheritance processes in germ cells. In mammalian reproduction, EVs have been shown to play an important role, either in vivo or in vitro, modulating a variety of processes in sperm, oocytes and embryos, and in their respective environments. Moreover, EVs represent a biodegradable, harmless and specific vehicle, which makes them attractive allies to consider when improving assisted reproductive technologies (ARTs). Therefore, the present review aims to describe the content of the main EVs involved in mammalian reproduction and how they can vary due to different factors, as well as to detail how EVs modulate, directly or indirectly, different molecular processes in gametes and embryos. In addition, we will highlight the mechanisms that remain to be elucidated. We will also propose new perspectives according to the characteristics of each particular EV to improve the different ARTs.

Keywords

EmbryosExtracellular VesiclemiRNAOocytesSperm
Type
Review Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 440 - 463
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abe, H., Sendai, Y., Satoh, T. and Hoshi, H. (1995). Bovine oviduct-specific glycoprotein: A potent factor for maintenance of viability and motility of bovine spermatozoa in vitro . Molecular Reproduction and Development, 42(2), 226–232. doi: 10.1002/mrd.1080420212 CrossRefGoogle ScholarPubMed
Alcântara-Neto, A. S., Fernandez-Rufete, M., Corbin, E., Tsikis, G., Uzbekov, R., Garanina, A. S., Coy, P., Almiñana, C. and Mermillod, P. (2020). Oviduct fluid extracellular vesicles regulate polyspermy during porcine in vitro fertilisation. Reproduction, Fertility and Development, 32(4), 409–418. doi: 10.1071/RD19058 CrossRefGoogle ScholarPubMed
Al-Dossary, A. A., Strehler, E. E. and Martin-DeLeon, P. A. (2013). Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: Association with oviductal exosomes and uptake in sperm. PLOS ONE, 8(11), e80181. doi: 10.1371/journal.pone.0080181 CrossRefGoogle ScholarPubMed
Al-Dossary, A. A., Bathala, P., Caplan, J. L. and Martin-DeLeon, P. A. (2015). Oviductosome-sperm membrane interaction in cargo delivery: Detection of fusion and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM). Journal of Biological Chemistry, 290(29), 17710–17723. doi: 10.1074/jbc.M114.633156 CrossRefGoogle Scholar
Almiñana, C., Corbin, E., Tsikis, G., Alcântara-Neto, A. S., Labas, V., Reynaud, K., Galio, L., Uzbekov, R., Garanina, A. S., Druart, X. and Mermillod, P. (2017). Oviduct extracellular vesicles protein content and their role during oviduct–embryo cross-talk. Reproduction, 154(3), 153–168. doi: 10.1530/REP-17-0054 CrossRefGoogle ScholarPubMed
Almiñana, C., Tsikis, G., Labas, V., Uzbekov, R., da Silveira, J. C., Bauersachs, S. and Mermillod, P. (2018). Deciphering the oviductal extracellular vesicles content across the estrous cycle: Implications for the gametes-oviduct interactions and the environment of the potential embryo. BMC Genomics, 19(1), 622. doi: 10.1186/s12864-018-4982-5 CrossRefGoogle ScholarPubMed
Álvarez, E. V., García, M. G., Corzo, P. R., Gutiérrez, E. H., de Bustamante, B. G. L. and Barcia, M. M. G. (2007). Clasificación y cultivo de los ovocitos. In Álvarez, E. V., Matorras, R. and Hernández, J. H. (Eds.), Estudio y Tratamiento de la Pareja Estéril (1st ed) (pp. 263–268). Adalia Farma.Google Scholar
Atif, S. M., Salam, N., Ahmad, N., Hasan, I. M., Jamal, H. S., Sudhanshu, A., Azevedo, V. and Owais, M. (2008). Sperm membrane lipid liposomes can evoke an effective immune response against encapsulated antigen in BALB/c mice. Vaccine, 26(46), 5874–5882. doi: 10.1016/j.vaccine.2008.08.013 CrossRefGoogle ScholarPubMed
Barkalina, N., Jones, C., Wood, M. J. and Coward, K. (2015). Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: Learning from nature. Human Reproduction Update, 21(5), 627–639. doi: 10.1093/humupd/dmv027 CrossRefGoogle ScholarPubMed
Batagov, A. O., Kuznetsov, V. A. and Kurochkin, I. V. (2011). Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics, 12, S18. doi: 10.1186/1471-2164-12-S3-S18 CrossRefGoogle ScholarPubMed
Bathala, P., Fereshteh, Z., Li, K., Al-Dossary, A. A., Galileo, D. S. and Martin-DeLeon, P. A. (2018). Oviductal extracellular vesicles (oviductosomes, OVS) are conserved in humans: Murine OVS play a pivotal role in sperm capacitation and fertility. Molecular Human Reproduction, 24(3), 143–157. doi: 10.1093/molehr/gay003 Google ScholarPubMed
Battaglia, R., Palini, S., Vento, M. E., La Ferlita, A., Lo Faro, M. J., Caroppo, E., Borzì, P., Falzone, L., Barbagallo, D., Ragusa, M., Scalia, M., D’Amato, G., Scollo, P., Musumeci, P., Purrello, M., Gravotta, E. and Di Pietro, C. (2019). Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid. Scientific Reports, 9(1), 84. doi: 10.1038/s41598-018-36452-7 CrossRefGoogle ScholarPubMed
Bazer, F. W., Ying, W., Wang, X., Dunlap, K. A., Zhou, B., Johnson, G. A. and Wu, G. (2015). The many faces of interferon tau. Amino Acids, 47(3), 449–460. doi: 10.1007/s00726-014-1905-x CrossRefGoogle ScholarPubMed
Beg, F., Wang, R., Saeed, Z., Devaraj, S., Kamalesh, M., Nakshatri, H. and Roudebush, R. L. (2017). Circulating free and exosomal microRNAs as biomarkers of systemic response to heart failure. Journal of the American College of Cardiology, 69(11), 689. doi: 10.1016/S0735-1097(17)34078-0 CrossRefGoogle Scholar
Bidarimath, M., Khalaj, K., Kridli, R. T., Kan, F. W., Koti, M. and Tayade, C. (2017). Extracellular vesicle mediated intercellular communication at the porcine maternal-fetal interface: A new paradigm for conceptus-endometrial cross-talk. Scientific Reports, 7, 40476. doi: 10.1038/srep40476 CrossRefGoogle ScholarPubMed
Blázquez, R., Sánchez-Margallo, F. M., Álvarez, V., Matilla, E., Hernández, N., Marinaro, F., Gómez-Serrano, M., Jorge, I., Casado, J. G. and Macías-García, B. (2018). Murine embryos exposed to human endometrial MSCs-derived extracellular vesicles exhibit higher VEGF/PDGF AA release, increased blastomere count and hatching rates. PLOS ONE, 13(4), e0196080. doi: 10.1371/journal.pone.0196080 CrossRefGoogle ScholarPubMed
Bongso, A., Ng, S. C. and Ratnam, S. (1990). Co-cultures: Their relevance to assisted reproduction. Human Reproduction, 5(8), 893–900. doi: 10.1093/oxfordjournals.humrep.a137216 CrossRefGoogle ScholarPubMed
Boué, F., Blais, J. and Sullivan, R. (1996). Surface localization of P34H, an epididymal protein, during maturation, capacitation and acrosome reaction of human spermatozoa. Biology of Reproduction, 54(5), 1009–1017. doi: 10.1095/biolreprod54.5.1009 CrossRefGoogle ScholarPubMed
Brasset, E., Taddei, A. R., Arnaud, F., Faye, B., Fausto, A. M., Mazzini, M., Giorgi, F. and Vaury, C. (2006). Viral particles of the endogenous retrovirus ZAM from Drosophila melanogaster use a pre-existing endosome/exosome pathway for transfer to the oocyte. Retrovirology, 3, 25. doi: 10.1186/1742-4690-3-25 CrossRefGoogle ScholarPubMed
Burg, M. B. (1995). Molecular basis of osmotic regulation. American Journal of Physiology, 268(6 Pt 2), F983–F996. doi: 10.1152/ajprenal.1995.268.6.F983 Google ScholarPubMed
Burns, G., Brooks, K., Wildung, M., Navakanitworakul, R., Christenson, L. K. and Spencer, T. E. (2014). Extracellular vesicles in luminal fluid of the ovine uterus. PLOS ONE, 9(3), e90913. doi: 10.1371/journal.pone.0090913 CrossRefGoogle ScholarPubMed
Burns, G. W., Brooks, K. E., O’Neil, E. V., Hagen, D. E., Behura, S. K. and Spencer, T. E. (2018). Progesterone effects on extracellular vesicles in the sheep uterus. Biology of Reproduction, 98(5), 612–622. doi: 10.1093/biolre/ioy011 CrossRefGoogle ScholarPubMed
Caballero, J., Frenette, G., D’Amours, O., Belleannée, C., Lacroix-Pepin, N., Robert, C. and Sullivan, R. (2012). Bovine sperm raft membrane associated glioma pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. Journal of Cellular Physiology, 227(12), 3876–3886. doi: 10.1002/jcp.24099 CrossRefGoogle Scholar
Caballero, J. N., Frenette, G., Belleannée, C. and Sullivan, R. (2013). CD9-positive microvesicles mediate the transfer of molecules to bovine spermatozoa during epididymal maturation. PLOS ONE, 8(6), e65364. doi: 10.1371/journal.pone.0065364 CrossRefGoogle ScholarPubMed
Canovas, S., Gutierrez-Adan, A. and Gadea, J. (2010). Effect of exogenous DNA on bovine sperm functionality using the sperm mediated gene transfer (SMGT) technique. Molecular Reproduction and Development, 77(8), 687–698. doi: 10.1002/mrd.21205 CrossRefGoogle ScholarPubMed
Cao, W., Aghajanian, H. K., Haig-Ladewig, L. A. and Gerton, G. L. (2009). Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase. Biology of Reproduction, 80(1), 124–133. doi: 10.1095/biolreprod.108.068882 CrossRefGoogle ScholarPubMed
Carlsson, L., Nilsson, O., Larsson, A., Stridsberg, M., Sahlén, G. and Ronquist, G. (2003). Characteristics of human prostasomes isolated from three different sources. Prostate, 54(4), 322–330. doi: 10.1002/pros.10189 CrossRefGoogle ScholarPubMed
Chávez, J. C., De Blas, G. A., De La Vega-Beltrán, J. L., Nishigaki, T., Chirinos, M., González-González, M. E., Larrea, F., Solís, A., Darszon, A. and Treviño, C. L. (2011). The opening of maitotoxin-sensitive calcium channels induces the acrosome reaction in human spermatozoa: Differences from the zona pellucida. Asian Journal of Andrology, 13(1), 159–165. doi: 10.1038/aja.2010.80 CrossRefGoogle ScholarPubMed
Chen, Y. G., Wang, Q., Lin, S. L., Chang, C. D., Chuang, J. and Ying, S. Y. (2006). Activin signaling and its role in regulation of cell proliferation, apoptosis and carcinogenesis. Experimental Biology and Medicine, 231(5), 534–544. doi: 10.1177/153537020623100507 CrossRefGoogle ScholarPubMed
Chivet, M., Javalet, C., Laulagnier, K., Blot, B., Hemming, F. J. and Sadoul, R. (2014). Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. Journal of Extracellular Vesicles, 3, 24722. doi: 10.3402/jev.v3.24722 CrossRefGoogle ScholarPubMed
Costa Verdera, H. C., Gitz-Francois, J. J., Schiffelers, R. M. and Vader, P. (2017). Cellular uptake of extracellular vesicles is mediated by clathrin-independent endocytosis and macropinocytosis. Journal of Controlled Release, 266, 100–108. doi: 10.1016/j.jconrel.2017.09.019 CrossRefGoogle ScholarPubMed
Crichton, E. G., Hinton, B. T., Pallone, T. L. and Hammerstedt, R. H. (1994). Hyperosmolality and sperm storage in hibernating bats: Prolongation of sperm life by dehydration. American Journal of Physiology, 267(5 Pt 2), R1363–R1370. doi: 10.1152/ajpregu.1994.267.5.R1363 Google ScholarPubMed
Cross, N. L. (2000). Sphingomyelin modulates capacitation of human sperm in vitro . Biology of Reproduction, 63(4), 1129–1134. doi: 10.1095/biolreprod63.4.1129 CrossRefGoogle ScholarPubMed
da Silveira, J. C., Veeramachaneni, D. N., Winger, Q. A., Carnevale, E. M. and Bouma, G. J. (2012). Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A possible new form of cell communication within the ovarian follicle. Biology of Reproduction, 86(3), 71–71. doi: 10.1095/biolreprod.111.093252 CrossRefGoogle ScholarPubMed
da Silveira, J. C., Carnevale, E. M., Winger, Q. A. and Bouma, G. J. (2014). Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare. Reproductive Biology and Endocrinology: RBandE, 12, 44. doi: 10.1186/1477-7827-12-44 CrossRefGoogle ScholarPubMed
da Silveira, J. C., Andrade, G. M., Del Collado, M., Sampaio, R. V., Sangalli, J. R., Silva, L. A., Pinaffi, F. V. L., Jardim, I. B., Cesar, M. C., Nogueira, M. F. G., Cesar, A. S. M., Coutinho, L. L., Pereira, R. W., Perecin, F. and Meirelles, F. V. (2017). Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development. PLOS ONE, 12(6), e0179451. doi: 10.1371/journal.pone.0179451 CrossRefGoogle ScholarPubMed
D’Amours, O., Frenette, G., Bordeleau, L. J., Allard, N., Leclerc, P., Blondin, P. and Sullivan, R. (2012). Epididymosomes transfer epididymal sperm binding protein 1 (ELSPBP1) to dead spermatozoa during epididymal transit in bovine. Biology of Reproduction, 87(4), 94. doi: 10.1095/biolreprod.112.100990 Google ScholarPubMed
D’Amours, O., Frenette, G., Caron, P., Belleannée, C., Guillemette, C. and Sullivan, R. (2016). Evidences of biological functions of biliverdin reductase A in the bovine epididymis. Journal of Cellular Physiology, 231(5), 1077–1089. doi: 10.1002/jcp.25200 CrossRefGoogle ScholarPubMed
de Ávila, A. C. F. C. M., Bridi, A., Andrade, G. M., del Collado, M., Sangalli, J. R., Nociti, R. P., da Silva Junior, W. A., Bastien, A., Robert, C., Meirelles, F. V., Perecin, F. and da Silveira, J. C. (2020). Estrous cycle impacts microRNA content in extracellular vesicles that modulate bovine cumulus cell transcripts during in vitro maturation†. Biology of Reproduction, 102(2), 362–375. doi: 10.1093/biolre/ioz177 CrossRefGoogle ScholarPubMed
del Collado, M., da Silveira, J. C., Sangalli, J. R., Andrade, G. M., da Silva Sousa, L. R., Silva, L. A. et al. (2017). Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in vitro maturation of bovine oocytes. Scientific Reports, 7, 1 CrossRefGoogle ScholarPubMed
Denzer, K., Kleijmeer, M. J., Heijnen, H. F., Stoorvogel, W. and Geuze, H. J. (2000). Exosome: From internal vesicle of the multivesicular body to intercellular signaling device. Journal of Cell Science, 113(19), 3365–3374. doi: 10.1242/jcs.113.19.3365 CrossRefGoogle ScholarPubMed
Desai, N. N., Kennard, E. A., Kniss, D. A. and Friedman, C. I. (1994). Novel human endometrial cell line promotes blastocyst development. Fertility and Sterility, 61(4), 760–766. doi: 10.1016/S0015-0282(16)56659-X CrossRefGoogle ScholarPubMed
Dias, B. G. and Ressler, K. J. (2014). Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17(1), 89–96. doi: 10.1038/nn.3594 CrossRefGoogle ScholarPubMed
Ding, C., Zhu, L., Shen, H., Lu, J., Zou, Q., Huang, C., Li, H. and Huang, B. (2020). Exosomal miRNA-17-5p derived from human umbilical cord mesenchymal stem cells improves ovarian function in premature ovarian insufficiency by regulating SIRT7. Stem Cells, 38(9), 1137–1148. doi: 10.1002/stem.3204 CrossRefGoogle ScholarPubMed
Dissanayake, K., Nõmm, M., Lättekivi, F., Ord, J., Ressaissi, Y., Godakumara, K., Reshi, Q. U. A., Viil, J., Jääger, K., Velthut-Meikas, A., Salumets, A., Jaakma, Ü and Fazeli, A. (2021). Oviduct as a sensor of embryo quality: Deciphering the extracellular vesicle (EV)-mediated embryo-maternal dialogue. Journal of Molecular Medicine, 99(5), 685–697. doi: 10.1007/s00109-021-02042-w CrossRefGoogle ScholarPubMed
Eaton, S. A., Jayasooriah, N., Buckland, M. E., Martin, D. I., Cropley, J. E. and Suter, C. M. (2015). Roll over Weismann: Extracellular vesicles in the transgenerational transmission of environmental effects. Epigenomics, 7(7), 1165–1171. doi: 10.2217/epi.15.58 CrossRefGoogle ScholarPubMed
Ebert, B., Kisiela, M. and Maser, E. (2015). Human DCXR–another’moonlighting protein’involved in sugar metabolism, carbonyl detoxification, cell adhesion and male fertility? Biological Reviews of the Cambridge Philosophical Society, 90(1), 254–278. doi: 10.1111/brv.12108 CrossRefGoogle ScholarPubMed
Eickhoff, R., Baldauf, C., Koyro, H. W., Wennemuth, G., Suga, Y., Seitz, J., Henkel, R. and Meinhardt, A. (2004). 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. Molecular Human Reproduction, 10(8), 605–611. doi: 10.1093/molehr/gah075 CrossRefGoogle ScholarPubMed
Eppig, J. J., Chesnel, F., Hirao, Y., O’Brien, M. J., Pendola, F. L., Watanabe, S. and Wigglesworth, K. (1997). Oocyte control of granulosa cell development: How and why. Human Reproduction, 12(11), Suppl., 127–132Google ScholarPubMed
Farooqi, A. A., Desai, N. N., Qureshi, M. Z., Librelotto, D. R. N., Gasparri, M. L., Bishayee, A., Nabavi, S. M., Curti, V. and Daglia, M. (2018). Exosome biogenesis, bioactivities and functions as new delivery systems of natural compounds. Biotechnology Advances, 36(1), 328–334. doi: 10.1016/j.biotechadv.2017.12.010 CrossRefGoogle ScholarPubMed
Fereshteh, Z., Bathala, P., Galileo, D. S. and Martin-DeLeon, P. A. (2019). Detection of extracellular vesicles in the mouse vaginal fluid: Their delivery of sperm proteins that stimulate capacitation and modulate fertility. Journal of Cellular Physiology, 234(8), 12745–12756. doi: 10.1002/jcp.27894 CrossRefGoogle ScholarPubMed
Ferraz, M., Fujihara, M., Nagashima, J. B., Noonan, M. J., Inoue-Murayama, M. and Songsasen, N. (2020). Follicular extracellular vesicles enhance meiotic resumption of domestic cat vitrified oocytes. Scientific Reports, 10, 1 Google Scholar
Flesch, F. M., Wijnand, E., Van de Lest, C. H. A., Colenbrander, B., Van Golde, L. M. G. and Gadella, B. M. (2001). Capacitation dependent activation of tyrosine phosphorylation generates two sperm head plasma membrane proteins with high primary binding affinity for the zona pellucida. Molecular Reproduction and Development, 60(1), 107–115. doi: 10.1002/mrd.1067 CrossRefGoogle ScholarPubMed
Franchi, A., Cubilla, M., Guidobaldi, H. A., Bravo, A. A. and Giojalas, L. C. (2016). Uterosome-like vesicles prompt human sperm fertilizing capability. Molecular Human Reproduction, 22(12), 833–841. doi: 10.1093/molehr/gaw066 Google ScholarPubMed
Frenette, G., Lessard, C. and Sullivan, R. (2004). Polyol pathway along the bovine epididymis. Molecular Reproduction and Development, 69(4), 448–456. doi: 10.1002/mrd.20170 CrossRefGoogle ScholarPubMed
Frenette, G., Légaré, C., Saez, F. and Sullivan, R. (2005). Macrophage migration inhibitory factor in the human epididymis and semen. Molecular Human Reproduction, 11(8), 575–582. doi: 10.1093/molehr/gah197 CrossRefGoogle ScholarPubMed
Frenette, G., Thabet, M. and Sullivan, R. (2006). Polyol pathway in human epididymis and semen. Journal of Andrology, 27(2), 233–239. doi: 10.2164/jandrol.05108 CrossRefGoogle ScholarPubMed
Funahashi, H., Ekwall, H., Kikuchi, K. and Rodriguez-Martinez, H. (2001). Transmission electron microscopy studies of the zona reaction in pig oocytes fertilized in vivo and in vitro . Reproduction, 122(3), 443–452. doi: 10.1530/rep.0.1220443 CrossRefGoogle ScholarPubMed
Giacomini, E., Vago, R., Sanchez, A. M., Podini, P., Zarovni, N., Murdica, V., Rizzo, R., Bortolotti, D., Candiani, M. and Viganò, P. (2017). Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Scientific Reports, 7(1), 5210. doi: 10.1038/s41598-017-05549-w CrossRefGoogle ScholarPubMed
Griffiths, G. S., Galileo, D. S., Reese, K. and Martin-DeLeon, P. A. (2008). Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Molecular Reproduction and Development, 75(11), 1627–1636. doi: 10.1002/mrd.20907 CrossRefGoogle ScholarPubMed
Gupta, S., Primakoff, P. and Myles, D. G. (2009). Can the presence of wild-type oocytes during insemination rescue the fusion defect of CD9 null oocytes? Molecular Reproduction and Development, 76(7), 602–602. doi: 10.1002/mrd.21040 CrossRefGoogle ScholarPubMed
Hailay, T., Hoelker, M., Poirier, M., Gebremedhn, S., Rings, F., Saeed-Zidane, M., Salilew-Wondim, D., Dauben, C., Tholen, E., Neuhoff, C., Schellander, K. and Tesfaye, D. (2019). Extracellular vesicle-coupled miRNA profiles in follicular fluid of cows with divergent post-calving metabolic status. Scientific Reports, 9(1), 12851. doi: 10.1038/s41598-019-49029-9 CrossRefGoogle ScholarPubMed
Hamlett, E. D., Goetzl, E. J., Ledreux, A., Vasilevko, V., Boger, H. A., LaRosa, A., Clark, D., Carroll, S. L., Carmona-Iragui, M., Fortea, J., Mufson, E. J., Sabbagh, M., Mohammed, A. H., Hartley, D., Doran, E., Lott, I. T. and Granholm, A. C. (2017). Neuronal exosomes reveal Alzheimer’s disease biomarkers in Down syndrome. Alzheimer’s and Dementia, 13(5), 541–549. doi: 10.1016/j.jalz.2016.08.012 CrossRefGoogle ScholarPubMed
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E. and Lumey, L. H. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences of the United States of America, 105(44), 17046–17049. doi: 10.1073/pnas.0806560105 CrossRefGoogle ScholarPubMed
Huang, B., Lu, J., Ding, C., Zou, Q., Wang, W. and Li, H. (2018). Exosomes derived from human adipose mesenchymal stem cells improve ovary function of premature ovarian insufficiency by targeting SMAD. Stem Cell Research and Therapy, 9(1), 216. doi: 10.1186/s13287-018-0953-7 CrossRefGoogle ScholarPubMed
Hung, W. T., Hong, X., Christenson, L. K. and McGinnis, L. K. (2015). Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biology of Reproduction, 93(5), 117. doi: 10.1095/biolreprod.115.132977 CrossRefGoogle ScholarPubMed
Hung, W. T., Navakanitworakul, R., Khan, T., Zhang, P., Davis, J. S., McGinnis, L. K. and Christenson, L. K. (2017). Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation. Biology of Reproduction, 97(4), 644–655. doi: 10.1093/biolre/iox106 CrossRefGoogle ScholarPubMed
Hur, Y. H., Feng, S., Wilson, K. F., Cerione, R. A. and Antonyak, M. A. (2021). Embryonic stem cell-derived extracellular vesicles maintain ESC stemness by activating FAK. Developmental Cell, 56(3), 277–291.e6. doi: 10.1016/j.devcel.2020.11.017 CrossRefGoogle ScholarPubMed
Imura, H. and Fukata, J. I. (1993). Endocrine–paracine interaction in communication between the immune and endocrine systems. Activation of the hypothalamic-pituitary-adrenal axis in inflammation. European Journal of Endocrinology, 130(1), 32–37. doi: 10.1530/eje.0.1300032 CrossRefGoogle Scholar
Inoue, Y., Munakata, Y., Shinozawa, A., Kawahara-Miki, R., Shirasuna, K. and Iwata, H. (2020). Prediction of major microRNAs in follicular fluid regulating porcine oocyte development. Journal of Assisted Reproduction and Genetics, 37(10), 2569–2579. doi: 10.1007/s10815-020-01909-0 CrossRefGoogle ScholarPubMed
Kim, N. H., Funahashi, H., Abeydeera, L. R., Moon, S. J., Prather, R. S. and Day, B. N. (1996). Effects of oviductal fluid on sperm penetration and cortical granule exocytosis during fertilization of pig oocytes in vitro . Journal of Reproduction and Fertility, 107(1), 79–86. doi: 10.1530/jrf.0.1070079 CrossRefGoogle ScholarPubMed
Kim, S. M., Yang, Y., Oh, S. J., Hong, Y., Seo, M. and Jang, M. (2017). Cancer-derived exosomes as a delivery platform of CRISPR/Cas9 confer cancer cell tropism-dependent targeting. Journal of Controlled Release, 266, 8–16. doi: 10.1016/j.jconrel.2017.09.013 CrossRefGoogle ScholarPubMed
King, R. S. and Killian, G. J. (1994). Purification of bovine estrus-associated protein and localization of binding on sperm. Biology of Reproduction, 51, 34–42 CrossRefGoogle ScholarPubMed
Koh, Y. Q., Peiris, H. N., Vaswani, K., Reed, S., Rice, G. E., Salomon, C. and Mitchell, M. D. (2016). Characterization of exosomal release in bovine endometrial intercaruncular stromal cells. Reproductive Biology and Endocrinology: RBandE, 14(1), 78. doi: 10.1186/s12958-016-0207-4 CrossRefGoogle ScholarPubMed
Kosinski, M., McDonald, K., Schwartz, J., Yamamoto, I. and Greenstein, D. (2005). C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development, 132(15), 3357–3369. doi: 10.1242/dev.01916 CrossRefGoogle ScholarPubMed
Kumar, A., Pandita, S., Ganguly, S., Soren, S. and Pagrut, N. (2018). Beneficial effects of seminal prostasomes on sperm functional parameters. Journal of Entomology and Zoology Studies, 6, 2464–2471.Google Scholar
Kvist, U. (1980). Sperm nuclear chromatin decondensation ability. Acta Physiologica Scandinavica, 486, 24.Google ScholarPubMed
Kvist, U., Kjellberg, S., Björndahl, L., Soufir, J. C. and Arver, S. (1990). Seminal fluid from men with agenesis of the Wolffian ducts: Zinc-binding properties and effects on sperm chromatin stability. International Journal of Andrology, 13(4), 245–252. doi: 10.1111/j.1365-2605.1990.tb01028.x CrossRefGoogle ScholarPubMed
Lamy, J., Nogues, P., Combes-Soia, L., Tsikis, G., Labas, V., Mermillod, P., Druart, X. and Saint-Dizier, M. (2018). Identification by proteomics of oviductal sperm-interacting proteins. Reproduction, 155(5), 457–466. doi: 10.1530/REP-17-0712 CrossRefGoogle ScholarPubMed
Lee, S. H., Oh, H. J., Kim, M. J. and Lee, B. C. (2020a). Exosomes derived from oviduct cells mediate the EGFR/MAPK signaling pathway in cumulus cells. Journal of Cellular Physiology, 235(2), 1386–1404. doi: 10.1002/jcp.29058 CrossRefGoogle ScholarPubMed
Lee, S. H., Oh, H. J., Kim, M. J. and Lee, B. C. (2020b). Canine oviductal exosomes improve oocyte development via EGFR/MAPK signaling pathway. Reproduction, 160(4), 613–625. doi: 10.1530/REP-19-0600 CrossRefGoogle ScholarPubMed
Litvin, T. N., Kamenetsky, M., Zarifyan, A., Buck, J. and Levin, L. R. (2003). Kinetic properties of ‘soluble’ adenylyl cyclase: Synergism between calcium and bicarbonate. Journal of Biological Chemistry, 278(18), 15922–15926. doi: 10.1074/jbc.M212475200 CrossRefGoogle ScholarPubMed
Liu, J., Cvirkaite-Krupovic, V., Commere, P. H., Yang, Y., Zhou, F., Shen, Y. et al. (2021). Archaeal extracellular vesicles are produced in an ESCRT-dependent manner and promote gene transfer and nutrient cycling in extreme environments. ISME Journal, 1, 1–14 Google Scholar
Lopera-Vásquez, R., Hamdi, M., Fernandez-Fuertes, B., Maillo, V., Beltrán-Breña, P., Calle, A., Redruello, A., López-Martín, S., Gutierrez-Adán, A., Yañez-Mó, M., Ramirez, M. Á and Rizos, D. (2016). Extracellular vesicles from BOEC in in vitro embryo development and quality. PLOS ONE, 11(2), e0148083. doi: 10.1371/journal.pone.0148083 CrossRefGoogle ScholarPubMed
Lopera-Vasquez, R., Hamdi, M., Maillo, V., Gutierrez-Adan, A., Bermejo-Alvarez, P., Ramírez, M. Á., Yáñez-Mó, M. and Rizos, D. (2017). Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro . Reproduction, 153(4), 461–470. doi: 10.1530/REP-16-0384 CrossRefGoogle ScholarPubMed
Lv, C., Yu, W. X., Wang, Y., Yi, D. J., Zeng, M. H. and Xiao, H. M. (2018). MiR-21 in extracellular vesicles contributes to the growth of fertilized eggs and embryo development in mice. Bioscience Reports, 38(4). doi: 10.1042/BSR20180036 CrossRefGoogle Scholar
Lyons, S. M. and Prasad, A. (2012). Cross-talk and information transfer in mammalian and bacterial signaling. PLOS ONE, 7(4), e34488. doi: 10.1371/journal.pone.0034488 CrossRefGoogle ScholarPubMed
Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M., Clarke, H. J., Khandjian, ÉW., Richard, F. J., Hyttel, P. and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biology of Reproduction, 91(4), 1–12. doi: 10.1095/biolreprod.114.119867 CrossRefGoogle Scholar
Mackeh, R., Marr, A. K., Fadda, A. and Kino, T. (2018). C2H2-type zinc finger proteins: Evolutionarily old and new partners of the nuclear hormone receptors. Nuclear Receptor Signaling, 15, 1550762918801071. doi: 10.1177/1550762918801071 CrossRefGoogle ScholarPubMed
Mancuso, F., Calvitti, M., Milardi, D., Grande, G., Falabella, G., Arato, I., Giovagnoli, S., Vincenzoni, F., Mancini, F., Nastruzzi, C., Bodo, M., Baroni, T., Castagnola, M., Marana, R., Pontecorvi, A., Calafiore, R. and Luca, G. (2018). Testosterone and FSH modulate Sertoli cell extracellular secretion: Proteomic analysis. Molecular and Cellular Endocrinology, 476, 1–7. doi: 10.1016/j.mce.2018.04.001 CrossRefGoogle ScholarPubMed
Mapes, J., Chen, Y. Z., Kim, A., Mitani, S., Kang, B. H. and Xue, D. (2012). CED-1, CED-7, and TTR-52 regulate surface phosphatidylserine expression on apoptotic and phagocytic cells. Current Biology, 22(14), 1267–1275. doi: 10.1016/j.cub.2012.05.052 CrossRefGoogle ScholarPubMed
Marinaro, F., Macías-García, B., Sánchez-Margallo, F. M., Blázquez, R., Álvarez, V., Matilla, E., Hernández, N., Gómez-Serrano, M., Jorge, I., Vázquez, J., González-Fernández, L., Pericuesta, E., Gutiérrez-Adán, A. and Casado, J. G. (2019). Extracellular vesicles derived from endometrial human mesenchymal stem cells enhance embryo yield and quality in an aged murine model†. Biology of Reproduction, 100(5), 1180–1192. doi: 10.1093/biolre/ioy263 CrossRefGoogle Scholar
Martin-DeLeon, P. A. (2016). Uterosomes: Exosomal cargo during the estrus cycle and interaction with sperm. Frontiers in Bioscience, 8(1), 115–122. doi: 10.2741/s451 CrossRefGoogle ScholarPubMed
Martinez, R. M., Baccarelli, A. A., Liang, L., Dioni, L., Mansur, A., Adir, M., Bollati, V., Racowsky, C., Hauser, R. and Machtinger, R. (2019). Body mass index in relation to extracellular vesicle–linked microRNAs in human follicular fluid. Fertility and Sterility, 112(2), 387–396.e3. doi: 10.1016/j.fertnstert.2019.04.001 CrossRefGoogle ScholarPubMed
Mathieu, M., Martin-Jaular, L., Lavieu, G. and Théry, C. (2019). Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nature Cell Biology, 21(1), 9–17. doi: 10.1038/s41556-018-0250-9 CrossRefGoogle ScholarPubMed
Mathieu, M., Névo, N., Jouve, M., Valenzuela, J. I., Maurin, M., Verweij, F. J., Palmulli, R., Lankar, D., Dingli, F., Loew, D., Rubinstein, E., Boncompain, G., Perez, F. and Théry, C. (2021). Specificities of exosome versus small ectosome secretion revealed by live intracellular tracking of CD63 and CD9. Nature Communications, 12(1), 4389. doi: 10.1038/s41467-021-24384-2 CrossRefGoogle ScholarPubMed
Matsuno, Y., Kanke, T., Maruyama, N., Fujii, W., Naito, K. and Sugiura, K. (2019). Characterization of mRNA profiles of the exosome-like vesicles in porcine follicular fluid. PLOS ONE, 14(6), e0217760. doi: 10.1371/journal.pone.0217760 CrossRefGoogle ScholarPubMed
Matthews, S. G. and Phillips, D. I. (2010). Minireview: Transgenerational inheritance of the stress response: A new frontier in stress research. Endocrinology, 151(1), 7–13. doi: 10.1210/en.2009-0916 CrossRefGoogle ScholarPubMed
Mellisho, E. A., Velásquez, A. E., Nuñez, M. J., Cabezas, J. G., Cueto, J. A., Fader, C., Castro, F. O. and Rodríguez-Álvarez, L. (2017). Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro . PLOS ONE, 12(5), e0178306. doi: 10.1371/journal.pone.0178306 CrossRefGoogle ScholarPubMed
Milasan, A., Tessandier, N., Tan, S., Brisson, A., Boilard, E. and Martel, C. (2016). Extracellular vesicles are present in mouse lymph and their level differs in atherosclerosis. Journal of Extracellular Vesicles, 5, 31427. doi: 10.3402/jev.v5.31427 CrossRefGoogle ScholarPubMed
Miyado, K., Yoshida, K., Yamagata, K., Sakakibara, K., Okabe, M., Wang, X., Miyamoto, K., Akutsu, H., Kondo, T., Takahashi, Y., Ban, T., Ito, C., Toshimori, K., Nakamura, A., Ito, M., Miyado, M., Mekada, E. and Umezawa, A. (2008). The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proceedings of the National Academy of Sciences of the United States of America, 105(35), 12921–12926. doi: 10.1073/pnas.0710608105 CrossRefGoogle ScholarPubMed
Morales Dalanezi, F., Mogollon Garcia, H. D., de Andrade Ferrazza, R., Fagali Franchi, F., Kubo Fontes, P., de Souza Castilho, A. C., Gouveia Nogueira, M. F., Dos Santos Schmidt, E. M., Sartori, R. and Pinheiro Ferreira, J. C. (2019). Extracellular vesicles of follicular fluid from heat-stressed cows modify the gene expression of in vitro-matured oocytes. Animal Reproduction Science, 205, 94–104. doi: 10.1016/j.anireprosci.2019.04.008 CrossRefGoogle ScholarPubMed
Navakanitworakul, R., Hung, W. T., Gunewardena, S., Davis, J. S., Chotigeat, W. and Christenson, L. K. (2016). Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles. Scientific Reports, 6, 25486. doi: 10.1038/srep25486 CrossRefGoogle ScholarPubMed
Ng, S. F., Lin, R. C., Laybutt, D. R., Barres, R., Owens, J. A. and Morris, M. J. (2010). Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature, 467(7318), 963–966. doi: 10.1038/nature09491 CrossRefGoogle ScholarPubMed
Ng, Y. H., Rome, S., Jalabert, A., Forterre, A., Singh, H., Hincks, C. L. and Salamonsen, L. A. (2013). Endometrial exosomes/microvesicles in the uterine microenvironment: A new paradigm for embryo-endometrial cross talk at implantation. PLOS ONE, 8(3), e58502. doi: 10.1371/journal.pone.0058502 CrossRefGoogle ScholarPubMed
Niu, Z., Pang, R. T. K., Liu, W., Li, Q., Cheng, R. and Yeung, W. S. B. (2017). Polymer-based precipitation preserves biological activities of extracellular vesicles from an endometrial cell line. PLOS ONE, 12(10), e0186534. doi: 10.1371/journal.pone.0186534 CrossRefGoogle ScholarPubMed
Nusse, R. and Clevers, H. (2017). Wnt/β-catenin signaling, disease and emerging therapeutic modalities. Cell, 169(6), 985–999. doi: 10.1016/j.cell.2017.05.016 CrossRefGoogle ScholarPubMed
Ortega, F. G., Roefs, M. T., de Miguel Perez, D., Kooijmans, S. A., de Jong, O. G., Sluijter, J. P., Schiffelers, R. M. and Vader, P. (2019). Interfering with endolysosomal trafficking enhances release of bioactive exosomes. Nanomedicine: Nanotechnology, Biology and Medicine, 20, 102014. doi: 10.1016/j.nano.2019.102014 CrossRefGoogle ScholarPubMed
Orton, R. J., Sturm, O. E., Vyshemirsky, V., Calder, M., Gilbert, D. R. and Kolch, W. (2005). Computational modelling of the receptor-tyrosine-kinase-activated MAPK pathway. Biochemical Journal, 392(2), 249–261. doi: 10.1042/BJ20050908 CrossRefGoogle ScholarPubMed
Pan, B., Toms, D., Shen, W. and Li, J. (2015). MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells. American Journal of Physiology. Endocrinology and Metabolism, 308(6), E525–E534. doi: 10.1152/ajpendo.00480.2014 CrossRefGoogle ScholarPubMed
Patel, G. K., Khan, M. A., Zubair, H., Srivastava, S. K., Khushman, M., Singh, S. and Singh, A. P. (2019). Comparative analysis of exosome isolation methods using culture supernatant for optimum yield, purity and downstream applications. Scientific Reports, 9(1), 5335. doi: 10.1038/s41598-019-41800-2 CrossRefGoogle ScholarPubMed
Pauerstein, C. J., Eddy, C. A., Koong, M. K. and Moore, G. D. (1990). Rabbit endosalpinx suppresses ectopic implantation. Fertility and Sterility, 54(3), 522–526. doi: 10.1016/S0015-0282(16)53774-1 CrossRefGoogle ScholarPubMed
Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., Golding, J. and ALSPAC Study Team. (2006). Sex-specific, male-line transgenerational responses in humans. European Journal of Human Genetics, 14(2), 159–166. doi: 10.1038/sj.ejhg.5201538 CrossRefGoogle ScholarPubMed
Piehl, L. L., Fischman, M. L., Hellman, U., Cisale, H. and Miranda, P. V. (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 CrossRefGoogle Scholar
Qiao, F., Ge, H., Ma, X., Zhang, Y., Zuo, Z., Wang, M., Zhang, Y. and Wang, Y. (2018). Bovine uterus-derived exosomes improve developmental competence of somatic cell nuclear transfer embryos. Theriogenology, 114, 199–205. doi: 10.1016/j.theriogenology.2018.03.027 CrossRefGoogle ScholarPubMed
Qu, P., Zhao, Y., Wang, R., Zhang, Y., Li, L., Fan, J. and Liu, E. (2019). Extracellular vesicles derived from donor oviduct fluid improved birth rates after embryo transfer in mice. Reproduction, Fertility and Development, 31(2), 324–332. doi: 10.1071/RD18203 CrossRefGoogle ScholarPubMed
Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J. and Geuze, H. J. (1996). B lymphocytes secrete antigen-presenting vesicles. Journal of Experimental Medicine, 183(3), 1161–1172. doi: 10.1084/jem.183.3.1161 CrossRefGoogle ScholarPubMed
Reilly, J. N., McLaughlin, E. A., Stanger, S. J., Anderson, A. L., Hutcheon, K., Church, K., Mihalas, B. P., Tyagi, S., Holt, J. E., Eamens, A. L. and Nixon, B. (2016). Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Scientific Reports, 6, 31794. doi: 10.1038/srep31794 CrossRefGoogle Scholar
Rodrigues, T. A., Alli, A., Paula-Lopes, F. F. and Hansen, P. (2018). 154 exosomes in follicular fluid protect the bovine oocyte from heat shock. Reproduction, Fertility and Development, 30(1), 217–217. doi: 10.1071/RDv30n1Ab154 CrossRefGoogle Scholar
Rodrigues, T. A., Tuna, K. M., Alli, A. A., Tribulo, P., Hansen, P. J., Koh, J. and Paula-Lopes, F. F. (2019). Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock. Reproduction, Fertility and Development, 31(5), 888–897. doi: 10.1071/RD18450 CrossRefGoogle ScholarPubMed
Ronquist, G. and Brody, I. (1985). The prostasome: Its secretion and function in man. Biochimica et Biophysica Acta, 822(2), 203–218. doi: 10.1016/0304-4157(85)90008-5 CrossRefGoogle ScholarPubMed
Ronquist, G., Brody, I., Gottfries, A. and 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 CrossRefGoogle ScholarPubMed
Ronquist, G., Nilsson, B. O. and Hjertën, S. (1990). Interaction between prostasomes and spermatozoa from human semen. Archives of Andrology, 24(2), 147–157. doi: 10.3109/01485019008986874 CrossRefGoogle ScholarPubMed
Ronquist, K. G., Ronquist, G., Carlsson, L. and Larsson, A. (2009). Human prostasomes contain chromosomal DNA. Prostate, 69(7), 737–743. doi: 10.1002/pros.20921 CrossRefGoogle ScholarPubMed
Ronquist, G. K., Larsson, A., Ronquist, G., Isaksson, A., Hreinsson, J., Carlsson, L. and Stavreus-Evers, A. (2011). Prostasomal DNA characterization and transfer into human sperm. Molecular Reproduction and Development, 78(7), 467–476. doi: 10.1002/mrd.21327 CrossRefGoogle ScholarPubMed
Ruiz-González, I., Xu, J., Wang, X., Burghardt, R. C., Dunlap, K. A. and Bazer, F. W. (2015). Exosomes, endogenous retroviruses and Toll-like receptors: Pregnancy recognition in ewes. Reproduction, 149(3), 281–291. doi: 10.1530/REP-14-0538 CrossRefGoogle ScholarPubMed
Russell, D. L., Gilchrist, R. B., Brown, H. M. and Thompson, J. G. (2016). Bidirectional communication between cumulus cells and the oocyte: Old hands and new players? Theriogenology, 86(1), 62–68. doi: 10.1016/j.theriogenology.2016.04.019 CrossRefGoogle ScholarPubMed
Saadeldin, I. M., Kim, S. J., Choi, Y. B. and Lee, B. C. (2014). Improvement of cloned embryos development by co-culturing with parthenotes: A possible role of exosomes/microvesicles for embryos paracrine communication. Cell Reprogram, 16(3), 223–234. doi: 10.1089/cell.2014.0003 CrossRefGoogle ScholarPubMed
Saeed-Zidane, M., Linden, L., Salilew-Wondim, D., Held, E., Neuhoff, C., Tholen, E., Hoelker, M., Schellander, K. and Tesfaye, D. (2017). Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress. PLOS ONE, 12(11), e0187569. doi: 10.1371/journal.pone.0187569 CrossRefGoogle ScholarPubMed
Saez, F., Frenette, G. and Sullivan, R. (2003). Epididymosomes and prostasomes: Their roles in posttesticular maturation of the sperm cells. Journal of Andrology, 24(2), 149–154. doi: 10.1002/j.1939-4640.2003.tb02653.x CrossRefGoogle ScholarPubMed
Salamone, D. F., Canel, N. G. and Rodríguez, M. B. (2017). Intracytoplasmic sperm injection in domestic and wild mammals. Reproduction, 154(6), F111–F124. doi: 10.1530/REP-17-0357 CrossRefGoogle ScholarPubMed
Sang, Q., Yao, Z., Wang, H., Feng, R., Wang, H., Zhao, X., Xing, Q., Jin, L., He, L., Wu, L. and Wang, L. (2013). Identification of microRNAs in human follicular fluid: Characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo . Journal of Clinical Endocrinology and Metabolism, 98(7), 3068–3079. doi: 10.1210/jc.2013-1715 CrossRefGoogle ScholarPubMed
Santonocito, M., Vento, M., Guglielmino, M. R., Battaglia, R., Wahlgren, J., Ragusa, M., Barbagallo, D., Borzì, P., Rizzari, S., Maugeri, M., Scollo, P., Tatone, C., Valadi, H., Purrello, M. and Di Pietro, C. (2014). Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: Bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertility and Sterility, 102(6), 1751–61.e1. doi: 10.1016/j.fertnstert.2014.08.005 CrossRefGoogle ScholarPubMed
Santos, G., Bottino, M. P., Santos, A. P. C., Simões, L. M. S., Souza, J. C., Ferreira, M. B. D., da Silveira, J. C., Ávila, A. C. F. C. M., Bride, A. and Sales, J. N. S. (2018). Subclinical mastitis interferes with ovulation, oocyte and granulosa cell quality in dairy cows. Theriogenology, 119, 214–219. doi: 10.1016/j.theriogenology.2018.04.028 CrossRefGoogle ScholarPubMed
Shen, Z., Xu, X., Lv, L., Dai, H., Chen, J. and Chen, B. (2020). miR-21 overexpression promotes esophageal squamous cell carcinoma invasion and migration by repressing tropomyosin 1. Gastroenterology Research and Practice, 2020, 6478653. doi: 10.1155/2020/6478653 CrossRefGoogle ScholarPubMed
Singh, V. K., Kumar, R. and Atreja, S. K. (2014). Cryo-survival, cryo-capacitation and oxidative stress assessment of buffalo spermatozoa cryopreserved in new soya milk extender. Livestock Science, 160, 214–218. doi: 10.1016/j.livsci.2013.12.013 CrossRefGoogle Scholar
Smith, K. and Spadafora, C. (2005). Sperm-mediated gene transfer: Applications and implications. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 27(5), 551–562. doi: 10.1002/bies.20211 CrossRefGoogle ScholarPubMed
Sohel, M. M. H., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K. and Tesfaye, D. (2013a). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: Implications for bovine oocyte developmental competence. PLOS ONE, 8(11), e78505. doi: 10.1371/journal.pone.0078505 CrossRefGoogle ScholarPubMed
Sohel, M. M. H., Salilew-Wondim, D., Hölker, M., Rings, F., Schellander, K. and Tesfaye, D. (2013b). 207 circulatory microRNA signatures in follicular fluid in relation to the growth status of bovine oocytes. Reproduction, Fertility and Development, 25(1), 251–252. doi: 10.1071/RDv25n1Ab207 CrossRefGoogle Scholar
Soria, F. N., Pampliega, O., Bourdenx, M., Meissner, W. G., Bezard, E. and Dehay, B. (2017). Exosomes, an unmasked culprit in neurodegenerative diseases. Frontiers in Neuroscience, 11, 26. doi: 10.3389/fnins.2017.00026 CrossRefGoogle ScholarPubMed
Steven, F. S., Griffin, M. M. and Chantler, E. N. (1982). Inhibition of human and bovine sperm acrosin by divalent metal ions. Possible role of zinc as a regulator of acrosin activity. International Journal of Andrology, 5(4), 401–412. doi: 10.1111/j.1365-2605.1982.tb00270.x CrossRefGoogle ScholarPubMed
Subra, C., Laulagnier, K., Perret, B. and Record, M. (2007). Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie, 89(2), 205–212. doi: 10.1016/j.biochi.2006.10.014 CrossRefGoogle ScholarPubMed
Sullivan, R. (2015). Epididymosomes: A heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian Journal of Andrology, 17(5), 726–729. doi: 10.4103/1008-682X.155255 Google ScholarPubMed
Sullivan, R., Saez, F., Girouard, J. and Frenette, G. (2005). Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells, Molecules and Diseases, 35(1), 1–10. doi: 10.1016/j.bcmd.2005.03.005 CrossRefGoogle ScholarPubMed
Tetta, C., Ghigo, E., Silengo, L., Deregibus, M. C. and Camussi, G. (2013). Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine, 44(1), 11–19. doi: 10.1007/s12020-012-9839-0 CrossRefGoogle ScholarPubMed
Théry, C. (2011). Exosomes: Secreted vesicles and intercellular communications. F1000 Biology Reports, 3, 15. doi: 10.3410/B3-15 CrossRefGoogle ScholarPubMed
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G. K., Ayre, D. C., Bach, J. M., Bachurski, D., Baharvand, H., Balaj, L., Baldacchino, S., Bauer, N. N., Baxter, A. A., Bebawy, M., Zuba-Surma, E. K. (2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. Journal of Extracellular Vesicles, 7(1), 1535750. doi: 10.1080/20013078.2018.1535750 CrossRefGoogle ScholarPubMed
Tumova, L., Zigo, M., Sutovsky, P., Sedmikova, M. and Postlerova, P. (2021). Ligands and receptors involved in the sperm-zona pellucida interactions in mammals. Cells, 10(1), 133. doi: 10.3390/cells10010133 CrossRefGoogle ScholarPubMed
Urbanelli, L., Buratta, S., Tancini, B., Sagini, K., Delo, F., Porcellati, S. and Emiliani, C. (2019). The role of extracellular vesicles in viral infection and transmission. Vaccines, 7(3), 102. doi: 10.3390/vaccines7030102 CrossRefGoogle ScholarPubMed
Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J. and Lötvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology, 9(6), 654–659. doi: 10.1038/ncb1596 CrossRefGoogle ScholarPubMed
Van Soom, A., Wrathall, A. E., Herrler, A. and Nauwynck, H. J. (2010). Is the zona pellucida an efficient barrier to viral infection? Reproduction, Fertility and Development, 22(1), 21–31. doi: 10.1071/RD09230 CrossRefGoogle ScholarPubMed
Vilella, F., Moreno-Moya, J. M., Balaguer, N., Grasso, A., Herrero, M., Martínez, S., Marcilla, A. and Simón, C. (2015). Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. Development, 142(18), 3210–3221. doi: 10.1242/dev.124289 CrossRefGoogle ScholarPubMed
Villarroya-Beltri, C., Gutiérrez-Vázquez, C., Sánchez-Cabo, F., Pérez-Hernández, D., Vázquez, J., Martin-Cofreces, N., Martinez-Herrera, D. J., Pascual-Montano, A., Mittelbrunn, M. and Sánchez-Madrid, F. (2013). SUMOylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nature Communications, 4, 2980. doi: 10.1038/ncomms3980 CrossRefGoogle ScholarPubMed
Visconti, P. E., Moore, G. D., Bailey, J. L., Leclerc, P., Connors, S. A., Pan, D., Olds-Clarke, P. and Kopf, G. S. (1995). Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development, 121(4), 1139–1150. doi: 10.1242/dev.121.4.1139 CrossRefGoogle ScholarPubMed
Wehman, A. M., Poggioli, C., Schweinsberg, P., Grant, B. D. and Nance, J. (2011). The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Current Biology, 21(23), 1951–1959. doi: 10.1016/j.cub.2011.10.040 CrossRefGoogle ScholarPubMed
Wong, W. Y., Flik, G., Groenen, P. M., Swinkels, D. W., Thomas, C. M., Copius-Peereboom, J. H., Merkus, H. M. and Steegers-Theunissen, R. P. (2001). The impact of calcium, magnesium, zinc and copper in blood and seminal plasma on semen parameters in men. Reproductive Toxicology, 15(2), 131–136. doi: 10.1016/s0890-6238(01)00113-7 CrossRefGoogle ScholarPubMed
Yan, H., Rao, J., Yuan, J., Gao, L., Huang, W., Zhao, L. and Ren, J. (2017). Long non-coding RNA MEG3 functions as a competing endogenous RNA to regulate ischemic neuronal death by targeting miR-21/PDCD4 signaling pathway. Cell Death and Disease, 8(12), 3211. doi: 10.1038/s41419-017-0047-y CrossRefGoogle ScholarPubMed
Yanagimachi, R., Kamiguchi, Y., Mikamo, K., Suzuki, F. and Yanagimachi, H. (1985). Maturation of spermatozoa in the epididymis of the Chinese hamster. American Journal of Anatomy, 172(4), 317–330. doi: 10.1002/aja.1001720406 CrossRefGoogle ScholarPubMed
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., et al. (2015). Biological properties of extracellular vesicles and their physiological functions. Journal of Extracellular Vesicles, 4, 27066. doi: 10.3402/jev.v4.27066 CrossRefGoogle ScholarPubMed
Yang, Q., Liu, L. and Huang, H. (2017). Extraction and identification of exosomes in follicular fluid from patients with polycystic ovary syndrome and isolation and detection of miRNAs in exosomes. Journal of Shanghai Jiaotong University (Medical Science), 37, 1085–1089.Google Scholar
Yang, W., Zhang, J., Xu, B., He, Y., Liu, W., Li, J., Zhang, S., Lin, X., Su, D., Wu, T. and Li, J. (2020). HucMSC-derived exosomes mitigate the age-related retardation of fertility in female mice. Molecular Therapy, 28(4), 1200–1213. doi: 10.1016/j.ymthe.2020.02.003 CrossRefGoogle ScholarPubMed
Yim, N., Ryu, S. W., Choi, K., Lee, K. R., Lee, S., Choi, H., Kim, J., Shaker, M. R., Sun, W., Park, J. H., Kim, D., Heo, W. D. and Choi, C. (2016). Exosome engineering for efficient intracellular delivery of soluble proteins using optically reversible protein–protein interaction module. Nature Communications, 7, 12277. doi: 10.1038/ncomms12277 CrossRefGoogle ScholarPubMed
Yudin, A. I., Li, M. W., Robertson, K. R., Tollner, T., Cherr, G. N. and Overstreet, J. W. (2002). Identification of a novel GPI-anchored CRISP glycoprotein, MAK248, located on the posterior head and equatorial segment of cynomolgus macaque sperm. Molecular Reproduction and Development, 63(4), 488–499. doi: 10.1002/mrd.10193 CrossRefGoogle ScholarPubMed
Zamith-Miranda, D., Nimrichter, L., Rodrigues, M. L. and Nosanchuk, J. D. (2018). Fungal extracellular vesicles: Modulating host–pathogen interactions by both the fungus and the host. Microbes and Infection, 20(9–10), 501–504. doi: 10.1016/j.micinf.2018.01.011 CrossRefGoogle ScholarPubMed