Abstract
In this study, the efficiency of the “Needle Immersed Vitrification” technique was tested on cryopreserved feline ovarian tissue. For vitrification, ovarian fragments (0.5–1.5 mm2) from each ovary were collected; the grafts were exposed to 7.5–15% ethylene glycol and 7.5–15% dimethyl sulfoxide at room temperature and stored in liquid nitrogen at least 1 week. Morphologic examinations, expression of genes such as B cell lymphoma 2, B-cell lymphoma-2-associated X protein, Bone morphogenetic protein 15, zone of polarizing activity, zona pellucida C protein and DNA (cytosine-5)-methyltransferase 1, ultrastructural analysis and viability tests were carried out from collected grafts. Light microscopy examinations revealed the percentage of morphologically normal primordial follicles in a fresh group which was significantly higher than the treatment groups (p < 0.001). Terminal deoxynucleotidyl transferase dUTP nick end labeling and anti-caspase-3 staining observed in oocytes, follicle cells, interstitial tissue showed higher rates of apoptosis for post-vitrification and -transplantation groups than freshly grafted ovarian tissues. Furthermore, we observed significant downregulation of zone of polarizing activity and zona pellucida C protein gene expression in vitrified ovarian tissue grafts than in the fresh grafts (p < 0.05). In conclusion, we suggest that the needle immersed vitrification method is a convenient, cheap, and feasible vitrification method for cat ovarian tissues. However, further studies need to be performed to determine more optimal vitrification solutions and equilibration times for the needle immersed vitrification method in order to adapt it for cat ovaries.
Similar content being viewed by others
References
Abedelahi A, Salehnia M, Allameh AA, Hajizadeh H (2009) Comparison of ultrastructure and morphology of mouse ovarian follicles after conventional and direct cover vitrification using different concentrations of ethylene glycol. Iran J Reprod Med 7:45–52
Abir R, Fisch B, Jessel S, Felz C, Ben-Haroush A, Orvieto R (2011) Improving posttransplantation survival of human ovarian tissue by treating the host and graft. Fertil Steril 15:1205–1210
Agca Y (2000) Cryopreservation of oocyte and ovarian tissue. ILAR J 41:207–220
Amorim CA, Curaba M, Langendonckt AV, Dolmas MM, Donnez J (2011) Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod Biomed Online 23:160–186
Baird DT, Webb R, Campbell BK, Harkness LM, Gosden RG (1999) Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at − 196 °C. Endocrinology 140:462–471
Blackmore DG, Baillie LR, Holt JE, Dierkx L, Aitken RJ, McLaughlin EA (2004) Biosynthesis of the canine zona pellucida requires the integrated participation of both oocytes and granulosacells. Biol Reprod 71:661–668
Bosch P, Hernandez-Fonseca H, 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
Candy CJ, Wood MJ, Whittingham DG (1995) Follicular development in cryopreserved marmoset ovarian tissue after transplantation. Hum Reprod 10:2334–2338
Carvalho AA, Faustino LR, Silva CMG, Castro SV, Luz HKM, Rossetto R, Lopes CAP, Campello CC, Figueiredo JR, Rodrigues APR, Costa APR (2011) Influence of vitrification techniques and solutions on the morphology and survival of preantral follicles after in vitro culture of caprine ovarian tissue. Theriogenology 76:933–941
Chen SU, Yang YS (2009) Slow freezing or vitrification of oocytes: their effects on survival and meiotic spindles, and the time schedule for clinical practice. Taiwan J Obstet Gynecol 48:15–22
Chen CH, Chen SG, Wu GJ, Wang J, Yu CP, Liu JY (2006) Autologous heterotopic transplantation of intact rabbit ovary after frozen banking at − 196 °C. Fertil Steril 86:1059–1066
Demeestere I, Simon P, Buxant F, Robin V, Fernandez SA, Centner J, Delbaere A, Englert Y (2006) Ovarian function and spontaneous pregnancy after combined heterotopic and orthotopic cryopreserved ovarian tissue transplantation in a patient previously treated with bone marrow transplantation: case report. Hum Reprod 21:2010–2014
Demirci B, Lornage J, Salle B, Poirel MT, Guerin JF, Franck M (2003) The cryopreservation of ovarian tissue: uses and indications in veterinary medicine. Theriogenology 60:999–1010
Diaz-Garcia C, Milenkovic M, Groth K, Dahm-Kahler P, Olausson M, Brannstorm M (2011) Ovarian cortex transplantation in the baboon: comparision of four different intra-abdominal transplantation sites. Hum Reprod 26:3303–3311
Dittrich R, Lotz L, Fehm T, Krüssel J, von Wolff M, Toth B, van der Ven H, Schüring AN, Würfel W, Hoffmann I, Beckmann MW (2015) Xenotransplantation of cryopreserved human ovarian tissue—a systematic review of MII oocyte maturation and discussion of it as a realistic option for restoring fertility after cancer treatment. Fertil Steril 103:1557–1565
Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, Martinez-Madrid B, Van Langendonckt A (2004) Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364:1405–1410
Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM (2006) Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update 12:519–535
Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O’Neill CL, Songsasen N, Woodruff RI, Woodruff TK (2016) Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice. Reproduction 152:201–210
Fatehi R, Ebrahimi B, Shahhosseini M, Farrokhi A, Fathi R (2014) Effect of ovarian tissue vitrification method on mice preantral follicular development and gene expression. Theriogenology 81:302–308
Fathi R, Valojerdi MR, Eimani H, Hasani F, Yazdi PE, Ajdaru Z, Tahaei LS (2011) Sheep ovarian tissue vitrification by two different dehydration protocols and needle immersing methods. CryoLetters 32:51–56
Faustino LR, Santos RR, Silva CMG, Pinto LC, Celestino JJH, Campello CC, Figueiredo JR, Rodrigues APR (2010) Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell. Anim Reprod Sci 122:90–97
Fonseca HJH (2002) Xenotransplantation of ovarian tissue into male immunodeficient mice. Ph.D. thesis, Athens, Georgica
Galiguis J, Pope CE, Gómez MC, Dumas C, Leibo SP (2012) 64 cryopreservation of cat ovarian tissue by vitrification. Reprod Fertil Dev 25:179
Gosden RG, Boulton MI, Grant K, Webb R (1994) Follicular development from ovarian xenografts in SCID mice. J Reprod Fertil 101:619–623
Gougeon A (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 17:121–155
Hussein MR, Bedaiwy MA, Falcone T (2006) Analysis of apoptotic cell death, Bcl-2, and p53 protein expression in freshly fixed and cryopreserved ovarian tissue after exposure to warm ischemia. Fertil Steril 85:1082–1092
Kagawa N, Silber S, Kuwayama M (2009) Succesful vitrification of bovine and human ovarian tissue. Reprod Biomed Online 18:568–577
Kasai M (2002) Advances in the cryopreservation of mammalian oocytes and embryos: development of ultrarapid vitrification. Reprod Med Biol 1:1–9
Klocke S, Bündgen N, Köster F, Eichenlaub-Ritter U, Griesinger G (2015) Slow-freezing versus vitrification for human ovarian tissue cryopreservation. Arch Gynecol Obstet 291:419–426
Liebermann J, Nawroth F, Isachenko V, Isachenko E, Rahimi G, Tucker MJ (2002) Potential importance of vitrification in reproductive medicine. Biol Reprod 67:1671–1680
Lima AKF, Silva AR, Santos RR, Sales DM, Evangelista AF, Figuiredo JR, Silva LDM (2006) Cryopreservation of preantral ovarian follicles in situ from domestic cats (Felis catus) using different cryoprotective agents. Theriogenology 66:1664–1666
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
Luvoni G, Tessaro I, Apparicio M, Ruggeri E, Luciano A, Modina S (2012) Effect of vitrification of feline ovarian cortex on follicular and oocyte quality and competence. Reprod Domest Anim 47:385–391
Marsella T, Sena P, Xella S, La Marca A, Giulini S, De Pol A, Volpe A, Marzona L (2008) Human ovarian tissue cryopreservation: effect of sucrose concentration on morphological features after thawing. Reprod Biomed Online 16:257–267
Mouttham L, Comizzoli P (2016) The preservation of vital functions in cat ovarian tissues during vitrification depends more on the temperature of the cryoprotectant exposure than on the sucrose supplementation. Cryobiology 73:187–195
Mouttham L, Comizzoli P (2017) Presence of sucrose in the vitrification solution and exposure for longer periods of time improve post-warming follicle integrity in cat ovarian tissues. Reprod Domest Anim 52(Suppl):224–229
Nugent D, Newton H, Gallivan L, Gosden RG (1998) Protective effect of vitamin E on ischaemia–reperfusion injury in ovarian grafts. J Reprod Fertil 114:341–346
Oktay K, Karlikaya G (2000) Ovarian function after transplantation of frozen, banked autologous ovarian tissue. N Engl J Med 342:1919
Oskam I, Azarbaijani AA, Santos RR (2010) Histologic and ultrastructural features of cryopreserved ovine ovarian tissue: deleterious effect of 1,2-propanediol applying different thawing protocols. Fertil Steril 93:2764–2766
Pegg DE (2001) The current status of tissue cryopreservation. CryoLetters 22:105–114
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for groupwise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:36
Pyne DG, Liu J, Abdelgawad M, Sun Y (2014) Digital microfluidic processing of mammalian embryos for vitrification. PLoS ONE 24:e108128
Radford JA, Lieberman BA, Brison DR, Smith AR, Critchlow JD, Russell SA, Watson JA, Harris M, Gosden RG, Shalet SM (2001) Orthotopic reimplantation of cryopreserved ovarian cortical strips after high-dose chemotherapy for Hodgkin’s lymphoma. Lancet 357:1172–1175
Rahimi G, Isachenko V, Kreienberg R, Sauer H, Todorov P, Tawadros S, Mallmann P, Nawroth F, Isachenko E (2010) Re-vascularisation in human ovarian tissue after conventional freezing or vitrification and xenotransplantation. Eur J Obstet Gynecol Reprod Biol 149:63–67
Rodrigues APR, Amorim CA, Costa SHF, Matos MHT, 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
Sánchez F, Adriaenssens T, Romero S, Smitz J (2009) Quantification of oocyte-specific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro. Mol Hum Reprod 15:539–550
Sanfilippo S, Canis M, Smitz J, Sion B, Darcha C, Janny L, Brugnon F (2015) Vitrification of human ovarian tissue: a practical and relevant alternative to slow freezing. Reprod Biol Endocrinol 25:67
Santos RR, Knijn HM, Vos PLAM, Oei CHY, van Loon T, Colenbrander B, Gadella BM, van den Hurk R, Roelen BAJ (2009) Complete follicular development and recovery of ovarian function of frozen-thawed, autotransplanted caprine ovarian cortex. Fertil Steril 91:1455–1458
Schmidt KL, Byskov AG, Nyboe Andersen A, Müller J, Yding Andersen C (2003) Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Hum Reprod 18:1158–1164
Shaw JM, Oranratnachai A, Trounson AO (2000) Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53:59–72
Silber SJ (2012) Ovary cryopreservation and transplantation for fertility preservation. Mol Hum Reprod 18:59–67
Silva JMM, Pinheiro LGP, Leite JAD, Melo LHF, Lunardi FO, Filho RCCB, Mendonça CV (2014) Histological study of rat ovaries cryopreserved by vitrification or slow freezing and reimplanted in the early or late postmenopausal stage. Acta Cir Bras 29:299–305
Tanpradit N, Chatdarong K (2011) Cat ovarian tissue cryopreservation using a passive cooling device. Thai J Vet Med Suppl 41:115–116
Tanpradit N, Comizzoli P, Srisuwatanasagul S, Chatdarong K (2015) Positive impact of sucrose supplementation during slow freezing of cat ovarian tissues on cellular viability, follicle morphology, and DNA integrity. Theriogenology 83:1553–1561
Ting AY, Yeoman RR, Lawson MS, Zelinski MB (2011) In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum Reprod 26:2461–2472
Wakasa I, Hayashi M, Abe Y, Suzuki H (2017) Distribution of follicles in canine ovarian tissues and xenotransplantation of cryopreserved ovarian tissues with even distribution of follicles. Reprod Domest Anim 52(Suppl):219–223
Wang Y, Xiao Z, Li L, Fan W, Li SW (2008) Novel needle immersed vitrification: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation. Hum Reprod 23:2256–2265
Woods EJ, Benson JD, Agca Y, Critser JK (2004) Fundamental cryobiology of reproductive cells and tissues. Cryobiology 48:146–156
Xiao Z, Wang Y, Li L, Luo S, Li SW (2010) Needle immersed vitrification can lower the concentration of cryoprotectant in human ovarian tissue cryopreservation. Fertil Steril 94:2323–2328
Yavin S, Arav A (2007) Measurement of essential physical properties of vitrification solutions. Theriogenology 67:81–89
Zhou XH, Wu YJ, Shi J, Xia YX, Zheng SS (2010) Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology 60:101–105
Acknowledgements
The authors would like to thank Dr. Yüksel Ağca for his valuable support and guidance. This research was supported by The Scientific and Technical Research Council of Turkey (TUBITAK) under the Grant Number 112O846.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors do not have any conflict of interest.
Rights and permissions
About this article
Cite this article
Demirel, M.A., Acar, D.B., Ekim, B. et al. The evaluation of xenotransplantation of feline ovarian tissue vitrified by needle immersed vitrification technique into male immunodeficient mice. Cell Tissue Bank 19, 133–147 (2018). https://doi.org/10.1007/s10561-017-9663-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10561-017-9663-0