Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-19T19:57:00.766Z Has data issue: false hasContentIssue false

Developmental competence of ovine oocyte following vitrification: effect of oocyte developmental stage, cumulus cells, cytoskeleton stabiliser, FBS concentration, and equilibration time

Published online by Cambridge University Press:  14 August 2012

Abolfazl Shirazi
Affiliation:
Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Shahid Beheshti University, P.O. Box: 19615-1177, Tehran, Iran. Research Institute of Animal Embryo Technology, Shahrekord University, P. O. Box: 115, Shahrekord, Iran.
Fatemeh Taheri
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, P. O. Box: 115, Shahrekord, Iran.
Hassan Nazari
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, P. O. Box: 115, Shahrekord, Iran.
Maryam Norbakhsh-nia
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, P. O. Box: 115, Shahrekord, Iran.
Ebrahim Ahmadi
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, P. O. Box: 115, Shahrekord, Iran.
Banafsheh Heidari*
Affiliation:
Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Shahid Beheshti University, P.O. Box: 19615-1177, Tehran, Iran.
*
All correspondence to: Banafsheh Heidari. Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Shahid Beheshti University, P.O. Box: 19615-1177, Tehran, Iran. Tel: +98 21 22404144. Fax: +98 21 22432021. e-mail: ban_heidari@yahoo.com or b.heidari@avicenna.ac.ir

Summary

The aim of the present study was to examine the effects of fetal bovine serum (FBS) concentration, equilibration time, and oocyte pre-treatment with cytochalasin B (CCB) on subsequent development of vitrified-warmed ovine immature (GVCOCs) and matured (MII) oocytes with (MIICOCs) or without cumulus cells (MIIDOs). In Experiment 1, the effects of FBS concentrations (10 and 20%) during the vitrification-warming procedure were examined. Survival rates after warming were not different between GVCOCs, MIICOCs and MIIDOs oocytes. After in vitro fertilization, rate of cleaved embryos in MIICOCs group at the presence of 20%FBS was higher than MIIDOs and GVCOCs groups. In Experiment 2, the effects of equilibration times (5, 7, and 10 min) were examined. There was no difference in survival rate of vitrified-warmed oocytes equilibrated at different times. Although, the rate of cleavage in MIICOCs and MIIDOs oocytes equilibrated for 10 and 7 min, respectively, was higher than 5 min equilibrated MIIDOs and 7 and 10 min equilibrated GVCOCs oocytes. In Experiment 3, the effects of oocyte pre-treatment with CCB were examined. Despite the insignificant difference in survival rate of vitrified-warmed ovine immature and matured oocytes, the rates of cleavage in CCB pretreated groups were significantly lower than untreated groups. Moreover, the blastocysts were only derived from those cumulus enclosed vitrified-warmed germinal vesicle (GV) and MII oocytes that had been exposed to 10% FBS in the absence of CCB. In conclusion, the presence of cumulus cells, 10% FBS, and the omission of CCB were beneficial for post-warming development of vitrified ovine oocytes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agca, Y., Liu, J., Peter, A.T., Critser, E.S. & Critser, J.K. (1998). Effect of developmental stage on bovine oocyte plasma membrane water and cryoprotectant permeability characteristics. Mol. Reprod. Dev. 49, 408–15.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Albarracin, J.L., Morato, R., Izquirerdo, D. & Mogas, T. (2005). Vitrification of calf oocytes: effects of maturation stage and prematuration treatment on the nuclear and cytoskeletal components of oocytes and their subsequent development. Mol. Reprod. Dev. 72, 239–49.CrossRefGoogle ScholarPubMed
Al-Aghbari, A.M. & Menino, A.R. Jr (2002). Survival of oocytes recovered from vitrified sheep ovarian tissues. Anim. Reprod. Sci. 71, 101–10.CrossRefGoogle ScholarPubMed
Arav, A., Zeron, Y., Leslie, S.B., Behboodi, E., Anderson, G.B. & Crowe, J.H. (1996). Phase transition temperature and chilling sensitivity of bovine oocytes. Cryobiology 33, 589–99.CrossRefGoogle ScholarPubMed
Bogliolo, L., Ariu, F., Fois, S., Rosati, I., Zedda, M.T., Leoni, G., Succu, S., Pau, S. & Ledda, S. (2007). Morphological and biochemical analysis of immature ovine oocytes vitrified with or without cumulus cells. Theriogenology 68, 1138–49.CrossRefGoogle ScholarPubMed
Boiso, I., Marti, M., Santalo, J., Ponsa, M., Barri, P.N. & Veiga, A. (2002). A confocal microscopy analysis of the spindle and chromosome configurations of human oocytes cryopreserved at the germinal vesicle and metaphase II stage. Hum. Reprod. 17, 1885–91.CrossRefGoogle ScholarPubMed
Carroll, J., Depypere, H. & Matthews, C.D. (1990). Freeze–thaw-induced changes of the zona pellucida explain decreased rates of fertilization in frozen–thawed mouse oocytes. J. Reprod. Fertil. 90, 547–53.CrossRefGoogle ScholarPubMed
Checura, C.M. & Seidel, G.E. Jr (2007). Effect of macromolecules in solutions for vitrification of mature bovine oocytes. Theriogenology 67, 919–30.CrossRefGoogle ScholarPubMed
Chian, R.C., Kuwayama, M., Tan, L., Tan, J., Kato, O. & Nagai, T. (2004). High survival rate of bovine oocytes matured in vitro following vitrification. J. Reprod. Dev. 50, 685–96.CrossRefGoogle ScholarPubMed
Diez, C., Duque, P., Gomez, E., Hidalgo, C.O., Tamargo, C., Rodriguez, A., Fernandez, L., de la Varga, S., Fernandez, A., Facal, N. & Carbajo, M. (2005). Bovine oocyte vitrification before or after meiotic arrest: effects on ultrastructure and developmental ability. Theriogenology 64, 317–33.CrossRefGoogle ScholarPubMed
Dobrinsky, J.R., Pursel, V.G., Long, C.R. & Johnson, L.A. (2000). Birth of piglets after transfer of embryos cryopreserved by cytoskeletal stabilisation and vitrification. Biol. Reprod. 62, 564–70.CrossRefGoogle ScholarPubMed
Fujihira, T., Kishida, R. & Fukui, Y. (2004). Developmental capacity of vitrified immature porcine oocytes following ICSI: effects of cytochalasin B and cryoprotectants. Cryobiology 49, 286–90.CrossRefGoogle ScholarPubMed
Fujihira, T., Nagai, H. & Fukui, Y. (2005). Relationship between equilibration times and the presence of cumulus cells, and effect of Taxol treatment for vitrification of in vitro matured porcine oocytes Cryobiology 51, 339–43.CrossRefGoogle ScholarPubMed
Fu, X.W., Shi, W.Q., Zhang, Q.J., Zhao, X.M., Yan, C.L., Hou, Y.P., Zhou, G.B., Fan, Z.Q., Suo, L. & Zhu, S.E. (2009). Positive effects of Taxol pre-treatment on morphology, distribution and ultrastructure of mitochondria and lipid droplets in vitrification of in vitro matured porcine oocytes. Anim. Reprod. Sci. 115, 158–68.CrossRefGoogle Scholar
George, M.A., Johnson, M.H. & Vincent, C. (1992). Use of fetal bovine serum to protect against zona hardening during preparation of mouse oocytes for cryopreservation. Hum. Reprod. 7, 408–12.CrossRefGoogle ScholarPubMed
Ghetler, Y., Skutelsky, B., Ben Nun, I., Bendor, L., Anihai, D. & Shalgi, R. (2006). Human oocyte cryopreservation and the fate of cortical granules. Fertil. Steril. 86, 210–6.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte–somatic cell interaction during follicle development in mammals. Anim. Reprod. Sci. 82, 431–46.CrossRefGoogle ScholarPubMed
Hochi, S., Ito, K., Hirabayashi, M., Ueda, M., Kimura, K. & Hanada, A. (1998). Effect of nuclear stages during IVM on the survival of vitrified–warmed bovine oocytes. Theriogenology 49, 787–96.CrossRefGoogle ScholarPubMed
Hurtt, A.E., Landim-Alvarenga, F., Seidel, G.E. & Squires, E.L. (2000). Vitrification of immature and mature equine and bovine oocytes in an ethylene glycol, ficoll and sucrose solution using open-pulled straws. Theriogenology 54, 119–28.CrossRefGoogle Scholar
Imoedemhe, D.G. & Sigue, A.B. (1992). Survival of human oocytes cryopreserved with or without the cumulus in 1,2-propanediol. J. Assist. Reprod. Genet. 9, 323–7.CrossRefGoogle ScholarPubMed
Isachenko, V., Soler, C., Isachenko, E., Perez-Sanchez, F. & Grishchenko, V. (1998). Vitrification of immature porcine oocytes: effects of lipid droplets, temperature, cytoskeleton, and addition and removal of cryoprotectant. Cryobiology 36, 250–3.CrossRefGoogle ScholarPubMed
Isachenko, V., Alabart, J.L., Nawroth, F., Isachenko, E., Vajta, G. & Folch, J. (2001). The open pulled straw vitrification of ovine GV-oocytes, positive effect of rapid cooling or rapid thawing or both? Cryo. Lett. 22, 157–62.Google ScholarPubMed
Kelly, J., Kleemann, D., Kuwayama, M. & Walker, S. (2006). Effect of cysteamine on survival of bovine and ovine oocytes vitrified using the minimal volume cooling (MCV) cryotop method. In: Proceedings of the Annual Conference of the International Embryo Transfer Society, p. 158.Google Scholar
Kuleshova, L.L., Shaw, J.M. & Trounson, A.O. (2001). Studies on replacing most of the penetrating cryoprotectant by polymers for embryo cryopreservation. Cryobiology 43, 2131.CrossRefGoogle ScholarPubMed
Le Gal, F.G., Basil, J.C. & Vallet, L. (1993). In vivo and in vitro survival of goat embryos after freezing with ethylene. Theriogenology 40, 771–7.CrossRefGoogle ScholarPubMed
Ledda, S., Bogliolo, L., Succu, S., Ariu, F., Bebbere, D., Leoni, G.G. & Naitana, S. (2007). Oocyte cryopreservation: oocyte assessment and strategies for improving survival. Reprod. Fertil. Dev. 19, 1323.CrossRefGoogle ScholarPubMed
Leibo, S.P. (1980). Water permeability and its activation energy of fertilized and unfertilized mouse ova. J. Membrane Biol. 53, 179–88.CrossRefGoogle ScholarPubMed
Li, G.P., Bunch, T.D., White, K.L., Rickords, L. & Session, B.R. (2006). Denuding and centrifugation of maturing bovine oocytes alters oocyte spindle integrity and viability of cytoplasm to support parthenogenetic and nuclear transfer embryo development. Mol. Reprod. Dev. 73, 446–51.CrossRefGoogle Scholar
Liu, R.H., Sun, Q.Y., Li, H.Y., Jiao, L.H. & Wang, W.H. (2003). Effects of cooling on meiotic spindle structure and chromosome alignment within in vitro matured porcine oocytes. Mol. Reprod. Dev. 65, 212–8.CrossRefGoogle ScholarPubMed
Men, H., Monson, R.L. & Rutledge, J.J. (2002). Effect of meiotic stages and maturation protocols on bovine oocyte's resistance to cryopreservation. Theriogenology 57, 1095–103.CrossRefGoogle ScholarPubMed
Men, H., Monson, R.L., Parrish, J.J. & Rutledge, J.J. (2003). Detection of DNA damage in bovine metaphase II oocytes resulting from cryopreservation. Mol. Reprod. Dev. 64, 245–50.CrossRefGoogle ScholarPubMed
Mezzalira, A., Vieira, A.D., Barbieri, D.P., Machado, M.F., Thaler Neto, A., Bernardi, M.L., Silva, C.A.M. & Rubin, M.I.B. (2002). Vitrification of matured bovine oocytes treated with cytochalasin B. Theriogenology 57, 472.Google Scholar
Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H. & Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–44.CrossRefGoogle ScholarPubMed
Palasz, A.T. & Mapletoft, R.J. (1996). Cryopreservation of mammalian embryos and oocytes: recent advances. Biotechnol. Adv. 14, 127–49.CrossRefGoogle ScholarPubMed
Papis, K., Shimizu, M. & Izaike, Y. (2000). Factors affecting the survivability of bovine oocytes vitrified in droplets. Theriogenology 15, 651–8.CrossRefGoogle Scholar
Park, S.E., Chung, H.M., Cha, K.Y., Hwang, W.S., Lee, E.S. & Lim, J.M. (2001). Cryopreservation of ICR mouse oocytes: improved post-thawed preimplantation development after vitrification using Taxol, a cytoskeleton stabilizer. Fertil. Steril. 75, 1177–84.CrossRefGoogle ScholarPubMed
Pukazhenthi, B.S. & Wildt, D.E. (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reprod. Fertil. Dev. 16, 3346.CrossRefGoogle ScholarPubMed
Rojas, C., Palomo, M. J., Albarracı ´n, J. L. & Mogas, T. (2004). Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules, and actin microfilaments. Cryobiology 49, 211–20.CrossRefGoogle ScholarPubMed
Shaw, J.M., Kuleshova, L.L., MacFarlane, D.R. & Trounson, A.O. (1997). Vitrification properties of solutions of ethylene glycol in saline containing PVP, Ficoll or dextran. Cryobiology 35, 219–29.CrossRefGoogle ScholarPubMed
Shaw, J.M., Oranratnachai, A. & Trounson, A. (2000). Cryopreservation of oocytes and embryos. In: Trounson, A, Gardner, DK, editors. Handbook of In Vitro Fertilization. 2nd ed., Boca Raton, FL: CRC Press, pp. 373412.Google Scholar
Shirazi, A., Soleimani, M., Karimi, M., Nazari, H., Ahmadi, E. & Heidari, B. (2010). Vitrification of in vitro produced ovine embryos at various developmental stages using two methods. Cryobiology 60, 204–10.CrossRefGoogle ScholarPubMed
Silvestre, M.A., Yaniz, J., Salvador, I., Santolaria, P. & Lopez-Gatius, F. (2006). Vitrification of pre-pubertal ovine cumulus–oocyte complexes: effect of cytochalasin B pre-treatment. Anim. Reprod. Sci. 93, 176–82.CrossRefGoogle ScholarPubMed
Succu, S., Leoni, G., Berlinguer, F., Mossa, F., Galioto, M. & Naitana, S. (2007). Vitrification devices affect structural and molecular status of in vitro matured ovine oocytes. Mol. Reprod. Dev. 74, 1337–44.CrossRefGoogle ScholarPubMed
Succu, S., Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G.G., Berlinguer, F., Naitana, S. & Ledda, S. (2008). Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Mol. Reprod. Dev. 75, 538–46.CrossRefGoogle ScholarPubMed
Sun, Q.Y., Wu, G.M., Lai, L.X., Park, K.W., Day, B.N., Prather, R.S. & Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–63.CrossRefGoogle ScholarPubMed
Tervit, H.R., Whittingham, D.G. & Rowson, L.E. (1972). Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil. 30, 493–7.CrossRefGoogle Scholar
Tharasanit, T., Colenbrander, B. & Stout, T.A.E. (2006a). Effect of maturation stage at cryopreservation on post-thaw cytoskeleton quality and fertilizability of equine oocytes. Mol. Reprod. Dev. 73, 627–37.CrossRefGoogle ScholarPubMed
Tharasanit, T., Colleonione, S., Lazzarione, G., Colenbrander, B., Galli, C. & Stout, T.A.E. (2006b). Effect of cumulus morphology and maturation stage on the cryopreservability of equine oocytes. Reproduction 132, 759–69.CrossRefGoogle ScholarPubMed
Vajta, G. (2000). Vitrification of the oocyte and embryos of domestic animals. Anim. Reprod. Sci. 60, 357–64.CrossRefGoogle ScholarPubMed
Vajta, G. & Kuwayama, M. (2006). Improving cryopreservation systems. Theriogenology 65, 236–44.CrossRefGoogle ScholarPubMed
Van Blerkom, J. (1991). Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed meiosis in cultured mouse oocytes. Proc. Natl. Acad. Sci. 88, 5031–5.CrossRefGoogle ScholarPubMed
Vieira, A.D., Mezzalira, A., Barbieri, D.P., Lehmkuhl, R.C., Rubin, M.I. & Vajta, G. (2002). Calves born after open pulled straw vitrification of immature bovine oocytes. Cryobiology 45, 91–4.CrossRefGoogle ScholarPubMed
Vincent, C., Pickering, S.J. & Johnson, M.H. (1990). The hardening effect of dimethylsulphoxide on the mouse zona pellucida requires the presence of an oocyte and is associated with a reduction in the number of cortical granules present. J. Reprod. Fertil. 89, 253–9.CrossRefGoogle ScholarPubMed
Whittingham, D.G. (1977). Fertilization in vitro and development to term of unfertilised mouse oocytes previously stored at −196°C. J. Reprod. Fertil. 49, 8994.CrossRefGoogle Scholar
Zeron, Y., Tomczak, M., Crowe, J. & Arav, A. (2002). The effect of liposomes on thermotropic membrane phase transitions of bovine spermatozoa and oocytes: implications for reducing chilling sensitivity. Cryobiology 45, 143–52.CrossRefGoogle ScholarPubMed
Zhang, J., Nedambale, T.L., Yang, M. & Li, J. (2009). Improved development of ovine matured oocyte following solid surface vitrification (SSV): Effect of cumulus cells and cytoskeleton stabilizer. Anim. Reprod. Sci. 110, 4655.CrossRefGoogle ScholarPubMed
Zhou, G.B. & Li, N. (2009). Cryopreservation of porcine oocytes: recent advances. Mol. Hum. Reprod. 15, 279–85.CrossRefGoogle Scholar