Modern achievements of the development of scientific research at obtaining in vitro sheep embryos


Keywords: embryo, oocyte, sheep, in vitro maturation, fertilization, culture

Abstract

New literature data on research aimed at improving the in vitro production of sheep embryos presents in the article. An analysis of the achievements of scientists from different countries to increase the efficiency of the main stages of embryo production in vitro: maturation of oocytes in vitro, their in vitro fertilization and in vitro embryo culture. In the literature experience has shown that the efficiency of oocyte maturation in vitro is significantly influenced by the experience and qualifications of scientists, the age of the egg donor, the improvement of the environment by adding roscovitin to inhibit meiosis, α-linolenic acid, cerium dioxide nanoparticles (CeO2 NPs) and sericin to accelerate nuclear maturation and increase the number of oocytes of the second meiotic metaphase (MII). The main factors influencing the effectiveness of in vitro fertilization have been identified, and the parameters of the limited time of fertilization ability of sperm and the ability of oocytes to fertilize, which is called the “fertile span”, have been determined. The main effective medium that increases the effectiveness of in vitro fertilization – synthetic oviduct fluid (SOF) with the addition of heparin and serum of cattle or sheep. The main parameters of sheep embryo culture in vitro are presented with the definition of the most commonly used media and their influence on embryonic development. Potential ways to improve the production of sheep embryos in vitro with the determination of morphological evaluation of categories of oocytes, methods of synchronization of their maturation in vitro are also highlighted. At the same time, literature data on the synchronization of oocyte-cumulus complexes with the use of a large number of inhibitors of meiotic division are presented, which according to many scientists may be a key factor in improving the efficiency of sheep embryo production in vitro. In addition, the results of studies of many scientists on the expansion of the fertile gap of oocytes of sheep cultured in vitro using certain biologically active substances were analyzed. In conclusion, the prospect of using the technology of in vitro production of sheep embryos in biomedical research is highlighted.

References

Aghaz, F., Hajarian, H., Shabankareh, H. K., & Abdol-mohammadi, A. (2015). Effect of sericin supplemen-tation in maturation medium on cumulus cell expan-sion, oocyte nuclear maturation, and subsequent em-bryo development in Sanjabi ewes during the breeding season. Theriogenology, 84(9), 1631–1635. doi: 10.1016/j.theriogenology.2015.08.013.

Aktas, H., Wheeler, M. B., First, N. L., & Leibfried Rutledge, M. L. (1995). Maintenance of meiotic arrest by increasing [cAMP]i may have physiological relevance in bovine oocytes. J. Reprod. Fertil, 105, 237–45. doi: 10.1530/jrf.0.1050237.

Amini, E., Asadpour, R., Roshangar, L., & Jafari-joozani, R. (2016). Effect of α-linoleic acid supplementation on in vitro maturation, embryo development and apoptotic related gene expression in ovine. Int. J. Reprod. Biomed (Yazd), 14(4), 255–262. URL: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4918772.

Amiridisa, G. S., & Cseh, S. (2012). Assisted reproductive technologies in the reproductive management of small ruminants. Anim Reprod Sci, 130(3-4), 152–161. doi: 10.1016/j.anireprosci.2012.01.009.

Ariu, F., Bogliolo, L., Pinna, A., Malfatti, L., Innocenzi, P., Falchi, L., Bebbere, D., & Ledda, S. (2017). Cerium oxide nanoparticles (CeO2 NPs) improve the developmental competence of in vitro-matured prepubertal ovine oocytes. Reprod Fertil Dev, 29(5), 1046–1056. doi: 10.1071/RD15521.

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology, 55(6), 1303–1322. doi: 10.1016/s0093-691x(01)00484-8.

Avery, B., Hay-Schmidt, A., Hyttel, P., & Greve, T. (1998). Embryo development, oocyte morphology, and kinetics of meiotic maturation in bovine oocytes exposed to 6-dimethylaminopurine prior to in vitro maturation. Mol. Reprod. Dev, 50(3), 334–344. URL: https://pubmed.ncbi.nlm.nih.gov/9621310.

Botigelli, R. C., Razza, E. M., Pioltine, E. M, & Nogueira, M. F. (2017). New approach regarding the in vitro maturation of oocytes: manipulating cyclic nucleotides and their partners in crime. JBRA Assisted Reprod, 21(1), 35–44. doi: 10.5935%2F1518-0557.20170010.

Buell, M., Chitwood, J. L., & Ross, P. J. (2015). cAMP modulation during sheep in vitro oocyte maturation delays progression of meiosis without affecting oocyte parthenogenetic developmental competence. Anim. Reprod. Sci., 154, 16–24. doi: 10.1016/j.anireprosci.2014.12.012.

Cheng, W. T. K., Moor, R. M., & Polge, C. E. (1986). In vitro fertilization of pig and sheep oocytes matured in vivo and in vitro. Theriogenology, 25, 14. URL: https://ci.nii.ac.jp/naid/10020372647.

Choi, I., Lee, J. H., Fisher, P., & Campbell, K. H. (2010). Caffeine treatment of ovine cytoplasts 661 regulates gene expression and foetal development of embryos produced by somatic cell nuclear transfer. Mol. Reprod. Dev., 77(10), 876–887. doi: 10.1002/mrd.21230.

Cognié, Y., Baril, G., Poulin, N., & Mermillod, P. (2003). Current status of embryo technologies in sheep and goat. Theriogenology, 59(1), 171–188. doi: 10.1016/s0093-691x(02)01270-0.

Coticchio, G., Dal Canto, M., Mignini Renzini, M., Guglielmo, M. C., Brambillasca, F., & Turchi, D. (2015). Oocyte maturation: gamete-somatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum. Reprod Update, 21(4), 427–454. doi: 10.1093/humupd/dmv011.

Cox, J. F., & Alfaro, V. (2007). In vitro fertilization and development of OPU derived goat and sheep oocytes. Reprod. Domest Anim, 42(1), 83–87. doi: 10.1111/j.1439-0531.2006.00735.x.

Crocomo, L. F., Ariu, F., Bogliolo, L., Bebbere, D., Ledda, S., & Bicudo, S. D. (2016). In vitro Developmental Competence of Adult Sheep Oocytes Treated with Roscovitine. Reprod. Domest. Anim., 51(2), 276–281. doi: 10.1111/rda.12677.

Crocomo, L. F., Ulian, C. M. V., da Silva Branchini, N., da Silva, D. T., Filho, W. C. M., da Cruz Landim Alvarenga, F., & Bicudo, S. D. (2015). Meiotic arrest of sheep oocytes using roscovitine under different medium compositions Small Ruminant Res, 126, 52–58. doi: 10.1016/j.smallrumres.2015.02.022.

De Souza-Fabjan, J. M. G., Panneau, B., Duffard, N., Locatelli, Y., De Figueiredo, J. R., De Figueirêdo Freitas, V. J., & Mermillod, P. (2014). In vitro production of small ruminant embryos: late improvements and further research (a review). Theriogenology, 81(9), 1149–1162. doi: 10.1016/j.theriogenology.2014.02.001.

Dode, M. A., & Adona, P. R. (2001). Developmental capacity of Bos indicus oocytes after 607 inhibitions of meiotic resuption by 6-dimethylaminopurine. Anim. Reprod. Sci., 65(3-4), 171–180. doi: 10.1016/s0378-4320(00)00207-4.

Dos Santos Neto, P. C., Vilariño, M., Barrera, N., Cuadro, F., Crispo, M., & Menchaca, A. (2015). Cryotolerance of Day 2 or Day 6 in vitro produced ovine embryos after vitrification by Cryotop or Spatula methods. Cryobiology, 70(1), 17–22. doi: 10.1016/j.cryobiol.2014.11.001.

Fernández-Gonzalez, R., Moreira, P., Bilbao, A., Jiménez, A., Pérez-Crespo, M., Ramírez, M.A., Rodríguez, De Fonseca, F., Pintado, B., & Gutiérrez-Adán, A. (2004). Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behaviour. Proc Natl Acad Sci USA, 101(16), 5880–5885. doi: 10.1073/pnas.0308560101.

Ferreira, E. M., Vireque A. A., Adona, P. R., Ferriani, R. A., Navarro, P. A. (2009). Prematuration of bovine oocytes with butyrolactone I reversibly arrests meiosis without increasing meiotic abnormalities after in vitro maturation. Eur. J. Obst. Gynecol. Reprod. Biol. 145, 76–80. doi: 10.1016/j.ejogrb.2009.03.016.

García-Álvarez, O., Maroto-Morales, A., Ramón, M., Del Olmo, E., Jiménez-Rabadán, P., & Fernández-Santos, M. R. (2014). Dynamics of sperm subpopulations based on motility and plasma membrane status in thawed ram spermatozoa incubated under conditions that support in vitro capacitation and fertilisation. Reprod Fertil Dev. 26(5), 725–732. doi: 10.1071/RD13034.

Gardner, D. K., Lane M., Spitzer A., Batt P.A. (1994). Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol Reprod, 50(2), 390–400. doi: 10.1095/biolreprod50.2.390.

German, S. D., Lee, J. H., Campbell, K. H., Sweetman, D., & Alberio, R. (2015). Actin depolymerization is associated with meiotic acceleration in cycloheximide-treated ovine oocytes. Biol. Reprod, 92(4), 103. doi: 10.1095/biolreprod.114.122341.

Ghaffarilaleh, V., Fouladi-Nashta, A., & Paramio, M. T. (2014). Effect of α-linolenic acid on oocyte matura-tion and embryo development of prepubertal sheep oocytes. Theriogenology, 82(5), 686–696. doi: 10.1016/j.theriogenology.2014.05.027.

Hashimoto, S., Minami, N., Takakura, R., & Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biol. Reprod, 66(6), 1696–1701. doi: 10.1095/biolreprod66.6.1696.

Hosseini, S. M., Asgari, V., Ostadhosseini, S., Hajian, M., Ghanaei, H. R., & Nasr-Esfahani, M. H. (2015). Developmental competence of ovine oocytes after vitrification: Differential effects of vitrification steps, embryo production methods, and parental origin of pronuclei. Theriogenology, 83(3), 366–376. doi: 10.1016/j.theriogenology.2014.09.031.

Khosla, S., Dean, W., Reik, W., & Feil, R. (2001). Culture of pre-implantation embryos and it long-term effects on gene expression and phenotype. Hum Reprod Update, 7(4), 419–427. doi: 10.1093/humupd/7.4.419.

Kochhar, H. P., Wu, B., Morris, L. H., Buckrell, B. C., Pollard, J. W., Basrur, P. K., & King, W. A. (2001). Maturation status, protein synthesis and developmental competence of oocytes derived from lambs and ewes. Reprod Domest Anim, 37(1), 19–25. doi: 10.1046/j.1439-0531.2002.00326.x.

Ledda, S., Idda, A., Kelly, J., Ariu, F., Bogliolo, L., & Bebbere, D. (2016). A novel technique for in vitro maturation of sheep oocytes in a liquid marble microbioreactor. J Assist Reprod Genet, 33(4), 513–518. doi: 10.1007/s10815-016-0666-8.

Lee, J. H., & Campbell, K. H. (2006). Effects of enucleation and caffeine on maturation- promoting factor (MPF) and mitogen-activated protein kinase (MAPK) activities in ovine oocytes used as recipient cytoplasts for nuclear transfer. Biol Reprod, 74(4), 691–698. doi: 10.1095/biolreprod.105.043885.

Leoni, G. G., Succu, S., Berlinguer, F., Rosati, I., Bebbere, D., Bogliolo, L., Ledda, S., & Naitana, S. (2006). Delay on the in vitro kinetic development of prepubertal ovine embryos. Formation Anim Reprod Sci, 92(3–4), 373–383. doi: 10.1016/j.anireprosci.2005.05.027.

Lonergan, P., Khatir, H., Carolan, C., & Mermillod, P. (1997). Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24h. J. Reprod. Fertil, 109(2), 355–365. doi: 10.1530/jrf.0.1090355.

López-Saucedo, J., Santiago-Moreno, J., Fierro, R., Izquierdo, D., Coloma, M. A., Catalá, M. G., Jiménez, I., Paramio, M. T. (2013). Fertilization capacity of cryopreserved Iberian ibex epididymal sperm in a heterologous in vitro fertilization assay. Zygote. Cambridge University Press, 23(1), 136–144. doi: 10.1017/S0967199413000518.

Maalouf, W. E., Lee, J.-H., & Campbell, K. H. S. (2009). Effects of caffeine, cumulus cell removal and aging on polyspermy and embryo development on in vitro matured and fertilized ovine oocytes. Theriogenology, 71(7), 1083–1092. doi: 10.1016/j.theriogenology.2008.12.001.

Mara, L., Sanna, D., Casu, S., Dattena, M., & Mayorga Muñoz, I. M. (2014). Blastocyst rate of in vitro embryo production in sheep is affected by season. Reprod. Dom. Anim, 49(4), 37–48. doi: 10.1017/S0967199412000706.

María-Gracia, C., Montserrat, R., Dolors, I., Roser M., Sondes, H., & María-Teresa, P. (2013). Blastocyst development, MPF activity and ATP content of lamb oocytes supplemented with insulin–transferrin–selenium (ITS) and ascorbic acid at IVM. Small Ruminant Res, 112(1–3), 103–107. doi: 10.1016/j.smallrumres.2012.12.007.

Marques, M. G., Nascimento, A. B., Gerger, R. P., Gonçalves, J. S., Coutinho, A. R., & Simões, R. (2011). Effect of culture media on porcine embryos produced by in vitro fertilization or parthenogenetic activation after oocyte maturation with cycloheximide. Zygote, 19(4), 331–337. doi: 10.1017/S0967199410000614.

Mermillod, P., Tomanek, M., RéJane, M., & Meijer, L. (2000). High Developmental Competence of Cattle Oocytes Maintained at the Germinal Vesicle Stage for 24 Hours in Culture by Specific Inhibition of MPF Kinase Activity. Mol. Reprod Dev, 55(1), 89–95. doi: 10.1002/(SICI)1098-2795(200001)55:1%3C89::AID-MRD12%3E3.0.CO;2-M.

Paramio, M. T., & Izquierdo, D. (2016). Recent advances in in vitro embryo production in small ruminants. Theriogenology, 86(1), 152–159. doi: 10.1016/j.theriogenology.2016.04.027.

Rizos, D., Clemente, M., Bermejo-Alvarez, P., de La Fuente, J., Lonergan, P., & Gutie’rrez-Ada’n, A. (2008). Consequences of In Vitro Culture Conditions on Embryo Development and Quality. Reprod Dom Anim, 43(4), 44–50. doi: 10.1111/j.1439-0531.2008.01230.x.

Rose, R. D., Gilchrist, R. B., Kelly, J. M., Thompson, J. G., & Sutton-McDowall, M. L. (2013). Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology, 564(79), 142–148. doi: 10.1016/ j.theriogenology.2012.09.020.

Sadeesh, E. M., Selokar, N. L., Balhara, A. K., & Yadav, P. S. (2016). Differences in developmental competence and gene expression profiles between buffalo (Bubalus bubalis) preimplantation embryos cultured in three different embryo culture media. Cytotechnology, 68(5), 1973–1986. doi: 10.1007/s10616-016-0010-2.

Saeki, K., Nagao, Y., Kishi, M., & Nagai, M. (1997). Developmental capacity of bovine oocytes following inhibition of meiotic resumption by cycloheximide or 6 dimethylaminopurine. Theriogenology, 48(7), 1161–1172. doi: 10.1016/s0093-691x(97)00349-x.

Sasaki, M., Kato, Y., Yamada, H., & Terada, S. (2005). Development of a novel serum-free freezing medium for mammalian cells using the silk protein sericin. Biotechnol Appl Biochem, 42(2), 183–188. doi: 10.1042/BA20050019.

Schwarzer, C., Esteves, T. C., Arau-Bravo, M. J., Le Gac, S., Nordhoff, V., & Schlatt, S. (2012). ART culture conditions change the probability of mouse embryo gestation through defined cellular and molecular responses. Hum. Reprod, 27(9), 2627–536 doi: 10.1093/humrep/des223.

Shi, J. M., Yi, J. Y., Tian, X. Z., Wang, F., Lian, Z. X., Han, H. B., Fu, J. C., Lv, W. F., & Liu, G. S. (2015). Effects of seasonal changes on the ovulation rate and em-bryo quality in superovulated Black Suffolk ewes. Neuro Endocrinol Lett. 36(4), 330–336. URL: https://pubmed.ncbi.nlm.nih.gov/26454488.

Shin, H. W. (2016). Animal Models in CRS and Patho-physiologic Insights Gained: A Systematic Review Laryngoscope Investig Otolaryngol, 1(5), 116–123.

Shirazi, A., Ardali, M. A., Ahmadi, E., Nazari, H., Mamuee, M., & Heidari, B. (2012). The Effect of Macromolecule Source and Type of Media During In vitro Maturation of Sheep Oocytes on Subsequent Embryo Development. J. Reprod. Infertil, 13(1), 13–19. URL: https://www.ncbi.nlm.nih.gov/pmc/articles/ PMC3719375.

Thomas, R. E., Thompson, J. G., Armstrong, D. T., & Gilchrist, R. B. (2004). Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol. Reprod, 71(1), 1142–1149 doi: 10.1095/biolreprod.103.024828.

Walker, S. K., Hill, J. L., Kleemann, D. O., & Nancarrow, C. D. (1996). Development of Ovine Embryos in Synthetic Oviductal Fluid Containing Amino Acids at Oviductal Fluid Concentrations. Biol Reprod, 55(3), 703–708. doi: 10.1095/biolreprod55.3.703.

Wei, X., Xiaoling, Z., Kai, M., Rui, W., Jing, X., Min, G., Zhonghong, W., Jianhui, T., Xinyu, Z., & Lei, A. (2016). Characterization and comparative analyses of transcriptomes for in vivo and in vitro produced peri-implantation conceptuses and endometria from sheep. J. Reprod. Dev, 62(3), 279–87. doi: 10.1262/jrd.2015-064.

Yasmin, C., Otoi, T., Setiadi, M.A., Karja, N. W. K. (2015). Maturation and fertilization of sheep oocytes cultured in serum-free medium containing silk protein sericin. Acta Vet. Hung, 63(1), 110–117. doi: 10.1556/AVet.2015.009.

Zhang, X, Liu, X., Chen, L., Wu, D.-Y., Nie, Z.-W., Gao, Y.-Y., & Miao, Y.-L. (2017). Caffeine delays oocyte aging and maintains the quality of aged oocytes safely in mouse. Oncotarget, 8(13), 20602–20611. doi: 10.18632/oncotarget.15292.

Zhu, J., Amarnath, D., Choi, I., Tsunoda, Y., & Campbell, K. (2015). Demecolcine can overcome rat oocyte spontaneous activation. J. Vet. Sci. Res, 2(1), 1–12. doi: 10.1016/j.ijvsm.2018.02.003.

Abstract views: 21
PDF Downloads: 10
Published
2020-09-21
How to Cite
Sharan, O., Stefanyk, V., & Shalovylo, S. (2020). Modern achievements of the development of scientific research at obtaining in vitro sheep embryos. Scientific Messenger of LNU of Veterinary Medicine and Biotechnologies. Series: Agricultural Sciences, 22(93), 60-68. https://doi.org/10.32718/nvlvet-a9311