Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Research

Structure of preantral follicles, oxidative status and developmental competence of in vitro matured oocytes after ovary storage at 4 °C in the domestic cat model

Authors: Anna Rita Piras, Giovanni Pietro Burrai, Federica Ariu, Laura Falchi, Maria Teresa Zedda, Salvatore Pau, Sergio Domenico Gadau, Elisabetta Antuofermo, Daniela Bebbere, Sergio Ledda, Luisa Bogliolo

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

Login to get access

Abstract

Background

Storage conditions during transportation of explanted ovaries are a critical step in setting up fertility preservation protocols in both animal and human fields. Here, we evaluated the effects of ovary storage at 4 °C on the preservation of preantral follicles and oocytes retrieved from antral follicles using the domestic cat as model.

Methods

Ovaries were harvested from fifty-five healthy domestic queens during ovariectomy and stored at 4 °C for 0 (control), 24, 48, 72 and 96 h. In Experiment 1, the effects of the storage period at 4 °C on the morphology, cytoskeleton (α/β tubulin) and DNA integrity (phosphorylation of histone H2AX) of preantral follicles were investigated. In Experiment 2, oocytes recovered from antral follicles were matured and fertilized in vitro to evaluate their meiotic and developmental competence. Reactive oxygen species (ROS), glutathione (GSH) and lipid peroxidation were measured in matured oocytes.

Results

The results showed that: a) storage up to 24 h did not affect the morphology and the DNA integrity of preantral follicles; b) extended storage times caused progressive morphological abnormalities, disassembling of microtubules and DNA damage; c) storage up to 48 h did not influence in vitro meiotic maturation of oocytes nor cleavage after in vitro fertilization. However, only oocytes stored within the ovary for 24 h produced blastocysts in a percentage similar to control oocytes; d) GSH levels of in vitro matured oocytes did not change at any time during ovary storage; a progressive increase in ROS levels was detected from 48 h associated with elevated lipid peroxidation at 72 and 96 h of storage.

Conclusions

Storage of cat ovaries for up to 24 h caused minimal alteration of preantral follicles and oocytes. The extension of the storage period beyond 24 h progressively impaired the structure of follicles, and modified the oxidative status of in vitro matured oocytes and their developmental competence after in vitro fertilization. This information may help when setting up programs for fertility conservation, especially for wild feline species which die in geographic areas located far away from ARTs centers.
Literature
2.
go back to reference Pope CE, Gomez MC, Dresser BL. In vitro embryo production and embryo transfer in domestic and non-domestic cats. Theriogenology. 2006;66:1518–4.CrossRefPubMed Pope CE, Gomez MC, Dresser BL. In vitro embryo production and embryo transfer in domestic and non-domestic cats. Theriogenology. 2006;66:1518–4.CrossRefPubMed
3.
go back to reference Amstislavsky S, Lindeberg H, Luvoni G. Reproductive technologies relevant to the genome resource bank in Carnivora. Reprod Domest Anim. 2012;47:164–75.CrossRefPubMed Amstislavsky S, Lindeberg H, Luvoni G. Reproductive technologies relevant to the genome resource bank in Carnivora. Reprod Domest Anim. 2012;47:164–75.CrossRefPubMed
4.
go back to reference Luu VV, Namula Z, Do LT, Sato Y, Taniguchi M, Karja NW, Otoi T. Nuclear status and DNA fragmentation of oocytes from porcine, bovine and feline ovaries stored at 4 degrees C for 5 days. Cryo Letters. 2014;35:48–53.PubMed Luu VV, Namula Z, Do LT, Sato Y, Taniguchi M, Karja NW, Otoi T. Nuclear status and DNA fragmentation of oocytes from porcine, bovine and feline ovaries stored at 4 degrees C for 5 days. Cryo Letters. 2014;35:48–53.PubMed
5.
go back to reference Naoi H, Otoi T, Shimamura T, Karja NW, Agung B, Shimizu R, Taniguchi M, Nagai T. Developmental competence of cat oocytes from ovaries stored at various temperature for 24 h. J Reprod Dev. 2007;53:271–7.CrossRefPubMed Naoi H, Otoi T, Shimamura T, Karja NW, Agung B, Shimizu R, Taniguchi M, Nagai T. Developmental competence of cat oocytes from ovaries stored at various temperature for 24 h. J Reprod Dev. 2007;53:271–7.CrossRefPubMed
6.
go back to reference Otoi T, Murakami M, Ooka A, Karja NW, Suzuki T. Effects of size and storage temperature on meiotic competence of domestic cat oocytes. Vet Rec. 2001;148:116–8.CrossRefPubMed Otoi T, Murakami M, Ooka A, Karja NW, Suzuki T. Effects of size and storage temperature on meiotic competence of domestic cat oocytes. Vet Rec. 2001;148:116–8.CrossRefPubMed
7.
go back to reference Johnston LA, Donoghue AM, O'Brien SJ, Wildt DE. Rescue and maturation in vitro of follicular oocytes collected from nondomestic felid species. Biol Reprod. 1991;45:898–906.CrossRefPubMed Johnston LA, Donoghue AM, O'Brien SJ, Wildt DE. Rescue and maturation in vitro of follicular oocytes collected from nondomestic felid species. Biol Reprod. 1991;45:898–906.CrossRefPubMed
8.
go back to reference Wood TC, Montali RJ, Wildt DE. Follicle-oocyte atresia and temporal taphonomy in cold-stored domestic cat ovaries. Mol Reprod Dev. 1997;46:190–200.CrossRefPubMed Wood TC, Montali RJ, Wildt DE. Follicle-oocyte atresia and temporal taphonomy in cold-stored domestic cat ovaries. Mol Reprod Dev. 1997;46:190–200.CrossRefPubMed
9.
go back to reference Wolfe BA, Wildt DE. Development to blastocysts of domestic cat oocytes matured and fertilized in vitro after prolonged cold storage. J Reprod Fertil. 1996;106:135–41.CrossRefPubMed Wolfe BA, Wildt DE. Development to blastocysts of domestic cat oocytes matured and fertilized in vitro after prolonged cold storage. J Reprod Fertil. 1996;106:135–41.CrossRefPubMed
10.
go back to reference Pope CE, Gomez MC, King AL, Harris RF, Dresser BL. Embryos produced in vitro after recovery of oocytes from cat ovaries stored at 4 °C for 24–28 h retain the competence to develop into live kittens after transfer to recipients. Theriogenology. 2003;59:308. Pope CE, Gomez MC, King AL, Harris RF, Dresser BL. Embryos produced in vitro after recovery of oocytes from cat ovaries stored at 4 °C for 24–28 h retain the competence to develop into live kittens after transfer to recipients. Theriogenology. 2003;59:308.
11.
go back to reference Luu VV, Hanatate K, Tanihara F, Sato Y, Do LT, Taniguchi M, Otoi T. The effect of relaxin supplementation of in vitro maturation medium on the development of cat oocytes obtained from ovaries stored at 4 degrees C. Reprod Biol. 2013;13:122–6.CrossRefPubMed Luu VV, Hanatate K, Tanihara F, Sato Y, Do LT, Taniguchi M, Otoi T. The effect of relaxin supplementation of in vitro maturation medium on the development of cat oocytes obtained from ovaries stored at 4 degrees C. Reprod Biol. 2013;13:122–6.CrossRefPubMed
12.
go back to reference Cocchia N, Corteggio A, Altamura G, Tafuri S, Rea S, Rosapane I, Sica A, Landolfi F, Ciani F. The effects of superoxide dismutase addition to the transport medium on cumulus-oocyte complex apoptosis and IVF outcome in cats (Felis catus). Reprod Biol. 2015;15:56–64.CrossRefPubMed Cocchia N, Corteggio A, Altamura G, Tafuri S, Rea S, Rosapane I, Sica A, Landolfi F, Ciani F. The effects of superoxide dismutase addition to the transport medium on cumulus-oocyte complex apoptosis and IVF outcome in cats (Felis catus). Reprod Biol. 2015;15:56–64.CrossRefPubMed
13.
go back to reference Jewgenow K, Paris MC. Preservation of female germ cells from ovaries of cat species. Theriogenology. 2006;66:93–100.CrossRefPubMed Jewgenow K, Paris MC. Preservation of female germ cells from ovaries of cat species. Theriogenology. 2006;66:93–100.CrossRefPubMed
14.
go back to reference Comizzoli P, Holt WV. Recent advances and prospects in germplasm preservation of rare and endangered species. Adv Exp Med Biol. 2014;753:331–56.CrossRefPubMed Comizzoli P, Holt WV. Recent advances and prospects in germplasm preservation of rare and endangered species. Adv Exp Med Biol. 2014;753:331–56.CrossRefPubMed
15.
go back to reference Bosch P, Hernandez-Fonseca HJ, Miller DM, Wininger JD, Massey JB, Lamb SV, Brackett BG. Development of antral follicles in cryopreserved cat ovarian tissue transplanted to immunodeficient mice. Theriogenology. 2004;61:581–94.CrossRefPubMed Bosch P, Hernandez-Fonseca HJ, Miller DM, Wininger JD, Massey JB, Lamb SV, Brackett BG. Development of antral follicles in cryopreserved cat ovarian tissue transplanted to immunodeficient mice. Theriogenology. 2004;61:581–94.CrossRefPubMed
16.
go back to reference Wiedemann C, Hribal R, Ringleb J, Bertelsen MF, Rasmusen K, Andersen CY, Kristensen SG, Jewgenow K. Preservation of primordial follicles from lions by slow freezing and xenotransplantation of ovarian cortex into an immunodeficient mouse. Reprod Domest Anim. 2012;47(Suppl 6):300–4.CrossRefPubMed Wiedemann C, Hribal R, Ringleb J, Bertelsen MF, Rasmusen K, Andersen CY, Kristensen SG, Jewgenow K. Preservation of primordial follicles from lions by slow freezing and xenotransplantation of ovarian cortex into an immunodeficient mouse. Reprod Domest Anim. 2012;47(Suppl 6):300–4.CrossRefPubMed
17.
go back to reference Fujihara M, Comizzoli P, Keefer CL, Wildt DE, Songsasen N. Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol Reprod. 2014;90:86.PubMed Fujihara M, Comizzoli P, Keefer CL, Wildt DE, Songsasen N. Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol Reprod. 2014;90:86.PubMed
18.
go back to reference Alves AE, Padilha-Nakaghi LC, Pires-Butler EA, Apparicio M, Silva N, Motheo TF, Vicente W, Luvoni GC. Viability and growth of feline preantral follicles in vitro cultured with insulin growth factor and epidermal growth factor supplemented medium. Reprod Domest Anim. 2016;52(Suppl 2):93–7.PubMed Alves AE, Padilha-Nakaghi LC, Pires-Butler EA, Apparicio M, Silva N, Motheo TF, Vicente W, Luvoni GC. Viability and growth of feline preantral follicles in vitro cultured with insulin growth factor and epidermal growth factor supplemented medium. Reprod Domest Anim. 2016;52(Suppl 2):93–7.PubMed
19.
go back to reference Green LJ, Shikanov A. In vitro culture methods of preantral follicles. Theriogenology. 2016;86:229–38.CrossRefPubMed Green LJ, Shikanov A. In vitro culture methods of preantral follicles. Theriogenology. 2016;86:229–38.CrossRefPubMed
20.
go back to reference Vilela JM, Leonel EC, D'Oliveira L, Paiva RE, Miranda-Vilela AL, Amorim CA, Pic-Taylor A, Lucci CM. Culture of domestic cat ovarian tissue in vitro and in the chick embryo chorioallantoic membrane. Theriogenology. 2016;86:1774–81.CrossRefPubMed Vilela JM, Leonel EC, D'Oliveira L, Paiva RE, Miranda-Vilela AL, Amorim CA, Pic-Taylor A, Lucci CM. Culture of domestic cat ovarian tissue in vitro and in the chick embryo chorioallantoic membrane. Theriogenology. 2016;86:1774–81.CrossRefPubMed
21.
go back to reference Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod. 1996;54:197–207.CrossRefPubMed Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod. 1996;54:197–207.CrossRefPubMed
22.
go back to reference Martins JLA, Lopes MD, de Souza FF, Possebon FS, Wibbelt G, Jewgenow K. Cat preantral follicle survival after prolonged cooled storage followed by vitrification. Cryobiology. 2018;81:94–100.CrossRefPubMed Martins JLA, Lopes MD, de Souza FF, Possebon FS, Wibbelt G, Jewgenow K. Cat preantral follicle survival after prolonged cooled storage followed by vitrification. Cryobiology. 2018;81:94–100.CrossRefPubMed
23.
go back to reference Silva JR, Lucci CM, Carvalho FC, Bao SN, Costa SH, Santos RR, Figueiredo JR. Effect of coconut water and Braun-Collins solutions at different temperatures and incubation times on the morphology of goat preantral follicles preserved in vitro. Theriogenology. 2000;54:809–22.CrossRefPubMed Silva JR, Lucci CM, Carvalho FC, Bao SN, Costa SH, Santos RR, Figueiredo JR. Effect of coconut water and Braun-Collins solutions at different temperatures and incubation times on the morphology of goat preantral follicles preserved in vitro. Theriogenology. 2000;54:809–22.CrossRefPubMed
24.
go back to reference Lopes CA, dos Santos RR, Celestino JJ, Melo MA, Chaves RN, Campello CC, Silva JR, Bao SN, Jewgenow K, de Figueiredo JR. Short-term preservation of canine preantral follicles: effects of temperature, medium and time. Anim Reprod Sci. 2009;115:201–14.CrossRefPubMed Lopes CA, dos Santos RR, Celestino JJ, Melo MA, Chaves RN, Campello CC, Silva JR, Bao SN, Jewgenow K, de Figueiredo JR. Short-term preservation of canine preantral follicles: effects of temperature, medium and time. Anim Reprod Sci. 2009;115:201–14.CrossRefPubMed
25.
go back to reference Gomes RG, Andrade ER, Lisboa LA, Ciquini A, Barreiros TR, Fonseca NA, Seneda MM. Effect of holding medium, temperature and time on structural integrity of equine ovarian follicles during the non-breeding season. Theriogenology. 2012;78:731–6.CrossRefPubMed Gomes RG, Andrade ER, Lisboa LA, Ciquini A, Barreiros TR, Fonseca NA, Seneda MM. Effect of holding medium, temperature and time on structural integrity of equine ovarian follicles during the non-breeding season. Theriogenology. 2012;78:731–6.CrossRefPubMed
26.
go back to reference Henry L, Fransolet M, Labied S, Blacher S, Masereel MC, Foidart JM, Noel A, Nisolle M, Munaut C. Supplementation of transport and freezing media with anti-apoptotic drugs improves ovarian cortex survival. J Ovarian Res. 2016;9:4.CrossRefPubMedPubMedCentral Henry L, Fransolet M, Labied S, Blacher S, Masereel MC, Foidart JM, Noel A, Nisolle M, Munaut C. Supplementation of transport and freezing media with anti-apoptotic drugs improves ovarian cortex survival. J Ovarian Res. 2016;9:4.CrossRefPubMedPubMedCentral
27.
go back to reference Kamoshita K, Okamoto N, Nakajima M, Haino T, Sugimoto K, Okamoto A, Sugishita Y, Suzuki N. Investigation of in vitro parameters and fertility of mouse ovary after storage at an optimal temperature and duration for transportation. Hum Reprod. 2016;31:774–81.CrossRefPubMed Kamoshita K, Okamoto N, Nakajima M, Haino T, Sugimoto K, Okamoto A, Sugishita Y, Suzuki N. Investigation of in vitro parameters and fertility of mouse ovary after storage at an optimal temperature and duration for transportation. Hum Reprod. 2016;31:774–81.CrossRefPubMed
28.
go back to reference Fisch B, Abir R. Female fertility preservation: past, present and future. Reproduction. 2018; 156(1):F11-F27. Fisch B, Abir R. Female fertility preservation: past, present and future. Reproduction. 2018; 156(1):F11-F27.
29.
go back to reference Jensen AK, Kristensen SG, Macklon KT, Jeppesen JV, Fedder J, Ernst E, Andersen CY. Outcomes of transplantations of cryopreserved ovarian tissue to 41 women in Denmark. Hum Reprod. 2015;30:2838–45.CrossRefPubMed Jensen AK, Kristensen SG, Macklon KT, Jeppesen JV, Fedder J, Ernst E, Andersen CY. Outcomes of transplantations of cryopreserved ovarian tissue to 41 women in Denmark. Hum Reprod. 2015;30:2838–45.CrossRefPubMed
30.
go back to reference Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG, Andersen AN, Andersen CY. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod BioMed Online. 2011;22:162–71.CrossRefPubMed Rosendahl M, Schmidt KT, Ernst E, Rasmussen PE, Loft A, Byskov AG, Andersen AN, Andersen CY. Cryopreservation of ovarian tissue for a decade in Denmark: a view of the technique. Reprod BioMed Online. 2011;22:162–71.CrossRefPubMed
31.
go back to reference Von Wolff M, Montag M, Dittrich R, Denschlag D, Nawroth F, Lawrenz B. Fertility preservation in women-a practical guide to preservation techniques and therapeutic strategies in breast cancer, Hodgkin's lymphoma and borderline ovarian tumours by the fertility preservation network. FertiPROTEKT. Arch Gynecol Obstet. 2011;284(2):427–35.CrossRefPubMedPubMedCentral Von Wolff M, Montag M, Dittrich R, Denschlag D, Nawroth F, Lawrenz B. Fertility preservation in women-a practical guide to preservation techniques and therapeutic strategies in breast cancer, Hodgkin's lymphoma and borderline ovarian tumours by the fertility preservation network. FertiPROTEKT. Arch Gynecol Obstet. 2011;284(2):427–35.CrossRefPubMedPubMedCentral
32.
go back to reference Bastings L, Liebenthron J, Westphal JR, Beerendonk CCM, Van der Ven H, Meinecke B, Montag M, Braat DDM, Peek R. Efficacy of ovarian tissue cryopreservation in a major European center. J Assist Reprod Genet. 2014;31(8):1003–12.CrossRefPubMedPubMedCentral Bastings L, Liebenthron J, Westphal JR, Beerendonk CCM, Van der Ven H, Meinecke B, Montag M, Braat DDM, Peek R. Efficacy of ovarian tissue cryopreservation in a major European center. J Assist Reprod Genet. 2014;31(8):1003–12.CrossRefPubMedPubMedCentral
34.
go back to reference Gracia CR, Chang J, Kondapalli L, Prewitt M, Carlson CA, Mattei P, Jeffers S, Ginsberg JP. Ovarian tissue cryopreservation for fertility preservation in cancer patients: successful establishment and feasibility of a multidisciplinary collaboration. J Assist Reprod Genet. 2012;29:495–502.CrossRefPubMedPubMedCentral Gracia CR, Chang J, Kondapalli L, Prewitt M, Carlson CA, Mattei P, Jeffers S, Ginsberg JP. Ovarian tissue cryopreservation for fertility preservation in cancer patients: successful establishment and feasibility of a multidisciplinary collaboration. J Assist Reprod Genet. 2012;29:495–502.CrossRefPubMedPubMedCentral
35.
go back to reference Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O’Neill CL, Songsasen N, Woodruff DR, Woodruff TK. Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice. Reproduction. 2016;152(6):201–10.CrossRef Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O’Neill CL, Songsasen N, Woodruff DR, Woodruff TK. Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice. Reproduction. 2016;152(6):201–10.CrossRef
36.
go back to reference Armstrong AG, Kimler BF, Smith BM, Woodruff TK, Pavone ME, Duncan FE. Ovarian tissue cryopreservation in young females through the Oncofertility Consortium's National Physicians Cooperative. Future Oncol. 2018;14(4):363–78.CrossRefPubMed Armstrong AG, Kimler BF, Smith BM, Woodruff TK, Pavone ME, Duncan FE. Ovarian tissue cryopreservation in young females through the Oncofertility Consortium's National Physicians Cooperative. Future Oncol. 2018;14(4):363–78.CrossRefPubMed
37.
go back to reference Irving Zeidman MD. Chemical factors in the mutual adhesiveness of epithelial cells. AACR Journals. 1947;7:386–9. Irving Zeidman MD. Chemical factors in the mutual adhesiveness of epithelial cells. AACR Journals. 1947;7:386–9.
38.
go back to reference Ueda MJ, Takeichi M. Two mechanisms in cell adhesion revealed by effects of divalent cations. Cell structure and function. 1976;1:377–88.CrossRef Ueda MJ, Takeichi M. Two mechanisms in cell adhesion revealed by effects of divalent cations. Cell structure and function. 1976;1:377–88.CrossRef
39.
go back to reference Bristol-Gould S, Woodruff TK. Folliculogenesis in the domestic cat (Felis catus). Theriogenology. 2006;66:5–13.CrossRefPubMed Bristol-Gould S, Woodruff TK. Folliculogenesis in the domestic cat (Felis catus). Theriogenology. 2006;66:5–13.CrossRefPubMed
40.
go back to reference Dowing KH, Nogales E. Tubulin and microtubule structure. Cell Biology. 1998;10:16–22. Dowing KH, Nogales E. Tubulin and microtubule structure. Cell Biology. 1998;10:16–22.
41.
go back to reference Comizzoli P, Wildt DE, Pukazhenthi BS. Effect of 1,2-propanediol versus 1,2-ethanediol on subsequent oocytes maturation, spindle integrity, fertilization, and embryo development in vitro in the domestic cat. Biol Reprod. 2004;71:598–604.CrossRefPubMed Comizzoli P, Wildt DE, Pukazhenthi BS. Effect of 1,2-propanediol versus 1,2-ethanediol on subsequent oocytes maturation, spindle integrity, fertilization, and embryo development in vitro in the domestic cat. Biol Reprod. 2004;71:598–604.CrossRefPubMed
42.
go back to reference Vanhoutte L, Cortvrindt R, Nogueira D, Smitz J. Effects of chilling on structural aspects of early preantral mouse follicles. Biol Reprod. 2004;70:1041–8.CrossRefPubMed Vanhoutte L, Cortvrindt R, Nogueira D, Smitz J. Effects of chilling on structural aspects of early preantral mouse follicles. Biol Reprod. 2004;70:1041–8.CrossRefPubMed
43.
go back to reference Yin XJ, Lee YH, Jin JY, Kim NH, Kong IK. Nuclear and microtubule remodeling and in vitro development of nuclear transferred cat oocytes with skin fibroblasts of the domestic cat (Felis silvestris catus) and leopard cat (Prionailurus bengalesis). Anim Reprod Sci. 2006;95:307–15.CrossRefPubMed Yin XJ, Lee YH, Jin JY, Kim NH, Kong IK. Nuclear and microtubule remodeling and in vitro development of nuclear transferred cat oocytes with skin fibroblasts of the domestic cat (Felis silvestris catus) and leopard cat (Prionailurus bengalesis). Anim Reprod Sci. 2006;95:307–15.CrossRefPubMed
44.
go back to reference Jin YX, Cui XS, Yu XF, Han JY, Kong IK, Kim NH. Alterations of spindle and microfilament assembly in aged cat oocytes. Reprod Dom Anim. 2010;45:865–71. Jin YX, Cui XS, Yu XF, Han JY, Kong IK, Kim NH. Alterations of spindle and microfilament assembly in aged cat oocytes. Reprod Dom Anim. 2010;45:865–71.
45.
go back to reference Petrillo SK, Desmeules P, Truong TQ, Devine PJ. Detection of DNA damage in oocytes of small ovarian follicles following phosphoramide mustard exposures of cultured rodent ovaries in vitro. Toxicol Appl Pharmacol. 2011;253:94–102.CrossRefPubMed Petrillo SK, Desmeules P, Truong TQ, Devine PJ. Detection of DNA damage in oocytes of small ovarian follicles following phosphoramide mustard exposures of cultured rodent ovaries in vitro. Toxicol Appl Pharmacol. 2011;253:94–102.CrossRefPubMed
46.
go back to reference Bogliolo L, Leoni G, Ledda S, Zedda MT, Bonelli P, Madau L, Santucciu C, Naitana S, Pau S. M-phase promoting factor (MPF) and mitogen activated protein kinases (MAPK) activities of domestic cat oocytes matured in vitro and in vivo. Cloning Stem Cells. 2004;6(1):15–23.CrossRefPubMed Bogliolo L, Leoni G, Ledda S, Zedda MT, Bonelli P, Madau L, Santucciu C, Naitana S, Pau S. M-phase promoting factor (MPF) and mitogen activated protein kinases (MAPK) activities of domestic cat oocytes matured in vitro and in vivo. Cloning Stem Cells. 2004;6(1):15–23.CrossRefPubMed
47.
go back to reference Sovernigo TC, Adona PR, Monzani PS, Guemra S, Barros F, Lopes FG, Leal C. Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim. 2017;52(4):561–9.CrossRefPubMed Sovernigo TC, Adona PR, Monzani PS, Guemra S, Barros F, Lopes FG, Leal C. Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim. 2017;52(4):561–9.CrossRefPubMed
48.
go back to reference Sobinoff AP, Beckett EL, Jarnicki AG, Sutherland JM, McCluskey A, Hansbro PM, McLaughlin EA. Scrambled and fried: cigarette smoke exposure causes antral follicle destruction and oocyte dysfunction through oxidative stress. Toxicol Appl Pharmacol. 2013;271(2):156–67.CrossRefPubMed Sobinoff AP, Beckett EL, Jarnicki AG, Sutherland JM, McCluskey A, Hansbro PM, McLaughlin EA. Scrambled and fried: cigarette smoke exposure causes antral follicle destruction and oocyte dysfunction through oxidative stress. Toxicol Appl Pharmacol. 2013;271(2):156–67.CrossRefPubMed
49.
go back to reference Bogliolo L, Leoni G, Ledda S, Naitana S, Zedda M, Carluccio A. Pau S:intracytoplasmic sperm injection of in vitro matured oocytes of domestic cats with frozen-thawed epididymal spermatozoa. Theriogenology. 2001;56(5):955–67.CrossRefPubMed Bogliolo L, Leoni G, Ledda S, Naitana S, Zedda M, Carluccio A. Pau S:intracytoplasmic sperm injection of in vitro matured oocytes of domestic cats with frozen-thawed epididymal spermatozoa. Theriogenology. 2001;56(5):955–67.CrossRefPubMed
50.
go back to reference Niżanski W, Dejneka GJ, Klimowicz M, Dubiel A. Evaluating some properties of domestic cat epididymal spermatozoa and their cryopreservation. Med Weter. 2005;61:173–8. Niżanski W, Dejneka GJ, Klimowicz M, Dubiel A. Evaluating some properties of domestic cat epididymal spermatozoa and their cryopreservation. Med Weter. 2005;61:173–8.
51.
go back to reference Tsutsui T, Wada M, Anzai M, Hori T. Artificial insemination with frozen epididymal sperm in cats. J Vet Med Sci. 2003;3:397–9.CrossRef Tsutsui T, Wada M, Anzai M, Hori T. Artificial insemination with frozen epididymal sperm in cats. J Vet Med Sci. 2003;3:397–9.CrossRef
52.
go back to reference Sananmuang T, Tharasanit T, Nguyen C, Phutikanit N, Techakumphu M. Culture medium and embryo density influence on developmental competence and gene expression of cat embryos. Theriogenology. 2011;75:1708–19.CrossRefPubMed Sananmuang T, Tharasanit T, Nguyen C, Phutikanit N, Techakumphu M. Culture medium and embryo density influence on developmental competence and gene expression of cat embryos. Theriogenology. 2011;75:1708–19.CrossRefPubMed
53.
go back to reference Schmidt KL, Ernst E, Byskov AG, Andersen AN, Andersen CY. Survival of primordial follicles following prolonged transportation of ovarian tissue prior to cryopreservation. Hum Reprod. 2003;18:2654–9.CrossRefPubMed Schmidt KL, Ernst E, Byskov AG, Andersen AN, Andersen CY. Survival of primordial follicles following prolonged transportation of ovarian tissue prior to cryopreservation. Hum Reprod. 2003;18:2654–9.CrossRefPubMed
54.
go back to reference Isachenko E, Isachenko V, Nawroth F, Rahimi G, Weiss JM. Effect of long-term exposure at suprazero temperatures on activity and viability of human ovarian cortex. Fertil Steril. 2009;91:1556–9.CrossRefPubMed Isachenko E, Isachenko V, Nawroth F, Rahimi G, Weiss JM. Effect of long-term exposure at suprazero temperatures on activity and viability of human ovarian cortex. Fertil Steril. 2009;91:1556–9.CrossRefPubMed
55.
go back to reference Isachenko V, Isachenko E, Mallmann P, Rahimi G. Long-time cooling of human ovarian tissue before cryopreservation as obvious procedure: stimulation of follicular development and neo-vascularisation. Clin Lab. 2012;58:1293–300.PubMed Isachenko V, Isachenko E, Mallmann P, Rahimi G. Long-time cooling of human ovarian tissue before cryopreservation as obvious procedure: stimulation of follicular development and neo-vascularisation. Clin Lab. 2012;58:1293–300.PubMed
56.
go back to reference Isachenko V, Isachenko E, Mallmann P, Rahimi G. Increasing follicular and stromal cell proliferation in cryopreserved human ovarian tissue after long-term precooling prior to freezing: in vitro versus chorioallantoic membrane (CAM) xenotransplantation. Cell Transplant. 2013;22:2053–61.CrossRefPubMed Isachenko V, Isachenko E, Mallmann P, Rahimi G. Increasing follicular and stromal cell proliferation in cryopreserved human ovarian tissue after long-term precooling prior to freezing: in vitro versus chorioallantoic membrane (CAM) xenotransplantation. Cell Transplant. 2013;22:2053–61.CrossRefPubMed
57.
go back to reference Laronda MM, Duncan FE, Hornick JE, Xu M, Pahnke JE, Whelan KA, Shea LD, Woodruff TK. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J Assist Reprod Genet. 2014;31(8):1013–28.CrossRefPubMedPubMedCentral Laronda MM, Duncan FE, Hornick JE, Xu M, Pahnke JE, Whelan KA, Shea LD, Woodruff TK. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J Assist Reprod Genet. 2014;31(8):1013–28.CrossRefPubMedPubMedCentral
58.
go back to reference Klocke S, Tappehorn C, Griesinger G. Effects of supra-zero storage on human ovarian cortex prior to vitrification-warming. Reprod BioMed Online. 2014;29(2):251–8.CrossRefPubMed Klocke S, Tappehorn C, Griesinger G. Effects of supra-zero storage on human ovarian cortex prior to vitrification-warming. Reprod BioMed Online. 2014;29(2):251–8.CrossRefPubMed
59.
go back to reference Isachenko V, Todorov P, Isachenko E, Rahimi G, Tchorbanov A, Mihaylova N, Manoylov I, Mallmann P, Merzenich M. Long-time cooling before cryopreservation decreased translocation of phosphatidylserine (Ptd-L-Ser) in human ovarian tissue. PLoS One. 2015;10(6):e0129108.CrossRefPubMedPubMedCentral Isachenko V, Todorov P, Isachenko E, Rahimi G, Tchorbanov A, Mihaylova N, Manoylov I, Mallmann P, Merzenich M. Long-time cooling before cryopreservation decreased translocation of phosphatidylserine (Ptd-L-Ser) in human ovarian tissue. PLoS One. 2015;10(6):e0129108.CrossRefPubMedPubMedCentral
60.
go back to reference Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, Schmidt KL, Andersen AN, Ernst E. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod. 2008;23:2266–72.CrossRefPubMed Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, Schmidt KL, Andersen AN, Ernst E. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod. 2008;23:2266–72.CrossRefPubMed
61.
go back to reference Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod. 2010;25:1280–1.CrossRefPubMed Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod. 2010;25:1280–1.CrossRefPubMed
62.
go back to reference Dittrich R, Lotz L, Keck G, Hoffmann I, Mueller A, Beckmann MW, van der Ven H, Montag M. Live birth after ovarian tissue autotransplantation following overnight transportation before cryopreservation. Fertil Steril. 2012;97:387–90.CrossRefPubMed Dittrich R, Lotz L, Keck G, Hoffmann I, Mueller A, Beckmann MW, van der Ven H, Montag M. Live birth after ovarian tissue autotransplantation following overnight transportation before cryopreservation. Fertil Steril. 2012;97:387–90.CrossRefPubMed
63.
go back to reference Muller A, Keller K, Wacker J, Dittrich R, Keck G, Montag M, Van der Ven H, Wachter D, Beckmann MW, Distler W. Retransplantation of cryopreserved ovarian tissue: the first live birth in Germany. Dtsch Arztebl Int. 2012;109:8–13.PubMedPubMedCentral Muller A, Keller K, Wacker J, Dittrich R, Keck G, Montag M, Van der Ven H, Wachter D, Beckmann MW, Distler W. Retransplantation of cryopreserved ovarian tissue: the first live birth in Germany. Dtsch Arztebl Int. 2012;109:8–13.PubMedPubMedCentral
64.
go back to reference Andrade ER, Rodrigues AP, Amorim CA, Carvalho FC, Dode MA, Figueiredo JR. Short term maintenance of sheep preantral follicles in situ in 0.9% saline and Braun-Collins solution. Small Rumin Res. 2001;41:141–9.CrossRefPubMed Andrade ER, Rodrigues AP, Amorim CA, Carvalho FC, Dode MA, Figueiredo JR. Short term maintenance of sheep preantral follicles in situ in 0.9% saline and Braun-Collins solution. Small Rumin Res. 2001;41:141–9.CrossRefPubMed
65.
go back to reference Lucci CM, Kacinskis MA, Rumpf R, Bao SN. Effects of lowered temperatures and media on short-term preservation of zebu (Bos indicus) preantral ovarian follicles. Theriogenology. 2004;61:461–72.CrossRefPubMed Lucci CM, Kacinskis MA, Rumpf R, Bao SN. Effects of lowered temperatures and media on short-term preservation of zebu (Bos indicus) preantral ovarian follicles. Theriogenology. 2004;61:461–72.CrossRefPubMed
66.
go back to reference Luvoni GC, Tessaro I, Apparício M, Ruggeri E, Luciano AM, Modina SC. Effect of vitrification of feline ovarian cortex on follicular and oocyte quality and competence. Reprod Domest Anim. 2012;47(3):385–91.CrossRefPubMed Luvoni GC, Tessaro I, Apparício M, Ruggeri E, Luciano AM, Modina SC. Effect of vitrification of feline ovarian cortex on follicular and oocyte quality and competence. Reprod Domest Anim. 2012;47(3):385–91.CrossRefPubMed
67.
go back to reference Tanpradit N, Comizzoli P, Srisuwatanasagul S, Chatdarong K. Positive impact of sucrose supplementation during slow freezing of cat ovarian tissues on cellular viability, follicle morphology, and DNA integrity. Theriogenology. 2015;83:1553–61.CrossRefPubMed Tanpradit N, Comizzoli P, Srisuwatanasagul S, Chatdarong K. Positive impact of sucrose supplementation during slow freezing of cat ovarian tissues on cellular viability, follicle morphology, and DNA integrity. Theriogenology. 2015;83:1553–61.CrossRefPubMed
68.
go back to reference Brito DCC, Domingues SFS, Silva JK, Wu X, Santos RR, Pieczarka JC. Detrimental effect of phenol red on the vitrification of cat (Felis catus) ovarian tissue. Biopreserv Biobank. 2016;14:17–22.CrossRefPubMed Brito DCC, Domingues SFS, Silva JK, Wu X, Santos RR, Pieczarka JC. Detrimental effect of phenol red on the vitrification of cat (Felis catus) ovarian tissue. Biopreserv Biobank. 2016;14:17–22.CrossRefPubMed
69.
go back to reference Mouttham L, Comizzoli P. The preservation of vital functions in cat ovarian tissues during vitrification depends more on the temperature of the cryoprotectant exposure than on the sucrose supplementation. Cryobiology. 2016;73(2):187–95.CrossRefPubMed Mouttham L, Comizzoli P. The preservation of vital functions in cat ovarian tissues during vitrification depends more on the temperature of the cryoprotectant exposure than on the sucrose supplementation. Cryobiology. 2016;73(2):187–95.CrossRefPubMed
70.
go back to reference Brito DCC, Domingues SFS, Rodrigues APR, Maside C, Lunardi FO, Wu X, Figueiredo JR, Pieczarka JC, Santos RR. Cryopreservation of domestic cat (Felis catus) ovarian tissue: comparison of two vitrification methods. Theriogenology. 2018;111:69–77.CrossRefPubMed Brito DCC, Domingues SFS, Rodrigues APR, Maside C, Lunardi FO, Wu X, Figueiredo JR, Pieczarka JC, Santos RR. Cryopreservation of domestic cat (Felis catus) ovarian tissue: comparison of two vitrification methods. Theriogenology. 2018;111:69–77.CrossRefPubMed
71.
go back to reference Demirel MA, Acar DB, Ekim B, Çelikkan FT, Alkan KK, Salar S, Erdemli EA, Özkavukçu S, Yar SS, Kanca H, Baştan A. The evaluation of xenotransplantation of feline ovarian tissue vitrified by needle immersed vitrification technique into male immunodeficient mice. Cell Tissue Bank. 2018;19(1):133–47.CrossRefPubMed Demirel MA, Acar DB, Ekim B, Çelikkan FT, Alkan KK, Salar S, Erdemli EA, Özkavukçu S, Yar SS, Kanca H, Baştan A. The evaluation of xenotransplantation of feline ovarian tissue vitrified by needle immersed vitrification technique into male immunodeficient mice. Cell Tissue Bank. 2018;19(1):133–47.CrossRefPubMed
72.
go back to reference Albertini DF. Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res. 1992;296:57–68.CrossRefPubMed Albertini DF. Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res. 1992;296:57–68.CrossRefPubMed
73.
go back to reference Brinkley BR, Cartwright J Jr. Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Ann N Y Acad Sci. 1975;253:428–39.CrossRefPubMed Brinkley BR, Cartwright J Jr. Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Ann N Y Acad Sci. 1975;253:428–39.CrossRefPubMed
74.
go back to reference Pickering SJ, Johnson MH. The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum Reprod. 1987;2:207–16.CrossRefPubMed Pickering SJ, Johnson MH. The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum Reprod. 1987;2:207–16.CrossRefPubMed
75.
go back to reference Vincent C, Johnson MH. Cooling, cryoprotectants, and the cytoskeleton of the mammalian oocyte. Oxf Rev Reprod Biol. 1992;14:73–100.PubMed Vincent C, Johnson MH. Cooling, cryoprotectants, and the cytoskeleton of the mammalian oocyte. Oxf Rev Reprod Biol. 1992;14:73–100.PubMed
76.
go back to reference Liu RH, Sun QY, Li YH, Jiao LH, Wang WH. Effects of cooling on meiotic spindle structure and chromosome alignment within in vitro matured porcine oocytes. Mol Reprod Dev. 2003;65:212–8.CrossRefPubMed Liu RH, Sun QY, Li YH, Jiao LH, Wang WH. Effects of cooling on meiotic spindle structure and chromosome alignment within in vitro matured porcine oocytes. Mol Reprod Dev. 2003;65:212–8.CrossRefPubMed
77.
go back to reference Evecen M, Cirit U, Demir K, Karaman E, Hamzaoglu AI, Bakirer G. Developmental competence of domestic cat oocytes from ovaries stored at various durations at 4 degrees C temperature. Anim Reprod Sci. 2009;116:169–72.CrossRefPubMed Evecen M, Cirit U, Demir K, Karaman E, Hamzaoglu AI, Bakirer G. Developmental competence of domestic cat oocytes from ovaries stored at various durations at 4 degrees C temperature. Anim Reprod Sci. 2009;116:169–72.CrossRefPubMed
78.
go back to reference Devine PJ, Perreault SD, Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod. 2012;86:27.CrossRefPubMed Devine PJ, Perreault SD, Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod. 2012;86:27.CrossRefPubMed
79.
80.
81.
go back to reference Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146:217–27.CrossRef Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146:217–27.CrossRef
82.
go back to reference Pastore A, Federici G, Bertini E, Piemonte F. Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta. 2003;333:19–39.CrossRefPubMed Pastore A, Federici G, Bertini E, Piemonte F. Analysis of glutathione: implication in redox and detoxification. Clin Chim Acta. 2003;333:19–39.CrossRefPubMed
83.
go back to reference Perreault SD, Barbee RR, Slott VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol. 1988;125:181–6.CrossRefPubMed Perreault SD, Barbee RR, Slott VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol. 1988;125:181–6.CrossRefPubMed
84.
go back to reference Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod. 1993;49:89–94.CrossRefPubMed Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel VG. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod. 1993;49:89–94.CrossRefPubMed
85.
go back to reference Miyamura M, Yoshida M, Hamano S, Kuwayama M. Glutathione concentration during maturation and fertilization in bovine oocytes. Theriogenology. 1995;43:282.CrossRef Miyamura M, Yoshida M, Hamano S, Kuwayama M. Glutathione concentration during maturation and fertilization in bovine oocytes. Theriogenology. 1995;43:282.CrossRef
86.
go back to reference Funahashi H, Day BN. Effect of cumulus cells on glutathione content of porcine oocytes during in vitro maturation. J Anim Sci. 1995;73:90. Funahashi H, Day BN. Effect of cumulus cells on glutathione content of porcine oocytes during in vitro maturation. J Anim Sci. 1995;73:90.
87.
go back to reference Furnus CC, de Matos DG, Picco S, Garcia PP, Inda AM, Mattioli G, Errecalde AL. Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim Reprod Sci. 2008;109:88–99.CrossRefPubMed Furnus CC, de Matos DG, Picco S, Garcia PP, Inda AM, Mattioli G, Errecalde AL. Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim Reprod Sci. 2008;109:88–99.CrossRefPubMed
88.
go back to reference Jiao GZ, Cao XY, Cui W, Lian HY, Miao YL, Wu XF, Han D, Tan JH. Developmental potential of prepubertal mouse oocytes is compromised due mainly to their impaired synthesis of glutathione. PLoS One. 2013;8:e58018.CrossRefPubMedPubMedCentral Jiao GZ, Cao XY, Cui W, Lian HY, Miao YL, Wu XF, Han D, Tan JH. Developmental potential of prepubertal mouse oocytes is compromised due mainly to their impaired synthesis of glutathione. PLoS One. 2013;8:e58018.CrossRefPubMedPubMedCentral
89.
go back to reference Abazari-Kia AH, Mohammadi-Sangcheshmeh A, Dehghani-Mohammadabadi M, Jamshidi-Adegani F, Veshkini A, Zhandi M, Cinar MU, Salehi M. Intracellular glutathione content, developmental competence and expression of apoptosis-related genes associated with G6PDH-activity in goat oocyte. J Assist Reprod Genet. 2014;31:313–21.CrossRefPubMed Abazari-Kia AH, Mohammadi-Sangcheshmeh A, Dehghani-Mohammadabadi M, Jamshidi-Adegani F, Veshkini A, Zhandi M, Cinar MU, Salehi M. Intracellular glutathione content, developmental competence and expression of apoptosis-related genes associated with G6PDH-activity in goat oocyte. J Assist Reprod Genet. 2014;31:313–21.CrossRefPubMed
90.
go back to reference Repetto M, Semprine J, Boveris A. Lipid peroxidation: chemical mechanism, biological implications and analytical determination. In: InTech, editor. Lipid Peroxidation; 2012. p. 4–29. Repetto M, Semprine J, Boveris A. Lipid peroxidation: chemical mechanism, biological implications and analytical determination. In: InTech, editor. Lipid Peroxidation; 2012. p. 4–29.
Metadata
Title
Structure of preantral follicles, oxidative status and developmental competence of in vitro matured oocytes after ovary storage at 4 °C in the domestic cat model
Authors
Anna Rita Piras
Giovanni Pietro Burrai
Federica Ariu
Laura Falchi
Maria Teresa Zedda
Salvatore Pau
Sergio Domenico Gadau
Elisabetta Antuofermo
Daniela Bebbere
Sergio Ledda
Luisa Bogliolo
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0395-1

Other articles of this Issue 1/2018

Reproductive Biology and Endocrinology 1/2018 Go to the issue