Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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The Effect of the Addition and Removal of Various Cryoprotectants on the Nuclear Maturation and ATP Content of Immature Porcine Oocytes

  • Tsuzuki, Y. (Laboratory of Animal Reproduction, Faculty of Agriculture, University of Miyazaki) ;
  • Nozawa, K. (Laboratory of Animal Reproduction, Faculty of Agriculture, University of Miyazaki) ;
  • Ashizawa, K. (Laboratory of Animal Reproduction, Faculty of Agriculture, University of Miyazaki)
  • Received : 2008.05.22
  • Accepted : 2008.09.30
  • Published : 2009.03.01
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Abstract

This study was undertaken to investigate the influence of exposure and removal of four different cryoprotectants (CPAs) on the ATP content of cumulus cell-enclosed (COs) and cumulus cell-denuded (DOs) immature porcine oocytes. The in vitro nuclear maturation of the COs, exposed to and removed from the CPAs was also assessed. Both COs and DOs were exposed to 1.5 M concentrations of each CPA (ethylene glycol (EG); propylene glycol (PG); dimethyl-sulfoxide (DMSO); and glycerol (G)) for durations of 5, 15, and 30 minutes at room temperature ($23.5{\pm}1.5^{\circ}C$), and immersed in physiological saline supplemented with 20% (v/v) fetal bovine serum for 5 minutes ($39^{\circ}C$) to remove each CPA. Before, during and after exposure to each CPA, the ATP content of both the COs and the DOs was measured. After removal from each CPA an aliquot of the COs was matured for 44${\pm}$2 h, and their nuclear maturation rates were measured up to the metaphase stage of the second meiotic division (the M-II stage). The maturation rates up to the M-II stage were not significantly different between all the groups that were exposed to each CPA for 5 minutes. For 15 and 30 minute exposures, the maturation rates of the COs exposed to PG, DMSO and EG were almost the same as those of the control groups; however, the rates of G group exposed for 15 and 30 minutes were significantly lower (p<0.05) than the control group. These groups were also found to have a decrease in the ATP content of COs and DOs during and after exposure for the same periods (p<0.05). In addition, although the ATP contents of the COs after exposure to EG for any period were the same as the controls, the ATP content of the DOs exposed to EG for any period were significantly lower (p<0.05) than those of the controls. When the ATP content of the COs and DOs of each CPA were compared, the DOs exposed to PG were found to have a significantly greater level (p<0.05) than DOs exposed to G for any duration. In addition, the ATP content of DOs exposed to PG for 30 min and removal was also higher (p<0.05) than when exposed to DMSO for the same period. These findings indicate that PG may be a useful CPA for the cryopreservation of immature porcine oocytes.

Keywords

References

  1. Agca, Y., J. Liu, A. T. Peter, E. S. Critser and J. K. Critser. 1998. Effect of developmental stage on bovine oocyte plasma membrane water and cryoprotectant permeability characteristics. Mol. Reprod. Dev. 49:408-415 https://doi.org/10.1002/(SICI)1098-2795(199804)49:4<408::AID-MRD8>3.0.CO;2-R
  2. Anchordoguy, T. J., A. S. Rudolph, J. F. Carpenter and J. H. Crowe. 1987. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24:324-331 https://doi.org/10.1016/0011-2240(87)90036-8
  3. Arav, A., D. Sheshu and M. Mattioli. 1993. Osmotic and cytotoxic study of vitrification of immature bovine oocytes. J. Reprod. Fert. 99:353-358 https://doi.org/10.1530/jrf.0.0990353
  4. Ashwood-Smith, M. J. 1987. Machanisms of cryoprotectant action. In: Temperature and animal cells (Ed. K. Bowler and B. J. Fuller). Company of Biologist, Cambridge, pp. 395-406
  5. Ba$\check{g}$is, H. and H. Odaman Mercan. 2005. Effect of three different cryoprotectant solutions in solid surface vitrification (SSV) techniques on the development rate of vitrified pronuclearstage mouse embryos. Turk. J. Vet. Anim. Sci. 29:621-627
  6. Brevini, T. A. L., F. Cillo, S. Antonini and F. Gandolfi. 2007. Cytoplasmic remodeling and the acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci. 98:23-38 https://doi.org/10.1016/j.anireprosci.2006.10.018
  7. Chian, R. C., M. Kuwayama, L. Tan, J. Tan, O. Kato and T. Nagai. 2004. High survival rate of bovine oocytes matured in vitro following vitrification. J. Reprod. Dev. 50:685-696 https://doi.org/10.1262/jrd.50.685
  8. Coticchio, G., M. A. Bonu, R. Sciajno, E. Sereni, V. Bianchi and A. Borini. 2007. Outlook: truths and myths of oocyte sensitivity to controlled rate freezing. Reprod. BioMed. Online 15:24-30 https://doi.org/10.1016/S1472-6483(10)60687-6
  9. Didion, B. A., D. Pomp, M. J. Martin, G. E. Homanics and C. L. Markert. 1990. Observations on the cooling and cryopreservation of pig oocytes at the germinal vesicle stage. J. Anim. Sci. 68:2803-2810
  10. Downs, S. M. 1993. Factors affecting the resumption of meiotic maturation in mammalian oocytes. Theriogenology 39:65-79 https://doi.org/10.1016/0093-691X(93)90024-Y
  11. Edashige, K., M. Sakamoto and M. Kasai. 2000. Expression of mRNAs of the aquaporin family in mouse oocytes and embryos. Cryobiology 40:171-175 https://doi.org/10.1006/cryo.1999.2228
  12. Edashige, K. and M. Kasai. 2007. The movement of water and cryoprotectants in mammalian oocytes and embryos and its relevance to cryopreservation. J. Mamm. Ova Res. 24:18-22 https://doi.org/10.1274/jmor.24.18
  13. Edashige, K., S. Ohta, M. Tanaka, T. Kuwano, D. M. Valdez, Jr., T. Hara, B. Jin, S. Takahashi, S. Seki, C. Koshimoto and M. Kasai. 2007. The role of aquaporin 3 in the movement of water and cryoprotectants in mouse morulae. Biol. Reprod. 77:365-375 https://doi.org/10.1095/biolreprod.106.059261
  14. Fabbri, R., E. Porcu, T. Marsella, G. Rocchetta, S. Venturoli and C. Flamigni. 2001. Human oocyte cryopreservation: new perspectives regarding oocyte survival. Hum. Reprod. 16:411-416 https://doi.org/10.1093/humrep/16.3.411
  15. Fahy, G. M., T. H. Lilley, H. Linsdell, M. ST. J. Douglas and H. T. Meryman. 1990. Cryoprotectant toxicity and cryoprotectant toxicity reduction: in search of molecular mechanisms. Cryobiology 27:247-268 https://doi.org/10.1016/0011-2240(90)90025-Y
  16. Fahy, G. M., B. Wowk, J. Wu and S. Paynter. 2004. Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology 48:22-35 https://doi.org/10.1016/j.cryobiol.2003.11.004
  17. Ford, P., J. Merot, A. Jawerbaum, M. A. F. Gimeno, C. Capurro and M. Parisi. 2000. Water permeability in rat oocytes at different maturity stages: aquaporin-9 expression. J. Membrane Biol. 176:151-158 https://doi.org/10.1007/s002320001084
  18. Friedler, S., L. C. Giudice and E. J. Lamb. 1988. Cryopreservation of embryos and ova. Fertil. Steril. 49:743-764
  19. Fujihira, T., H. Nagai and Y. Fukui. 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 51:339-343 https://doi.org/10.1016/j.cryobiol.2005.08.002
  20. Fuller, B. J. 2004. Cryoprotectants: the essential antifreezes to protect life in the frozen state. CryoLetters 25:375-388
  21. Gardner, D. K., C. B. Sheehan, L. Rienzi, M. Katz-Jaffe and M. G. Larman. 2007. Analysis of oocyte physiology to improve cryopreservation procedures. Theriogenology 67:64-72 https://doi.org/10.1016/j.theriogenology.2006.09.012
  22. Gupta, M. K., S. J. Uhm and H. T. Lee. 2007. Cryopreservation of immature and in vitro matured porcine oocytes by solid surface vitrification. Theriogenology 67:238-248 https://doi.org/10.1016/j.theriogenology.2006.07.015
  23. Herrick, J. R., A. M. Brad and R. L. Krisher. 2006. Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reprod. 131:289-298 https://doi.org/10.1530/rep.1.00835
  24. Huang, W.T. and W. Holtz. 2002. Effects of meiotic stages, cryoprotectants, cooling and vitrification on the cryopreservation of porcine oocytes. Asian-Aust. J. Anim. Sci. 15:485-493
  25. Hunter, R. H. and C. Polge. 1966. Maturation of follicular oocytes in the pig after injection of human chorionic gonadotrophin. J. Reprod. Fertil. 12:525-531 https://doi.org/10.1530/jrf.0.0120525
  26. Jain, J. K. and R. J. Paulson. 2006. Oocyte cryopreservation. Fertil. Steril. 86(Suppl. 3):1037-1046
  27. Kleinhans, F. W. and P. Mazur. 2007. Comparison of actual vs. synthesized ternary phase diagrams for solutes of cryobiological interest. Cryobiology 54:212-222 https://doi.org/10.1016/j.cryobiol.2007.01.007
  28. Kubota, C., X. Yang, A. Dinnyes, J. Todoroki, H. Yamakuchi, K. Mizoshita, S. Inohae and N. Tabata. 1998. In vitro and in vivo survival of frozen-thawed bovine oocytes after IVF, nuclear transfer, and parthenogenetic activation. Mol. Reprod. Dev. 51:281-286 https://doi.org/10.1002/(SICI)1098-2795(199811)51:3<281::AID-MRD7>3.0.CO;2-L
  29. Ledda, S., L. Bogliolo, S. Succu, F. Ariu, D. Bebbere, G. G. Leoni and S. Naitana. 2007. Oocyte cryopreservation: oocyte assessment and strategies for improving survival. Reprod. Fertil. Dev. 19:13-23 https://doi.org/10.1071/RD06126
  30. Leibo, S. P. 2008. Cryopreservation of oocytes and embryos: optimization by theoretical versus empirical analysis. Theriogenology 69:37-47 https://doi.org/10.1016/j.theriogenology.2007.10.006
  31. Magnusson, V., W. B. Feitosa, M. D. Goissis, C. Yamada, L. M. T. Tavares, M. E. O. D'A. Assump$\c{c}$$\tilde{a}$o and J. A. Visintin. 2007. Bovine oocyte vitrification: effect of ethylene glycol concentrations and meiotic stages. Anim. Reprod. Sci. 106:265-273 https://doi.org/10.1016/j.anireprosci.2007.05.001
  32. Mukaida, T. and M. Kasai. 2004. Cryobiology: slow freezing and vitrification of embryos. In: A laboratory guide to the mammalian embryo (Ed. D. K. Gardner, M. Lane and A. J. Watson). Oxford University Press, Inc., New York, pp. 375-390
  33. Nagano, M., S. Katagiri and Y. Takahashi. 2006. ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies. Zygote 14:299-304 https://doi.org/10.1017/S0967199406003807
  34. Otoi, T., S. Tachikawa, S. Kondo, M. Takagi and T. Suzuki. 1994. Developmental competence of bovine oocytes frozen at different cooling rates. Cryobiology 31:344-348 https://doi.org/10.1006/cryo.1994.1041
  35. Otoi, T., K. Yamamoto, N. Koyama and T. Suzuki. 1995. In vitro fertilization and development of immature and mature bovine oocytes cryopreserved by ethylene glycol with sucrose. Cryobiology 32:455-460 https://doi.org/10.1006/cryo.1995.1045
  36. Paynter, S. J. and B. J. Fuller. 2007. Cryopreservation of mammalian oocytes. Methods. Mol. Biol. 368:313-324 https://doi.org/10.1007/978-1-59745-362-2_22
  37. Pedro, P. B., E. Yokoyama, S. E. Zhu, N. Yoshida, D. M. Valdez Jr., M. Tanaka, K. Edashige and M. Kasai. 2005. Permeability of mouse oocytes and embryos at various developmental stages to five cryoprotectants. J. Reprod. Dev. 51:235-246 https://doi.org/10.1262/jrd.16079
  38. Petters, R. M. and K. D. Wells. 1993. Culture of pig embryos. J. Reprod. Fertil. Suppl. 48:61-73
  39. Pickering, S. J., P. R. Braude, M. H. Johnson, A. Cant and J. Currie. 1990. Transient cooling to room temperature can cause irreversible disruption of the meiotic spindle in the human oocyte. Fertil. Steril. 54:102-108
  40. Poldelski, V., A. Johnson, S. Wright, V. D. Rosa and R. A. Zager. 2001. Ethylene glycol-mediated tubular injury: identification of critical metabolites and injury pathways. Am. J. Kidney Dis. 38:339-348 https://doi.org/10.1053/ajkd.2001.26099
  41. Rall, W. F. 1987. Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology 24:387-402 https://doi.org/10.1016/0011-2240(87)90042-3
  42. Rittmeyer, I. C. and U. E. Nydegger. 1992. Influence of the cryoprotective agents glycerol and hydroxyethyl starch on red blood cell ATP and 2,3-diphosphoglyceric acid levels. Vox Sang 62:141-145 https://doi.org/10.1111/j.1423-0410.1992.tb01187.x
  43. Rojas, C., M. J. Palomo, J. L. Albarracín and T. Mogas. 2004. Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules, and actin microfilaments. Cryobiology 49:211-220 https://doi.org/10.1016/j.cryobiol.2004.07.002
  44. Russell, D. L. and R. L. Robker. 2007. Molecular mechanisms of ovulation: co-ordination though the cumulus complex. Hum. Reprod. Update 13:289-312 https://doi.org/10.1093/humupd/dml062
  45. Shaw, J. M. and G. M. Jones. 2003. Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum. Reprod. Update 9:583-605 https://doi.org/10.1093/humupd/dmg041
  46. Shimizu, T. and K. Kouketsu. 1988. Reversible effects of glycerol on the metabolism of platelets kept at room temperature. Cryobiology 25:164-169 https://doi.org/10.1016/0011-2240(88)90010-7
  47. Stachecki, J. J. and S. M. Willadsen. 2000. Cryopreservation of mouse oocytes using a medium with low sodium content: effect of plunge temperature. Cryobiology 40:4-12 https://doi.org/10.1006/cryo.1999.2215
  48. Stachecki, J. J., J. Cohen, J. Garrisi, S. Munn$\acute{e}$, C. Burgess and S. M. Willadsen. 2006. Cryopreservation of unfertilized human oocytes. Reprod. BioMed. Online 13:222-227 https://doi.org/10.1016/S1472-6483(10)60619-0
  49. Stojkovic, M., S. A. Machado, P. Stojkovic, V. Zakhartchenko, P. Hutzler, P. B. Gonçalves and E. Wolf. 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. 64:904-909 https://doi.org/10.1095/biolreprod64.3.904
  50. Tharasanit, T., S. Colleoni, G. Lazzari, B. Colenbrander, C. Galli and T. A. E. Stout. 2006. Effect of cumulus morphology and maturation stage on the cryopreservability of equine oocytes. Reprod. 132:759-769 https://doi.org/10.1530/rep.1.01156
  51. Tsuzuki, Y., M. Hisanaga, K. Ashizawa and N. Fujihara. 2001. The effects of dimethyl-sulfoxide and sucrose as a cryoprotectant on the adenosine triphosphate and ultrastructure of bovine oocytes matured in vitro. Asian-Aust. J. Anim. Sci. 14:1353-1359
  52. Tsuzuki, Y., M. Ugajin and K. Ashizawa. 2008. The effect of adding glucose to the maturation medium on the nuclear maturation and ATP content of porcine oocytes. J. Mamm. Ova Res. 25:172-176 https://doi.org/10.1274/0916-7625-25.3.172
  53. Van Blerkom, J., P. W. Davis and J. Lee. 1995. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10:415-424
  54. Van der Elst, J., S. Nerinckx and A. C. Van Steirteghem. 1992. In vitro maturation of mouse germinal vesicle-stage oocytes following cooling, exposure to cryoprotectants and ultrarapid freezing: limited effect on the morphology of the second meiotic spindle. Hum. Reprod. 7:1440-1446
  55. Vincent, C., S. J. Pickering and M. H. Johnson. 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. 89:253-259 https://doi.org/10.1530/jrf.0.0890253
  56. Wani, N. A., A. K. Misra and S. N. Maurya. 2004. Maturation rates of vitrified-thawed immature buffalo (Bubalus bubalis) oocytes: effect of different types of cryoprotectants. Anim. Reprod. Sci. 84:327-335 https://doi.org/10.1016/j.anireprosci.2004.02.007
  57. Wu, C., R. Rui, J. Dai, C. Zhang, S. Ju, B. Xie, X. Lu and X. Zheng. 2006. Effects of cryopreservation on the developmental competence, ultrastructure and cytoskeletal structure of porcine oocytes. Mol. Reprod. Dev. 73:1454-1462 https://doi.org/10.1002/mrd.20579
  58. Yamada, C., H. V. A. Caetano, R. Sim$\tilde{o}$es, A. C. Nicacio, W. B. Feitosa, M. E. O. D'$\acute{A}$. Assump$\c{c}$$\tilde{a}$o and J. A. Visintin. 2007. Immature bovine oocyte cryopreservation: comparison of different associations with ethylene glycol, glycerol and dimethylsulfoxide. Anim. Reprod. Sci. 99:384-388 https://doi.org/10.1016/j.anireprosci.2006.07.001
  59. Yavin, S. and A. Arav. 2007. Measurement of essential physical properties of vitrification solutions. Theriogenology 67:81-89 https://doi.org/10.1016/j.theriogenology.2006.09.029
  60. Yokoo, M. and E. Sato. 2004. Cumulus-oocyte complex interactions during oocyte maturation. Int. Rev. Cytol. 235:251-291 https://doi.org/10.1016/S0074-7696(04)35006-0
  61. Yu, Z. W. and P. J. Quinn. 1998. Solvation effects of dimethyl sulphoxide on the structure of phospholipid bilayers. Biophysic. Chem. 70:35-39 https://doi.org/10.1016/S0301-4622(97)00100-2

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