Role of extracellular vesicles during oocyte maturation and early embryo development
A. C. F. C. M. de Ávila A and J. C. da Silveira A B
+ Author Affiliations
- Author Affiliations
A Department of Veterinary Medicine, Faculty of Animal Sciences and Food Engineering, University of São Paulo, Avenida Duque de Caxias Norte 225, 13635-900 Pirassununga, São Paulo, Brazil.
B Corresponding author. Email: julianodasilveira@usp.br
Reproduction, Fertility and Development 32(2) 56-64 https://doi.org/10.1071/RD19389
Published: 2 December 2019
Abstract
The follicle is a dynamic microenvironment in the ovary where the oocyte develops. Intercellular communication between somatic cells and the oocyte inside the follicle is essential to generate a competent gamete. Extracellular vesicles are nanoparticles secreted by cells that mediate cell-to-cell communication in the follicle microenvironment and can be obtained from the follicular fluid. These extracellular vesicles have been studied as biomarkers and supplementation tools to mimic physiological conditions during assisted reproductive techniques because they are vehicles of bioactive molecules. Therefore, this paper reviews the importance of changes in the ovarian follicle and the effects of extracellular vesicles from follicular fluid during oocyte maturation and early embryo development. Finally, we propose that is important to consider the source of the extracellular vesicles to improve diagnostic methods and to increase in vitro embryo production.
Additional keywords: exosomes, follicle, in vitro embryo production.
References
Adams, G. P., Jaiswal, R., Singh, J., and Malhi, P. (2008). Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 69, 72–80.| Progress in understanding ovarian follicular dynamics in cattle.Crossref | GoogleScholarGoogle Scholar | 17980420PubMed |
Albertini, D. F., and Rider, V. (1994). Patterns of intercellular connectivity in the mammalian cumulus–oocyte complex. Microsc. Res. Tech. 27, 125–133.
| Patterns of intercellular connectivity in the mammalian cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 8123905PubMed |
Albertini, D. F., Combelles, C. M. H., Benecchi, E., and Carabatsos, M. J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–653.
| Cellular basis for paracrine regulation of ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 11427152PubMed |
Andrade, G. M., Meirelles, F. V., Perecin, F., and da Silveira, J. C. (2017). Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle. Reprod. Domest. Anim. 52, 1036–1045.
| Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 28691325PubMed |
Aparicio, I. M., Garcia-Herreros, M., O’Shea, L. C., Hensey, C., Lonergan, P., and Fair, T. (2011). Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol. Reprod. 84, 910–921.
| Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 21228216PubMed |
Bao, B., and Garverick, H. A. (1998). Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J. Anim. Sci. 76, 1903–1921.
| Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review.Crossref | GoogleScholarGoogle Scholar | 9690647PubMed |
Bender, K., Walsh, S., Evans, A. C. O., Fair, T., and Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–1055.
| Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows.Crossref | GoogleScholarGoogle Scholar | 20385782PubMed |
Bisinotto, R. S., Chebel, R. C., and Santos, J. E. P. (2010). Follicular wave of the ovulatory follicle and not cyclic status influences fertility of dairy cows. J. Dairy Sci. 93, 3578–3587.
| Follicular wave of the ovulatory follicle and not cyclic status influences fertility of dairy cows.Crossref | GoogleScholarGoogle Scholar | 20655426PubMed |
Cocucci, E., Racchetti, G., and Meldolesi, J. (2009). Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43–51.
| Shedding microvesicles: artefacts no more.Crossref | GoogleScholarGoogle Scholar | 19144520PubMed |
da Silveira, J. C., Veeramachaneni, D. N. R., 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. Biol. Reprod. 86, 71.
| Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 22116803PubMed |
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. Reprod. Biol. Endocrinol. 12, 44.
| Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare.Crossref | GoogleScholarGoogle Scholar | 24884710PubMed |
da Silveira, J. C., Winger, Q. A., Bouma, G. J., and Carnevale, E. M. (2015). Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-β signalling during follicle development in the mare. Reprod. Fertil. Dev. 27, 897–905.
| Effects of age on follicular fluid exosomal microRNAs and granulosa cell transforming growth factor-β signalling during follicle development in the mare.Crossref | GoogleScholarGoogle Scholar | 25945781PubMed |
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, e0179451.
| Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 28922408PubMed |
Dalanezi, F. M., Garcia, H. D. M., Ferrazza, R. A., Franchi, F. F., Fontes, P. K., Castilho, A. C. S., Nogueira, M. F. G., Schmidt, E. M. S., Sartori, R., and Ferreira, J. C. P. (2019). Extracellular vesicles of follicular fluid from heat-stressed cows modify the gene expression of in vitro-matured oocytes. Anim. Reprod. Sci. 205, 94–104.
| Extracellular vesicles of follicular fluid from heat-stressed cows modify the gene expression of in vitro-matured oocytes.Crossref | GoogleScholarGoogle Scholar |
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. (2019). Estrous cycle impacts miRNA content in extracellular vesicles that modulate bovine cumulus cells transcripts during in vitro maturation. Biol. Reprod. , ioz177.
| Estrous cycle impacts miRNA content in extracellular vesicles that modulate bovine cumulus cells transcripts during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Denicol, A. C., Lopes, G., Mendonça, L. G. D., Rivera, F. A., Guagnini, F., Perez, R. V., Lima, J. R., Bruno, R. G. S., Santos, J. E. P., and Chebel, R. C. (2012). Low progesterone concentration during the development of the first follicular wave reduces pregnancy per insemination of lactating dairy cows. J. Dairy Sci. 95, 1794–1806.
| Low progesterone concentration during the development of the first follicular wave reduces pregnancy per insemination of lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 22459828PubMed |
Dieleman, S. J., Kruip, T. A. M., Fontijne, P., Jong, W. H. R., and Van der Weyden, G. C. (1983). Changes in oestradiol, progesterone and testosterone concentrations in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone. J. Endocrinol. 97, 31–42.
| Changes in oestradiol, progesterone and testosterone concentrations in follicular fluid and in the micromorphology of preovulatory bovine follicles relative to the peak of luteinizing hormone.Crossref | GoogleScholarGoogle Scholar | 6682433PubMed |
Diez-Fraile, A., Lammens, T., Tilleman, K., Witkowski, W., Verhasselt, B., De Sutter, P., Benoit, Y., Espeel, M., and D’Herde, K. (2014). Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization. Hum. Fertil. (Camb.) 17, 90–98.
| Age-associated differential microRNA levels in human follicular fluid reveal pathways potentially determining fertility and success of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 24684237PubMed |
Edson, M. A., Nagaraja, A. K., and Matzuk, M. M. (2009). The mammalian ovary from genesis to revelation. Endocr. Rev. 30, 624–712.
| The mammalian ovary from genesis to revelation.Crossref | GoogleScholarGoogle Scholar | 19776209PubMed |
Eyestone, W. H., and First, N. L. (1989). Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium. J. Reprod. Fertil. 85, 715–720.
| Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium.Crossref | GoogleScholarGoogle Scholar | 2704004PubMed |
Fortune, J. E. (1986). Bovine theca and granulosa cells interact to promote androgen production. Biol. Reprod. 35, 292–299.
| Bovine theca and granulosa cells interact to promote androgen production.Crossref | GoogleScholarGoogle Scholar | 3768456PubMed |
Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
| Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.Crossref | GoogleScholarGoogle Scholar | 18175787PubMed |
Gimenes, L. U., Ferraz, M. L., Fantinato-Neto, P., Chiaratti, M. R., Mesquita, L. G., Sá Filho, M. F., Meirelles, F. V., Trinca, L. A., Rennó, F. P., Watanabe, Y. F., and Baruselli, P. S. (2015). The interval between the emergence of pharmacologically synchronized ovarian follicular waves and ovum pickup does not significantly affect in vitro embryo production in Bos indicus, Bos taurus, and Bubalus bubalis. Theriogenology 83, 385–393.
| The interval between the emergence of pharmacologically synchronized ovarian follicular waves and ovum pickup does not significantly affect in vitro embryo production in Bos indicus, Bos taurus, and Bubalus bubalis.Crossref | GoogleScholarGoogle Scholar | 25447149PubMed |
Hagemann, L. J., Beaumont, S. E., Berg, M., Donnison, M. J., Ledgard, A., Peterson, A. J., Schurmann, A., and Tervit, H. R. (1999). Development during single IVP of bovine oocytes from dissected follicles: Interactive effects of estrous cycle stage, follicle size and atresia. Mol. Reprod. Dev. 53, 451–458.
| Development during single IVP of bovine oocytes from dissected follicles: Interactive effects of estrous cycle stage, follicle size and atresia.Crossref | GoogleScholarGoogle Scholar | 10398421PubMed |
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. Sci. Rep. 9, 12851.
| Extracellular vesicle-coupled miRNA profiles in follicular fluid of cows with divergent post-calving metabolic status.Crossref | GoogleScholarGoogle Scholar | 31492906PubMed |
Hung, W.-T., Hong, X., Christenson, L. K., and Mcginnis, L. K. (2015). Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biol. Reprod. 93, 117.
| Extracellular vesicles from bovine follicular fluid support cumulus expansion.Crossref | GoogleScholarGoogle Scholar | 26423123PubMed |
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. Biol. Reprod. 97, 644–655.
| Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation.Crossref | GoogleScholarGoogle Scholar | 29025042PubMed |
Hyttel, P. (2010). Gametogenesis. In ‘Essentials of Domestic Animals Embryology’. (Eds P. Hyttel, F. Sinowatz, and M. Vejlsted.) pp. 32–55 (Saunders Elsevier: Toronto.)
Hyttel, P., Fair, T., Callesen, H., and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
| Oocyte growth, capacitation and final maturation in cattle.Crossref | GoogleScholarGoogle Scholar |
Ireland, J. J., and Roche, J. F. (1983). Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins. Endocrinology 112, 150–156.
| Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins.Crossref | GoogleScholarGoogle Scholar | 6291914PubMed |
Ireland, J. J., Coulson, P. B., and Murphree, R. L. (1979). Follicular development during four stages of the estrous cycle of beef cattle. J. Anim. Sci. 49, 1261–1269.
| Follicular development during four stages of the estrous cycle of beef cattle.Crossref | GoogleScholarGoogle Scholar | 575533PubMed |
Knight, P. G., and Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191–206.
| TGF-beta superfamily members and ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 16885529PubMed |
Kruip, T. A. M., and Dieleman, S. J. (1985). Steroid hormone concentration in the fluid of bovine follicles relative to size, quality and stage of the oestrus cycle. Theriogenology 24, 395–408.
| Steroid hormone concentration in the fluid of bovine follicles relative to size, quality and stage of the oestrus cycle.Crossref | GoogleScholarGoogle Scholar |
Leroy, J. L. M. R., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E. J., and Kruif, A. (2004a). Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Anim. Reprod. Sci. 80, 201–211.
| Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Leroy, J. L. M. R., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E. J., Dewulf, J., and Kruif, A. (2004b). Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 62, 1131–1143.
| Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum.Crossref | GoogleScholarGoogle Scholar |
Lötvall, J., Hill, A. F., Hochberg, F., Buzás, E. I., Di Vizio, D., Gardiner, C., Gho, Y. S., Kurochkin, I. V., Mathivanan, S., Quesenberry, P., Sahoo, S., Tahara, H., Wauben, M. H., Witwer, K. W., and Théry, C. (2014). Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles 3, 26913.
| Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles.Crossref | GoogleScholarGoogle Scholar | 25536934PubMed |
Macaulay, A. D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., Sirard, M.-A., Clarke, H. J., Khandjian, É. W., Richard, F. J., Hyttel, P., and Robert, C. (2014). The gametic synapse: RNA transfer to the bovine oocyte. Biol. Reprod. 91, 90.
| The gametic synapse: RNA transfer to the bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 25143353PubMed |
Martinez, R. M., Liang, L., Racowsky, C., Dioni, L., Mansur, A., Adir, M., Bollati, V., Baccarelli, A. A., Hauser, R., and Machtinger, R. (2018). Extracellular microRNAs profile in human follicular fluid and IVF outcomes. Sci. Rep. 8, 17036.
| Extracellular microRNAs profile in human follicular fluid and IVF outcomes.Crossref | GoogleScholarGoogle Scholar | 30451969PubMed |
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. Fertil. Steril. 112, 387–396.e3.
| Body mass index in relation to extracellular vesicle-linked microRNAs in human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 31146888PubMed |
Mathivanan, S., Ji, H., and Simpson, R. J. (2010). Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73, 1907–1920.
| Exosomes: extracellular organelles important in intercellular communication.Crossref | GoogleScholarGoogle Scholar | 20601276PubMed |
Matoba, S., Bender, K., Fahey, A. G., Mamo, S., Brennan, L., Lonergan, P., and Fair, T. (2014). Predictive value of bovine follicular components as markers of oocyte developmental potential. Reprod. Fertil. Dev. 26, 337–345.
| Predictive value of bovine follicular components as markers of oocyte developmental potential.Crossref | GoogleScholarGoogle Scholar | 23514964PubMed |
Matsuda, F., Inoue, N., Manabe, N., and Ohkura, S. (2012). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev. 58, 44–50.
| Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells.Crossref | GoogleScholarGoogle Scholar | 22450284PubMed |
Matsuno, Y., Onuma, A., Fujioka, Y. A., Yasuhara, K., Fujii, W., Naito, K., and Sugiura, K. (2017). Effects of exosome-like vesicles on cumulus expansion in pigs in vitro. J. Reprod. Dev. 63, 51–58.
| Effects of exosome-like vesicles on cumulus expansion in pigs in vitro.Crossref | GoogleScholarGoogle Scholar | 28163264PubMed |
Molyneaux, K. A., Stallock, J., Schaible, K., and Wylie, C. (2001). Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 240, 488–498.
| Time-lapse analysis of living mouse germ cell migration.Crossref | GoogleScholarGoogle Scholar | 11784078PubMed |
Nasser, L. F., Filho, M. F. S., Reis, E. L., Rezende, C. R., Mapletoft, R. J., Bó, G. A., and Baruselli, P. S. (2011). Exogenous progesterone enhances ova and embryo quality following superstimulation of the first follicular wave in Nelore (Bos indicus) donors. Theriogenology 76, 320–327.
| Exogenous progesterone enhances ova and embryo quality following superstimulation of the first follicular wave in Nelore (Bos indicus) donors.Crossref | GoogleScholarGoogle Scholar | 21496903PubMed |
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. Sci. Rep. 6, 25486.
| Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles.Crossref | GoogleScholarGoogle Scholar | 27158133PubMed |
O’Brien, Y., Wingfield, M., and O’Shea, L. C. (2019). Anti-Müllerian hormone and progesterone levels in human follicular fluid are predictors of embryonic development. Reprod. Biol. Endocrinol. 17, 47.
| 31217014PubMed |
O’Gorman, A., Wallace, M., Cottell, E., Gibney, M. J., McAuliffe, F. M., Wingfield, M., and Brennan, L. (2013). Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence. Reproduction 146, 389–395.
| Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 23886995PubMed |
O’Shea, L. C., Mehta, J., Lonergan, P., Hensey, C., and Fair, T. (2012). Developmental competence in oocytes and cumulus cells: candidate genes and networks. Syst Biol Reprod Med 58, 88–101.
| Developmental competence in oocytes and cumulus cells: candidate genes and networks.Crossref | GoogleScholarGoogle Scholar | 22313243PubMed |
O’Shea, L. C., Daly, E., Hensey, C., and Fair, T. (2017). ATRX is a novel progesterone-regulated protein and biomarker of low developmental potential in mammalian oocytes. Reproduction 153, 671–682.
| ATRX is a novel progesterone-regulated protein and biomarker of low developmental potential in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 28250240PubMed |
Orsi, N. M., and Reischl, J. B. (2007). Mammalian embryo co-culture: trials and tribulations of a misunderstood method. Theriogenology 67, 441–458.
| Mammalian embryo co-culture: trials and tribulations of a misunderstood method.Crossref | GoogleScholarGoogle Scholar | 17118433PubMed |
Orsi, N. M., Gopichandran, N., Leese, H. J., Picton, H. M., and Harris, S. E. (2005). Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle. Reproduction 129, 219–228.
| Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 15695616PubMed |
Pan, B. T., Teng, K., Wu, C., Adam, M., and Johnstone, R. M. (1985). Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol. 101, 942–948.
| Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes.Crossref | GoogleScholarGoogle Scholar | 2993317PubMed |
Peluso, J. J. (2006). Multiplicity of progesterone’s actions and receptors in the mammalian ovary. Biol. Reprod. 75, 2–8.
| Multiplicity of progesterone’s actions and receptors in the mammalian ovary.Crossref | GoogleScholarGoogle Scholar | 16452458PubMed |
Raposo, G., and Stoorvogel, W. (2013). Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373–383.
| Extracellular vesicles: exosomes, microvesicles, and friends.Crossref | GoogleScholarGoogle Scholar | 23420871PubMed |
Reader, K. L., Stanton, J.-A., and Juengel, J. L. (2017). The role of oocyte organelles in determining developmental competence. Biology (Basel) 6, 35.
| The role of oocyte organelles in determining developmental competence.Crossref | GoogleScholarGoogle Scholar |
Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., De la Fuente, J., and Gutiérrez-Adán, A. (2002a). Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol. Reprod. 66, 589–595.
| Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 11870062PubMed |
Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002b). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 11803560PubMed |
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. Reprod. Fertil. Dev. 31, 888–897.
| Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock.Crossref | GoogleScholarGoogle Scholar | 30760387PubMed |
Saadeldin, I. M., Oh, H. J., and Lee, B. C. (2015). Embryonic–maternal cross-talk via exosomes: potential implications. Stem Cells Cloning 8, 103–107.
| 26185458PubMed |
Santonocito, M., Vento, M., Guglielmino, M. R., Battaglia, R., Wahlgren, J., Ragusa, M., Barbagallo, D., Borzí, 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. Fertil. Steril. 102, 1751–1761.e1.
| Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation.Crossref | GoogleScholarGoogle Scholar | 25241362PubMed |
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.
| Subclinical mastitis interferes with ovulation, oocyte and granulosa cell quality in dairy cows.Crossref | GoogleScholarGoogle Scholar | 30036745PubMed |
Satitmanwiwat, S., Changsangfah, C., Faisaikarm, T., Promthep, K., Thammawung, S., Saikhun, K., and Kaeoket, K. (2017). Proteome profiling of bovine follicular fluid-specific proteins and their effect on in vitro embryo development. J. Vet. Med. Sci. 79, 842–847.
| Proteome profiling of bovine follicular fluid-specific proteins and their effect on in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 28260700PubMed |
Scaramuzzi, R. J., Baird, D. T., Campbell, B. K., Driancourt, M. A., Dupont, J., Fortune, J. E., Gilchrist, R. B., Martin, G. B., McNatty, K. P., McNeilly, A. S., Monget, P., Monniaux, D., Viñoles, C., and Webb, R. (2011). Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod. Fertil. Dev. 23, 444–467.
| Regulation of folliculogenesis and the determination of ovulation rate in ruminants.Crossref | GoogleScholarGoogle Scholar | 21426863PubMed |
Serta, R. T., Michalopoulos, J., Seibel, M. M., and Kiessling, A. A. (1995). The developmental potential of mouse oocytes matured in serum-free culture conditions. Hum. Reprod. 10, 1810–1815.
| The developmental potential of mouse oocytes matured in serum-free culture conditions.Crossref | GoogleScholarGoogle Scholar | 8582987PubMed |
Simpson, R. J., Jensen, S. S., and Lim, J. W. E. (2008). Proteomic profiling of exosomes: current perspectives. Proteomics 8, 4083–4099.
| Proteomic profiling of exosomes: current perspectives.Crossref | GoogleScholarGoogle Scholar | 18780348PubMed |
Sirard, M. A. (2016). Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle. Theriogenology 86, 54–61.
| Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle.Crossref | GoogleScholarGoogle Scholar | 27158126PubMed |
Sirard, M. A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
| Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar | 16256189PubMed |
Skog, J., Würdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Curry, W. T., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470–1476.
| Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers.Crossref | GoogleScholarGoogle Scholar | 19011622PubMed |
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. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: Implications for bovine oocyte developmental competence. PLoS One 8, e78505.
| Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: Implications for bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |
Stremersch, S., Smedt, S. C., and Raemdonck, K. (2016). Therapeutic and diagnostic applications of extracellular vesicles. J. Control. Release 244, 167–183.
| Therapeutic and diagnostic applications of extracellular vesicles.Crossref | GoogleScholarGoogle Scholar | 27491882PubMed |
Subra, C., Laulagnier, K., Perret, B., and Record, M. (2007). Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 89, 205–212.
| Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies.Crossref | GoogleScholarGoogle Scholar | 17157973PubMed |
Tannetta, D., Dragovic, R., Alyahyaei, Z., and Southcombe, J. (2014). Extracellular vesicles and reproduction-promotion of successful pregnancy. Cell. Mol. Immunol. 11, 548–563.
| Extracellular vesicles and reproduction-promotion of successful pregnancy.Crossref | GoogleScholarGoogle Scholar | 24954226PubMed |
Taylor, D. D., and Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13–21.
| MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer.Crossref | GoogleScholarGoogle Scholar | 18589210PubMed |
Théry, C., Zitvogel, L., and Amigorena, S. (2002). Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569–579.
| Exosomes: composition, biogenesis and function.Crossref | GoogleScholarGoogle Scholar | 12154376PubMed |
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., Beckham, C., et al. (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. J. Extracell. Vesicles 7, 1535750.
| 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.Crossref | GoogleScholarGoogle Scholar | 30637094PubMed |
Thompson, J. G., and Peterson, A. J. (2000). Bovine embryo culture in vitro: new developments and post-transfer consequences. Hum. Reprod. 15, 59–67.
| Bovine embryo culture in vitro: new developments and post-transfer consequences.Crossref | GoogleScholarGoogle Scholar | 11263538PubMed |
Urrego, R., Rodriguez-Osorio, N., and Niemann, H. (2014). Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle. Epigenetics 9, 803–815.
| Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle.Crossref | GoogleScholarGoogle Scholar | 24709985PubMed |
Ursely, J., and Leymarie, P. (1979). Varying response to luteinizing hormone of two luteal cell types isolated from bovine corpus luteum. J. Endocrinol. 83, 303–310.
| Varying response to luteinizing hormone of two luteal cell types isolated from bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 395265PubMed |
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. Nat. Cell Biol. 9, 654–659.
| Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.Crossref | GoogleScholarGoogle Scholar | 17486113PubMed |
van Niel, G., D’Angelo, G., and Raposo, G. (2018). Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell. Biol. 19, 213–228.
| Shedding light on the cell biology of extracellular vesicles.Crossref | GoogleScholarGoogle Scholar | 29339798PubMed |
Vassena, R., Mapletoft, R. J., Allodi, S., Singh, J., and Adams, G. P. (2003). Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology 60, 923–932.
| Morphology and developmental competence of bovine oocytes relative to follicular status.Crossref | GoogleScholarGoogle Scholar | 12935869PubMed |
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. Nat. Commun. 4, 2980.
| Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs.Crossref | GoogleScholarGoogle Scholar | 24356509PubMed |
Watson, A. J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85, E1–E3.
| Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence.Crossref | GoogleScholarGoogle Scholar | 17322120PubMed |
Witwer, K. W., Buzás, E. I., Bemis, L. T., Bora, A., Lässer, C., Lötvall, J., Nolte-’t Hoen, E. N., Piper, M. G., Sivaraman, S., Skog, J., Théry, C., Wauben, M. H., and Hochberg, F. (2013). Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles 2, 20360.
| Standardization of sample collection, isolation and analysis methods in extracellular vesicle research.Crossref | GoogleScholarGoogle Scholar |
Yang, M. Y., and Fortune, J. E. (2008). The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol. Reprod. 78, 1153–1161.
| The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes.Crossref | GoogleScholarGoogle Scholar | 18305225PubMed |
Yoshioka, Y., Kosaka, N., Konishi, Y., Ohta, H., Okamoto, H., Sonoda, H., Nonaka, R., Yamamoto, H., Ishii, H., Mori, M., Furuta, K., Nakajima, T., Hayashi, H., Sugisaki, H., Higashimoto, H., Kato, T., Takeshita, F., and Ochiya, T. (2014). Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen. Nat. Commun. 5, 3591.
| Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen.Crossref | GoogleScholarGoogle Scholar | 24710016PubMed |
