Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T09:24:54.491Z Has data issue: false hasContentIssue false
  • English
  • Français

Porcine oocyte vitrification in optimized low toxicity solution with open pulled straws

Published online by Cambridge University Press:  29 October 2012

F. Marco-Jiménez ,
L. Casares-Crespo  and
J.S. Vicente
F. Marco-Jiménez*
Affiliation:
Laboratory of Biotechnology of Reproduction, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain.
L. Casares-Crespo
Affiliation:
Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción, Universidad Politécnica de Valencia, Valencia 46022, Spain.
J.S. Vicente
Affiliation:
Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción, Universidad Politécnica de Valencia, Valencia 46022, Spain.
*
All correspondence to: Francisco Marco Jiménez, Laboratory of Biotechnology of Reproduction, Institute of Science and Animal Technology (ICTA) at the Polytechnic University of Valencia, C/Camino de Vera s/n, 46022 Valencia, Spain. Tel: +34 96 3879435. Fax: +34 96 3877439. e-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

One of the greatest challenges for reproductive cryobiologists today is to develop an efficient cryopreservation method for human and domestic animal oocytes. The objective of the present study was to optimize a low toxicity solution called VM3 to vitrify porcine oocytes using an open pulled straw (OPS) device and to evaluate the effects on viability, chromosomal organization and cortical granules distribution. Two experiments were conducted in this study. Firstly, we determined the minimum concentration of cryoprotectant present in the VM3 solution required (7.6 M) for vitrification using an OPS device. The appearance of opacity was observed when using a cooling solution at –196°C; no observable opacity was noted as vitrification. In addition, the ultrastructure of oocytes in VM3 or VM3 optimized solution was examined using cryo-scanning electron microscopy. The minimum total cryoprotectant concentration present in VM3 solution necessary for apparent vitrification was 5.6 M when combined with use of an OPS device. Use of both vitrification solutions showed a characteristic plasticized surface. In the second experiment, the relative cytotoxicity of vitrification solutions (VM3 and VM3 optimized) was studied. Oocyte viability, chromosomal organization and the cortical granules distribution were assessed by fluorescent stain. After warming, oocyte survival rate was similar to that of fresh oocytes. The vitrification process significantly reduced correct chromosomal organization and cortical granules distribution rates compared with the fresh oocytes group. However, correct chromosomal organization and cortical granules distribution rates did not differ among oocytes placed in different vitrification solutions. In conclusion, our data demonstrated that the VM3 solution can be optimized and that reduction in concentration to 5.6 M enabled vitrification of oocytes with an OPS device, however use of the VM3 optimised solution had no beneficial effect on vitrification of porcine oocytes.

Keywords

Ice blockersOPSToxicityVM3
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 204 - 212
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

Abe, Y., Hara, K., Matsumoto, H., Kobayashi, J., Sasada, H., Ekwall, H., Rodriguez-Martinez, H. & Sato, E. (2005). Feasibility of a nylon-mesh holder for vitrification of bovine germinal vesicle oocytes in subsequent production of viable blastocysts. Biol. Reprod. 72, 1416–20.Google Scholar
Aono, N., Abe, Y., Hara, K., Sasada, H., Sato, E. & Yoshida, H. (2005). Production of live offspring from mouse germinal vesicle-stage oocytes vitrified by an optimized stepwise method, SWEID. Fertil. Steril. 84, 1078–82.Google Scholar
Bos-Mikich, A., Wood, M.J., Candy, C.J. & Whittingham, D.G. (1995). Cytogenetical analysis and developmental potential of vitrified mouse oocytes. Biol. Reprod. 53, 780–5.Google Scholar
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.Google Scholar
Connors, S.A., Kanatsu-Shinohara, M., Schultz, R.M. & Kopf, G.S. (1998). Involvement of the cytoskeleton in the movement of cortical granules during oocyte maturation, and cortical granule anchoring in mouse eggs. Dev. Biol. 200, 103–15.Google Scholar
Coticchio, G., Borini, A., Distratis, V., Maione, M., Scaravelli, G., Bianchi, V., Macchiarelli, G. & Nottola, S.A. (2010). Qualitative and morphometric analysis of the ultrastructure of human oocytes cryopreserved by two alternative slow cooling protocols. J. Assist. Reprod. Genet. 27, 131–40.Google Scholar
de Graaf, I.A., Draaisma, A.L., Schoeman, O., Fahy, G.M., Groothuis, G.M. & Koster, H.J. (2007). Cryopreservation of rat precision-cut liver and kidney slices by rapid freezing and vitrification. Cryobiology 54, 1–12.Google Scholar
Dobrinsky, J.R. (2002). Advancements in cryopreservation of domestic animal embryos. Theriogenology 57, 285–302.Google Scholar
Du, Y., Pribenszky, C.S., Molnar, M., Zhang, X., Yang, H., Kuwayama, M., Pedersen, A.M., Villemoes, K., Bolund, L. & Vajta, G. (2008). High hydrostatic pressure: a new way to improve in vitro developmental competence of porcine matured oocytes after vitrification. Reproduction 135, 13–17.Google Scholar
Ebrahimi, B., Valojerdi, M.R., Eftekhari-Yazdi, P., Baharvand, H. & Farrokhi, A. (2010). IVM and gene expression of sheep cumulus–oocyte complexes following different methods of vitrification. Reprod. Biomed. Online 20, 26–34.Google Scholar
Fadini, R., Brambillasca, F., Renzini, M.M., Merola, M., Comi, R., De Ponti, E. & Dal Canto, M.B. (2009). Human oocyte cryopreservation: comparison between slow and ultrarapid methods. Reprod. Biomed. Online 19, 171–80.Google Scholar
Fahy, G.M. (1986). The relevance of cryoprotectant “toxicity” to cryobiology. Cryobiology 23, 1–13.Google Scholar
Fahy, G.M., Wowk, B., Wu, J. & Paynter, S. (2004). Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology 48, 22–35.Google Scholar
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., Wusiman, A., Wang, Y.P. & Zhu, S.E. (2009). Positive effects of Taxol pretreatment on morphology, distribution and ultrastructure of mitochondria and lipid droplets in vitrification of in vitro matured porcine oocytes. Anim. Reprod. Sci. 115, 158–68.Google Scholar
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.Google Scholar
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.Google Scholar
Genicot, G., Leroy, J.L., Soom, A.V. & Donnay, I. (2005). The use of a fluorescent dye, Nile red, to evaluate the lipid content of single mammalian oocytes. Theriogenology 63, 1181–94.Google Scholar
Ghetler, Y., Skutelsky, E., Ben Nun, I., Ben Dor, L., Amihai, D. & Shalgi, R. (2006). Human oocyte cryopreservation and the fate of cortical granules. Fertil. Steril. 86, 210–16.Google Scholar
Gómez, M.C., Kagawa, N., Pope, C. E., Kuwayama, M., Leibo, S. P. & Dresser, B.L. (2007). In vivo survival of domestic cat oocytes after vitrification, intracytoplasmic sperm injection, and transfer to recipients. Reprod. Fertil. Dev. 20, 118.Google Scholar
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2007). Cryopreservation of immature and in vitro matured porcine oocytes by solid surface vitrification. Theriogenology 67, 238–48.Google Scholar
Hara, K., Abe, Y., Kumada, N., Aono, N., Kobayashi, J., Matsumoto, H., Sasada, H. & Sato, E. (2005). Extrusion and removal of lipid from the cytoplasm of porcine oocytes at the germinal vesicle stage: centrifugation under hypertonic conditions influences vitrification. Cryobiology 50, 216–22.Google Scholar
Huang, J., Li, Q., Zhao, R., Li, W., Han, Z., Chen, X., Xiao, B., Wu, S., Jiang, Z., Hu, J. & Liu, L. (2008). Effect of sugars on maturation rate of vitrified-thawed immature porcine oocytes. Anim. Reprod. Sci. 106, 25–35.Google Scholar
Hunter, J.E., Bernard, A. & Fuller, B.J. (1992). Measurements of the membrane water permeability (Lp) and its temperature dependence (activation energy) in human fresh and failed-to-fertilize oocytes and mouse oocyte. Cryobiology 29, 240–9.Google Scholar
Hyttel, P., Vajta, G. & Callesen, H. (2000). Vitrification of bovine oocytes with the open pulled straw method: ultrastructural consequences. Mol. Reprod. Dev. 56, 80–8.Google Scholar
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., Isachenko, E., Michelmann, H.W., Alabart, J.L., Vazquez, I., Bezugly, N. & Nawroth, F. (2001). Lipolysis and ultrastructural changes of intracellular lipid vesicles after cooling of bovine and porcine GV-oocytes. Anat. Histol. Embryol. 30, 333–8.Google Scholar
Kuwayama, M. (2007). Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology 67, 73–80.Google Scholar
Kuwayama, M., Vajta, G., Ieda, S. & Kato, O. (2005). Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination. Reprod. Biomed. Online 11, 608–14.Google Scholar
Larman, M.G., Sheehan, C.B. & Gardner, D.K. (2006). Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 131, 53–61.Google Scholar
Lawson, A., Ahmad, H. & Sambanisa, A. (2011). Cytotoxicity effects of cryoprotectants as single-component and cocktail vitrification solutions. Cryobiology 62, 115–22.Google Scholar
Lee, H.J., Elmoazzen, H., Wright, D., Biggers, J., Rueda, B.R., Heo, Y.S., Toner, M. & Toth, T.L. (2010). Ultra-rapid vitrification of mouse oocytes in low cryoprotectant concentrations. Reprod. Biomed. Online 20, 201–8.Google Scholar
Liebermann, J., Tucker, M.J., Graham, J.R., Han, T., Davis, A. & Levy, M.J. (2002). Blastocyst development after vitrification of multipronuclear zygotes using the flexipet denuding pipette. Reprod. Biomed. Online 4, 146–50.Google Scholar
Liu, R.H., Sun, Q.Y., Li, Y.H., Jiao, L.H. & Wang, W.H. (2003). Maturation of porcine oocytes after cooling at the germinal vesicle stage. Zygote 11, 299–305.Google Scholar
Lopes, C.A., dos Santos, R.R., Celestino, J.J., Melo, M.A., Chaves, R.N., Campello, C.C., Silva, J.R., Báo, S.N., Jewgenow, K. & de Figueiredo, J.R. (2009). Short-term preservation of canine preantral follicles: effects of temperature, medium and time. Anim. Reprod. Sci. 115, 201–14.Google Scholar
Maclellan, L.J., Carnevale, E.M., Coutinhoda Silva, M.A., Scoggin, C.F., Bruemmer, J.E. & Squires, E.L. (2002). Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology 58, 911–9.Google Scholar
Mavrides, A. & Morroll, D. (2005). Bypassing the effect of zona pellucida changes on embryo formation following cryopreservation of bovine oocytes. Eur. J. Obstet. Gynecol. Reprod. Biol. 118, 66–70.Google Scholar
Mazur, P. (1963). Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing. J. Gen. Physiol. 47, 347–69.Google Scholar
McGrath, J.J. (1997). Quantitative measurement of cell membrane transport: technology and applications. Cryobiology 34, 315–34.Google Scholar
Morato, 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 chromosomes configuration and embryo development. Cryobiology 57, 137–41.Google Scholar
Nottola, S.A., Coticchio, G., Sciajno, R., Gambardella, A., Maione, M., Scaravelli, G., Bianchi, S., Macchiarelli, G. & Borini, A. (2009). Ultrastructural markers of quality in human mature oocytes vitrified using cryoleaf and cryoloop. Reprod. Biomed. Online 19, 17–27.Google Scholar
Ogawa, B., Ueno, S., Nakayama, N., Matsunari, H., Nakano, K., Fujiwara, T., Ikezawa, Y. & Nagashima, H. (2010). Developmental ability of porcine in vitro matured oocytes at the meiosis II stage after vitrification. J. Reprod. Dev. 56, 356–61.Google Scholar
Park, K.E., Kwon, I.K., Han, M.S. & Niwa, K. (2005). Effects of partial removal of cytoplasmic lipid on survival of vitrified germinal vesicle stage pig oocytes. J. Reprod. Dev. 51, 151–60.Google Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. 48, 61–73.Google Scholar
Pichugin, Y., Fahy, G.M. & Morin, R. (2006). Cryopreservation of rat hippocampal slices by vitrification. Cryobiology 52, 228–40.Google Scholar
Porcu, E., Fabbri, R., Damiano, G., Giunchi, S., Fratto, R., Ciotti, S., Venturoli, P.M. & Flamigni, C. (2000). Clinical experience and applications of oocyte cryopreservation. Mol. Cell. Endocrinol. 169, 33–7.Google Scholar
Pribenszky, C., Du, Y., Molnár, M., Harnos, A. & Vajta, G. (2008). Increased stress tolerance of matured pig oocytes after high hydrostatic pressure treatment. Anim. Reprod. Sci. 106, 200–7.Google Scholar
Rall, W.F. & Fahy, G.M. (1985). Ice-free cryopreservation of mouse embryos at −196 degrees C by vitrification. Nature 313, 573–5.Google Scholar
Rojas, C., Palomo, M.J., Albarracin, 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.Google Scholar
Santos, R.R., Tharasanit, T., Figueiredo, J.R., van Haeften, T. & van den Hurk, R. (2006). Preservation of caprine preantral follicle viability after cryopreservation in sucrose and ethylene glycol. Cel. Tissue Res. 325, 523–31.Google Scholar
Shi, W.Q., Zhu, S.E., Zhang, D., Wang, W.H., Tang, G.L., Hou, Y.P. & Tian, S.J. (2006). Improved development by Taxol pretreatment after vitrification of in vitro matured porcine oocytes. Reproduction 131, 795–804.CrossRefGoogle ScholarPubMed
Shi, L.Y., Jin, H.F., Kim, J.G., Mohana Kumar, B., Balasubramanian, S. & Choe, S.Y. (2007) Ultra-structural changes and developmental potential of porcine oocytes following vitrification. Anim. Reprod. Sci. 100, 128–40.Google Scholar
Somfai, T., Ozawa, M., Noguchi, J., Kaneko, H., KurianiKarja, N.W. & Farhudin, M. (2007). Developmental competence of in vitro fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology 55, 115–26.Google Scholar
Somfai, T., Dinnyés, A., Sage, D., Marosán, M., Carnwath, J.W., Ozawa, M., Kikuchi, K. & Niemann, H. (2006). Development to the blastocyst stage of parthenogenetically activated in vitro matured porcine oocytes after solid surface vitrification (SSV). Theriogenology 66, 415–22.Google Scholar
Somfai, T., Kashiwazaki, N., Ozawa, M., Nakai, M., Maedomari, N., Noguchi, J., Kaneko, H., Nagai, T. & Kikuchi, K. (2008). Effect of centrifugation treatment before vitrification on the viability of porcine mature oocytes and zygotes produced in vitro. J. Reprod. Dev. 54, 149–55.Google Scholar
Somfai, T., Noguchi, J., Kaneko, H., Nakai, M., Ozawa, M., Kashiwazaki, N., Egerszegi, I., Rátky, J., Nagai, T. & Kikuchi, K. (2010). Production of good-quality porcine blastocysts by in vitro fertilization of follicular oocytes vitrified at the germinal vesicle stage. Theriogenology 73, 147–56.Google Scholar
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.Google Scholar
Succu, S., Leoni, G.G., Berlinguer, F., Madeddu, M., Bebbere, D., Mossa, F., Bogliolo, L., Ledda, S. & Naitana, S. (2007). Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology 68, 107–14.Google Scholar
Sun, Q.Y., Lai, L., Wu, G.M., Park, K.W., Day, B.N., Prather, R.S. & Schatten, H. (2001). Microtubule assembly after treatment of pig oocytes with taxol: correlation with chromosomes, gamma-tubulin, and MAP kinase. Mol. Reprod. Dev. 60, 481–90.Google Scholar
Takahashi, T., Igarashi, H., Doshida, M., Takahashi, K., Nakahara, K., Tezuka, N. & Kurachi, H. (2004). Lowering intracellular and extracellular calcium contents prevents cytotoxic effects of ethylene glycol-based vitrification solution in unfertilized mouse oocytes. Mol. Reprod. Dev. 68, 250–8.Google Scholar
Tan, X., Song, E., Liu, X., You, W. & Wan, F. (2009). Factors affecting the survival, fertilization, and embryonic development of mouse oocytes after vitrification using glass capillaries. In Vitro Cell Dev. Biol. Anim. 45, 420–9.Google Scholar
Vajta, G. & Kuwayama, M. (2006). Improving cryopreservation systems. Theriogenology 65, 236–44.Google Scholar
Vajta, G., Holm, P., Kuwayama, M., Booth, P.J., Jacobsen, H., Greve, T. & Callesen, H. (1998). Open pulled straw (OPS) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol. Reprod. Dev. 51, 53–8.Google Scholar
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.Google Scholar
Wu, C., Rui, R., Dai, J., Zhang, C., Ju, S. & Xie, B. (2006). Effects of cryopreservation on the developmental competence, ultrastructure and cytoskeletal structure of porcine oocytes. Mol. Reprod. Dev. 73, 1454–62.Google Scholar
Yavin, S. & Arav, A. (2007). Measurement of essential physical properties of vitrification solutions. Theriogenology 67, 81–9.Google Scholar
Yavin, S., Aroyo, A., Roth, Z. & Arav, A. (2009). Embryo cryopreservation in the presence of low concentration of vitrification solution with sealed pulled straws in liquid nitrogen slush. Hum. Reprod. 24, 797–804.Google Scholar
Zhou, G.B. & Li, N. (2009). Cryopreservation of porcine oocytes: recent advances. Mol. Hum. Reprod. 15, 279–85.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