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RESEARCH ARTICLE

Assessment of DNA damage in goat preantral follicles after vitrification of the ovarian cortex

Luciana R. Faustino A F , Adeline A. Carvalho A , Cleidson M. G. Silva A , Rafael Rossetto A , Cláudio A. P. Lopes A , Maurício F. van Tilburg B , Pedro B. M. Carneiro C , Sônia N. Báo D , Arlindo A. A. Moura B , Vilceu Bordignon E , José R. Figueiredo A and Ana Paula R. Rodrigues A
+ Author Affiliations
- Author Affiliations

A Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), Faculty of Veterinary, State University of Ceará, Av. Paranjana, 1700, Campus do Itaperi, Fortaleza, CE 60740-930, Brazil.

B Laboratory of Animal Physiology, Department of Animal Science, Federal University of Ceará, Av. Mister Hull, s/n Campus do Pici, Fortaleza, CE 60021-970, Brazil.

C Institute of Marine Science (LABOMAR), Federal University of Ceará, Av. Abolição, 3207, Meireles, Fortaleza, CE 60165-081, Brazil.

D Laboratory of Electron Microscopy, Department of Cell Biology, University of Brasilia, Campus Darcy Ribeiro, Asa Norte, Brasília, DF 70919-970, Brazil.

E Department of Animal Science, McGill University, 21,111 Lakeshore Road, Ste. Anne de Bellevue, Quebec, H9X 3V9, Canada.

F Corresponding author. Email: lrfaustino@fulbrightmail.org

Reproduction, Fertility and Development 27(3) 440-448 https://doi.org/10.1071/RD13164
Submitted: 29 May 2013  Accepted: 23 November 2013   Published: 3 January 2014

Abstract

Effective methods for gamete preservation should have low impact on DNA integrity. The present study investigated the effects of vitrification of goat ovarian tissues on the occurrence of DNA fragmentation and DNA double-stand breaks using the terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL) assay and detection of phosphorylated histone H2AX (γH2AX), respectively. Goat ovaries were collected at a local abattoir and 12 tissue fragments were prepared from each ovarian pair. Tissue fragments were used as fresh control samples or were cultured in vitro, vitrified or vitrified and cultured. Vitrification was performed using the Ovarian Tissue Cryosystem. Fragments from all groups (control and treatments) were processed for histology, transmission electron microscopy, TUNEL assay and immunofluorescence. Compared with fresh control samples, a lower percentage of morphologically normal follicles was detected in the vitrification followed by culture treatment group (P < 0.05). Normal follicular ultrastructure was observed in all groups. Immunofluorescence revealed the presence of γH2AX foci in few oocytes and ovarian stromal cells. TUNEL-positive follicles were found in samples without significant differences among groups (P > 0.05). In conclusion, the vitrification protocol used in the present study did not increase DNA damage in preantral follicles enclosed in goat ovarian tissues.

Additional keywords: DNA fragmentation, γH2AX, oocyte, terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL) assay.


References

Acker, J. P., Elliott, J. A. W., and McGann, L. E. (2001). Intercellular ice propagation: experimental evidence for ice growth through membrane pores. Biophys. J. 81, 1389–1397.
Intercellular ice propagation: experimental evidence for ice growth through membrane pores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtlCktro%3D&md5=95efea62153aafa7c42a741e0e79d5b0CAS | 11509353PubMed |

Amorim, C. A., David, A., Van Langendonckt, A., Dolmans, M. M., and Donnez, J. (2011). Vitrification of human ovarian tissue: effect of different solutions and procedures. Fertil. Steril. 95, 1094–1097.
Vitrification of human ovarian tissue: effect of different solutions and procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitFGlsbc%3D&md5=160d78309f35b18a9c8f524ab6a5a4e5CAS | 21168134PubMed |

Amorim, C. A., Dolmans, M. M., David, A., Jaeger, J., Vanacker, J., Camboni, A., Donnez, J., and Van Langendonckt, A. (2012). Vitrification and xenografting of human ovarian tissue. Fertil. Steril. 98, 1291–1298.
Vitrification and xenografting of human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 22883570PubMed |

Anderson, R. A., Wallace, W. H. B., and Baird, D. T. (2008). Ovarian cryopreservation for fertility preservation: indications and outcomes. Reproduction 136, 681–689.
Ovarian cryopreservation for fertility preservation: indications and outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1Cktg%3D%3D&md5=e44822017a6b213b918e994ea16be997CAS | 18682546PubMed |

Bhardwaj, J. K., and Sharma, R. K. (2012). Detection of apoptosis during follicular atresia in caprine ovary by tunel and fluorescence microscopy. J. Cell Tissue Research 12, 3273–3278.

Borges, E. N., Silva, R. C., Futino, D. O., Rocha-Junior, C. M., Amorim, C. A., Báo, S. N., and Lucci, C. M. (2009). Cryopreservation of swine ovarian tissue: effect of different cryoprotectants on the structural preservation of preantral follicle oocytes. Cryobiology 59, 195–200.
Cryopreservation of swine ovarian tissue: effect of different cryoprotectants on the structural preservation of preantral follicle oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKgu7nK&md5=1d3dc9c1d9e2a63544480887639fdb7dCAS | 19616533PubMed |

Boutron, P. (1986). Comparison with the theory of the kinetics and extent of ice crystallization and of the glass-forming tendency in aqueous cryoprotective solutions. Cryobiology 23, 88–102.
Comparison with the theory of the kinetics and extent of ice crystallization and of the glass-forming tendency in aqueous cryoprotective solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xhs1equrk%3D&md5=b88cc20c88f43d055d7159f3d25aa545CAS | 3956232PubMed |

Carvalho, A. A., Faustino, L. R., Silva, C. M., Castro, S. V., Luz, H. K., Rossetto, R., Lopes, C. A., Campello, C. C., Figueiredo, J. R., Rodrigues, A. P. R., and Costa, A. P. (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.
Influence of vitrification techniques and solutions on the morphology and survival of preantral follicles after in vitro culture of caprine ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjmsVGhtw%3D%3D&md5=c15ce1a5fed5179d8a5709feca871369CAS | 21719087PubMed |

Carvalho, A. A., Faustino, L. R., Silva, C. M., Castro, S. V., Lopes, C. A., Santos, R. R., Báo, S. N., Figueiredo, J. R., and Rodrigues, A. P. R. (2013). Novel wide-capacity method for vitrification of caprine ovaries: Ovarian Tissue Cryosystem (OTC). Anim. Reprod. Sci. 138, 220–227.
Novel wide-capacity method for vitrification of caprine ovaries: Ovarian Tissue Cryosystem (OTC).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFCjtLg%3D&md5=9f647dc7899c92a0225837bef1c45877CAS | 23522695PubMed |

Castro, S. V., Carvalho, A. A., Silva, C. M., Faustino, L. R., Campello, C. C., Lucci, C. M., Báo, S. N., Figueiredo, J. R., and Rodrigues, A. P. (2011). Freezing solution containing dimethylsulfoxide and fetal calf serum maintains survival and ultrastructure of goat preantral follicles after cryopreservation and in vitro culture of ovarian tissue. Cell Tissue Res. 346, 283–292.
Freezing solution containing dimethylsulfoxide and fetal calf serum maintains survival and ultrastructure of goat preantral follicles after cryopreservation and in vitro culture of ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVyls7zK&md5=59f1c4edc41ae95a65b5c1b2f235a106CAS | 22006251PubMed |

Celestino, J. J. H., Santos, R. R., Lopes, C. A. P., Martins, F. S., Matos, M. H. T., Melo, M. A. P., Báo, S. N., Rodrigues, A. P. R., Silva, J. R. V., and Figueiredo, J. R. (2008). Preservation of bovine preantral follicle viability and ultra-structure after cooling and freezing ovarian tissue. Anim. Reprod. Sci. 108, 309–318.
Preservation of bovine preantral follicle viability and ultra-structure after cooling and freezing ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFais7zN&md5=0e251c5cb6203a9cb70d48c29e8c2ed8CAS |

Charier, G., Couprie, J., Alpha-Bazin, B., Meyer, V., Quéméneur, E., Guérois, R., Callebaut, I., Gilquin, B., and Zinn-Justin, S. (2004). The tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Structure 12, 1551–1562.
The tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntleltbw%3D&md5=84436b55ddf22cddab916d3f8bed6d9eCAS | 15341721PubMed |

Chen, S. U., Chien, C. L., Wu, M. Y., Chen, T. H., Lai, S. M., Lin, C. W., and Yang, Y. S. (2006). Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum. Reprod. 21, 2794–2800.
Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice.Crossref | GoogleScholarGoogle Scholar | 16982660PubMed |

Deanesly, R. (1954). Immature rat ovaries grafted after freezing and thawing. J. Endocrinol. 11, 197–200.
Immature rat ovaries grafted after freezing and thawing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FhtleisA%3D%3D&md5=2fda9a36272e031a245fddca47e0a4a9CAS | 13201707PubMed |

Demirci, B., Salle, B., Frappart, L., Franck, M., Guerin, J. F., and Lornage, J. (2002). Morphological alterations and DNA fragmentation in oocytes from primordial and primary follicles after freezing–thawing of ovarian cortex in sheep. Fertil. Steril. 77, 595–600.
Morphological alterations and DNA fragmentation in oocytes from primordial and primary follicles after freezing–thawing of ovarian cortex in sheep.Crossref | GoogleScholarGoogle Scholar | 11872218PubMed |

Eimani, H., Behbahanian, A., Zeinali, B., Valoujerdi, M. R., Eftekhari, P., Shahverdi, A., Gourabi, H., and Golkar-Narenji, A. (2011). Heterotopic autotransplantation of vitrified mouse ovary. Reprod. Med. Biol. 10, 267–275.
Heterotopic autotransplantation of vitrified mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsF2it7%2FO&md5=2a9306919c64687b2ac2dbafbef2a337CAS |

Fahy, G. M. (1986). The relevance of cryoprotectant ‘toxicity’ to cryobiology. Cryobiology 23, 1–13.
The relevance of cryoprotectant ‘toxicity’ to cryobiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhsVWmtLg%3D&md5=879892d05a53898e725e14cfcd65a007CAS | 3956226PubMed |

Fahy, G. M., MacFarlane, D. R., Angell, C. A., and Meryman, H. T. (1984). Vitrification as an approach to cryopreservation. Cryobiology 21, 407–426.
Vitrification as an approach to cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKltLw%3D&md5=26639ef138f76e1b57837ab411743e66CAS | 6467964PubMed |

Fahy, G. M., Wowk, B., and Wu, J. (2006). Cryopreservation of complex systems: the missing link in the regenerative medicine supply chain. Rejuvenation Res. 9, 279–291.
Cryopreservation of complex systems: the missing link in the regenerative medicine supply chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xks1ajtLc%3D&md5=8294b091dc31915b27a4091bc986272cCAS | 16706656PubMed |

Fathi, R., Valojerdi, M. R., Eimani, H., Hasani, F., Yazdi, P. E., Ajdari, Z., and Tahaei, L. S. (2011). Sheep ovarian tissue vitrification by two different dehydration protocols and needle immersing methods. Cryo Letters 32, 51–56.
| 21468453PubMed |

Faustino, L. R., Santos, R. R., Silva, C. M. G., Pinto, L. C., Celestino, J. J. H., Campello, C. C., Figueiredo, J. R., and Rodrigues, A. P. R. (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.
Goat and sheep ovarian tissue cryopreservation: effects on the morphology and development of primordial follicles and density of stromal cell.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfot1CktQ%3D%3D&md5=8d5206b6e29c343febd602c52f978836CAS | 20800393PubMed |

Faustino, L. R., Rossetto, R., Lima, I. M., Silva, C. M., Saraiva, M. V., Lima, L. F., Silva, A. W., Donato, M. A., Campello, C. C., Peixoto, C. A., Figueiredo, J. R., and Rodrigues, A. P. (2011). Expression of keratinocyte growth factor in goat ovaries and its effects on preantral follicles within cultured ovarian cortex. Reprod. Sci. 18, 1222–1229.
Expression of keratinocyte growth factor in goat ovaries and its effects on preantral follicles within cultured ovarian cortex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Cqsr3M&md5=e5579a6e554c6bb450c2cca39286a3f6CAS | 21693780PubMed |

Giunta, S., and Jackson, S. P. (2011). Give me a break, but not in mitosis: the mitotic DNA damage response marks DNA double-strand breaks with early signaling events. Cell Cycle 10, 1215–1221.
Give me a break, but not in mitosis: the mitotic DNA damage response marks DNA double-strand breaks with early signaling events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1SqsrjF&md5=fa69172c14dd097c82d47ded7b2d39f1CAS | 21412056PubMed |

Giunta, S., Belotserkovskaya, R., and Jackson, S. P. (2010). DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197–207.
DNA damage signaling in response to double-strand breaks during mitosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGlur%2FF&md5=c5307ee4a99da2918dfab6f207992850CAS | 20660628PubMed |

González-Marín, C., Gosálvez, J., and Roy, R. (2012). Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int. J. Mol. Sci. 13, 14 026–14 052.
Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells.Crossref | GoogleScholarGoogle Scholar |

Hanoux, V., Pairault, C., Bakalska, M., Habert, R., and Livera, G. (2007). Caspase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary. Cell Death Differ. 14, 671–681.
Caspase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjt1Sku7w%3D&md5=0bac8fe35b6978ef89ce3e59f12b9eaeCAS | 17082817PubMed |

Huang, L., Mo, Y., Wang, W., Li, Y., Zhang, Q., and Yang, D. (2008). Cryopreservation of human ovarian tissue by solid-surface vitrification. Eur. J. Obstet. Gynecol. Reprod. Biol. 139, 193–198.
Cryopreservation of human ovarian tissue by solid-surface vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsValu7k%3D&md5=5c7aa1e186e99012b1324e7bde23b8c9CAS | 18455864PubMed |

Ishijima, T., Kobayashi, Y., Lee, D. S., Ueta, Y. Y., Matzui, M., Lee, J. Y., Suwa, Y., Miyahara, K., and Suzuki, H. (2006). Cryopreservation of canine ovaries by vitrification. J. Reprod. Dev. 52, 293–299.
Cryopreservation of canine ovaries by vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlKisbg%3D&md5=1e9e64d101fe15c55da213185a8e413aCAS | 16394621PubMed |

Jacobson, M. D., Weil, M., and Raff, M. C. (1997). Programmed cell death in animal development. Cell 88, 347–354.
Programmed cell death in animal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtFahtbw%3D&md5=1a1134ede6ff07bd8550448eed5d6ae5CAS | 9039261PubMed |

Jaroudi, S., and SenGupta, S. (2007). DNA repair in mammalian embryos. Mutat. Res. 635, 53–77.
DNA repair in mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1CntQ%3D%3D&md5=08fa1bd944dac893d43dc0581591e8f0CAS | 17141556PubMed |

Kagawa, N., Silber, S., and Kuwayama, M. (2009). Successful vitrification of bovine and human ovarian tissue. Reprod. Biomed. Online 18, 568–577.
Successful vitrification of bovine and human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 19401001PubMed |

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. Hum. Reprod. 24, 1670–1683.
Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslGkurg%3D&md5=bdadb64435100c4880fa7279ca47c01bCAS | 19359339PubMed |

Kim, D. H., No, J. G., Park, J. J., Park, J. K., and Yoo, J. G. (2012). Successful in vitro development of preantral follicles isolated from vitrified mouse whole ovaries. Reprod. Dev. Biol. 36, 255–260.
Successful in vitro development of preantral follicles isolated from vitrified mouse whole ovaries.Crossref | GoogleScholarGoogle Scholar |

Lee, S., Song, J. Y., Ku, S. Y., Kim, S. H., and Kim, T. (2012). Fertility preservation in women with cancer. Clin. Exp. Reprod. Med. 39, 46–51.
Fertility preservation in women with cancer.Crossref | GoogleScholarGoogle Scholar | 22816069PubMed |

Lima, I. M. T., Celestino, J. J. H., Faustino, L. R., Magalhães-Padilha, D. M., Rossetto, R., Brito, I. R., Donato, M. A. M., Lopes, C. A. P., Campello, C. C., Peixoto, C. A., Figueiredo, J. R., and Rodrigues, A. P. (2012). Dynamic medium containing kit ligand and follicle-stimulating hormone promotes follicular survival, activation, and growth during long-term in vitro culture of caprine preantral follicles. Cells Tissues Organs 195, 260–271.
Dynamic medium containing kit ligand and follicle-stimulating hormone promotes follicular survival, activation, and growth during long-term in vitro culture of caprine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVGiu7Y%3D&md5=aa475b32398488bec97ad078902694e7CAS |

Lucci, C. M., Silva, R. V., Carvalho, C. A., Figueiredo, R., and Báo, N. (2001). Light microscopical and ultrastructural characterization of goat preantral follicles. Small Rumin. Res. 41, 61–69.
Light microscopical and ultrastructural characterization of goat preantral follicles.Crossref | GoogleScholarGoogle Scholar | 11423235PubMed |

Mazoochi, T., Salehnia, M., Valojerdi, M. R., and Mowla, S. J. (2008). Morphologic, ultrastructural, and biochemical identification of apoptosis in vitrified-warmed mouse ovarian tissue. Fertil. Steril. 90, 1480–1486.
Morphologic, ultrastructural, and biochemical identification of apoptosis in vitrified-warmed mouse ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 17888428PubMed |

Mazur, P. (1984). Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247, C125–C142.
| 1:CAS:528:DyaL2cXls1Ors7w%3D&md5=87942b9dbe23f3e309c9d5f31fd208d9CAS | 6383068PubMed |

Otala, M., Erkkilä, K., Tuuri, T., Sjöberg, J., Suomalainen, L., Suikkari, A. M., Pentikäinen, V., and Dunkel, L. (2002). Cell death and its suppression in human ovarian tissue culture. Mol. Hum. Reprod. 8, 228–236.
Cell death and its suppression in human ovarian tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XislSms7s%3D&md5=d508e7a5a66a49f2208de96eda4858e9CAS | 11870230PubMed |

Parrott, D. M. V. (1960). The fertility of mice with orthotopic ovarian grafts derived from frozen tissue. J. Reprod. Fertil. 1, 230–241.
The fertility of mice with orthotopic ovarian grafts derived from frozen tissue.Crossref | GoogleScholarGoogle Scholar |

Paynter, S. J., Cooper, A., Fuller, B. J., and Shaw, R. W. (1999). Cryopreservation of bovine ovarian tissue: structural normality of follicles after thawing and culture in vitro. Cryobiology 38, 301–309.
Cryopreservation of bovine ovarian tissue: structural normality of follicles after thawing and culture in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzktlKhtA%3D%3D&md5=77424bfbea49fa9a094c6ee5830b2a64CAS | 10413573PubMed |

Pegg, D. E. (2007). Principles of cryopreservation. In ‘Cryopreservation and Freeze-Drying Protocols’. (Eds J. G. Day and G. N. Stacey.) pp. 39–57. (Humana Press: Totowa, NJ.)

Petrillo, S. K., Desmeules, P., Truong, T. Q., and Devine, P. J. (2011). Detection of DNA damage in oocytes of small ovarian follicles following phosphoramide mustard exposures of cultured rodent ovaries in vitro. Toxicol. Appl. Pharmacol. 253, 94–102.
Detection of DNA damage in oocytes of small ovarian follicles following phosphoramide mustard exposures of cultured rodent ovaries in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvVahsr4%3D&md5=28c38d94386c934d3c5a792aa5a03f1bCAS | 21439308PubMed |

Pinto, L. C., Santos, R. R., Faustino, L. R., Silva, C. M. G., Luz, V. B., Júnior, J. E. M., Soares, A. A. X., Celestino, J. J. H., Mafezoli, J., Campello, C. C., Figueiredo, J. R., and Rodrigues, A. P. (2008). Quantification of dimethyl sulfoxide perfusion in sheep ovarian tissue: a predictive parameter for follicular survival to cryopreservation. Biopreserv. Biobanking 6, 269–276.
Quantification of dimethyl sulfoxide perfusion in sheep ovarian tissue: a predictive parameter for follicular survival to cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFert7o%3D&md5=97abafda1f8795b0fdb856c7a4af3cfdCAS |

Podhorecka, M., Skladanowski, A., and Bozko, P. (2010). H2AX phosphorylation: its role in DNA damage response and cancer therapy. J. Nucleic Acids 2010, Article ID 920161.

Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858–5868.
DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsleiu7g%3D&md5=06ed3715f25e8d7e71d7e000a924d26fCAS | 9488723PubMed |

Salama, M., Winkler, K., Murach, K. F., Seeber, B., Ziehr, S. C., and Wildt, L. (2013). Female fertility loss and preservation: threats and opportunities. Ann. Oncol. 24, 598–608.
Female fertility loss and preservation: threats and opportunities.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s7htFGluw%3D%3D&md5=a3cf056c6b798817cdc0a92c59ee1fceCAS | 23129121PubMed |

Santos, R. R., Tharasanit, T., Van Haeften, T., Figueiredo, J. R., Silva, J. R. V., and Van den Hurk, R. (2007). Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods. Cell Tissue Res. 327, 167–176.
Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28nptFCitA%3D%3D&md5=e25fa184853f51274646adb359e46ccaCAS | 16937112PubMed |

Santos, R. R., Knijn, H. M., Vos, P. L., Oei, C. H., Van Loon, T., Colenbrander, B., Gadella, B. M., van den Hurk, R., and Roelen, B. A. (2009). Complete follicular development and recovery of ovarian function of frozen-thawed, autotransplanted caprine ovarian cortex. Fertil. Steril. 91, 1455–1458.
Complete follicular development and recovery of ovarian function of frozen-thawed, autotransplanted caprine ovarian cortex.Crossref | GoogleScholarGoogle Scholar | 18722611PubMed |

Seneda, M. M., Godmann, M., Murphy, B. D., Kimmins, S., and Bordignon, V. (2008). Developmental regulation of histone H3 methylation at lysine 4 in the porcine ovary. Reproduction 135, 829–838.
Developmental regulation of histone H3 methylation at lysine 4 in the porcine ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVOksrc%3D&md5=d805c3112df4147e736cf087176b11cfCAS | 18502896PubMed |

Sheikhi, M., Hultenby, K., Niklasson, B., Lundqvist, M., and Hovatta, O. (2011). Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue. Hum. Reprod. 26, 594–603.
Clinical grade vitrification of human ovarian tissue: an ultrastructural analysis of follicles and stroma in vitrified tissue.Crossref | GoogleScholarGoogle Scholar | 21217141PubMed |

Trapphoff, T., El Hajj, N., Zechner, U., Haaf, T., and Eichenlaub-Ritter, U. (2010). DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles. Hum. Reprod. 25, 3025–3042.
DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFSgsbbF&md5=ec38fe4efd9e9993e254debeda359417CAS | 20940142PubMed |

Wanderley, L. S., Luz, H. K. M., Faustino, L. R., Lima, I. M. T., Lopes, C. A. P., Silva, A. R., Báo, S. N., Campello, C. C., Rodrigues, A. P. R., and Figueiredo, J. R. (2012). Ultrastructural features of agouti (Dasyprocta aguti) preantral follicles cryopreserved using dimethyl sulfoxide, ethylene glycol and propanediol. Theriogenology 77, 260–267.
Ultrastructural features of agouti (Dasyprocta aguti) preantral follicles cryopreserved using dimethyl sulfoxide, ethylene glycol and propanediol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1Sqsw%3D%3D&md5=bf7e4a07b9a2f187ee63af1486ef525fCAS | 21924476PubMed |

Xing, W., Zhou, C., Bian, J., Montag, M., Xu, Y., Li, Y., and Li, T. (2010). Solid-surface vitrification is an appropriate and convenient method for cryopreservation of isolated rat follicles. Reprod. Biol. Endocrinol. 8, 42.
Solid-surface vitrification is an appropriate and convenient method for cryopreservation of isolated rat follicles.Crossref | GoogleScholarGoogle Scholar | 20459796PubMed |

Yeoman, R. R., Wolf, D. P., and Lee, D. M. (2005). Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing. Fertil. Steril. 83, 1248–1254.
Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing.Crossref | GoogleScholarGoogle Scholar | 15831299PubMed |

Zhivotovsky, B., and Kroemer, G. (2004). Apoptosis and genomic instability. Nat. Rev. Mol. Cell Biol. 5, 752–762.
Apoptosis and genomic instability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFCms7o%3D&md5=57448b1995d7d1e051f2bb90b875ab76CAS | 15340382PubMed |

Zhou, X. H., Wu, Y. J., Shi, J., Xia, Y. X., and Zheng, S. S. (2010). Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology 60, 101–105.
Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivFemt74%3D&md5=1280e5308e22fcd4c625d578e0c0dfd0CAS | 19800618PubMed |