Cryoprotective effect of antifreeze protein III on the rabbit ovary
Qin Zeng
A # , Kai Wang B # , Li-Bin He A , Ting-Ting Wang A , Xue-Mei Fan C and Wei-Xin Liu A *
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Reproductive Medicine, Sichuan Provincial Maternity and Child Health Care Hospital, The Affiliated Women’s and Children’s Hospital of Chengdu Medical College, Chengdu 610045, China.
B Department of Acute Care Surgery, Sichuan Provincial People’s Hospital, Sichuan Academy of Medical Sciences, Chengdu 610072, China.
C School of Medical and Life Sciences/Reproductive & Women-Children Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu 610041, China.
* Correspondence to: liuweixind@163.com
# These authors contributed equally to this paper
Handling Editor: Ye Yuan
Reproduction, Fertility and Development 34(9) 645-657 https://doi.org/10.1071/RD21324
Published online: 22 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)
Abstract
Context: Ovarian tissue cryopreservation is effective in preserving fertility in cancer patients who have concerns about fertility loss due to cancer treatment. However, ischemia reduces the lifespan of grafts. Microvascular transplantation of cryopreserved whole ovary may allow immediate revascularisation, but the damage incurred during the cryopreservation procedure may cause follicular depletion; hence, preventing chilling injury would help maintain ovarian function.
Aim: This study was designed to investigate the beneficial effects of antifreeze protein III (AFP III) on rabbit ovary cryopreservation.
Methods: Ovaries (n = 25) obtained from 5-month-old female rabbits (n = 13) were frozen by slow freezing and vitrification. Cryoprotectant media were supplemented with and without 1 mg/mL of AFP III. The experiment was divided into five groups: fresh control group (F), slow freezing group (S), slow freezing group with AFP III (AFP III-S), vitrification group (V) and vitrification group with AFP III (AFP III-V). All groups of ovaries were examined by histological characteristics analysis, ultrastructural analysis, apoptosis detection and follicle viability test.
Key results: With slow freezing, the normal rate of change in follicle morphology, density of stromal cells and the survival rate of follicles in the AFP III supplemented group were significantly higher than those in the non-supplemented group, and a lower oocyte apoptotic rate was shown in the AFP III supplemented group. In the vitrification groups, the normal rate of change in follicle morphology and density of stromal cells in the AFP III supplemented group were significantly higher than those in the non-supplemented group, and a lower oocyte apoptotic rate was found in the AFP III supplemented group. But there was no obvious difference in the survival rate of follicles between the two groups. There was also no significant difference in the normal rate of change in follicle morphology, the survival rate of follicles and the apoptotic rate of oocytes between the vitrification and slow freezing groups (P > 0.05), but the density of stromal cells in the vitrification groups was statistically higher than that of the slow freezing group (P < 0.05).
Conclusions: The addition of AFP III in slow freezing and vitrification could improve the cryoprotective effect of ovaries, which was more evident in slow freezing.
Implications: The findings of this study provide a foundation for further research on the effects of AFP III in human ovarian tissue.
Keywords: antifreeze protein III, cancer patients, cryopreservation, infertility, reproduction, slow freezing, vitrification, whole ovaries.
References
Asgari, F, Valojerdi, MR, Ebrahimi, B, and Fatehi, R (2015). Three dimensional in vitro culture of preantral follicles following slow-freezing and vitrification of mouse ovarian tissue. Cryobiology 71, 529–536.| Three dimensional in vitro culture of preantral follicles following slow-freezing and vitrification of mouse ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 26586099PubMed |
Bagis, H, Tas, A, and Kankavi, O (2008). Determination of the expression of fish antifreeze protein (AFP) in 7th generation transgenic mice tissues and serum. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 309A, 255–261.
| Determination of the expression of fish antifreeze protein (AFP) in 7th generation transgenic mice tissues and serum.Crossref | GoogleScholarGoogle Scholar |
Baird, DT, Webb, R, Campbell, BK, et al. (1999). Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at −196 C. Endocrinology 140, 462.
| Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at −196 C.Crossref | GoogleScholarGoogle Scholar | 9886858PubMed |
Carpenter, JF, and Hansen, TN (1992). Antifreeze protein modulates cell survival during cryopreservation: mediation through influence on ice crystal growth. Proceedings of the National Academy of Sciences of the United States of America 89, 8953–8957.
| Antifreeze protein modulates cell survival during cryopreservation: mediation through influence on ice crystal growth.Crossref | GoogleScholarGoogle Scholar | 1409591PubMed |
Chao, H, Davies, PL, and Carpenter, JF (1996). Effects of antifreeze proteins on red blood cell survival during cryopreservation. Journal of Experimental Biology 199, 2071–2076.
| Effects of antifreeze proteins on red blood cell survival during cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Courbiere, B, Odagescu, V, Baudot, A, Massardier, J, Mazoyer, C, Salle, B, and Lornage, J (2006). Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols. Fertility and Sterility 86, 1243–1251.
| Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols.Crossref | GoogleScholarGoogle Scholar | 16978623PubMed |
Courbiere, B, Caquant, L, Mazoyer, C, Franck, M, Lornage, J, and Salle, B (2009). Difficulties improving ovarian functional recovery by microvascular transplantation and whole ovary vitrification. Fertility and Sterility 91, 2697–2706.
| Difficulties improving ovarian functional recovery by microvascular transplantation and whole ovary vitrification.Crossref | GoogleScholarGoogle Scholar | 18440531PubMed |
Davies, PL, and Hew, CL (1990). Biochemistry of fish antifreeze proteins. The FASEB Journal 4, 2460–2468.
| Biochemistry of fish antifreeze proteins.Crossref | GoogleScholarGoogle Scholar | 2185972PubMed |
DeVries, AL, and Wohlschlag, DE (1969). Freezing resistance in some Antarctic fishes. Science 163, 1073–1075.
| Freezing resistance in some Antarctic fishes.Crossref | GoogleScholarGoogle Scholar | 5764871PubMed |
Donnez, J, Dolmans, MM, Demylle, D, et al. (2004). Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. The Lancet 364, 1405–1410.
| Livebirth after orthotopic transplantation of cryopreserved ovarian tissue.Crossref | GoogleScholarGoogle Scholar |
Fabbri, R, Pasquinelli, G, Keane, D, Magnani, V, Paradisi, R, and Venturoli, S (2010). Optimization of protocols for human ovarian tissue cryopreservation with sucrose, 1,2-propanediol and human serum. Reproductive BioMedicine Online 21, 819–828.
| Optimization of protocols for human ovarian tissue cryopreservation with sucrose, 1,2-propanediol and human serum.Crossref | GoogleScholarGoogle Scholar | 21050819PubMed |
Faustino, LR, Santos, RR, Silva, CMG, Pinto, LC, Celestino, JJH, Campello, CC, Figueiredo, JR, and Rodrigues, APR (2010). Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell. Animal Reproduction Science 122, 90–97.
| Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell.Crossref | GoogleScholarGoogle Scholar | 20800393PubMed |
Gage, AA, and Baust, J (1998). Mechanisms of tissue injury in cryosurgery. Cryobiology 37, 171–186.
| Mechanisms of tissue injury in cryosurgery.Crossref | GoogleScholarGoogle Scholar | 9787063PubMed |
Hreinsson, J, Zhang, P, Swahn, ML, Hultenby, K, and Hovatta, O (2003). Cryopreservation of follicles in human ovarian cortical tissue. Comparison of serum and human serum albumin in the cryoprotectant solutions. Human Reproduction 18, 2420–2428.
| Cryopreservation of follicles in human ovarian cortical tissue. Comparison of serum and human serum albumin in the cryoprotectant solutions.Crossref | GoogleScholarGoogle Scholar | 14585896PubMed |
Imhof, M, Hofstetter, G, Bergmeister, H, Rudas, M, Kain, R, Lipovac, M, and Huber, J (2004). Cryopreservation of a whole ovary as a strategy for restoring ovarian function. Journal of Assisted Reproduction and Genetics 21, 459–465.
| Cryopreservation of a whole ovary as a strategy for restoring ovarian function.Crossref | GoogleScholarGoogle Scholar | 15704522PubMed |
Imhof, M, Bergmeiter, H, Lipovac, M, Rudas, M, Hofstetter, G, and Huber, J (2006). Orthotopic microvascular reanastomosis of whole cryopreserved ovine ovaries resulting in pregnancy and live birth. Fertility and Sterility 85, 1208–1215.
| Orthotopic microvascular reanastomosis of whole cryopreserved ovine ovaries resulting in pregnancy and live birth.Crossref | GoogleScholarGoogle Scholar | 16616094PubMed |
Jacobs, LA, and Pucci, DA (2013). Adult survivors of childhood cancer: the medical and psychosocial late effects of cancer treatment and the impact on sexual and reproductive health. The Journal of Sexual Medicine 10, 120–126.
| Adult survivors of childhood cancer: the medical and psychosocial late effects of cancer treatment and the impact on sexual and reproductive health.Crossref | GoogleScholarGoogle Scholar | 23387917PubMed |
Jo, JW, Jee, BC, Lee, JR, et al. (2011). Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertility and Sterility 96, 1239–1245.
| Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 21917250PubMed |
Jo, JW, Jee, BC, Suh, CS, and Kim, SH (2012). The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes. PLoS ONE 7, e37043.
| The beneficial effects of antifreeze proteins in the vitrification of immature mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 22649508PubMed |
Kamijima, T, Sakashita, M, Miura, A, Nishimiya, Y, and Tsuda, S (2013). Antifreeze protein prolongs the life-time of insulinoma cells during hypothermic preservation. PLoS ONE 8, e73643.
| Antifreeze protein prolongs the life-time of insulinoma cells during hypothermic preservation.Crossref | GoogleScholarGoogle Scholar | 24069217PubMed |
Keros, V, Xella, S, Hultenby, K, Pettersson, K, Sheikhi, M, Volpe, A, Hreinsson, J, and Hovatta, O (2009). Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Human Reproduction 24, 1670–1683.
| Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 19359339PubMed |
Kim, MK, Kong, HS, Youm, HW, and Jee, BC (2017). Effects of supplementation with antifreeze proteins on the follicular integrity of vitrified-warmed mouse ovaries: comparison of two types of antifreeze proteins alone and in combination. Clinical and Experimental Reproductive Medicine 44, 8–14.
| Effects of supplementation with antifreeze proteins on the follicular integrity of vitrified-warmed mouse ovaries: comparison of two types of antifreeze proteins alone and in combination.Crossref | GoogleScholarGoogle Scholar | 28428938PubMed |
Knight, CA, Hallett, J, and DeVries, AL (1988). Solute effects on ice recrystallization: an assessment technique. Cryobiology 25, 55–60.
| Solute effects on ice recrystallization: an assessment technique.Crossref | GoogleScholarGoogle Scholar | 3349811PubMed |
Lee, SG, Koh, HY, Lee, JH, Kang, S-H, and Kim, HJ (2012). Cryopreservative effects of the recombinant ice-binding protein from the arctic yeast Leucosporidium sp. on red blood cells. Applied Biochemistry and Biotechnology 167, 824–834.
| Cryopreservative effects of the recombinant ice-binding protein from the arctic yeast Leucosporidium sp. on red blood cells.Crossref | GoogleScholarGoogle Scholar | 22622645PubMed |
Lee, J, Kim, SK, Youm, HW, et al. (2015a). Effects of three different types of antifreeze proteins on mouse ovarian tissue cryopreservation and transplantation. PLoS ONE 10, e0126252.
| Effects of three different types of antifreeze proteins on mouse ovarian tissue cryopreservation and transplantation.Crossref | GoogleScholarGoogle Scholar | 25938445PubMed |
Lee, JR, Youm, HW, Lee, HJ, Jee, BC, Suh, CS, and Kim, SH (2015b). Effect of antifreeze protein on mouse ovarian tissue cryopreservation and transplantation. Yonsei Medical Journal 56, 778–784.
| Effect of antifreeze protein on mouse ovarian tissue cryopreservation and transplantation.Crossref | GoogleScholarGoogle Scholar | 25837185PubMed |
Leinala, EK, Davies, PL, Doucet, D, Tyshenko, MG, Walker, VK, and Jia, Z (2002). A beta-helical antifreeze protein isoform with increased activity. Structural and functional insights. Journal of Biological Chemistry 277, 33349–33352.
| A beta-helical antifreeze protein isoform with increased activity. Structural and functional insights.Crossref | GoogleScholarGoogle Scholar |
Lundy, T, Smith, P, O’Connell, A, Hudson, NL, and McNatty, KP (1999). Populations of granulosa cells in small follicles of the sheep ovary. Reproduction 115, 251–262.
| Populations of granulosa cells in small follicles of the sheep ovary.Crossref | GoogleScholarGoogle Scholar |
Martinez-Madrid, B, Dolmans, M-M, Van Langendonckt, A, Defrère, S, and Donnez, J (2004). Freeze-thawing intact human ovary with its vascular pedicle with a passive cooling device. Fertility and Sterility 82, 1390–1394.
| Freeze-thawing intact human ovary with its vascular pedicle with a passive cooling device.Crossref | GoogleScholarGoogle Scholar | 15533365PubMed |
Milenkovic, M, Diaz-Garcia, C, Wallin, A, and Brännström, M (2012). Viability and function of the cryopreserved whole rat ovary: comparison between slow-freezing and vitrification. Fertility and Sterility 97, 1176–1182.
| Viability and function of the cryopreserved whole rat ovary: comparison between slow-freezing and vitrification.Crossref | GoogleScholarGoogle Scholar | 22341373PubMed |
Nishijima, K, Tanaka, M, Sakai, Y, et al. (2014). Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit. Cryobiology 69, 22–25.
| Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit.Crossref | GoogleScholarGoogle Scholar | 24809634PubMed |
Neto, V, Buff, S, Lornage, J, Bottollier, B, Guérin, P, and Joly, T (2008). Effects of different freezing parameters on the morphology and viability of preantral follicles after cryopreservation of doe rabbit ovarian tissue. Fertility and Sterility 89, 1348–1356.
| Effects of different freezing parameters on the morphology and viability of preantral follicles after cryopreservation of doe rabbit ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 17604027PubMed |
Petru, E (2010). Fertility preservation and infertility treatment in breast cancer patients. Wiener Medizinische Wochenschrift 160, 487–492.
| Fertility preservation and infertility treatment in breast cancer patients.Crossref | GoogleScholarGoogle Scholar | 20972713PubMed |
(2014). Ovarian tissue cryopreservation: a committee opinion. Fertility and Sterility 101, 1237–1243.
| Ovarian tissue cryopreservation: a committee opinion.Crossref | GoogleScholarGoogle Scholar | 24684955PubMed |
Raymond, JA, and DeVries, AL (1977). Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proceedings of the National Academy of Sciences of the United States of America 74, 2589–2593.
| Adsorption inhibition as a mechanism of freezing resistance in polar fishes.Crossref | GoogleScholarGoogle Scholar | 267952PubMed |
Rubinsky, L, Raichman, N, Lavee, J, Frenk, H, Ben-Jacob, E, and Bickler, PE (2010). Antifreeze protein suppresses spontaneous neural activity and protects neurons from hypothermia/re-warming injury. Neuroscience Research 67, 256–259.
| Antifreeze protein suppresses spontaneous neural activity and protects neurons from hypothermia/re-warming injury.Crossref | GoogleScholarGoogle Scholar | 20398707PubMed |
Schmidt, KLT, Andersen, CY, Loft, A, Byskov, AG, Ernst, E, and Andersen, AN (2005). Follow-up of ovarian function post-chemotherapy following ovarian cryopreservation and transplantation. Human Reproduction 20, 3539–3546.
| Follow-up of ovarian function post-chemotherapy following ovarian cryopreservation and transplantation.Crossref | GoogleScholarGoogle Scholar |
Sheikhi, M, Hultenby, K, Niklasson, B, Lundqvist, M, and Hovatta, O (1989). Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Metallurgical Transactions A 20, 1585–1591.
Wang, J-H (2000). A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation. Cryobiology 41, 1–9.
| A comprehensive evaluation of the effects and mechanisms of antifreeze proteins during low-temperature preservation.Crossref | GoogleScholarGoogle Scholar | 11017755PubMed |
Wang XJ (2011) ‘The influence of cryoprotectan perfusion time on the frozen-thawed whole rabbit ovary.’ (Wenzhou Medical College: Zhejiang)
Wu F (2013) ‘A comparative study of the cryopreservation effect for whole rabbit ovary program med freezing and vitrification.’ (Zhejiang: Wenzhou Medical College)
Xu, Z, Wang, X, Wu, Y, Meng, Y, Wu, F, Zhou, N, Chen, W, Ye, B, Liu, J, and Zhou, Y (2012). Slow-controlled freezing versus speed-cooling for cryopreservation of whole guinea pig ovaries. Theriogenology 77, 483–491.
| Slow-controlled freezing versus speed-cooling for cryopreservation of whole guinea pig ovaries.Crossref | GoogleScholarGoogle Scholar | 21958638PubMed |
Yang, DSC, Sax, M, Chakrabartty, A, and Hew, CL (1988). Crystal structure of an antifreeze polypeptide and its mechanistic implications. Nature 333, 232–237.
| Crystal structure of an antifreeze polypeptide and its mechanistic implications.Crossref | GoogleScholarGoogle Scholar |
Yeh, Y, and Feeney, RE (1996). Antifreeze proteins: structures and mechanisms of function. Chemical Reviews 96, 601–618.
| Antifreeze proteins: structures and mechanisms of function.Crossref | GoogleScholarGoogle Scholar | 11848766PubMed |
Younis, AI, Rooks, B, Khan, S, et al. (1998). The effects of antifreeze peptide III (AFP) and insulin transferrin selenium (ITS) on cryopreservation of chimpanzee (Pan troglodytes) spermatozoa. Journal of Andrology 19, 207–214.
| 9570745PubMed |
Zhang, J-M, Li, L-X, Yang, Y-X, Liu, X-L, and Wan, X-P (2009). Is caspase inhibition a valid therapeutic strategy in cryopreservation of ovarian tissue? Journal of Assisted Reproduction and Genetics 26, 415–420.
| Is caspase inhibition a valid therapeutic strategy in cryopreservation of ovarian tissue?Crossref | GoogleScholarGoogle Scholar | 19697118PubMed |
Zhang, J-M, Sheng, Y, Cao, YZ, et al. (2011). Cryopreservation of whole ovaries with vascular pedicles: vitrification or conventional freezing? Journal of Assisted Reproduction and Genetics 28, 445–452.
| Cryopreservation of whole ovaries with vascular pedicles: vitrification or conventional freezing?Crossref | GoogleScholarGoogle Scholar | 21287401PubMed |
