DOI QR코드

DOI QR Code

Fertility preservation in pig using ovarian tissues by vitrification method

  • Hwang, In-Sul (Columbia Center for Translational Immunology, Columbia University Irving Medical Center, Columbia University)
  • Received : 2022.05.31
  • Accepted : 2022.06.15
  • Published : 2022.06.30

Abstract

Cryopreservation of porcine ovarian tissue by vitrification method is a promising approach to preserve genetic materials for future use. However, information is not enough and technology still remains in a challenge stage in pig. Therefore, the objective of present study was to determine possibility of vitrification method to cryopreserve porcine ovarian tissue and to confirm an occurrence of cryoinjuries. Briefly, cryoinjuries and apoptosis patterns in vitrified-warmed ovarian tissue were examined by histological evaluation and TUNEL assay respectively. In results, a damaged morphology of oocytes was detected among groups and the rate was significantly (p < 0.05) lower in vitrification group (25.8%) than freezing control group (67.7%), while fresh control group (6.6%) showed significantly (p < 0.05) lower than both groups. In addition, cryoinjury that form a wave pattern of tissues around follicles was found in the frozen control group, but not in the fresh control group as well as in the vitrification group. Apoptotic cells in follicle was observed only in freezing control group while no apoptotic cell was found in both fresh control and vitrification. Similarly, apoptotic patterns of tissues not in follicle were comparable between fresh control and vitrification groups while freezing control group showed increased tendency. Conclusively, it was confirmed that vitrification method has a prevention effect against cryoinjury and this method could be an alternative approach for cryopreservation of genetic material in pigs. Further study is needed to examine the viability of oocytes derived from vitrified-warmed ovarian tissue.

Keywords

Acknowledgement

This work was supported by the Cooperative Research Program for Agriculture Science and Technology Development (project no. PJ01335401), Rural Development Administration, Republic of Korea.

References

  1. Borges EN, Silva RC, Futino DO, Rocha-Junior CM, Amorim CA, Bao SN, Lucci CM. 2009. Cryopreservation of swine ovarian tissue: effect of different cryoprotectants on the structural preservation of preantral follicle oocytes. Cryobiology 59:195-200. https://doi.org/10.1016/j.cryobiol.2009.07.003
  2. Bosch P, Hernandez-Fonseca HJ, Miller DM, Wininger JD, Massey JB, Lamb SV, Brackett BG. 2004. Development of antral follicles in cryopreserved cat ovarian tissue transplanted to immunodeficient mice. Theriogenology 61:581-594. https://doi.org/10.1016/S0093-691X(03)00244-9
  3. Brandao FAS, Alves KA, de Brito DCC, Pereira LMC, de Morais GB, Naupas LVS, de Souza SS, Alves BG, Rodrigues APR, Teixeira DIA. 2021. Vitrification of canine ovarian tissue using the Ovarian Tissue Cryosystem (OTC) device. Reprod. Domest. Anim. 56:1156-1161. https://doi.org/10.1111/rda.13979
  4. Damasio LC, Soares-Junior JM, Iavelberg J, Maciel GA, de Jesus Simoes M, dos Santos Simoes R, da Motta EV, Baracat MCP, Baracat EC. 2016. Heterotopic ovarian transplantation results in less apoptosis than orthotopic transplantation in a minipig model. J. Ovarian Res. 9:14. https://doi.org/10.1186/s13048-016-0223-1
  5. Donnez J and Dolmans MM. 2017. Fertility preservation in women. N. Engl. J. Med. 377:1657-1665. https://doi.org/10.1056/NEJMra1614676
  6. Fathi R, Valojerdi MR, Eimani H, Hasani F, Yazdi PE, Ajdari Z, Tahaei LS. 2011. Sheep ovarian tissue vitrification by two different dehydration protocols and needle immersing methods. Cryo Letters 32:51-56.
  7. Forman EJ. 2018. Ovarian tissue cryopreservation: still experimental? Fertil. Steril. 109:443-444. https://doi.org/10.1016/j.fertnstert.2017.12.031
  8. Gabriel PR, Torres P, Fratto MC, Cisale H, Claver JA, Lombardo DM, Fischman ML. 2017. Effects of different sucrose concentrations on vitrified porcine preantral follicles: qualitative and quantitative analysis. Cryobiology 76:1-7. https://doi.org/10.1016/j.cryobiol.2017.05.005
  9. Gandolfi F, Paffoni A, Papasso Brambilla E, Bonetti S, Brevini TA, Ragni G. 2006. Efficiency of equilibrium cooling and vitrification procedures for the cryopreservation of ovarian tissue: comparative analysis between human and animal models. Fertil. Steril. 85 Suppl 1:1150-1156. https://doi.org/10.1016/j.fertnstert.2005.08.062
  10. Gook DA, Edgar DH, Borg J, Archer J, Lutjen PJ, McBain JC. 2003. Oocyte maturation, follicle rupture and luteinization in human cryopreserved ovarian tissue following xenografting. Hum. Reprod. 18:1772-1781. https://doi.org/10.1093/humrep/deg365
  11. Gook DA, McCully BA, Edgar DH, McBain JC. 2001. Development of antral follicles in human cryopreserved ovarian tissue following xenografting. Hum. Reprod. 16:417-422. https://doi.org/10.1093/humrep/16.3.417
  12. Hwang IS, Hara H, Chung HJ, Hirabayashi M, Hochi S. 2013. Rescue of vitrified-warmed bovine oocytes with rho-associated coiled-coil kinase inhibitor. Biol. Reprod. 89:26.
  13. Hwang IS, Kwon D, Kwak TU, Lee JW, Im GS, Hwang S. 2016. Improved survival and developmental rates in vitrified-warmed pig oocytes after recovery culture with coenzyme Q10. Cryo Letters 37:59-67.
  14. Hwang IS, Park MR, Kwak TU, Park SH, Lim JH, Kim SW, Hwang S. 2018. Effect of cytochalasin B treatment on the improvement of survival rate in vitrified pig oocyte. Dev. Reprod. 22:245-252. https://doi.org/10.12717/DR.2018.22.3.245
  15. Hwang IS, Park MR, Lee HS, Kwak TU, Son HY, Kang JK, Lee JW, Lee K, Park EW, Hwang S. 2020. Developmental and degenerative characterization of porcine parthenogenetic fetuses during early pregnancy. Animals (Basel) 10:622. https://doi.org/10.3390/ani10040622
  16. Hwang IS and Hochi S. 2014. Recent progress in cryopreservation of bovine oocytes. Biomed Res. Int. 2014:570647. https://doi.org/10.1155/2014/570647
  17. Kagawa N, Silber S, Kuwayama M. 2009. Successful vitrification of bovine and human ovarian tissue. Reprod. Biomed. Online 18:568-577. https://doi.org/10.1016/S1472-6483(10)60136-8
  18. Kaneko H, Kikuchi K, Noguchi J, Hosoe M, Akita T. 2003. Maturation and fertilization of porcine oocytes from primordial follicles by a combination of xenografting and in vitro culture. Biol. Reprod. 69:1488-1493. https://doi.org/10.1095/biolreprod.103.017038
  19. Kikuchi K, Kaneko H, Nakai M, Noguchi J, Ozawa M, Ohnuma K, Kashiwazaki N. 2006. In vitro and in vivo developmental ability of oocytes derived from porcine primordial follicles xenografted into nude mice. J. Reprod. Dev. 52:51-57. https://doi.org/10.1262/jrd.17065
  20. Leonel ECR, Corral A, Risco R, Camboni A, Taboga SR, Kilbride P, Vazquez M, Morris J, Dolmans MM, Amorim CA. 2019. Stepped vitrification technique for human ovarian tissue cryopreservation. Sci. Rep. 9:20008. https://doi.org/10.1038/s41598-019-56585-7
  21. Lotz L, Hauenstein T, Nichols-Burns SM, Strissel P, Hoffmann I, Findeklee S, Dittrich R, Beckmann MW, Oppelt PG. 2015. Comparison of whole ovary cryotreatments for fertility preservation. Reprod. Domest. Anim. 50:958-964. https://doi.org/10.1111/rda.12615
  22. Lu XL, Yu J, Zhang G, Wei ZT, Li JT, Zhang JM. 2014. Effects of varying tissue sizes on the efficiency of baboon ovarian tissue vitrification. Cryobiology 69:79-83. https://doi.org/10.1016/j.cryobiol.2014.05.006
  23. Nichols-Burns SM, Lotz L, Schneider H, Adamek E, Daniel C, Stief A, Grigo C, Klump D, Hoffmann I, Beckmann MW, Dittrich R. 2014. Preliminary observations on whole-ovary xenotransplantation as an experimental model for fertility preservation. Reprod. Biomed. Online 29:621-626. https://doi.org/10.1016/j.rbmo.2014.07.017
  24. Nyachieo A, Spiessens C, Chai DC, Kiulia NM, Willemen D, Mwenda JM, Bourgain C, D'Hooghe TM. 2013. Ovarian tissue cryopreservation by vitrification in olive baboons (papio anubis): a pilot study. Gynecol. Obstet. Invest. 75:157-162. https://doi.org/10.1159/000346084
  25. Picton HM. 2018. Preservation of female fertility in humans and animal species. Anim. Reprod. 15:301-309. https://doi.org/10.21451/1984-3143-ar2018-0089
  26. Ramezani M, Salehnia M, Jafarabadi M. 2017. Short term culture of vitrified human ovarian cortical tissue to assess the cryopreservation outcome: molecular and morphological analysis. J. Reprod. Infertil. 18:162-171.
  27. Rodrigues AP, Amorim CA, Costa SH, Matos MH, Santos RR, Lucci CM, Bao SN, Ohashi OM, Figueiredo JR. 2004. Cryopreservation of caprine ovarian tissue using glycerol and ethylene glycol. Theriogenology 61:1009-1024. https://doi.org/10.1016/j.theriogenology.2003.04.001
  28. Salehnia M, Abbasian Moghadam E, Rezazadeh Velojerdi M. 2002. Ultrastructure of follicles after vitrification of mouse ovarian tissue. Fertil. Steril. 78:644-645. https://doi.org/10.1016/S0015-0282(02)03287-9
  29. Santos RR, Amorim C, Cecconi S, Fassbender M, Imhof M, Lornage J, Paris M, Schoenfeldt V, Martinez-Madrid B. 2010. Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds. Anim. Reprod. Sci. 122:151-163. https://doi.org/10.1016/j.anireprosci.2010.08.010
  30. Shi Q, Xie Y, Wang Y, Li S. 2017. Vitrification versus slow freezing for human ovarian tissue cryopreservation: a systematic review and meta-anlaysis. Sci. Rep. 7:8538. https://doi.org/10.1038/s41598-017-09005-7
  31. Snow M, Cox SL, Jenkin G, Trounson A, Shaw J. 2002. Generation of live young from xenografted mouse ovaries. Science 297:2227. https://doi.org/10.1126/science.1073693
  32. Takeo T, Nakao S, Nakagawa Y, Sztein JM, Nakagata N. 2020. Cryopreservation of mouse resources. Lab. Anim. Res. 36:33. https://doi.org/10.1186/s42826-020-00066-w
  33. Terraciano PB, Garcez TA, Berger M, Durli I, Kuhl CP, Batista VO, Schneider RA, Festa J, Pilar E, Ferreira C, Passos EP, Lima EC. 2020. Ovarian tissue vitrification is more efficient than slow freezing to preserve ovarian stem cells in CF-1 mice. JBRA Assist. Reprod. 24:13-19.
  34. Whyte JJ and Prather RS. 2011. Genetic modifications of pigs for medicine and agriculture. Mol. Reprod. Dev. 78:879-891. https://doi.org/10.1002/mrd.21333
  35. Zhou GB and Li N. 2009. Cryopreservation of porcine oocytes: recent advances. Mol. Hum. Reprod. 15:279-285. https://doi.org/10.1093/molehr/gap016