Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T23:18:36.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Extracellular vesicles from seminal plasma improved development of in vitro-fertilized mouse embryos

Published online by Cambridge University Press:  22 June 2022

Yefei Ma Open the ORCID record for Yefei Ma [Opens in a new window] ,
Jingyi Wang ,
Fang Qiao  and
Yongsheng Wang
Yefei Ma*
Affiliation:
Department of Obstetrics and Gynecology, The Reproductive Medicine Center, Tangdu Hospital, Air Force Medical University, Xi’an, Shaanxi, China College of Veterinary Medicine, Northwest A&F University, Key Laboratory of Animal Biotechnology of the Ministry of Agriculture, Yangling, Shaanxi Province, China
Jingyi Wang
Affiliation:
Department of Obstetrics and Gynecology, The Reproductive Medicine Center, Tangdu Hospital, Air Force Medical University, Xi’an, Shaanxi, China
Fang Qiao
Affiliation:
College of Veterinary Medicine, Northwest A&F University, Key Laboratory of Animal Biotechnology of the Ministry of Agriculture, Yangling, Shaanxi Province, China Xi’an Angel Maternity Hospital, Xi’an, Shaanxi, China
Yongsheng Wang*
Affiliation:
College of Veterinary Medicine, Northwest A&F University, Key Laboratory of Animal Biotechnology of the Ministry of Agriculture, Yangling, Shaanxi Province, China
*
Authors for correspondence: Yefei Ma, Department of Obstetrics and Gynecology, The Reproductive Medicine Center, Tangdu Hospital, Air Force Medical University, Xi’an, Shaanxi, China. E-mail: [email protected]; Yongsheng Wang. Xi’an Angel Maternity Hospital, Xi’an, Shaanxi, China. E-mail: [email protected]
Authors for correspondence: Yefei Ma, Department of Obstetrics and Gynecology, The Reproductive Medicine Center, Tangdu Hospital, Air Force Medical University, Xi’an, Shaanxi, China. E-mail: [email protected]; Yongsheng Wang. Xi’an Angel Maternity Hospital, Xi’an, Shaanxi, China. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In vitro fertilization (IVF) has wide application in human infertility and animal breeding. It is also used for research on reproduction, fertility and development. However, IVF embryos are still inferior to their in vivo counterparts. Some substances in seminal plasma appear to have important roles in embryo development, and during the traditional IVF procedure, the seminal plasma is washed away. In this study, extracellular vesicles (EVs) were concentrated from seminal plasma by ultracentrifugation, visualized using transmission electron microscopy, and particle size distributions and concentrations were determined with a NanoSight particle analyzer. We found particles of various sizes in the seminal plasma, the majority having diameters ranging from 100 to 200 nm and concentrations of 6.07 × 1010 ± 2.91 × 109 particles/ml. Addition of seminal plasma EVs (SP-EVs) to the IVF medium with mouse oocytes and sperm significantly increased the rate of blastocyst formation and the inner cell mass (ICM)/trophectoderm (TE) cell ratio, and reduced the apoptosis of blastocysts. Our findings provide new insights into the role of seminal plasma EVs in mediating embryo development and it suggests that SP-EVs may be used to improve the developmental competence of IVF embryos, which has important significance for assisted reproduction in animals and humans.

Keywords

Embryo developmentExtracellular vesiclesIn vitro fertilizationMiceSemen plasma
Type
Research Article
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 619 - 624
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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
Barceló, M., Mata, A., Bassas, L. and Larriba, S. (2018). Exosomal microRNAs in seminal plasma are markers of the origin of azoospermia and can predict the presence of sperm in testicular tissue. Human Reproduction, 33(6), 1087–1098. doi: 10.1093/humrep/dey072 CrossRefGoogle ScholarPubMed
Barranco, I., Padilla, L., Parrilla, I., Álvarez-Barrientos, A., Pérez-Patiño, C., Peña, F. J., Martínez, E. A., Rodriguez-Martínez, H. and Roca, J. (2019). Extracellular vesicles isolated from porcine seminal plasma exhibit different tetraspanin expression profiles. Scientific Reports, 9(1), 11584. doi: 10.1038/s41598-019-48095-3 CrossRefGoogle ScholarPubMed
Basatemur, E. and Sutcliffe, A. (2008). Follow-up of children born after ART. Placenta, 29, Suppl. B, 135–140. doi: 10.1016/j.placenta.2008.08.013 CrossRefGoogle ScholarPubMed
Bromfield, J. J. (2014). Seminal fluid and reproduction: Much more than previously thought. Journal of Assisted Reproduction and Genetics, 31(6), 627–636. doi: 10.1007/s10815-014-0243-y CrossRefGoogle ScholarPubMed
Bromfield, J. J. (2016). A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction, 152(6), R223–R232. doi: 10.1530/REP-16-0313 CrossRefGoogle ScholarPubMed
Bromfield, J. J. and Sheldon, I. M. (2011). Lipopolysaccharide initiates inflammation in bovine granulosa cells via the TLR4 pathway and perturbs oocyte meiotic progression in vitro . Endocrinology, 152(12), 5029–5040. doi: 10.1210/en.2011-1124 CrossRefGoogle ScholarPubMed
Bromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J. and Robertson, S. A. (2014). Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proceedings of the National Academy of Sciences of the United States of America, 111(6), 2200–2205. doi: 10.1073/pnas.1305609111 CrossRefGoogle ScholarPubMed
Chandra, A., Copen, C. E. and Stephen, E. H. (2014). Infertility service use in the United States: Data from the National Survey of Family Growth, 1982–2010. National Health Statistics Reports, 73(73), 1–21.Google Scholar
Chronopoulou, E. and Harper, J. C. (2015). IVF culture media: Past, present and future. Human Reproduction Update, 21(1), 39–55. doi: 10.1093/humupd/dmu040 CrossRefGoogle ScholarPubMed
Costa, F., Barbisan, F., Assmann, C. E., Araújo, N. K. F., de Oliveira, A. R., Signori, J. P., Rogalski, F., Bonadiman, B., Fernandes, M. S. and da Cruz, I. B. M. (2017). Seminal cell-free DNA levels measured by PicoGreen fluorochrome are associated with sperm fertility criteria. Zygote, 25(2), 111–119. doi: 10.1017/S0967199416000307 CrossRefGoogle ScholarPubMed
Dorostghoal, M., Kazeminejad, S. R., Shahbazian, N., Pourmehdi, M. and Jabbari, A. (2017). Oxidative stress status and sperm DNA fragmentation in fertile and infertile men. Andrologia, 49(10). doi: 10.1111/and.12762 CrossRefGoogle ScholarPubMed
Druart, X. and de Graaf, S. (2018). Seminal plasma proteomes and sperm fertility. Animal Reproduction Science, 194, 33–40. doi: 10.1016/j.anireprosci.2018.04.061 CrossRefGoogle ScholarPubMed
Eswaran, N., Agaram Sundaram, V., Rao, K. A. and Thalaivarisai Balasundaram, S. (2018). Simple isolation and characterization of seminal plasma extracellular vesicle and its total RNA in an academic lab. 3 Biotech, 8(3), 139. doi: 10.1007/s13205-018-1157-7 CrossRefGoogle Scholar
Guo, X. Y., Liu, X. M., Jin, L., Wang, T. T., Ullah, K., Sheng, J. Z. and Huang, H. F. (2017). Cardiovascular and metabolic profiles of offspring conceived by assisted reproductive technologies: A systematic review and meta-analysis. Fertility and Sterility, 107(3), 622–631.e5. doi: 10.1016/j.fertnstert.2016.12.007 CrossRefGoogle ScholarPubMed
Hartmann, C., Gerner, W., Walter, I., Saalmüller, A. and Aurich, C. (2018). Influences of intrauterine semen administration on regulatory T lymphocytes in the oestrous mare (Equus caballus). Theriogenology, 118, 119–125. doi: 10.1016/j.theriogenology.2018.05.030 CrossRefGoogle Scholar
Hopkins, B. R., Sepil, I. and Wigby, S. (2017). Seminal fluid. Current Biology, 27(11), R404–R405. doi: 10.1016/j.cub.2017.03.063 CrossRefGoogle ScholarPubMed
Jia, L., Ding, B., Shen, C., Luo, S., Zhang, Y., Zhou, L., Ding, R., Qu, P. and Liu, E. (2019). Use of oocytes selected by brilliant cresyl blue staining enhances rabbit cloned embryo development in vitro . Zygote, 27(3), 166–172. doi: 10.1017/S0967199419000200 CrossRefGoogle ScholarPubMed
Juyena, N. S. and Stelletta, C. (2012). Seminal plasma: An essential attribute to spermatozoa. Journal of Andrology, 33(4), 536–551. doi: 10.2164/jandrol.110.012583 CrossRefGoogle ScholarPubMed
Kaczmarek, M. M., Krawczynski, K., Blitek, A., Kiewisz, J., Schams, D. and Ziecik, A. J. (2010). Seminal plasma affects prostaglandin synthesis in the porcine oviduct. Theriogenology, 74(7), 1207–1220. doi: 10.1016/j.theriogenology.2010.05.024 CrossRefGoogle ScholarPubMed
Machtinger, R., Laurent, L. C. and Baccarelli, A. A. (2016). Extracellular vesicles: Roles in gamete maturation, fertilization and embryo implantation. Human Reproduction Update, 22(2), 182–193. doi: 10.1093/humupd/dmv055 Google ScholarPubMed
Mandawala, A. A., Harvey, S. C., Roy, T. K. and Fowler, K. E. (2016). Cryopreservation of animal oocytes and embryos: Current progress and future prospects. Theriogenology, 86(7), 1637–1644. doi: 10.1016/j.theriogenology.2016.07.018 CrossRefGoogle ScholarPubMed
Morrell, J. M., Georgakas, A., Lundeheim, N., Nash, D., Davies Morel, M. C. and Johannisson, A. (2014). Effect of heterologous and homologous seminal plasma on stallion sperm quality. Theriogenology, 82(1), 176–183. doi: 10.1016/j.theriogenology.2014.03.020 CrossRefGoogle ScholarPubMed
Mulcahy, L. A., Pink, R. C. and Carter, D. R. (2014). Routes and mechanisms of extracellular vesicle uptake. Journal of Extracellular Vesicles, 3. doi: 10.3402/jev.v3.24641 CrossRefGoogle ScholarPubMed
Niederberger, C., Pellicer, A., Cohen, J., Gardner, D. K., Palermo, G. D., O’Neill, C. L., Chow, S., Rosenwaks, Z., Cobo, A., Swain, J. E., Schoolcraft, W. B., Frydman, R., Bishop, L. A., Aharon, D., Gordon, C., New, E., Decherney, A., Tan, S. L., Paulson, R. J. and LaBarbera, A. R. (2018). Forty years of IVF. Fertility and Sterility, 110(2), 185–324.e5. doi: 10.1016/j.fertnstert.2018.06.005 CrossRefGoogle ScholarPubMed
Palermo, G. D., Neri, Q. V., Takeuchi, T., Squires, J., Moy, F. and Rosenwaks, Z. (2008). Genetic and epigenetic characteristics of ICSI children. Reproductive Biomedicine Online, 17(6), 820–833. doi: 10.1016/s1472-6483(10)60411-7 CrossRefGoogle ScholarPubMed
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., Qing, S., Liu, R., Qin, H., Wang, W., Qiao, F., Ge, H., Liu, J., Zhang, Y., Cui, W. and Wang, Y. (2017). Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS ONE, 12(3), e0174535. doi: 10.1371/journal.pone.0174535 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
Rizo, J. A., Ibrahim, L. A., Molinari, P. C. C., Harstine, B. R., Piersanti, R. L. and Bromfield, J. J. (2019). Effect of seminal plasma or transforming growth factor on bovine endometrial cells. Reproduction, 158(6), 529–541. doi: 10.1530/REP-19-0421 CrossRefGoogle ScholarPubMed
Robertson, S. A. and Sharkey, D. J. (2016). Seminal fluid and fertility in women. Fertility and Sterility, 106(3), 511–519. doi: 10.1016/j.fertnstert.2016.07.1101 CrossRefGoogle ScholarPubMed
Rocha, D. R., Martins, J. A., van Tilburg, M. F., Oliveira, R. V., Moreno, F. B., Monteiro-Moreira, A. C., Moreira, R. A., Araújo, A. A. and Moura, A. A. (2015). Effect of increased testicular temperature on seminal plasma proteome of the ram. Theriogenology, 84(8), 1291–1305. doi: 10.1016/j.theriogenology.2015.07.008 CrossRefGoogle ScholarPubMed
Samanta, L., Parida, R., Dias, T. R. and Agarwal, A. (2018). The enigmatic seminal plasma: A proteomics insight from ejaculation to fertilization. Reproductive Biology and Endocrinology: RB&E, 16(1), 41. doi: 10.1186/s12958-018-0358-6 CrossRefGoogle Scholar
Schjenken, J. E., Glynn, D. J., Sharkey, D. J. and Robertson, S. A. (2015). TLR4 signaling is a major mediator of the female tract response to seminal fluid in mice. Biology of Reproduction, 93(3), 68. doi: 10.1095/biolreprod.114.125740 CrossRefGoogle ScholarPubMed
Siciliano, L., Marcianò, V. and Carpino, A. (2008). Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reproductive Biology and Endocrinology: RB&E, 6, 5. doi: 10.1186/1477-7827-6-5 CrossRefGoogle ScholarPubMed
Silva, E., Frost, D., Li, L., Bovin, N. and Miller, D. J. (2017). Lactadherin is a candidate oviduct Lewis X trisaccharide receptor on porcine spermatozoa. Andrology, 5(3), 589–597. doi: 10.1111/andr.12340 CrossRefGoogle ScholarPubMed
Sirard, M. A. (2018). 40 years of bovine IVF in the new genomic selection context. Reproduction, 156(1), R1–R7. doi: 10.1530/REP-18-0008 CrossRefGoogle ScholarPubMed
Skalnikova, H. K., Bohuslavova, B., Turnovcova, K., Juhasova, J., Juhas, S., Rodinova, M. and Vodicka, P. (2019). Isolation and characterization of small extracellular vesicles from porcine blood plasma, cerebrospinal fluid, and seminal plasma. Proteomes, 7(2). doi: 10.3390/proteomes7020017 CrossRefGoogle ScholarPubMed
Song, Z. H., Li, Z. Y., Li, D. D., Fang, W. N., Liu, H. Y., Yang, D. D., Meng, C. Y., Yang, Y. and Peng, J. P. (2016). Seminal plasma induces inflammation in the uterus through the gammadelta T/IL-17 pathway. Scientific Reports, 6, 25118. doi: 10.1038/srep25118 CrossRefGoogle ScholarPubMed
Talbot, N. C., Powell, A. M., Camp, M. and Ealy, A. D. (2007). Establishment of a bovine blastocyst-derived cell line collection for the comparative analysis of embryos created in vivo and by in vitro fertilization, somatic cell nuclear transfer, or parthenogenetic activation. In Vitro Cellular and Developmental Biology. Animal, 43(2), 59–71. doi: 10.1007/s11626-007-9013-9 CrossRefGoogle ScholarPubMed
Urrego, R., Bernal-Ulloa, S. M., Chavarría, N. A., Herrera-Puerta, E., Lucas-Hahn, A., Herrmann, D., Winkler, S., Pache, D., Niemann, H. and Rodriguez-Osorio, N. (2017). Satellite DNA methylation status and expression of selected genes in Bos indicus blastocysts produced in vivo and in vitro . Zygote, 25(2), 131–140. doi: 10.1017/S096719941600040X CrossRefGoogle ScholarPubMed
Watkins, A. J., Dias, I., Tsuro, H., Allen, D., Emes, R. D., Moreton, J., Wilson, R., Ingram, R. J. M. and Sinclair, K. D. (2018). Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proceedings of the National Academy of Sciences of the United States of America, 115(40), 10064–10069. doi: 10.1073/pnas.1806333115 CrossRefGoogle ScholarPubMed
Xiong, X. R., Wang, L. J., Wang, Y. S., Hua, S., Zi, X. D. and Zhang, Y. (2014). Different preferences of IVF and SCNT bovine embryos for culture media. Zygote, 22(1), 1–9. doi: 10.1017/S0967199412000184 CrossRefGoogle ScholarPubMed
Zelli, R., Orlandi, R., Verstegen, J., Troisi, A., Elad Ngonput, A., Menchetti, L., Cardinali, L. and Polisca, A. (2017). Addition of different concentrations of prostasome-like vesicles at neutral or slightly alkaline pH decreases canine sperm motility. Andrology, 5(1), 160–168. doi: 10.1111/andr.12286 CrossRefGoogle ScholarPubMed
Zuo, Z., Niu, Z., Liu, Z., Ma, J., Qu, P., Qiao, F., Su, J., Zhang, Y. and Wang, Y. (2020). The effects of glycine-glutamine dipeptide replaced l-glutamine on bovine parthenogenetic and IVF embryo development. Theriogenology, 141, 82–90. doi: 10.1016/j.theriogenology.2019.09.005 CrossRefGoogle ScholarPubMed