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Reduced competence of immature and mature oocytes vitrified by Cryotop method: assessment by in vitro fertilization and parthenogenetic activation in a bovine model

Published online by Cambridge University Press:  10 January 2017

Daiane L. Bulgarelli ,
Alessandra A. Vireque ,
Caroline P. Pitangui-Molina ,
Marcos F. Silva-de-Sá  and
Ana Carolina J. de Sá Rosa-e-Silva
Daiane L. Bulgarelli
Affiliation:
Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Alessandra A. Vireque
Affiliation:
Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Caroline P. Pitangui-Molina
Affiliation:
Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Marcos F. Silva-de-Sá
Affiliation:
Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Ana Carolina J. de Sá Rosa-e-Silva*
Affiliation:
Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
*
All correspondence to Ana Carolina J. de Sá Rosa-e-Silva. Department of Obstetrics and Gynecology, School of Medicine of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. Fax, +55 16 3602 2817. E-mail: anasars@fmrp.usp.br
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Summary

This study aimed to evaluate the embryo development competence, the nuclear maturation and the viability of germinal vesicle (GV) and metaphase II (MII) oocytes vitrified by the Cryotop method. Cumulus–oocyte complexes were derived from bovine ovaries and three experiments were conducted. In Experiment 1, GV oocytes were vitrified and underwent in vitro maturation (IVM) or not and their nuclear maturation was assessed by orcein staining. In Experiment 2, GV oocytes and MII oocytes were vitrified or not and the viability was assessed by calcein/ethidium homodimer-1 staining. In Experiment 3, MII oocytes matured before or after vitrification were submitted to in vitro fertilization (IVF) and parthenogenetic activation (PA) in order to evaluate embryo development. No difference was found for the nuclear maturation rate in the GV group (50%) and the GV control group (67%; P = 0.23) and for viability rate (56%; 77%; P = 0.055, respectively). However, in the MII group (27%) viability was significantly lower than that of the MII control group (84%; P < 0.0001). The cleavage rate by IVF and PA was similar in the GV group and the MII group. In contrast, vitrified MII oocytes showed no capacity for blastocyst development after IVF or PA and vitrified GV oocytes were able to develop to blastocysts only after PA, but not after IVF. In conclusion, oocyte vitrification by the Cryotop method reduced the capacity for embryo development. Vitrification of GV oocytes, however, did not influence the capacity of meiotic nuclear maturation and they exhibited higher viability following vitrification at the MII stage.

Keywords

Bovine oocyteEmbryo DevelopmentViabilityVitrification
Type
Short Communication
Information
Zygote , Volume 25 , Issue 2 , April 2017 , pp. 222 - 230
Copyright
Copyright © Cambridge University Press 2017 

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References

Aman, R.R. & Parks, J.E. (1994). Effects of cooling and rewarming on the meiotic spindle and chromosomes of in vitro-matured bovine oocytes. Biol. Reprod. 50, 103–10.CrossRefGoogle ScholarPubMed
Arcarons, N., Morató, R., Spricigo, J.F., Ferraz, M.A. & Mogas, T. (2015). Spindle configuration and developmental competence of in vitro-matured bovine oocytes exposed to NaCl or sucrose prior to Cryotop vitrification. Reprod. Fertil. [Epub ahead of print]Google Scholar
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
Brunet, S., Pahlavan, G., Taylor, S. & Maro, B. (2003). Functionality of the spindle checkpoint during the first meiotic division of mammalian oocytes. Reproduction 126, 443–50.Google Scholar
Buccione, R., Schroeder, A.C. & Eppig, J.J. (1990). Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod. 43, 543–7.Google Scholar
Carroll, J., Depypere, H. & Matthews, C.D. (1990) Freeze-thaw-induced changes of the zona pellucida explains decreased rates of fertilization in frozen-thawed mouse oocytes. J. Reprod. Fertil. 90, 2, 547–53.Google Scholar
Cha, K.Y. & Chian, R.C. (1998). Maturation in vitro of immature human oocytes for clinical use. Hum. Reprod. Update 4, 103–20.Google Scholar
Chian, R.C., Niwa, K., & Sirard, M.A. (1994). Effects of cumulus cells on male pronuclear formation and subsequent early development of bovine oocytes in vitro . Theriogenology 41, 1499–508.Google Scholar
Chian, R.C., Kuwayama, M., Tan, L., Tan, J., Kato, O. & Nagai, T. (2004). High survival rate of 461 bovine oocytes matured in vitro following vitrification, J. Reprod. Dev. 50, 685–96.Google Scholar
Cobo, A., Romero, J.L., Pérez, S., de los Santos, S.M.J., Meseguer, M. & Remohí, J. (2010). Storage of human oocytes in the vapor phase of nitrogen. Fertil. Steril. 94, 1903–7.Google Scholar
Cortvrindt, R.G. & Smitz, J.E. (2001). Fluorescent probes allow rapid and precise recording of follicle density and staging in human cortical biopsy samples. Fertil. Steril. 75, 588–93.Google Scholar
González, C., Devesa, M., Boada, M., Coroleu, B., Veiga, A. & Barri, P.N. (2011). Combined strategy for fertility preservation in an oncologic patient: vitrification of in vitro matured oocytes and ovarian tissue freezing. J. Assist. Reprod. Genet. 28, 1147–9.Google Scholar
Gook, D.A., Osborn, S.M., Bourne, H. & Johnston, W.I. (1994). Fertilization of human oocytes following cryopreservation; normal karyotypes and absence of stray chromosomes. Hum. Reprod. 9, 684–91Google Scholar
Gordon, I. (1994). Laboratory Production of Cattle Embryos. London: Cambridge University Press.Google Scholar
Herrero, L., Martinez, M. & Garcia-Velasco, J.A. (2011). Current status of human oocyte and embryo cryopreservation. Curr. Opin. Obstet. Gynecol. 23, 245–50.Google Scholar
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.Google Scholar
Hochi, S., Kozawa, M., Fujimoto, T., Hondo, E., Yamada, J. & Oguri, N. (1996). In vitro maturation and transmission electron microscopic observation of horse oocytes after vitrification. Cryobiology 33, 300–10.Google Scholar
Jin, B., Kawai, Y., Hara, T., Takeda, S., Seki, S., Nakata, Y., Matsukawa, K., Koshimoto, C., Kasai, M. & Edashge, K. (2011). Pathway for the movement of water and cryoprotectants in bovine oocytes and embryos. Biol. Reprod. 85, 834–47.Google Scholar
Ka, H.H., Sawai, K., Wang, W.H, Im, K.S. & Niwa, K. (1997). Amino acids in maturation medium and presence of cumulus cells at fertilization promote male pronuclear formation in porcine oocytes matured and penetrated in vitro . Biol. Reprod. 57, 1478–83.Google Scholar
Kano, F., Takenaka, K., Yamamoto, A., Nagayama, K., Nishida, E. & Murata, M. (2000). MEK and Cdc2 kinase are sequentially required for Golgi disassembly in MDCK cells by the mitotic Xenopus extracts. J. Cell. Biol. 17, 357–68.Google Scholar
Katayama, K.P., Stehlik, J., Kuwayama, M., Kato, O. & Stehlik, E. (2003). High survival rate of vitrified human oocytes results in clinical pregnancy. Fertil. Steril. 80, 223–4.Google Scholar
Kubelka, M., Motlík, J., Schultz, R.M. & Pavlok, A. (2000). Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes, Without influencing chromosome condensation activity. Biol. Reprod. 62, 2, 292–302.Google Scholar
Kuwayama, M., Vajta, G., Kato, O. & Leibo, S.P. (2005) Highly efficient vitrification method for cryopreservation of human oocytes. Reprod. Biomed. Online 11, 300–8.Google Scholar
Kuwayama, M. (2007). Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology 67, 73–80.CrossRefGoogle ScholarPubMed
Lee, J.A., Barritt, J., Moschini, R.M., Slifkin, R.E. & Copperman, A.B. (2013). Optimizing human oocyte cryopreservation for fertility preservation patients: Should we mature then freeze or freeze than mature? Fertil. Steril. 99, 1356–62.Google Scholar
Lefebvre, C., Terret, M.E., Djiane, A., Rassinier, P., Maro, B. & Verlhac, M.H. (2002). Meiotic spindle stability depends on MAPK-interacting and spindle-stabilizing protein (MISS), a new MAPK substrate. J. Cell. Biol. 13, 603–13.Google Scholar
Lin, Y.H. & Hwang, J.L. (2006). In vitro maturation of human oocytes. Taiwan J. Obstet. Gynecol. 45, 95–9.CrossRefGoogle ScholarPubMed
Mara, L., Carta, A. & Dattena, M. (2013). Cryobank of farm animal gametes and embryos as a means of conserving livestock genetics. Anim. Reprod. Sci. 138, 25–38.Google Scholar
Martinez-Madrid, B., Dolmans, M.M., Langendonckt, A.V., Defrère, S., Van Eyck, A.S. & Donnez, J. (2004) Ficoll density gradient method for recovery of isolated human ovarian primordial follicles. Fertil. Steril. 82, 1648–53.Google Scholar
Massip, A. (2003). Cryopreservation of bovine oocytes: current status and recent developments. Reprod. Nutr. Dev. 43, 325–30.Google Scholar
Mcwilliams, R.B., Gibbons, W.E. & Leibo, S.P. (1995). Osmotic and physiological responses of mouse zygotes and human oocytes to mono- and disaccharides. Hum. Reprod. 10, 1163–71.Google Scholar
Meirelles, F.V., Caetano, A.R., Watanabe, Y.F., Ripamonte, P., Carambula, S.F., Merighe, G.K. & Garcia, S.M. (2004). Genome activation and developmental block in bovine embryos. Anim. Reprod. Sci. 82, 13–20.Google Scholar
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.Google Scholar
Merdassi, G., Mazoyer, C., Guerin, J.F., Saad, A., Salle, B. & Lornage, J. (2011). Examination of viability and quality of ovarian tissue after cryopreservation using simple laboratory methods in ewe. Reprod. Biol. Endocrinol. 8, 78.Google Scholar
Morató, R., Izquierdo, D., Paramio, M.T. & Mogas, T. (2008). Cryotops versus open-pulled straws (OPS) as carriers for the cryopreservation of bovine oocytes: effects on spindle and chromosome configuration and embryo development. Cryobiology 57, 137–41.Google Scholar
Mukaida, T. & Oka, C. (2012). Vitrification of oocytes, embryos and blastocysts. Best. Pract. Res. Clin. Obstet. Gynaecol. 26, 789–803.Google Scholar
Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S., Murakami, M., Kikkawa, Y. & Suzuki, T. (1997). Cryopreservation of mature bovine oocytes following centrifugation treatment. Cryobiology 34, 36–41.Google Scholar
Parrish, J.J., Susko-Parrish, J., Winer, M.A. & First, N.L. (1988) Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–80.Google Scholar
Practice Committees of American Society for Reproductive Medicine; Society for Assisted Reproductive Technology. (2013). Mature oocyte cryopreservation: a guideline. Fertil Steril. 99, 37–43.CrossRefGoogle Scholar
Prentice, J.R., Singh, J., Dochi, O. & Anzar, M. (2011). Factors affecting nuclear maturation, cleavage and embryo development of vitrified bovine cumulus–oocyte complexes. Theriogenology 75, 602–9.Google Scholar
Rall, W.F. & Fahy, G.M. (1985). Ice-free cryopreservation of mouse embryos at −196°C by vitrification. Nature 313, 573–5.CrossRefGoogle Scholar
Rienzi, L., Romano, S., Albricci, L., Maggiulli, R., Capalbo, A., Baroni, E., Colamaria, S., Sapienza, F. & Ubaldi, F. (2010). Embryo development of fresh versus vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum. Reprod. 25, 66–73.Google Scholar
Rojas, C., Palomo, M.J., Albarracín, 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
Rosenkrans, C.F. Jr & First, N.L. (1994). Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro . J. Anim. Sci. 72, 434–7.Google Scholar
Sanfilippo, S., Canis, M., Ouchchane, L., Botchorishvili, R., Artonne, C., Janny, L. & Brugnon, F. (2011). Viability assessment of fresh and frozen/thawed isolated human follicles: reliability of two methods (trypan blue and calcein AM/ethidium homodimer-1). J. Assist. Reprod. Genet. 28, 1151–6.Google Scholar
Shaw, J.M., Oranratnachai, A. & Trounson, A.O. (2000). Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology 53, 59–72.Google Scholar
Sirard, M.A., Richard, F. & Mayes, M. (1998). Controlling meiotic resumption in bovine oocytes: a review. Theriogenology 49, 483–97.Google Scholar
Sprícigo, J.F.W., Morais, K., Ferreira, A.R., Machado, G.M., Gomes, A.C.M., Rumpf, R., Franco, M.M. & Dode, M.A.N. (2014). Vitrification of bovine oocytes at different meiotic stages using the Cryotop method: assessment of morphological, molecular and functional patterns. Cryobiology 69, 256–65.Google Scholar
Sripunya, N., Liang, Y., Panyawai, K., Srirattana, K., Ngernsoungnern, A., Ngernsoungnern, P., Ketudat-Cairns, M. & Parnpai, R. (2014). Cytochalasin B efficiency in the cryopreservation of immature bovine oocytes by Cryotop and solid surface vitrification methods. Cryobiology 69, 496–9.Google Scholar
Stojkovic, M., Machado, S.A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P.B. & Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–9.Google Scholar
Süss, U., Wuthrich, K. & Stranzinger, G. (1988). Chromosome configurations and time sequence of the first meiotic division in bovine oocytes matured in vitro . Biol. Reprod. 38, 871–80.CrossRefGoogle ScholarPubMed
Tucker, M.J., Wright, G., Morton, P.C. & Massey, J.B. (1998). Birth after cryopreservation of immature oocytes with subsequent in vitro maturation. Fertil. Steril. 70, 578–9.Google Scholar
Versieren, K., Heindryckx, B., O'Leary, T., De Croo, I., Van den Abbeel, E. & Gerris, J. (2011). Slow controlled-rate freezing of human in vitro matured oocytes: effects on maturation rate and kinetics and parthenogenetic activation. Fertil. Steril. 96, 624–8.Google Scholar
Zhou, X.L., Al Naib, A., Sun, D.W. & Lonergan, P. (2010). Bovine oocyte vitrification using the Cryotop method: effect of cumulus cells and vitrification protocol on survival and subsequent development. Cryobiology 61, 66–72.Google Scholar