Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

In vitro growth and development of isolated secondary follicles from vitrified caprine ovarian cortex

Érica S. S. Leal A , Luis A. Vieira A , Naíza A. R. Sá A , Gerlane M. Silva A , Franciele O. Lunardi A , Anna C. A. Ferreira A , Cláudio C. Campello A , Benner G. Alves A , Francielli W. S. Cibin B , Johan Smitz C , José R. Figueiredo A and Ana P. R. Rodrigues A D
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Medicine, LAMOFOPA, PPGCV, State University of Ceará, Av. Dr Silas Munguba, 1700 – Campus of Itaperi, Fortaleza – CE – CEP 60741-903, Brazil.

B University Federal of Pampa, Uruguaiana-Rio Grande do Sul, Av. General Osório, 900 – São Jorge Bagé, RS – CE – 96400-100, Brazil.

C Follicle Biology Laboratory, Center for Reproductive Medicine, UZ Brussel, Laarbeeklaan 101, B-1090 Brussels, Belgium.

D Corresponding author. Email: aprrodriguespapers@gmail.com

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16487
Submitted: 14 May 2016  Accepted: 17 June 2017   Published online: 3 August 2017

Abstract

The aim of this study was to evaluate the viability, antrum formation and in vitro development of isolated secondary follicles from vitrified caprine ovarian cortex in a medium previously established for fresh isolated secondary follicles, in the absence (α-minimum essential medium (α-MEM+) alone) or presence of FSH and vascular endothelial growth factor (VEGF; α-MEM++FSH+VEGF). Ovarian fragments were distributed among five treatments (T1 to T5): fresh follicles were fixed immediately (T1), follicles from fresh tissue were cultured in vitro in α-MEM+ (T2) or α-MEM++FSH+VEGF (T3) and follicles from vitrified tissue were cultured in vitro in α-MEM+ (T4) or α-MEM++FSH+VEGF (T5). After 6 days of culture, treated follicles (T2, T3, T4 and T5) were evaluated for morphology, viability and follicular development (growth, antrum formation and proliferation of granulosa cells by Ki67 and argyrophilic nucleolar organiser region (AgNOR) staining). The levels of reactive oxygen species (ROS) in the culture media were also assessed. Overall, morphology of vitrified follicles was altered (P < 0.05) compared with the fresh follicles. Follicular viability, antrum formation and ROS were similar between treatments (P > 0.05). The average overall and daily follicular growth was highest (P < 0.05) in T3. Granulosa cells in all treatments (T1, T2, T3, T4 and T5) stained positive for Ki67. However, fresh follicles from T3 had significantly higher AgNOR staining (P < 0.05) compared with follicles of T1, T2, T4 and T5. In conclusion, secondary follicles can be isolated from vitrified and warmed ovarian cortex and survive and form an antrum when growing in an in vitro culture for 6 days.

Additional keywords: folliculogenesis, hormone, preantral follicle, vitrification.


References

Abir, R., Roizman, P., Fisch, B., Nitke, S., Okon, E., Orvieto, R., and Ben Rafael, Z. (1999). Pilot study of isolated early human follicles cultured in collagen gels for 24 hours. Hum. Reprod. 14, 1299–1301.
Pilot study of isolated early human follicles cultured in collagen gels for 24 hours.CrossRef | 1:STN:280:DyaK1M3mt1Ohtg%3D%3D&md5=2a379006fd52db84a2f2954423c6037dCAS | open url image1

Abir, R., Fisch, B., Nitke, S., Okon, E., Raz, A., and Ben Rafael, Z. (2001). Morphological study of fully and partially isolated early human follicles. Fertil. Steril. 75, 141–146.
Morphological study of fully and partially isolated early human follicles.CrossRef | 1:STN:280:DC%2BD3MzitF2jsA%3D%3D&md5=09d7ffccadc86099c5cff28caadbb068CAS | open url image1

Apolloni, L. B., Bruno, J. B., Alves, B. G., Ferreira, A. C. A., Paes, V. M., Moreno, J. R. C., Aguiar, F. L. N., Brandão, F. Z., Smitz, J., Apgar, G., and Figueiredo, J. R. (2016). Accelerated follicle growth during the culture of isolated caprine preantral follicles is detrimental to follicular survival and oocyte meiotic resumption. Theriogenology 86, 1530–1540.
Accelerated follicle growth during the culture of isolated caprine preantral follicles is detrimental to follicular survival and oocyte meiotic resumption.CrossRef | 1:CAS:528:DC%2BC28XpvVWrurw%3D&md5=f215516b34fdce2e47feae60d41e0496CAS | open url image1

Araújo, V. R., Silva, G. M., Duarte, A. B. G., Magalhães, D. M., Almeida, A. P., Gonçalves, R. F. B., Bruno, J. B., Silva, T. F., Campello, C. C., Rodrigues, A. P., and Figueiredo, J. R. (2011). Vascular endothelial growth factor-A165 (VEGFA165) stimulates the in vitro development and oocyte competence of goat preantral follicles. Cell Tissue Res. 346, 273–281.
Vascular endothelial growth factor-A165 (VEGFA165) stimulates the in vitro development and oocyte competence of goat preantral follicles.CrossRef | open url image1

Bagchi, A., Woods, E. J., and Critser, J. K. (2008). Cryopreservation and vitrification: recent advances in fertility preservation technologies. Expert Rev. Med. Devices 5, 359–370.
Cryopreservation and vitrification: recent advances in fertility preservation technologies.CrossRef | open url image1

Barberino, R. S., Barros, V. R. P., Menezes, V. G., Santos, L. P., Araújo, V. R., Queiroz, M. A. A., Almeida, J. R. G. S., Palheta, J. R. C., and Matos, M. H. T. (2016). Amburana cearensis leaf extract maintains survival and promotes in vitro development of ovine secondary follicles. Zygote 24, 277–285.
Amburana cearensis leaf extract maintains survival and promotes in vitro development of ovine secondary follicles.CrossRef | 1:CAS:528:DC%2BC28XltVKnsLw%3D&md5=8a9d8d5ed93297542dfbf948e93df44cCAS | open url image1

Bruno, J. B., Celestino, J. J., Lima-Verde, I. B., Lima, L. F., Matos, M. H., Araujo, V. R., Saraiva, M. V., Martins, F. S., Name, K. P., Campello, C. C., Bao, S. N., Silva, J. R., and Figueiredo, J. R. (2009). Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod. Fertil. Dev. 21, 679–687.
Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF.CrossRef | 1:CAS:528:DC%2BD1MXmsVCrurs%3D&md5=f714479c33f363e153ce1b1440cae97bCAS | open url image1

Carvalho, A. A., Faustino, L. R., Silva, C. M. G., Castro, S. V., Luz, H. K. M., Rossetto, R., Lopes, C. A. P., Campello, C. C., Figueiredo, J. R., Rodrigues, A. P. R., and Costa, A. P. R. (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 | 1:STN:280:DC%2BC3MjmsVGhtw%3D%3D&md5=05250aba95c418251b7f0048d8a3e8ffCAS | open url image1

Carvalho, A. A., Faustino, L. R., Silva, C. M. G., Castro, S. V., Lopes, C. A. P., 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 | 1:CAS:528:DC%2BC3sXksFCjtLg%3D&md5=02df659f15ffbcd56d57b4a420715cdfCAS | open url image1

Carvalho, A. A., Faustino, L. R., Silva, C. M., Castro, S. V., Lobo, C. H., Santos, F. W., Santos, R. R., Campello, C. C., Bordignon, V., Figueiredo, J. R., and Rodrigues, A. P. (2014). Catalase addition to vitrification solutions maintains goat ovarian preantral follicles stability. Res. Vet. Sci. 97, 140–147.
Catalase addition to vitrification solutions maintains goat ovarian preantral follicles stability.CrossRef | 1:CAS:528:DC%2BC2cXhtlSqs7vJ&md5=eab1494ce06560c6d2e7bc048b3ed8d2CAS | open url image1

Cecconi, S., Capacchietti, G., Russo, V., Berardinelli, P., Mattioli, M., and Barboni, B. (2004). In vitro growth of preantral follicles isolated from cryopreserved ovine ovarian tissue. Biol. Reprod. 70, 12–17.
In vitro growth of preantral follicles isolated from cryopreserved ovine ovarian tissue.CrossRef | 1:CAS:528:DC%2BD2cXhvVOl&md5=4cff20ae242d2623fe660dbae772ea3dCAS | open url image1

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 | open url image1

Choi, J. Y., Lee, B. E., Lee, E. Y., Yoon, B.-K., Bae, D. S., and Choi, D. S. (2008). Cryopreservation of ovarian tissues temporarily suppresses the proliferation of granulosa cells in mouse preantral follicles. Cryobiology 56, 36–42.
Cryopreservation of ovarian tissues temporarily suppresses the proliferation of granulosa cells in mouse preantral follicles.CrossRef | 1:CAS:528:DC%2BD1cXpt1Kruw%3D%3D&md5=4edf99e825521c86a9e4398e61d4b968CAS | open url image1

Chun, S. Y., Eisenhauer, K. M., Minami, S., Billig, H., Perlas, E., and Hsueh, A. J. (1996). Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinology 137, 1447–1456.
Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor.CrossRef | 1:CAS:528:DyaK28XhvVegtLk%3D&md5=8f60bade73461a3842f1fed0fc10b67dCAS | open url image1

Courbiere, B., Odagescu, V., Baudot, A., Massardier, M., Mazoyer, C., Salle, B., and Lornage, J. (2006). Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols. Fertil. Steril. 86, 1243–1251.
Cryopreservation of the ovary by vitrification as an alternative to slow-cooling protocols.CrossRef | open url image1

Demant, M., Trapphoff, T., Thomas, F. T., Arnold, G. J., and Eichenlaub-Ritte, U. (2012). Vitrification at the pre-antral stage transiently alters inner mitochondrial membrane potential but proteome of in vitro grown and matured mouse oocytes appears unaffected. Hum. Reprod. 27, 1096–1111.
Vitrification at the pre-antral stage transiently alters inner mitochondrial membrane potential but proteome of in vitro grown and matured mouse oocytes appears unaffected.CrossRef | 1:CAS:528:DC%2BC38XksVarsbg%3D&md5=debd6a2181ce82936d8cc4479fff94deCAS | open url image1

Greenaway, J., Connor, K., Pedersen, H. G., Coomber, B. L., LaMarre, J., and Petrik, J. (2004). Vascular endothelial growth factor and its receptor, flk-1/kdr, are cytoprotective in the extravascular compartment of the ovarian follicle. Endocrinology 145, 2896–2905.
Vascular endothelial growth factor and its receptor, flk-1/kdr, are cytoprotective in the extravascular compartment of the ovarian follicle.CrossRef | 1:CAS:528:DC%2BD2cXkt12gu7w%3D&md5=56c4e7a5cc66b38108f201071a20335fCAS | open url image1

Hatami, S., Zavareh, S., Salehnia, M., Lashkarbolouki, T., Taghi, M., Ghorbanian, M. T., and Karimi, I. (2014). Total oxidative status of mouse vitrified pre-antral follicles with pre-treatment of alpha lipoic acid. Iran. Biomed. J. 18, 181–188.
| 1:CAS:528:DC%2BC2cXhs1SgtrjL&md5=dbc4430240c2886afe1798e57f60f4e4CAS | open url image1

Herraiz, S., Novella-Maestre, E., Rodríguez, B., Díaz, C., Sánchez-Serrano, M., Mirabet, V., and Pellicer, A. (2014). Improving ovarian tissue cryopreservation for oncologic patients: slow freezing versus vitrification, effect of different procedures and devices. Fertil. Steril. 101, 775–784.e1.
Improving ovarian tissue cryopreservation for oncologic patients: slow freezing versus vitrification, effect of different procedures and devices.CrossRef | 1:CAS:528:DC%2BC3sXitVWjtbjF&md5=fef796cd399c3e389bc3cac238e9b66bCAS | open url image1

Hulshof, S. C., Figueiredo, J. R., Beckers, J. F., Bevers, M. M., Vanderstichele, H., and Van den Hurk, R. (1997). Bovine preantral follicles and activin: immunohistochemistry for activin and activin receptor and the effect of bovine activin A in vitro. Theriogenology 48, 133–142.
Bovine preantral follicles and activin: immunohistochemistry for activin and activin receptor and the effect of bovine activin A in vitro.CrossRef | 1:CAS:528:DyaK2sXkslanurc%3D&md5=f1ff338f0a3c076543bda94328eba932CAS | open url image1

Isachenko, V., Montag, M., Isachenko, E., Ven, K. V., Dorn, C., Roesing, B., Braun, F., Sadek, F., and Ven, H. (2006). Effective method for in vitro culture of cryopreserved human ovarian tissue. Reprod. Biomed. Online 13, 228–234.
Effective method for in vitro culture of cryopreserved human ovarian tissue.CrossRef | open url image1

Kreeger, P. K., Fernandes, N. N., Woodruff, T. K., and Shea, L. D. (2005). Regulation of mouse follicle development by follicle-stimulating hormone in a three dimensional in vitro culture system is dependent on follicle stage and dose. Biol. Reprod. 73, 942–950.
Regulation of mouse follicle development by follicle-stimulating hormone in a three dimensional in vitro culture system is dependent on follicle stage and dose.CrossRef | 1:CAS:528:DC%2BD2MXhtFGktb%2FM&md5=b2dea649a0918099e3258734b0324421CAS | open url image1

Loetchutinat, C., Kothan, S., Dechsupa, J., Meesungnoen, J., and Jay-Gerin, S. M. (2005). Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 2′,7′-dichlorofluorescein diacetate assay. Radiat. Phys. Chem. 72, 323–331.
Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 2′,7′-dichlorofluorescein diacetate assay.CrossRef | 1:CAS:528:DC%2BD2cXhtVamtLzF&md5=d9fd53f32a39404bd57e368e1410e06aCAS | open url image1

Lunardi, F. O., Chaves, R., Lima, L., Araújo, V., Brito, I., and Azevedo, C. (2015). Vitrified sheep isolated secondary follicles are able to grow and form antrum after a short period of in vitro culture. Cell Tissue Res. 362, 241–251.
Vitrified sheep isolated secondary follicles are able to grow and form antrum after a short period of in vitro culture.CrossRef | open url image1

Lunardi, F. O., Aguiar, F. L. N., Duarte, A. B. G., Araújo, V. R., Lima, L. F., Sá, N. A. R., Correia, H. H. V., Domingues, S. F. S., Campello, C. C., Smitz, J., Figueiredo, J. R., and Rodrigues, A. P. R. (2016). Ovine secondary follicles vitrified out the ovarian tissue grow and develop in vitro better than those vitrified into the ovarian fragments. Theriogenology 85, 1203–1210.
Ovine secondary follicles vitrified out the ovarian tissue grow and develop in vitro better than those vitrified into the ovarian fragments.CrossRef | open url image1

Luyckx, V., Dolmans, M. M., Vanacker, J., Legat, C., Moya, C. F., Donnez, J., and Amorim, C. A. (2014). A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil. Steril. 101, 1149–1156.
A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold.CrossRef | open url image1

Luz, V. B., Araújo, V. R., Duarte, A. B. G., Silva, G. M., Chaves, R. N., Brito, I. R., Serafim, M. K. B., Campello, C. C., Feltrin, C., Bertolini, M., Almeida, A. P., Santos, R. R., and Figueiredo, J. R. (2013). Kit ligand and insulin-like growth factor I affect the in vitro development of ovine preantral follicles. Small Rumin. Res. 115, 99–102.
Kit ligand and insulin-like growth factor I affect the in vitro development of ovine preantral follicles.CrossRef | open url image1

Magalhães, D. M., Duarte, A. B., Araújo, V. R., Brito, I. R., Soares, T. G., Lima, I. M. T., Lopes, C. A. P., Campello, C. C., Rodrigues, A. P. R., and Figueiredo, J. R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–188.
In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone.CrossRef | open url image1

Martinez-Madrid, B., Dolmans, M.-M., Van Langendonckt, A., Defrère, S., Van Eyck, A.-S., and Donnez, J. (2004). Ficoll density gradient method for recovery of isolated human ovarian primordial follicles. Fertil. Steril. 82, 1648–1653.
Ficoll density gradient method for recovery of isolated human ovarian primordial follicles.CrossRef | open url image1

Matos, M. H. T., Lima-Verde, I. B., Luque, M. C. A., Maia, J. E., Silva, J. R. V., Celestino, J. J. H., Martins, F. S., Bao, S. N., Lucci, C. M., and Figueiredo, J. R. (2007). Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173–182.
Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro.CrossRef | 1:CAS:528:DC%2BD2sXkvVWqtb0%3D&md5=6d87eefe83e879b589de425184ee2a01CAS | open url image1

Moniruzzaman, M., Bao, R. M., Taketsuru, H., and Miyano, T. (2009). Development of vitrified porcine primordial follicles in xenografts. Theriogenology 72, 280–288.
Development of vitrified porcine primordial follicles in xenografts.CrossRef | 1:CAS:528:DC%2BD1MXnsFSjt7w%3D&md5=a643e4b01b982c185a93b1773dea9d16CAS | open url image1

Nasrabadi, H. T., Gavami, M., Akbarzadeh, A., Beheshti, R., Mohammadnejad, D., and Abedelahi, A. (2015). Preservation of mouse ovarian tissue follicle morphology and ultra-structure after vitrifying in biotechnological protocols. J. Ovarian Res. 6, 7.
Preservation of mouse ovarian tissue follicle morphology and ultra-structure after vitrifying in biotechnological protocols.CrossRef | open url image1

Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9–22.
Vascular endothelial growth factor (VEGF) and its receptors.CrossRef | 1:CAS:528:DyaK1MXlt1ygsQ%3D%3D&md5=84ed456c3fc2dd1916f8636ffc5d5f7dCAS | open url image1

Newton, H., and Illingworth, P. (2001). In vitro growth of murine pre-antral follicles after isolation from cryopreserved ovarian tissue. Hum. Reprod. 16, 423–429.
In vitro growth of murine pre-antral follicles after isolation from cryopreserved ovarian tissue.CrossRef | 1:STN:280:DC%2BD3M3gs1ajsQ%3D%3D&md5=24379540be051319db96244dd1db018cCAS | open url image1

Oktem, O., Alper, E., Balaban, B., Palaoglu, E., Peker, K., Karakaya, C., and Urman, B. (2011). Vitrified human ovaries have fewer primordial follicles and produce less antiMüllerian hormone than slow-frozen ovaries. Fertil. Steril. 95, 2661–2664.e1.
Vitrified human ovaries have fewer primordial follicles and produce less antiMüllerian hormone than slow-frozen ovaries.CrossRef | open url image1

Peng, X., Yang, M., Wang, L., Tong, C., and Guo, Z. (2010). In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium. J. Assist. Reprod. Genet. 27, 247–257.
In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium.CrossRef | open url image1

Sá, N. A. R., Araújo, V. R., Correia, H. H. V., Ferreira, A. C. A., Guerreiro, D. D., Sampaio, A. M., Escobar, E., Santos, F. W., Moura, A. A., Lôbo, C. H., Ceccatto, V. M., Campello, C. C., Rodrigues, A. P. R., Leal-Cardoso, J. H., and Figueiredo, J. R. (2017). Anethole improves the in vitro development of isolated caprine secondary follicles. Theriogenology 89, 226–234.
Anethole improves the in vitro development of isolated caprine secondary follicles.CrossRef | open url image1

Sales, A. D., Duarte, A. B. G., Rodrigues, G. Q., Lima, L. F., Silva, G. M., Carvalho, A. A., Brito, I. R., Maranguape, R. M. S., Lobo, C. H., Aragão, J. A. S., Moura, A. A., Figueiredo, J. R., and Rodrigues, A. P. R. (2015). Steady-state level of messenger RNA and immunolocalization of aquaporins 3, 7, and 9 during in vitro growth of ovine preantral follicles. Theriogenology 84, 1–10.
Steady-state level of messenger RNA and immunolocalization of aquaporins 3, 7, and 9 during in vitro growth of ovine preantral follicles.CrossRef | 1:CAS:528:DC%2BC2MXmsFSmsLg%3D&md5=f4a3042a2cf21c59db77a666e64d65feCAS | open url image1

Sánchez, F., Romero, S., and Smitz, J. (2011). Oocyte and cumulus cell transcripts from cultured mouse follicles are induced to deviate from normal in vivo condition by combinations of insulin, follicle-stimulating hormone, and human chorionic gonadotropin. Biol. Reprod. 85, 565–574.
Oocyte and cumulus cell transcripts from cultured mouse follicles are induced to deviate from normal in vivo condition by combinations of insulin, follicle-stimulating hormone, and human chorionic gonadotropin.CrossRef | open url image1

Saraiva, M. V., Rossetto, R., Brito, I. R., Celestino, J. J., Silva, C. M., Faustino, L. R., Almeida, A. P., Bruno, J. B., Magalhães, D. M., Matos, M. H., Campello, C. C., and Figueiredo, J. R. (2010). Dynamic medium produces caprine embryo from preantral follicles grown in vitro. Reprod. Sci. 17, 1135–1143.
Dynamic medium produces caprine embryo from preantral follicles grown in vitro.CrossRef | 1:CAS:528:DC%2BC3cXhs1akt77F&md5=a6c82f1985a06114ab97e53e56e4828aCAS | open url image1

Scalercio, S. R. R. A., Brito, A. B., Domingues, S. F. S., Santos, R. R., and Amorim, C. A. (2015). Immunolocalization of growth, inhibitory, and proliferative factors involved in initial ovarian folliculogenesis from adult common squirrel monkey (Saimiri collinsi). Reprod. Sci. 22, 68–74.
Immunolocalization of growth, inhibitory, and proliferative factors involved in initial ovarian folliculogenesis from adult common squirrel monkey (Saimiri collinsi).CrossRef | 1:CAS:528:DC%2BC2MXitVWmu7g%3D&md5=682781ce77243c21f023c339d6b5c128CAS | open url image1

Shen, M., Liu, Z., Li, B., Teng, Y., Zhang, J., Tang, Y., Sun, S. C., and Liu, H. (2014). Involvement of FoxO1 in the effects of follicle-stimulating hormone on inhibition of apoptosis in mouse granulosa cells. Cell Death Dis. 5, e1475.
Involvement of FoxO1 in the effects of follicle-stimulating hormone on inhibition of apoptosis in mouse granulosa cells.CrossRef | 1:CAS:528:DC%2BC2cXhsl2htbbM&md5=53285373ac58253be2bb1120823eaecaCAS | open url image1

Silva, G. M., Rossetto, R., Chaves, R. N., Duarte, A. B. G., Araújo, V. R., Feltrin, C., Bernuci, M. P., Anselmo-Franci, J. A., Xu, M., Woodruff, T. K., Campello, C. C., and Figueiredo, J. R. (2015). In vitro development of secondary follicles from pre-pubertal and adult goats cultured in two-dimensional or three-dimensional systems. Zygote 23, 475–484.
In vitro development of secondary follicles from pre-pubertal and adult goats cultured in two-dimensional or three-dimensional systems.CrossRef | 1:CAS:528:DC%2BC2MXhtF2isrbO&md5=38b445e6b7441ba5d9deedbcef7f11c7CAS | open url image1

Soares, M., Sahrari, K., Chiti, M. C., Amorim, C. A., Ambroise, J., Donnez, J., and Dolmans, M. M. (2015). The best source of isolated stromal cells for the artificial ovary: medulla or cortex, cryopreserved or fresh? Hum. Reprod. 30, 1589–1598.
The best source of isolated stromal cells for the artificial ovary: medulla or cortex, cryopreserved or fresh?CrossRef | 1:STN:280:DC%2BC2MfmtVOhtg%3D%3D&md5=8f27c78da89b1e0d75dbc5f78aca09d6CAS | open url image1

Taketsuru, H., Takajo, A., Bao, R. M., Hamawaki, A., Yoshikawa, M., and Miyano, T. (2011). Bovine oocytes in secondary follicles grow in medium containing bovine plasma after vitrification. J. Reprod. Dev. 57, 99–106.
Bovine oocytes in secondary follicles grow in medium containing bovine plasma after vitrification.CrossRef | 1:CAS:528:DC%2BC3MXkt1Cnsr4%3D&md5=bb1818c44028b62ddd4c32fbe6f8666eCAS | open url image1

Ting, A. Y., Yeoman, R. R., Lawson, M. S., and Zelinski, M. B. (2011). In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum. Reprod. 26, 2461–2472.
In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification.CrossRef | open url image1

Ting, A. Y., Yeoman, R. R., Lawson, M. S., and Zelinski, M. B. (2012). Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles. Cryobiology 65, 1–11.
Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles.CrossRef | 1:CAS:528:DC%2BC38Xnt1Cgur4%3D&md5=cf473e43094dd7a2bfff0768e3a5a593CAS | open url image1

Ting, A. Y., Yeoman, R. R., Campos, J. R., Lawson, M. S., Mullen, S. F., Fahy, G. M., and Zelinski, M. B. (2013). Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum. Reprod. 28, 1267–1279.
Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system.CrossRef | 1:CAS:528:DC%2BC3sXmtlagsLw%3D&md5=a20965aee6ea5ea1c51035c598fda1e5CAS | open url image1

Tsai-Turton, M., and Luderer, U. (2006). Opposing effects of glutathione depletion and FSH on reactive oxygen species and apoptosis in cultured preovulatory rat follicles. Endocrinology 147, 1224–1236.
Opposing effects of glutathione depletion and FSH on reactive oxygen species and apoptosis in cultured preovulatory rat follicles.CrossRef | 1:CAS:528:DC%2BD28XhvFygtrY%3D&md5=6b8cacb1dfdf51dc54f095624581c0a7CAS | open url image1

Vandelaer, M., Thiry, M., and Goessens, G. (1999). AgNOR proteins from morphologically intact isolated nucleoli. Life Sci. 64, 2039–2047.
AgNOR proteins from morphologically intact isolated nucleoli.CrossRef | 1:CAS:528:DyaK1MXjtVKltrw%3D&md5=5cb0f577b03f8fc140355568137ff934CAS | open url image1

Wang, Y., Xiao, Z., Li, L., Fan, W., and Li, S. W. (2008). Novel needle immersed vitrification 2008: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation. Hum. Reprod. 23, 2256–2265.
Novel needle immersed vitrification 2008: a practical and convenient method with potential advantages in mouse and human ovarian tissue cryopreservation.CrossRef | 1:CAS:528:DC%2BD1cXhtFCiu7fJ&md5=99ae40580ad62ab7faef9bf0248ceac0CAS | open url image1

Xu, J., Bernuci, M. P., Lawson, M. S., Yeoman, R. R., Fisher, T. E., Zelinski, M. B., and Stouffer, R. L. (2010). Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 140, 685–697.
Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin.CrossRef | 1:CAS:528:DC%2BC3cXhsFCnsbfK&md5=ac95599fb4eff801085ff1245d5f844eCAS | open url image1

Xu, J., McGee, W. K., Bishop, C. V., Park, B. S., Cameron, J. L., Zelinski, M. B., and Stouffer, R. L. (2015). Exposure of female macaques to western-style diet with or without chronic T in vivo alters secondary follicle function during encapsulated 3-dimensional culture. Endocrinology 156, 1133–1142.
Exposure of female macaques to western-style diet with or without chronic T in vivo alters secondary follicle function during encapsulated 3-dimensional culture.CrossRef | 1:CAS:528:DC%2BC2MXktF2ltb8%3D&md5=4e4626fb39ccbc3851ec4e7d29842a6eCAS | open url image1

Yeo, J. E., and Kang, S. K. (2007). Selenium effectively inhibits ROS-mediated apoptotic neural precursor cell death in vitro and in vivo in traumatic brain injury. Biochim. Biophys. Acta 1772, 1199–1210.
Selenium effectively inhibits ROS-mediated apoptotic neural precursor cell death in vitro and in vivo in traumatic brain injury.CrossRef | 1:CAS:528:DC%2BD2sXhsVCgtbnP&md5=f35d6f8d97ec4d67dab1e550b73ed02fCAS | open url image1

Zhou, J., Kumar, T. R., Matzuk, M. M., and Bondy, C. (1997). Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol. Endocrinol. 11, 1924–1933.
Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary.CrossRef | 1:CAS:528:DyaK2sXnvVCrt7k%3D&md5=0e86685c51c70df6d4c996d595a32167CAS | open url image1

Zhou, X. H., Wu, Y. J., Shi, J., Ya-xian, 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 | 1:CAS:528:DC%2BC3cXivFemt74%3D&md5=6d3a4fab52d7e332cb90feccf08d6ce6CAS | open url image1



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