Characterisation and cryopreservation of the ovarian preantral follicle population from Spix’s yellow-toothed cavies (Galea spixii Wagler, 1831)
Érica C. G. Praxedes A , Gabriela L. Lima A , Andréia M. Silva A , Carlos A. C. Apolinário A , José A. B. Bezerra A , Ana L. P. Souza A , Moacir F. Oliveira A , Ana P. R. Rodrigues B and Alexandre R. Silva A C
+ Author Affiliations
- Author Affiliations
A Laboratory on Animal Germplasm Conservation, Universidade Federal Rural do Semi-Árido (UFERSA), BR 110, Km 47, Costa e Silva, 59625-900, Mossoró, RN, Brazil.
B Laboratory of Manipulation of Oocytes Enclosed in Preantral Follicles (LAMOFOPA), Veterinary Faculty, Universidade Estadual do Ceará (UECE), Paranjana Avenue, 1700, Itaperi, 60740-000, Fortaleza, CE, Brazil.
C Corresponding author. Email: legio2000@yahoo.com
Reproduction, Fertility and Development 29(3) 594-602 https://doi.org/10.1071/RD15249
Submitted: 20 June 2015 Accepted: 31 August 2015 Published: 8 October 2015
Abstract
The aim of the present study was to characterise the ovarian preantral follicle (PF) population and to establish a solid surface vitrification (SSV) process using dimethyl sulfoxide (DMSO) as a cryoprotectant for preservation of ovarian tissue from yellow-toothed cavies (Galea spixii). Ovaries were fixed for PF population analysis or were subjected to the SSV process. The mean (± s.e.m.) PF population per ovarian pair was estimated to be 416.0 ± 342.8. There were 140.0 ± 56.0 (63.4%) and 125.0 ± 58.0 (64.0%) primary follicles on the right and left ovaries, respectively. The proportion of this follicle category was significantly greater than that of other follicle categories (P < 0.05). The diameter of follicles (123.7 ± 18.3 µm), oocytes (50.1 ± 5.0 µm) and nuclei (14.27 ± 2.01 µm) was larger for secondary ones when compared with other PFs categories. Most PFs were morphologically normal (94.6%), with light microscopy identifying only a few atretic follicles (5.4%). After SSV, there was a reduction in the proportion of morphologically normal PFs compared with the non-vitrified group (69.5% vs 91.2%, respectively). Transmission electron microscopy revealed preservation of oocytes and granulosa cell membranes and the morphological aspect of follicles; the primary change observed in some vitrified PFs was the presence of vacuoles in the oocytes and granulosa cells cytoplasm and turgid mitochondria. In conclusion, the present study provides an estimative and characterization for the PF population in ovaries of G. spixii. Moreover, we report its PFs cryopreservation using an SSV process.
Additional keywords: Caviidae, cryopreservation, germplasm bank, preantral follicles, rodents.
References
Aerts, J. M. J., De Clercq, J. B. P., Andries, S., Leroy, J. L. M. R., Van Aelst, S., and Bols, P. E. J. (2008). Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after Cryologic solid surface vitrification or slow-rate freezing. Cryobiology 57, 163–169.| Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after Cryologic solid surface vitrification or slow-rate freezing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFyltrrE&md5=7f47e41b20278de98ee09aae3437b41fCAS |
Amorim, C. A., Curaba, M., Van Langendonckt, A., Dolmans, M. M., and Donnez, J. (2011). Vitrification as an alternative means of cryopreserving ovarian tissue. Reprod. Biomed. Online 23, 160–186.
| Vitrification as an alternative means of cryopreserving ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 21676653PubMed |
Amstislavsky, S., Brusentsev, E., Kizilova, E., Igonina, T., Abramova, T., and Rozhkova, I. (2015). Embryo cryopreservation and in vitro culture of preimplantation embryos in Campbell’s hamster (Phodopus campbelli). Theriogenology 83, 1056–1063.
| Embryo cryopreservation and in vitro culture of preimplantation embryos in Campbell’s hamster (Phodopus campbelli).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXos1eiug%3D%3D&md5=e4e42fb24180dea5175a93f7430c32bdCAS | 25583223PubMed |
Antoine, N., Lepoint, A., Baeckeland, E., and Goessens, G. (1987). Evolution of the rat oocyte nucleolus during follicular growth. Biol. Cell 59, 107–112.
| Evolution of the rat oocyte nucleolus during follicular growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2szgtVantg%3D%3D&md5=65d3d2983edc4369ff7579d512cfb12cCAS | 2957008PubMed |
Antoine, N., Thiry, M., and Goessens, G. (1989). Ultrastructural and cytochemical studies on extranucleolar bodies in rat oocytes at the preovulatory follicle stage. Biol. Cell 65, 61–66.
| Ultrastructural and cytochemical studies on extranucleolar bodies in rat oocytes at the preovulatory follicle stage.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3gsl2nug%3D%3D&md5=214fb83eea5e7919d00a7baa9584548fCAS | 2468376PubMed |
Au, H. K., Yeh, T. S., Kao, S. H., Tzeng, C. R., and Hsieh, R. H. (2005). Abnormal mitochondrial structure in human unfertilized oocytes and arrested embryos. Ann. N. Y. Acad. Sci. 1042, 177–185.
| Abnormal mitochondrial structure in human unfertilized oocytes and arrested embryos.Crossref | GoogleScholarGoogle Scholar | 15965061PubMed |
Aye, M., Di Giorgio, C., De Mo, M., Botta, A., Perrin, J., and Courbiere, B. (2010). Assessment of the genotoxicity of three cryoprotectants used for human oocyte vitrification: dimethyl sulfoxide, ethylene glycol and propylene glycol. Food Chem. Toxicol. 48, 1905–1912.
| Assessment of the genotoxicity of three cryoprotectants used for human oocyte vitrification: dimethyl sulfoxide, ethylene glycol and propylene glycol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFSiuro%3D&md5=ffa561b9ca8b114779a411d72de22667CAS | 20433889PubMed |
Bernhard, W., and Rouiller, C. (1956). Close topographical relationship between mitochondria and ergastoplasm of liver cells in a definitive phase of cellular activity. J. Biophys. Biochem. Cytol. 2, 73–78.
| Close topographical relationship between mitochondria and ergastoplasm of liver cells in a definitive phase of cellular activity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2s%2FgtlGkug%3D%3D&md5=5a39fbb284a21755a3ef08bf8b314cedCAS | 13357525PubMed |
Bodemer, C. W., and Warnick, S. (1961). Polyovular follicles in the immature hamster ovary. II. The effects of gonadotropic hormones on polyovular follicles. Fertil. Steril. 12, 353–364.
| 1:CAS:528:DyaF38XmvFOmug%3D%3D&md5=96aba0ef6bb713cce00a3eb205a5279aCAS |
Borges, E. N., Silva, R. C., Futino, D. O., Rocha-Junior, C. M. C., 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=4eed9a0e799409e98be6fcd190ab4526CAS | 19616533PubMed |
Braw-Tal, R. (2002). The initiation of follicle growth: the oocyte or the somatic cells? Mol. Cell. Endocrinol. 187, 11–18.
| The initiation of follicle growth: the oocyte or the somatic cells?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1SqsL0%3D&md5=73f3e23ef03a7df66ed53cc5da6f4e14CAS | 11988306PubMed |
Brower, P. T., and Schultz, R. M. (1982). Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev. Biol. 90, 144–153.
| Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387jvFOrsQ%3D%3D&md5=c6574b2e3939d0f8a00c68db40ddfe1cCAS | 7199496PubMed |
Chouinard, L. A. (1971). A light and electron microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse. J. Cell. Sci. 9, 637–663.
| 1:STN:280:DyaE387nvVClsw%3D%3D&md5=af482cf087e89ac90a173b15ceba2b79CAS | 4112474PubMed |
Coss, R. A., Dewey, D. C., and Bamburg, J. R. (1979). Effects of hyperthermia (41.5°C) on Chinese hamster ovary cells analyzed in mitosis. Cancer Res. 39, 1911–1918.
| 1:STN:280:DyaE1M7ovFeqtQ%3D%3D&md5=27746c5d71ef03a344606bcd2e3e4fabCAS | 445391PubMed |
Dalcin, L., Silva, R. C., Paulini, F., Silva, B. D. M., Neves, J. P., and Lucci, C. M. (2013). Cytoskeleton structure, pattern of mitochondrial activity and ultrastructure of frozen or vitrified sheep embryos. Cryobiology 67, 137–145.
| Cytoskeleton structure, pattern of mitochondrial activity and ultrastructure of frozen or vitrified sheep embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWlsrfN&md5=35f24a2f52bebc9c6e0de0a5f34669a8CAS | 23770514PubMed |
Dean, J. (2002). Oocyte-specific genes regulate follicle formation, fertility and early mouse development. J. Reprod. Immunol. 53, 171–180.
| Oocyte-specific genes regulate follicle formation, fertility and early mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1Kjtrs%3D&md5=0f96e1c6c38ef348351b9dc5e42eeda5CAS | 11730914PubMed |
Dumollard, R., Marangos, P., Fitzharris, G., Swann, K., Duchen, M., and Carroll, J. (2004). Sperm triggered [Ca2+] oscillation and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131, 3057–3067.
| Sperm triggered [Ca2+] oscillation and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFKlsb0%3D&md5=36d1ff554931340655c1201a3b67abb8CAS | 15163630PubMed |
Dunbar, B. S., Avery, S., Lee, V., Prasad, S., Schwahn, D., Schwoebel, E., Skinner, S., and Wilkins, B. (1994). The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology and developmental expression. Reprod. Fertil. Dev. 6, 331–347.
| The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology and developmental expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhvFehs7Y%3D&md5=f93f6885f4610819fbe7a095ee74d028CAS | 7831484PubMed |
Eichenlaub-Ritter, U., Wieczorek, M., Lüke, S., and Seidel, T. (2011). Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion 11, 783–796.
| Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsr%2FF&md5=be81660b4e365615908ca88a3002ef97CAS | 20817047PubMed |
Faustino, L. R., Silva, C. M. G., Rossetto, R., Rodrigues, G. Q., Figueiredo, J. R., and Rodrigues, A. P. R. (2011). Estado atual e desafios da criopreservação de tecido ovariano em mamíferos. Rev. Bras. Reprod. Anim., Belo Horizonte. 35, 3–15.
Felipe, A., Cabodevila, J., and Callejas, S. (1999). Anatomico histological characteristics of the ovary of the coypy (Myocastor coypus). Anat. Histol. Embryol. 28, 89–95.
| Anatomico histological characteristics of the ovary of the coypy (Myocastor coypus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzhtlOrsg%3D%3D&md5=778aa89842dea992fb91393f2f00fab4CAS | 10386002PubMed |
Flamini, M. A., Barbeito, C. G., Gimeno, E. J., and Portiansky, E. L. (2009). Histology, histochemistry and morphometry of the ovary of the adult plains viscacha (Lagostomus maximus) in different reproductive stages. Acta. Zool. 90, 390–400.
| Histology, histochemistry and morphometry of the ovary of the adult plains viscacha (Lagostomus maximus) in different reproductive stages.Crossref | GoogleScholarGoogle Scholar |
Gibbons, A., Cueto, M. I., and Pereyra Bonnet, F. (2011). A simple vitrification technique for sheep and goat embryo cryopreservation. Small Rumin. Res. 95, 61–64.
| A simple vitrification technique for sheep and goat embryo cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Harrison, R. J., and Weir, B. J. (1977). Structure of the mammalian ovary. In ‘The ovary’. (Eds P. L. Zuckerman and B. J. Weir.) pp. 112–217. (Academic Press: London.)
Hasegawa, A., Mochida, N., Ogasawara, T., and Koyama, K. (2006). Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization. Fertil. Steril. 86, 1182–1192.
| Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 16963048PubMed |
Hatami, S., Zavareh, S., Salehnia, M., Lashkarbolouki, T., and Karimi, I. (2014). Comparison of oxidative status of mouse pre-antral follicles derived from vitrified whole ovarian tissue and vitrified pre-antral follicles in the presence of alpha lipoic acid. J. Obstet. Gynaecol. Res. 40, 1680–1688.
| Comparison of oxidative status of mouse pre-antral follicles derived from vitrified whole ovarian tissue and vitrified pre-antral follicles in the presence of alpha lipoic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpsVemurs%3D&md5=858423a160d63cfc550143a889fdc7d4CAS | 24888934PubMed |
Hirshfield, A. N. (1989). Granulosa cell proliferation in very small follicles of cycling rats studied by long-term continuous tritiated-thymidine infusion. Biol. Reprod. 41, 309–316.
| Granulosa cell proliferation in very small follicles of cycling rats studied by long-term continuous tritiated-thymidine infusion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGhtA%3D%3D&md5=1e5a7e9e0395a62f0333e50cc4571719CAS | 2804222PubMed |
Iguchi, T., Kamiya, K., Uesugi, Y., Sayama, K., and Takasugi, N. (1991). In vitro fertilization of oocytes from polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol. In Vivo 5, 359–363.
| 1:STN:280:DyaK383jvFKktg%3D%3D&md5=ecdc2df889b9033f8fe440b95a792badCAS | 1810421PubMed |
Jori, F., Lopez-Bejar, M., Mayor, P., and Lopez, C. (2002). Functional anatomy of the ovaries of wild brush-tailed porcupines (Atherurus africanus, Gray 1842) from Gabon. J. Zool. (Lond.) 256, 35–43.
| Functional anatomy of the ovaries of wild brush-tailed porcupines (Atherurus africanus, Gray 1842) from Gabon.Crossref | GoogleScholarGoogle Scholar |
Kaasik, A., Safiulina, D., Choubey, V., Kuum, M., Zharkovsky, A., and Veksler, V. (2007). Mitochondrial swelling impairs the transport of organelles in cerebellar granule neurons J. Biol. Chem. 282, 32 821–32 826.
| Mitochondrial swelling impairs the transport of organelles in cerebellar granule neuronsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1CltbbF&md5=b458c02284d4a6d82d60287ee7d7db0aCAS |
Kagabu, S., and Umezu, M. (2000). Transplantation of cryopreserved mouse, Chinese hamster, rabbit, Japanese monkey and rat ovaries into rat recipient. Exp. Anim. 49, 17–21.
| Transplantation of cryopreserved mouse, Chinese hamster, rabbit, Japanese monkey and rat ovaries into rat recipient.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3mt1OitQ%3D%3D&md5=f0318e77637d2642bf41467fdda9ae02CAS | 10803357PubMed |
Kim, G. A., Kim, H. Y., Kim, J. W., Lee, G., Lee, E., and Lim, J. M. (2010). Ultrastructural deformity of ovarian follicles induced by different cryopreservation protocols. Fertil. Steril. 94, 1548–1550.e1.
| Ultrastructural deformity of ovarian follicles induced by different cryopreservation protocols.Crossref | GoogleScholarGoogle Scholar | 20110089PubMed |
Lancher, Jr., J. R. (1981). The comparative social behavior of Kerondon rupestres and Galea spixii and the ovulation of behaviour in the caviidae. Bull. Carnegie. Mus. Nat. Hist 17, 1–71.
Lucci, C. M., Amorim, C. A., Rodrigues, A. P. R., Figueiredo, J. R., Bao, S. N., Silva, J. R. V., and Goncalves, P. B. D. (1999). Study of preantral follicle population in situ and after mechanical isolation from caprine ovaries at different reproductive stages. Anim. Reprod. Sci. 56, 223–236.
| Study of preantral follicle population in situ and after mechanical isolation from caprine ovaries at different reproductive stages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1Mvis1ajtA%3D%3D&md5=ebb0877c5594ae0505832c1eb75360c3CAS | 10497918PubMed |
Lucci, C. M., Rumpf, R., Figueiredo, J. R., and Bao, S. N. (2002). Zebu (Bos indicus) ovarian preantral follicles: morphological characterization and development of an efficient isolation method. Theriogenology 57, 1467–1483.
| Zebu (Bos indicus) ovarian preantral follicles: morphological characterization and development of an efficient isolation method.Crossref | GoogleScholarGoogle Scholar | 12054205PubMed |
Marshall, W. F. (2003). Gene expression and nuclear architecture during development and differentiation. Mech. Dev. 120, 1217–1230.
| Gene expression and nuclear architecture during development and differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVWgu7c%3D&md5=f6b060edac3344c447ba4742a41f654eCAS | 14623434PubMed |
Matos, M. H. T., Lima-Verde, L. B., Luque, M. C. A., Maia, Jr., J. E., Silva, J. R. V., Celestino, J. J. H., Martins, F. S., Báo, 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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVWqtb0%3D&md5=fef526bdde44cb565fbbe6d4cc331261CAS |
Maxfield, F. R., and Wüstner, D. (2002). Intracellular cholesterol transport. J. Clin. Invest. 110, 891–898.
| Intracellular cholesterol transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnslSksLk%3D&md5=f45d6634a190854d58bdf572e40a9c09CAS | 12370264PubMed |
Mayor, P., Bodmer, R. E., and Lopez-Bejar, M. (2011). Functional anatomy of the female genital organs of the wild black agouti (Dasyprocta fuliginosa) female in the Peruvian Amazon. Anim. Reprod. Sci. 123, 249–257.
| Functional anatomy of the female genital organs of the wild black agouti (Dasyprocta fuliginosa) female in the Peruvian Amazon.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3gtFyhsQ%3D%3D&md5=3de36758977eb991909f3cc448bf60cbCAS | 21216112PubMed |
McClellan, K. A., Gosden, R., and Taketo, T. (2003). Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Dev. Biol. 258, 334–348.
| Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVyrs7g%3D&md5=0ede8aedf13016c0f30a4435b5c304beCAS | 12798292PubMed |
Misteli, T., and Spector, D. L. (1998). The cellular organization of gene expression. Curr. Opin. Cell Biol. 10, 323–331.
| The cellular organization of gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvFelsr8%3D&md5=e887940c09c86f297f0026ed9c1b0064CAS | 9640532PubMed |
Nagy, Z. P., Chang, C. C., Shapiro, D. B., Bernal, D. P., Elsner, C. W., Mitchell-Leef, D., Toledo, A. A., and Kort, H. I. (2009). Clinical evaluation of the efficiency of an oocyte donation program using egg cryobanking. Fertil. Steril. 92, 520–526.
| Clinical evaluation of the efficiency of an oocyte donation program using egg cryobanking.Crossref | GoogleScholarGoogle Scholar | 18692830PubMed |
Oliveira, J. A., and Bonvicino, C. R. (2006). Ordem Rodentia. In ‘Mamíferos do Brasil’. (Eds N. R. Reis, A. L. Peracchi, W. A. Pedro and L. P. Lima.) pp. 347–399. (Universidade Estadual de Londrina – UEL: Londrina.)
Oliveira, M. F., Mess, A., Ambrósio, C. E., Dantas, C. A. G., Favaron, P. O., and Miglino, M. A. (2008). Chorioallantoic placentation in Galea spixii (Rodentia, Caviomorpha, Caviidae). Reprod. Biol. Endocrinol. 6, 39.
| Chorioallantoic placentation in Galea spixii (Rodentia, Caviomorpha, Caviidae).Crossref | GoogleScholarGoogle Scholar | 18771596PubMed |
Peters, H. (1969). The development of the mouse ovary from birth to maturity. Acta Endocrinol. (Copenh.) 62, 98–116.
| 1:STN:280:DyaF1M3psl2lsg%3D%3D&md5=34891d428a1fb05e11007b309f377962CAS | 5394354PubMed |
Picton, H. M., Harris, S. E., Muruvi, W., and Chambers, E. L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–715.
| The in vitro growth and maturation of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1CktA%3D%3D&md5=3169c95f5e75bc1097a0ba5494e96129CAS | 19074213PubMed |
Sánchez-Toranzo, G., Torres-Luque, A., Gramajo-Bühler, M. C., and Bühler, M. I. (2014). Histology of the ovary of Chinchilla lanigera in captivity. Anim. Reprod. Sci. 148, 205–211.
| Histology of the ovary of Chinchilla lanigera in captivity.Crossref | GoogleScholarGoogle Scholar | 24939708PubMed |
Santos, R. R., Amorim, C., Cecconi, S., Fassbender, M., Imhof, M., Lornage, J., Paris, M., Schoenfeldt, V., and 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.
| Cryopreservation of ovarian tissue: an emerging technology for female germline preservation of endangered species and breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahs73E&md5=a003021a935fccb8676658e51430680eCAS | 20832203PubMed |
Santos, P. R. S., Oliveira, M. F., Arroyo, M. A. M., Silva, A. R., Rici, R. E. G., Miglino, M. A., and Assis Neto, A. C. (2014a). Ultrastructure of spermatogenesis in Spix’s yellow-toothed cavy (Galea spixii). Reproduction 147, 13–19.
| 1:CAS:528:DC%2BC2cXhtV2ksb0%3D&md5=54630462c632a803cd21909b4fb1c0bcCAS |
Santos, A. C., Bertassoli, B. M., Viana, D. V., Vasconcelos, B. G., Oliveira, M. F., Miglino, M. A., and Assis Neto, A. C. (2014b). The morphology of female genitalia in Galea spixii (Caviidae, Caviinae). Biosci. J. 30, 1793–1802.
Saragusty, J., and Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.
| Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehsrc%3D&md5=1a2599da9194fe55317a525c1c8976e0CAS | 20974741PubMed |
Shaw, J. M., Oranratnachal, A., and Trounson, A. O. (2000). Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53, 59–72.
| Fundamental cryobiology of mammalian oocytes and ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFagtQ%3D%3D&md5=87da3f6973d00098a9f5af0ebf02f079CAS | 10735062PubMed |
Silva, J. R. V., Brasil, A. F., Santos, R. R., Costa, S. H. F., Rodrigues, A. P. R., Ferreira, M. A. L., Machado, V. P., and Figueiredo, J. R. (2003). Degeneration rate of goat primordial follicles maintained in TCM 199 or PBS at different temperatures and incubation times. Cienc. Rural 33, 913–919.
| Degeneration rate of goat primordial follicles maintained in TCM 199 or PBS at different temperatures and incubation times.Crossref | GoogleScholarGoogle Scholar |
Silva, J. R. V., Van Den Hurk, R., Costa, S. H. F., Andrade, E. R., Nunes, A. P. A., Ferreira, F. V. A., Lôbo, R. N. B., and Figueiredo, J. R. (2004). Survival and growth of goat primordial follicles after in vitro culture of ovarian cortical slices in media containing coconut water. Anim. Reprod. Sci. 81, 273–286.
| Survival and growth of goat primordial follicles after in vitro culture of ovarian cortical slices in media containing coconut water.Crossref | GoogleScholarGoogle Scholar |
Sobaniec-Lotowska, M. E., and Lebensztejn, D. Z. (2006). Ultrastructure of Kupffer cells and hepatocytes in the Dubin–Johnson syndrome: a case report. World J. Gastroenterol. 12, 987–989.
| 16521235PubMed |
Šutovsky, P., Jelínková, L., Antalíková, L., and Motlík, J. (1993). Ultrastructural cytochemistry of the nucleus and nucleolus in growing rabbit oocytes. Biol. Cell. 77, 173–180.
| Ultrastructural cytochemistry of the nucleus and nucleolus in growing rabbit oocytes.Crossref | GoogleScholarGoogle Scholar | 8364396PubMed |
Takeuchi, I. K., Sonta, S., and Takeuchi, Y. K. (1984). Association of perichromatin granules with nuclear pores of growing Chinese hamster oocytes. J. Electron. Microsc. (Tokyo) 33, 388–394.
| 1:STN:280:DyaL2M3js1Skug%3D%3D&md5=375b81c7013663af55b6834f013d56eeCAS | 6535828PubMed |
Tullberg, T. (1899). Ueber das system der Nagetiere: Eine phylogenetische studie. (Akademische Buchdruckerei: Upsala.)
Van Blerkom, J. (1991). Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured oocytes. Proc. Natl Acad. Sci. USA 88, 5031–5035.
| Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ntFehtw%3D%3D&md5=b253ea0cd0750c68ada457a552ba0096CAS | 2052585PubMed |
Wanderley, L. S., Luz, H. K., Faustino, L. R., Lima, I. M., Lopes, C. A., Silva, A. R., Báo, S. N., Campello, C. C., Rodrigues, A. P., 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=60e24e6fd0071aaea17d690146cea4b7CAS | 21924476PubMed |
Wang, C., and Roy, S. K. (2007). Development of primordial follicles in the hamster: role of estradiol-17β. Endocrinology 148, 1707–1716.
| Development of primordial follicles in the hamster: role of estradiol-17β.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOht7s%3D&md5=a05df71b73251d6fc5f59682f8809195CAS | 17194746PubMed |
Weir, B. J. (1974). Reproductive characteristics of hystricomorph rodents. In ‘The Biology of Hystricomorph Rodents’. (Eds I. W. Rowlands and B. J. Weir.) pp. 264–299. (Zoological Society of London, Academy Press: London.)
Winkler-Crepaz, K., Nederegger, V., Ayuandari, S., Rosenfellner, D., Zervomanolakis, I., Hofer, S., Wildt, L., and Ziehr, S. C. (2014). Novel dynamic culture system to support initiation of primordial follicle growth in prepubertal mouse ovaries. Fertil. Steril. 102, 864–870.e2.
| Novel dynamic culture system to support initiation of primordial follicle growth in prepubertal mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 24996500PubMed |
Xu, Z., Wang, X., Wu, Y., Meng, Y., Wu, F., Zhoua, N., Chen, W., Ye, B., Liu, J., and Zhoua, 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 |
Zuccotti, M., Garagna, S., Merico, V., Monti, M., and Redi, C. A. (2005). Chromatin organisation and nuclear architecture in growing mouse oocytes. Mol. Cell. Endocrinol. 234, 11–17.
| Chromatin organisation and nuclear architecture in growing mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Sqt7k%3D&md5=dd62ff0be3572935a240351fa954847eCAS | 15836948PubMed |
