Effect of Transport Condition on the Structural Integrity of Ovarian Tissue and the Development of Sheep Embryos In-Vitro

Abstract

The oocyte quality decreases during ovarian tissue transport to the laboratories of in vitro embryo production. To provide additional information on how the conditions of transporting sheep ovaries impact the ovarian tissue and oocytes’ ability to develop into blastocyst stages, we have studied new transport media Ankara University Zootekni (AUZ1, AUZ2) supplemented with antioxidants (melatonin, Vit E, and Vit A), buffer solution, and energy substrates, and compared them with the traditional transport media: Phosphate-Buffered Saline (PBS), and Charles Rosenkrans 1 (CR1), Normal Saline (NS) at different temperatures (-6 to 30 °C). We also studied and compared how well different transport media preserve the ovarian tissue's structural integrity while transporting sheep ovaries at 4°C. Our findings indicated that various temperatures and transport media play critical roles in embryo development. The embryo development rates showed that when sheep ovaries are transported in AUZ1, they produce oocytes with a higher embryo development rate than other transport media at any temperature. In addition, histology examination revealed that the transport of sheep ovarian tissue in any medium at a temperature of 4 °C did not negatively impact the viability and histomorphology of the primordial, primary, and secondary follicles. In contrast to other transport media, the AUZ1 medium maintained the normal morphology of antral follicles, Graafian follicles, and the cumulus oophorus of sheep ovarian tissue. In conclusion, adding melatonin, buffer solution, and energy substrates to the transportation medium of ovarian tissues has a beneficial and positive role in maintaining ovarian tissue and increasing the rates of embryonic development.

Keywords

• Sheep
• Embryo development
• Ovarian tissue
• Transport medium
• Melatonin

References

1. Adriaens, I., Jacquet, P., Cortvrindt, R., Janssen, K., & Smitz, J. (2006). Melatonin has dose-dependent effects on folliculogenesis, oocyte maturation capacity and steroidogenesis. Toxicology, 228, 333-343. doi: 10.1016/j.tox.2006.09.018
2. Arat, S., Caputcu, A. T., Cevik, M., Akkoc, T., Cetinkaya, G., & Bagis, H. (2016). Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos. Zygote, 24, 554-562. doi: 10.1017/S0967199415000519
3. Ateşşahin, A., Şahna, E., Türk, G., Çeribaşi, A. O., Yılmaz, S., Yüce, A., & Bulmuş, Ö. (2006). Chemoprotective effect of melatonin against cisplatin‐induced testicular toxicity in rats. J. Pineal Res., 41, 21-27. doi: 10.1111/j.1600-079X.2006.00327.x.
4. Bohlooli, S. H., Bozoğlu, Ş., & Cedden, F. (2015). HEPES buffer in ovary-transportation medium influences developmental competence of cattle oocytes. South African Journal of Animal Science, 45, 538-546. doi: 10.4314/sajas.v45i5.11
5. Cantu, E., & Zaas, D. (2011). Organ donor management and procurement. In Klein, A. A., Lewis, C. J., & Madsen, J. C. (Eds.), Organ Transplantation: A Clinical Guide (pp. 53–62). Cambridge University Press. doi: 10.1017/cbo9780511994876.010
6. Cao, Z., Gao, D., Tong, X., Xu, T., Zhang, D., Wang, Y., ... & Pu, Y. (2019). Melatonin improves developmental competence of oocyte-granulosa cell complexes from porcine preantral follicles. Theriogenology, 133, 149-158. doi:10.1016/j.theriogenology.2019.05.003
7. Chaves, R. N., Martins, F. S., Saraiva, M. V. A., Celestino, J. J. H., Lopes, C. A. P., Correia, J. C., ... & Figueiredo, J. R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reproduction, Fertility and Development, 20(5), 640-647. doi: 10.1071/rd07195
8. Combelles, C. M., Gupta, S., & Agarwal, A. (2009). Could oxidative stress influence the in-vitro maturation of oocytes?. Reproductive Biomedicine Online, 18(6), 864-880. doi: 10.1016/s1472-6483(10)60038-7

9. Cruz, M. H. C., Leal, C. L. V., Cruz, J. F. D., Tan, D. X., & Reiter, R. J. (2014). Essential actions of melatonin in protecting the ovary from oxidative damage. Theriogenology, 82(7), 925-932. doi:10.1016/j.theriogenology.2014.07.011
10. Ferraz, M. A., Rho, H. S., Hemerich, D., Henning, H. H., van Tol, H. T., Hölker, M., ... & Gadella, B. M. (2018). An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming. Nature Communications, 9(1), 4934. doi: 10.1038/s41467-018-07119-8
11. Galli, C., Duchi, R., Colleoni, S., Lagutina, I., & Lazzari, G. (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology, 81(1), 138-151. doi: 10.1016/j.theriogenology.2013.09.008
12. García-Álvarez, O., Maroto-Morales, A., Berlinguer, F., Fernández-Santos, M. R., Esteso, M. C., Mermillod, P., ... & Soler, A. J. (2011). Effect of storage temperature during transport of ovaries on in vitro embryo production in Iberian red deer (Cervus elaphus hispanicus). Theriogenology, 75(1), 65-72. doi: 10.1016/j.theriogenology.2010.07.011
13. Guibert, E. E., Petrenko, A. Y., Balaban, C. L., Somov, A. Y., Rodriguez, J. V., & Fuller, B. J. (2011). Organ preservation: current concepts and new strategies for the next decade. Transfusion Medicine and Hemotherapy, 38(2), 125-142. doi: 10.1159/000327033
14. Jiao, G. Z., Cui, W., Yang, R., Lin, J., Gong, S., Lian, H. Y., ... & Tan, J. H. (2016). Optimized protocols for in vitro maturation of rat oocytes dramatically improve their developmental competence to a level similar to that of ovulated oocytes. Cellular Reprogramming, 18(1), 17-29. doi: 10.1089/cell.2015.0055.
15. Liu, Y., Zhu, X., Wu, C., Lang, Y., Zhao, W., & Li, Y. (2022). Melatonin protects against ovarian damage by inhibiting autophagy in granulosa cells in rats. Clinics, 77, 100119.
16. Love, L. B., Choi, Y. H., Love, C. C., Varner, D. D., & Hinrichs, K. (2003). Effect of ovary storage and oocyte transport method on maturation rate of horse oocytes. Theriogenology, 59(3-4), 765-774. doi:10.1016/s0093-691x(02)01133-0
17. Majeed, A., Al-Timimi, I. H., & AL-Saigh, M. N. (2019). Effect of season on embryo production in Iraqi local black goat. Iraqi Journal of Veterinary Sciences, 33(1), 59-65. doi: 10.33899/ijvs.2019.125514.1036
18. Martín-Maestro, A., Sánchez-Ajofrín, I., Maside, C., Peris-Frau, P., Medina-Chávez, D. A., Cardoso, B., ... & Soler, A. J. (2020). Cellular and molecular events that occur in the oocyte during prolonged ovarian storage in sheep. Animals, 10(12), 2414. doi: 10.3390/ani10122414
19. Matsushita, S., Tani, T., Kato, Y., & Tsunoda, Y. (2004). Effect of low-temperature bovine ovary storage on the maturation rate and developmental potential of follicular oocytes after in vitro fertilization, parthenogenetic activation, or somatic cell nucleus transfer. Animal Reproduction Science, 84(3-4), 293-301. doi:10.1016/j.anireprosci.2004.02.008
20. Mohammadghasemi, F., Jahromi, S. K., Hajizadeh, H., Homafar, M. A., & Saadat, N. (2012). The protective effects of exogenous melatonin on nicotine-induced changes in mouse ovarian follicles. Journal of Reproduction & Infertility, 13(3), 143. doi: https://doi.org/10.2478/intox-2014-0007
21. Naoi, H., Otoi, T., Shimamura, T., Karja, N. W. K., Agung, B., Shimizu, R., ... & Nagai, T. (2007). Developmental competence of cat oocytes from ovaries stored at various temperature for 24 h. Journal of Reproduction and Development, 53(2), 271-277. doi: 10.1262/jrd.18115
22. Nikiforov, D., Junping, C., Cadenas, J., Shukla, V., Blanshard, R., Pors, S. E., ... & Andersen, C. Y. (2020). Improving the maturation rate of human oocytes collected ex vivo during the cryopreservation of ovarian tissue. Journal of assisted reproduction and genetics, 37, 891-904. doi: 10.1007/s10815-020-01724-7
23. Pacchiarotti, A., Valeri, C., Antonini, G., Biagiotti, G., Prapas, N., & Pacchiarotti, A. (2015). Antioxidative capacity of melatonin in follicular fluid of aged IVF patients: beneficial effects on oocytes and embryo. J Gynecol Neonatal Biol, 1(2), 32-6. doi: 10.15436/2380-5595.15.009
24. Reiter, R. J., Tan, D. X., Manchester, L. C., Paredes, S. D., Mayo, J. C., & Sainz, R. M. (2009). Melatonin and reproduction revisited. Biology of Reproduction, 81(3), 445-456. doi: 10.1095/biolreprod.108.075655
25. Reynolds, L. P., Grazul‐Bilska, A. T., & Redmer, D. A. (2002). Angiogenesis in the female reproductive organs: pathological implications. International Journal of Experimental Pathology, 83(4), 151-164. doi: h10.1046/j.1365-2613.2002.00277.x
26. Romeu, L. R. G., da Motta, E. L. A., Maganhin, C. C., Oshima, C. T., Fonseca, M. C., Barrueco, K. F., ... & Soares-Junior, J. M. (2011). Effects of melatonin on histomorphology and on the expression of steroid receptors, VEGF, and PCNA in ovaries of pinealectomized female rats. Fertility and Sterility, 95(4), 1379-1384. doi: 10.1016/j.fertnstert.2010.04.042
27. Sánchez-Ajofrín, I., Iniesta-Cuerda, M., Peris-Frau, P., Martín-Maestro, A., Medina-Chávez, D. A., Maside, C., ... & Soler, A. J. (2020). Beneficial effects of melatonin in the ovarian transport medium on In Vitro embryo production of iberian red deer (Cervus elaphus hispanicus). Animals, 10(5), 763. doi: 10.3390/ani10050763
28. Sánchez-Ajofrín, I., Iniesta-Cuerda, M., Sánchez-Calabuig, M. J., Peris-Frau, P., Martín-Maestro, A., Ortiz, J. A., ... & Soler, A. J. (2020). Oxygen tension during in vitro oocyte maturation and fertilization affects embryo quality in sheep and deer. Animal Reproduction Science, 213, 106279. doi: 10.1016/j.anireprosci.2020.106279.
29. Schornack, P. A., & Gillies, R. J. (2003). Contributions of cell metabolism and H+ diffusion to the acidic pH of tumors. Neoplasia, 5(2), 135-145. doi: 10.1016/s1476-5586(03)80005-2
30. Soto-Heras, S., & Paramio, M. T. (2020). Impact of oxidative stress on oocyte competence for in vitro embryo production programs. Research in Veterinary Science, 132, 342-350. doi: 10.1016/j.rvsc.2020.07.013
31. Tamura, H., Takasaki, A., Miwa, I., Taniguchi, K., Maekawa, R., Asada, H., ... & Sugino, N. (2008). Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. Journal of Pineal Research, 44(3), 280-287. doi: 10.1111/j.1600-079X.2007.00524.x
32. Taş, M., Evecen, M., Özdaş, Ö. B., Cirit, Ü., Demir, K., Birler, S., & Pabuccuoğlu, S. (2006). Effect of transport and storage temperature of ovaries on in vitro maturation of bitch oocytes. Animal Reproduction Science, 96, 30-34. doi: 10.1016/j.anireprosci.2005.11.001
33. Tellado, M. N., Alvarez, G. M., Dalvit, G. C., & Cetica, P. D. (2014). The conditions of ovary storage affect the quality of porcine oocytes. Advances in Reproductive Sciences, 2, 56-67. doi: 10.4236/arsci.2014.23007
34. Tian, X., Wang, F., He, C., Zhang, L., Tan, D., Reiter, R. J., ... & Liu, G. (2014). Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. Journal of Pineal Research, 57(3), 239-247. doi: 10.1111/jpi.12163
35. Wang, Q., & Sun, Q. Y. (2006). Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reproduction, Fertility and Development, 19(1), 1-12. doi: 10.1071/rd06103
36. Wang, T., Gao, Y. Y., Chen, L., Nie, Z. W., Cheng, W., Liu, X., ... & Miao, Y. L. (2017). Melatonin prevents postovulatory oocyte aging and promotes subsequent embryonic development in the pig. Aging (albany NY), 9(6), 1552. doi: 10.18632/aging.101252
37. Wang, Y. S., Zhao, X., Su, J. M., An, Z. X., Xiong, X. R., Wang, L. J., ... & Zhang, Y. (2011). Lowering storage temperature during ovary transport is beneficial to the developmental competence of bovine oocytes used for somatic cell nuclear transfer. Animal Reproduction Science, 124(1-2), 48-54. doi:10.1016/j.anireprosci.2011.01.015
38. Wieczorek, J., Koseniuk, J., Skrzyszowska, M., & Cegła, M. (2020). L-OPU in goat and sheep—different variants of the oocyte recovery method. Animals, 10(4), 658. doi: 10.3390/ani10040658
39. Wongsrikeao, P., Otoi, T., Karja, N. W. K., Agung, B., Nii, M., & Nagai, T. (2005). Effects of ovary storage time and temperature on DNA fragmentation and development of porcine oocytes. Journal of Reproduction and Development, 51(1), 87-97. doi: 10.1262/jrd.51.87
40. Youm, H. W., Lee, J. R., Lee, J., Jee, B. C., Suh, C. S., & Kim, S. H. (2014). Optimal vitrification protocol for mouse ovarian tissue cryopreservation: effect of cryoprotective agents and in vitro culture on vitrified–warmed ovarian tissue survival. Human Reproduction, 29(4), 720-730. doi: 10.1093/humrep/det449
41. Zhang, M., Lu, Y., Chen, Y., Zhang, Y., & Xiong, B. (2020). Insufficiency of melatonin in follicular fluid is a reversible cause for advanced maternal age-related aneuploidy in oocytes. Redox Biology, 28, 101327. doi: 10.1016/j.redox.2019.101327