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Extracellular Vesicles Mediate the Embryonic-Maternal Paracrine Communication

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Role of Exosomes in Biological Communication Systems

Abstract

In the last decade, tremendous works have shown the essential involvement of extracellular vesicles (EVs) in paracrine cellular signaling in both physiological and pathological conditions. EVs including exosomes are nanosized vesicles capable of transferring molecular cargoes such as mRNA, miRNA, proteins, and lipids among different cells. Notably, there is a need to elucidate the roles of EVs in embryonic-maternal cross-talk and their possible involvement in the reproductive physiology and pathology. In this chapter, I highlight the literature regarding the mutual dialogue that exists between embryos, oviduct, and endometrium mediated through EVs such as embryonic communication, maternal recognition of pregnancy, and the implantation. A better comprehension of this molecular language would help in developing novel regulatory, diagnostic, biological, and pharmaceutical agents for enhancement or impairing the early embryonic and reproductive physiology.

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Abbreviations

ARTs:

Assisted reproductive techniques

DEGs:

Differentially expressed genes

EVs:

Extracellular vesicles

ICM:

Inner cell mass

miRNA:

Micro RNA

mRNA:

Messenger RNA

NTA:

Nanoparticle tracking analysis

References

  • Abu-Halima M, Hausler S, Backes C, Fehlmann T, Staib C, Nestel S, Nazarenko I, Meese E, Keller A (2017) Micro-ribonucleic acids and extracellular vesicles repertoire in the spent culture media is altered in women undergoing in vitro fertilization. Sci Rep 7:13525

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alcântara-Neto AS, Fernandez-Rufete M, Corbin E, Tsikis G, Uzbekov R, Garanina AS, Coy P, Almiñana C, Mermillod P (2020) Oviduct fluid extracellular vesicles regulate polyspermy during porcine in vitro fertilisation. Reprod Fertil Dev 32:409

    Article  PubMed  CAS  Google Scholar 

  • Al-Dossary AA, Strehler EE, Martin-Deleon PA (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:e80181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Al-Dossary AA, Bathala P, Caplan JL, Martin-DeLeon PA (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). J Biol Chem 290:17710–17723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alminana C, Bauersachs S (2020) Extracellular vesicles: multi-signal messengers in the gametes/embryo-oviduct cross-talk. Theriogenology

    Google Scholar 

  • Alminana C, Corbin E, Tsikis G, Alcantara-Neto AS, Labas V, Reynaud K, Galio L, Uzbekov R, Garanina AS, Druart X et al (2017) Oviduct extracellular vesicles protein content and their role during oviduct-embryo cross-talk. Reproduction 154:153–168

    Article  PubMed  Google Scholar 

  • Alminana C, Tsikis G, Labas V, Uzbekov R, da Silveira JC, Bauersachs S, 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 19:622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altmae S, Koel M, Vosa U, Adler P, Suhorutsenko M, Laisk-Podar T, Kukushkina V, Saare M, Velthut-Meikas A, Krjutskov K et al (2017) Meta-signature of human endometrial receptivity: a meta-analysis and validation study of transcriptomic biomarkers. Sci Rep 7:10077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Andrade GM, Bomfim MM, Del Collado M, Meirelles FV, Perecin F, da Silveira JC (2019) Oxygen tension modulates extracellular vesicles and its miRNA contents in bovine embryo culture medium. Mol Reprod Dev 86:1067–1080

    Article  CAS  PubMed  Google Scholar 

  • Balaguer N, Moreno I, Herrero M, Gonzalez M, Simon C, Vilella F (2018) Heterogeneous nuclear ribonucleoprotein C1 may control miR-30d levels in endometrial exosomes affecting early embryo implantation. Mol Hum Reprod 24:411–425

    Article  CAS  PubMed  Google Scholar 

  • Barkalina N, Jones C, Wood MJ, Coward K (2015) Extracellular vesicle-mediated delivery of molecular compounds into gametes and embryos: learning from nature. Hum Reprod Update 21:627–639

    Article  CAS  PubMed  Google Scholar 

  • Bathala P, Fereshteh Z, Li K, Al-Dossary AA, Galileo DS, Martin-DeLeon PA (2018) Oviductal extracellular vesicles (oviductosomes, OVS) are conserved in humans: murine OVS play a pivotal role in sperm capacitation and fertility. Mol Hum Reprod 24(3):143–157

    CAS  PubMed  PubMed Central  Google Scholar 

  • Battaglia R, Palini S, Vento ME, La Ferlita A, Lo Faro MJ, Caroppo E, Borzi P, Falzone L, Barbagallo D, Ragusa M et al (2019) Identification of extracellular vesicles and characterization of miRNA expression profiles in human blastocoel fluid. Sci Rep 9:1

    Article  CAS  Google Scholar 

  • Bauersachs S, Mermillod P, Alminana C (2020) The oviductal extracellular vesicles’ RNA cargo regulates the bovine embryonic transcriptome. Int J Mol Sci 21:1303

    Article  CAS  PubMed Central  Google Scholar 

  • Bemis LT, McCue PM, Hatzel JN, Bemis J, Ferris RA (2012) Evidence for production of early pregnancy factor (Hsp10), microRNAs and exosomes by day 8 equine embryos. J Equine Veter Sci 32:398

    Article  Google Scholar 

  • Bidarimath M, Khalaj K, Kridli RT, Kan FW, Koti M, Tayade C (2017) Extracellular vesicle mediated intercellular communication at the porcine maternal-fetal interface—a new paradigm for conceptus-endometrial cross-talk. Sci Rep 7:40476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blazquez R, Sanchez-Margallo FM, Alvarez V, Matilla E, Hernandez N, Marinaro F, Gomez-Serrano M, Jorge I, Casado JG, Macias-Garcia 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:e0196080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bognar Z, Csabai TJ, Pallinger E, Balassa T, Farkas N, Schmidt J, Gorgey E, Berta G, Szekeres-Bartho J, Bodis J (2019) The effect of light exposure on the cleavage rate and implantation capacity of preimplantation murine embryos. J Reprod Immunol 132:21–28

    Article  PubMed  Google Scholar 

  • Bridi A, Perecin F, Silveira JCD (2020) Extracellular vesicles mediated early embryo-maternal interactions. Int J Mol Sci 21:1163

    Article  PubMed Central  Google Scholar 

  • Burns GW, Brooks KE, Spencer TE (2016) Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biol Reprod 94:56

    Article  PubMed  CAS  Google Scholar 

  • Cai J, Han Y, Ren H, Chen C, He D, Zhou L, Eisner GM, Asico LD, Jose PA, Zeng C (2013) Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol 5:227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capalbo A, Ubaldi FM, Cimadomo D, Noli L, Khalaf Y, Farcomeni A, Ilic D, Rienzi L (2016) MicroRNAs in spent blastocyst culture medium are derived from trophectoderm cells and can be explored for human embryo reproductive competence assessment. Fertil Steril 105:225–235.e221-223

    Article  CAS  PubMed  Google Scholar 

  • Capalbo A, Romanelli V, Patassini C, Poli M, Girardi L, Giancani A, Stoppa M, Cimadomo D, Ubaldi FM, Rienzi L (2018) Diagnostic efficacy of blastocoel fluid and spent media as sources of DNA for preimplantation genetic testing in standard clinical conditions. Fertil Steril 110:870–879.e875

    Article  CAS  PubMed  Google Scholar 

  • Desrochers LM, Bordeleau F, Reinhart-King CA, Cerione RA, Antonyak MA (2016) Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun 7:11958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dissanayake K, Nõmm M, Lättekivi F, Ressaissi Y, Godakumara K, Lavrits A, Midekessa G, Viil J, Bæk R, Jørgensen MM et al (2020) Individually cultured bovine embryos produce extracellular vesicles that have the potential to be used as non-invasive embryo quality markers. Theriogenology 149:104–116

    Article  CAS  PubMed  Google Scholar 

  • Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, Sadovsky Y (2012) The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod 18:417–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fereshteh Z, Schmidt SA, Al-Dossary AA, Accerbi M, Arighi C, Cowart J, Song JL, Green PJ, Choi K, Yoo S et al (2018) Murine oviductosomes (OVS) microRNA profiling during the estrous cycle: delivery of OVS-borne microRNAs to sperm where miR-34c-5p localizes at the centrosome. Sci Rep 8:16094

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ferraz M, Carothers A, Dahal R, Noonan MJ, Songsasen N (2019) Oviductal extracellular vesicles interact with the spermatozoon’s head and mid-piece and improves its motility and fertilizing ability in the domestic cat. Sci Rep 9:9484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gatien J, Mermillod P, Tsikis G, Bernardi O, Janati Idrissi S, Uzbekov R, Le Bourhis D, Salvetti P, Alminana C, Saint-Dizier M (2019) Metabolomic profile of oviductal extracellular vesicles across the estrous cycle in cattle. Int J Mol Sci 20:6339

    Article  CAS  PubMed Central  Google Scholar 

  • Giacomini E, Vago R, Sanchez AM, Podini P, Zarovni N, Murdica V, Rizzo R, Bortolotti D, Candiani M, Vigano P (2017) Secretome of in vitro cultured human embryos contains extracellular vesicles that are uptaken by the maternal side. Sci Rep 7:5210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Greening DW, Nguyen HP, Elgass K, Simpson RJ, Salamonsen LA (2016) Human endometrial exosomes contain hormone-specific cargo modulating trophoblast adhesive capacity: insights into endometrial-embryo interactions. Biol Reprod 94:38

    Article  PubMed  CAS  Google Scholar 

  • Gross N, Kropp J, Khatib H (2017) Sexual dimorphism of miRNAs secreted by bovine in vitro-produced embryos. Front Genet 8:39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Homer H, Rice GE, Salomon C (2017) Review: embryo- and endometrium-derived exosomes and their potential role in assisted reproductive treatments-liquid biopsies for endometrial receptivity. Placenta 54:89–94

    Article  CAS  PubMed  Google Scholar 

  • Jamaludin NA, Thurston LM, Witek KJ, Meikle A, Basatvat S, Elliott S, Hunt S, Andronowska A, Fazeli A (2019) Efficient isolation, biophysical characterisation and molecular composition of extracellular vesicles secreted by primary and immortalised cells of reproductive origin. Theriogenology 135:121–137

    Article  CAS  PubMed  Google Scholar 

  • Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A et al (2014) 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 289:3869–3875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Lee J, Lee TB, Jun JH (2019) Embryotrophic effects of extracellular vesicles derived from outgrowth embryos in pre- and peri-implantation embryonic development in mice. Mol Reprod Dev 86:187–196

    Article  CAS  PubMed  Google Scholar 

  • Koh YQ, Peiris HN, Vaswani K, Reed S, Rice GE, Salomon C, Mitchell MD (2016) Characterization of exosomal release in bovine endometrial intercaruncular stromal cells. Reprod Biol Endocrinol 14:78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kropp J, Khatib H (2015a) Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development. J Dairy Sci 98:6552–6563

    Article  CAS  PubMed  Google Scholar 

  • Kropp J, Khatib H (2015b) mRNA fragments in in vitro culture media are associated with bovine preimplantation embryonic development. Front Genet 6:273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kropp J, Salih SM, Khatib H (2014) Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front Genet 5:91

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kurian NK, Modi D (2019) Extracellular vesicle mediated embryo-endometrial cross talk during implantation and in pregnancy. J Assist Reprod Genet 36:189–198

    Article  PubMed  Google Scholar 

  • Kusama K, Nakamura K, Bai R, Nagaoka K, Sakurai T, Imakawa K (2018) Intrauterine exosomes are required for bovine conceptus implantation. Biochem Biophys Res Commun 495:1370–1375

    Article  CAS  PubMed  Google Scholar 

  • Laezer I, Palma-Vera SE, Liu F, Frank M, Trakooljul N, Vernunft A, Schoen J, Chen S (2020) Dynamic profile of EVs in porcine oviductal fluid during the periovulatory period. Reproduction 159:371–382

    Article  CAS  PubMed  Google Scholar 

  • Lange-Consiglio A, Perrini C, Albini G, Modina S, Lodde V, Orsini E, Esposti P, Cremonesi F (2017) Oviductal microvesicles and their effect on in vitro maturation of canine oocytes. Reproduction 154:167–180

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, El Andaloussi S, Wood MJA (2012) Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21:R125–R134

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Oh HJ, Kim MJ, Lee BC (2020) Exosomes derived from oviduct cells mediate the EGFR/MAPK signaling pathway in cumulus cells. J Cell Physiol 235:1386–1404

    Article  CAS  PubMed  Google Scholar 

  • Lin X, Beckers E, Mc Cafferty S, Gansemans Y, Joanna Szymanska K, Chaitanya Pavani K, Catani JP, Van Nieuwerburgh F, Deforce D, De Sutter P et al (2019) Bovine embryo-secreted microRNA-30c is a potential non-invasive biomarker for hampered preimplantation developmental competence. Front Genet 10:315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopera-Vasquez R, Hamdi M, Fernandez-Fuertes B, Maillo V, Beltran-Brena P, Calle A, Redruello A, Lopez-Martin S, Gutierrez-Adan A, Yanez-Mo M et al (2016) Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 11:e0148083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lopera-Vasquez R, Hamdi M, Maillo V, Gutierrez-Adan A, Bermejo-Alvarez P, Ramirez MA, Yanez-Mo M, Rizos D (2017) Effect of bovine oviductal extracellular vesicles on embryo development and quality in vitro. Reproduction 153(4):461–470

    Article  CAS  PubMed  Google Scholar 

  • Lv C, Yu WX, Wang Y, Yi DJ, Zeng MH, Xiao HM (2018) MiR-21 in extracellular vesicles contributes to the growth of fertilized eggs and embryo development in mice. Biosci Rep 38(4):BSR20180036

    Article  PubMed  PubMed Central  Google Scholar 

  • Macaulay AD, Gilbert I, Caballero J, Barreto R, Fournier E, Tossou P, Sirard MA, Clarke HJ, Khandjian EW, Richard FJ et al (2014) The gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod 91:90

    Article  PubMed  CAS  Google Scholar 

  • Machtinger R, Laurent LC, Baccarelli AA (2016) Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum Reprod Update 22:182–193

    CAS  PubMed  Google Scholar 

  • Marin D, Scott RT Jr (2018) Extracellular vesicles: a promising tool for assessment of embryonic competence. Curr Opin Obstet Gynecol 30:171–178

    Article  PubMed  Google Scholar 

  • Mellisho EA, Velasquez AE, Nunez MJ, Cabezas JG, Cueto JA, Fader C, Castro FO, Rodriguez-Alvarez L (2017) Identification and characteristics of extracellular vesicles from bovine blastocysts produced in vitro. PLoS One 12:e0178306

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakamura K, Kusama K, Bai R, Sakurai T, Isuzugawa K, Godkin JD, Suda Y, Imakawa K (2016) Induction of IFNT-stimulated genes by conceptus-derived exosomes during the attachment period. PLoS One 11:e0158278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakano S, Yamamoto S, Okada A, Nakajima T, Sato M, Takagi T, Tomooka Y (2017) Role of extracellular vesicles in the interaction between epithelial and mesenchymal cells during oviductal ciliogenesis. Biochem Biophys Res Commun 483:245–251

    Article  CAS  PubMed  Google Scholar 

  • Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA (2013) Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS One 8:e58502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pallinger E, Bognar Z, Bodis J, Csabai T, Farkas N, Godony K, Varnagy A, Buzas E, Szekeres-Bartho J (2017) A simple and rapid flow cytometry-based assay to identify a competent embryo prior to embryo transfer. Sci Rep 7:39927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pallinger E, Bognar Z, Bogdan A, Csabai T, Abraham H, Szekeres-Bartho J (2018) PIBF+ extracellular vesicles from mouse embryos affect IL-10 production by CD8+ cells. Sci Rep 8:4662

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parks JC, McCallie BR, Patton AL, Al-Safi ZA, Polotsky AJ, Griffin DK, Schoolcraft WB, Katz-Jaffe MG (2018) The impact of infertility diagnosis on embryo-endometrial dialogue. Reproduction 155:543–552

    Article  CAS  PubMed  Google Scholar 

  • Pavani KC, Hendrix A, Van Den Broeck W, Couck L, Szymanska K, Lin X, De Koster J, Van Soom A, Leemans B (2018) Isolation and characterization of functionally active extracellular vesicles from culture medium conditioned by bovine embryos in vitro. Int J Mol Sci 20:38

    Article  PubMed Central  CAS  Google Scholar 

  • Pavani KC, Lin X, Hamacher J, Broeck WVD, Couck L, Peelman L, Hendrix A, Van Soom A (2020) The separation and characterization of extracellular vesicles from medium conditioned by bovine embryos. Int J Mol Sci 21:2942

    Article  CAS  PubMed Central  Google Scholar 

  • Qiao F, Ge H, Ma X, Zhang Y, Zuo Z, Wang M, Zhang Y, Wang Y (2018) Bovine uterus-derived exosomes improve developmental competence of somatic cell nuclear transfer embryos. Theriogenology 114:199–205

    Article  PubMed  Google Scholar 

  • Qu P, Qing S, Liu R, Qin H, Wang W, Qiao F, Ge H, Liu J, Zhang Y, Cui W et al (2017) Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS One 12:e0174535

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qu P, Zhao Y, Wang R, Zhang Y, Li L, Fan J, Liu E (2018) Extracellular vesicles derived from donor oviduct fluid improved birth rates after embryo transfer in mice. Reprod Fertil Dev 31(2):324–332

    Article  CAS  Google Scholar 

  • Rosenbluth EM, Shelton DN, Wells LM, Sparks AE, Van Voorhis BJ (2014) Human embryos secrete microRNAs into culture media—a potential biomarker for implantation. Fertil Steril 101:1493–1500

    Article  CAS  PubMed  Google Scholar 

  • Saadeldin IM, Kim SJ, Choi YB, Lee BC (2014) Improvement of cloned embryos development by co-culturing with parthenotes: a possible role of exosomes/microvesicles for embryos paracrine communication. Cell Reprogram 16:223–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saadeldin IM, Oh HJ, Lee BC (2015) Embryonic-maternal cross-talk via exosomes: potential implications. Stem Cells Cloning 8:103–107

    PubMed  PubMed Central  Google Scholar 

  • Saint-Dizier M, Marnier C, Tahir MZ, Grimard B, Thoumire S, Chastant-Maillard S, Reynaud K (2014) OVGP1is expressed in the canine oviduct at the time and place of oocyte maturation and fertilization. Mol Reprod Dev 81:972–982

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Ribas I, Diaz-Gimeno P, Quinonero A, Ojeda M, Larreategui Z, Ballesteros A, Dominguez F (2019) NGS analysis of human embryo culture media reveals miRNAs of extra embryonic origin. Reprod Sci 26:214–222

    Article  CAS  PubMed  Google Scholar 

  • Simon B, Bolumar D, Amadoz A, Jimenez-Almazan J, Valbuena D, Vilella F, Moreno I (2020) Identification and characterization of extracellular vesicles and its DNA cargo secreted during murine embryo development. Genes (Basel) 11:203

    Article  CAS  Google Scholar 

  • Tan Q, Shi S, Liang J, Zhang X, Cao D, Wang Z (2020) MicroRNAs in small extracellular vesicles indicate successful embryo implantation during early pregnancy. Cell 9:645

    Article  CAS  Google Scholar 

  • Taqi MO, Saeed-Zidane M, Gebremedhn S, Salilew-Wondim D, Khadrawy O, Rings F, Neuhoff C, Hoelker M, Schellander K, Tesfaye D (2019) Sexual dimorphic expression and release of transcription factors in bovine embryos exposed to oxidative stress. Mol Reprod Dev 86(12):2005–2019

    Article  CAS  PubMed  Google Scholar 

  • Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J et al (2014) Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res 24:766–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    Article  CAS  PubMed  Google Scholar 

  • Vilella F, Moreno-Moya JM, Balaguer N, Grasso A, Herrero M, Martinez S, Marcilla A, Simon C (2015) Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. Development 142:3210–3221

    Article  CAS  PubMed  Google Scholar 

  • Vyas P, Balakier H, Librach CL (2019) Ultrastructural identification of CD9 positive extracellular vesicles released from human embryos and transported through the zona pellucida. Syst Biol Reprod Med 65:273–280

    Article  PubMed  Google Scholar 

  • Wang X, Tian F, Chen C, Feng Y, Sheng X, Guo Y, Ni H (2019) Exosome-derived uterine microRNAs isolated from cows with endometritis impede blastocyst development. Reprod Biol 19:204–209

    Article  CAS  PubMed  Google Scholar 

  • Wei Z, Batagov AO, Carter DR, Krichevsky AM (2016) Fetal bovine serum RNA interferes with the cell culture derived extracellular RNA. Sci Rep 6:31175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willms E, Johansson HJ, Mäger I, Lee Y, Blomberg KEM, Sadik M, Alaarg A, Smith CIE, Lehtiö J, El Andaloussi S et al (2016) Cells release subpopulations of exosomes with distinct molecular and biological properties. Sci Rep 6:22519

    Article  CAS  PubMed  PubMed Central  Google 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

    Article  PubMed  Google Scholar 

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Acknowledgments

Conflict of interest: The author declares no conflict of interest.

Funding: The author received no specific funding for this work.

Disclosure statement: This article does not contain any studies with human or animal participants.

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Authors and Affiliations

  1. Department of Physiology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt

    Islam M. Saadeldin

  2. Department of Animal Production, King Saud University, Riyadh, Saudi Arabia

    Islam M. Saadeldin

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  1. Islam M. Saadeldin
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Correspondence to Islam M. Saadeldin .

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Editors and Affiliations

  1. Department of Biochemistry, ESC Research Unit, Faculty of Science King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia

    Faisal A. Alzahrani

  2. Department of Animal Production, King Saud University, Riyadh, Saudi Arabia

    Islam M. Saadeldin

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Saadeldin, I.M. (2021). Extracellular Vesicles Mediate the Embryonic-Maternal Paracrine Communication. In: Alzahrani, F.A., Saadeldin, I.M. (eds) Role of Exosomes in Biological Communication Systems. Springer, Singapore. https://doi.org/10.1007/978-981-15-6599-1_3

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