High Developmental Rates of Mouse Oocytes Cryopreserved by an Optimized Vitrification Protocol: The Effects of Cryoprotectants, Calcium and Cumulus Cells
Unfertilized oocytes are one of the most desired germ cell stages for cryopreservation because these cryopreserved oocytes can be used for assisted reproductive technologies, including in vitro fertilization (IVF) and intracytoplasmic sperm injection. However, in general, the fertility and developme...
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| Published in | Journal of Reproduction and Development Vol. 57; no. 6; pp. 675 - 680 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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Japan
THE SOCIETY FOR REPRODUCTION AND DEVELOPMENT
01.12.2011
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| Abstract | Unfertilized oocytes are one of the most desired germ cell stages for cryopreservation because these cryopreserved oocytes can be used for assisted reproductive technologies, including in vitro fertilization (IVF) and intracytoplasmic sperm injection. However, in general, the fertility and developmental ability of cryopreserved oocytes are still low. The aim of the present study was to improve vitrification of mouse oocytes. First, the effects of calcium and cryoprotectants, dimethyl sulfoxide and ethylene glycol (EG), in vitrification medium on survival and developmental ability of vitrified oocytes were evaluated. Oocytes were vitrified by a minimal volume cooling procedure using different cryoprotectants. Most of the vitrified oocytes were morphologically normal after warming, but their fertility and development were low independently of calcium and cryoprotectants. Second, the effect of cumulus cells on ability of oocytes to be fertilized and develop in vitro was examined. The fertility and developmental ability of denuded oocytes (DOs) after IVF were reduced compared with cumulus-oocyte complexes (COCs) both in fresh and cryopreserved groups. Vitrified COCs showed significantly (P<0.05) higher fertility and ability to develop to the 2-cell and blastocyst stages than those of vitrified DOs with cumulus cells and vitrified DOs alone. The vitrified COCs developed to term at a high success rate equivalent to the rate obtained with IVF using fresh COCs. Taken together, the current results clearly demonstrate that, in the presence of surrounding cumulus cells, matured mouse oocytes vitrified using calcium-free media and EG retain their developmental competence. These findings will contribute to improve oocyte vitrification in not only experimental animals but also clinical application for human infertility. |
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| AbstractList | Unfertilized oocytes are one of the most desired germ cell stages for cryopreservation because these cryopreserved oocytes can be used for assisted reproductive technologies, including in vitro fertilization (IVF) and intracytoplasmic sperm injection. However, in general, the fertility and developmental ability of cryopreserved oocytes are still low. The aim of the present study was to improve vitrification of mouse oocytes. First, the effects of calcium and cryoprotectants, dimethyl sulfoxide and ethylene glycol (EG), in vitrification medium on survival and developmental ability of vitrified oocytes were evaluated. Oocytes were vitrified by a minimal volume cooling procedure using different cryoprotectants. Most of the vitrified oocytes were morphologically normal after warming, but their fertility and development were low independently of calcium and cryoprotectants. Second, the effect of cumulus cells on ability of oocytes to be fertilized and develop in vitro was examined. The fertility and developmental ability of denuded oocytes (DOs) after IVF were reduced compared with cumulus-oocyte complexes (COCs) both in fresh and cryopreserved groups. Vitrified COCs showed significantly (P<0.05) higher fertility and ability to develop to the 2-cell and blastocyst stages than those of vitrified DOs with cumulus cells and vitrified DOs alone. The vitrified COCs developed to term at a high success rate equivalent to the rate obtained with IVF using fresh COCs. Taken together, the current results clearly demonstrate that, in the presence of surrounding cumulus cells, matured mouse oocytes vitrified using calcium-free media and EG retain their developmental competence. These findings will contribute to improve oocyte vitrification in not only experimental animals but also clinical application for human infertility. Unfertilized oocytes are one of the most desired germ cell stages for cryopreservation because these cryopreserved oocytes can be used for assisted reproductive technologies, including in vitro fertilization (IVF) and intracytoplasmic sperm injection. However, in general, the fertility and developmental ability of cryopreserved oocytes are still low. The aim of the present study was to improve vitrification of mouse oocytes. First, the effects of calcium and cryoprotectants, dimethyl sulfoxide and ethylene glycol (EG), in vitrification medium on survival and developmental ability of vitrified oocytes were evaluated. Oocytes were vitrified by a minimal volume cooling procedure using different cryoprotectants. Most of the vitrified oocytes were morphologically normal after warming, but their fertility and development were low independently of calcium and cryoprotectants. Second, the effect of cumulus cells on ability of oocytes to be fertilized and develop in vitro was examined. The fertility and developmental ability of denuded oocytes (DOs) after IVF were reduced compared with cumulus-oocyte complexes (COCs) both in fresh and cryopreserved groups. Vitrified COCs showed significantly (P |
| Author | FUJIWARA, Katsuyoshi KASHIWAZAKI, Naomi ITO, Junya KOHAYA, Natsuki |
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| Cites_doi | 10.1093/molehr/gap016 10.1093/oxfordjournals.humrep.a136849 10.1538/expanim1978.40.4_493 10.1016/j.theriogenology.2006.09.014 10.1002/(SICI)1098-2795(199612)45:4<503::AID-MRD13>3.0.CO;2-X 10.1006/cryo.1995.1007 10.1016/0011-2240(92)90051-3 10.1530/rep.1.00878 10.1016/j.cryobiol.2009.07.007 10.1016/S0093-691X(03)00232-2 10.1095/biolreprod.107.064113 10.1073/pnas.0805699105 10.1262/jrd.19058 10.1095/biolreprod.108.072918 10.1242/dev.020461 10.1111/j.1740-0929.2009.00699.x 10.1006/cryo.1997.2043 10.1038/313573a0 10.1095/biolreprod17.4.527 10.1002/mrd.10102 10.1530/jrf.0.0490089 10.1242/dev.01056 10.1095/biolreprod.108.070383 10.1046/j.1439-0531.2002.00345.x 10.1016/S0015-0282(01)01809-X 10.1002/mrd.1080410214 10.1016/S0015-0282(03)00551-X 10.1210/mend.16.6.0859 10.1016/S0140-6736(86)90989-X |
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| References | 30. Songsasen N, Buckrell BC, Plante C, Leibo SP. In vitro and in vivo survival of cryopreserved sheep embryos. Cryobiology 1995; 32: 78-91. 16. Van Soom A, Tanghe S, De Pauw I, Maes D, de Kruif A. Function of the cumulus oophorus before and during mammalian fertilization. Reprod Domest Anim 2002; 37: 144-151. 9. Fuku E, Kojima T, Shioya Y, Marcus GJ, Downey BR. In vitro fertilization and development of frozen-thawed bovine oocytes. Cryobiology 1992; 29: 485-492. 12. Endoh K, Mochida K, Ogonuki N, Ohkawa M, Shinmen A, Ito M, Kashiwazaki N, Ogura A. The developmental ability of vitrified oocytes from different mouse strains assessed by parthenogenetic activation and intracytoplasmic sperm injection. J Reprod Dev 2007; 53: 1199-1206. 4. Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes. Theriogenology 2007; 67: 73-80. 25. Toyoda Y, Yokoyama M, Hosi T. Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn J Anim Reprod 1972; 16: 147-151. 32. Dinnyés A, Dai Y, Jiang S, Yang X. High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer. Biol Reprod 2000; 63: 513-518. 17. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 2002; 61: 414-424. 31. Martino A, Pollard JW, Leibo SP. Effect of chilling bovine oocytes on their developmental competence. Mol Reprod Dev 1996; 45: 503-512. 3. Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at -196 degrees C by vitrification. Nature 1985; 313: 573-575. 1. Mazur P, Leibo SP, Seidel GE Jr Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions. Biol Reprod 2008; 78: 2-12. 15. Ito J, Yoshida T, Kasai Y, Wakai T, Parys JB, Fissore RA, Kashiwazaki N. Phosphorylation of inositol 1,4,5-triphosphate receptor 1 during in vitro maturation of porcine oocytes. Anim Sci J 2010; 81: 34-41. 19. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 2004; 131: 1577-1586. 22. Whittingham DG. Culture of mouse ova. J Reprod Fertil Suppl 1971; 7-21. 11. Park SE, Chung HM, Cha KY, Hwang WS, Lee ES, Lim JM. Cryopreservation of ICR mouse oocytes: improved post-thawed preimplantation development after vitrification using Taxol, a cytoskeleton stabilizer. Fertil Steril 2001; 75: 1177-1184. 8. al-Hasani S, Kirsch J, Diedrich K, Blanke S, van der Ven H, Krebs D. Successful embryo transfer of cryopreserved and in-vitro fertilized rabbit oocytes. Hum Reprod 1989; 4: 77-79. 34. Hochi S, Terao T, Kamei M, Kato M, Hirabayashi M, Hirao M. Successful vitrification of pronuclear-stage rabbit zygotes by minimum volume cooling procedure. Theriogenology 2004; 61: 267-275. 21. Tamba S, Yodoi R, Segi-Nishida E, Ichikawa A, Narumiya S, Sugimoto Y. Timely interaction between prostaglandin and chemokine signaling is a prerequisite for successful fertilization. Proc Nat Acad Sci USA 2008; 105: 14539-14544. 14. Larman MG, Sheehan CB, Gardner DK. Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 2006; 131: 53-61. 13. Eroglu A, Bailey SE, Toner M, Toth TL. Successful cryopreservation of mouse oocytes by using low concentrations of trehalose and dimethylsulfoxide. Biol Reprod 2009; 80: 70-78. 20. Shimada M, Yanai Y, Okazaki T, Noma N, Kawashima I, Mori T, Richards JS. Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 2008; 135: 2001-2011. 5. Parkening TA, Chang MC. Effects of cooling rates and maturity of the animal on the recovery and fertilization of frozen-thawed rodent eggs. Biol Reprod 1977; 17: 527-531. 28. Seita Y, Sugio S, Ito J, Kashiwazaki N. Generation of live rats produced by in vitro fertilization using cryopreserved spermatozoa. Biol Reprod 2009; 80: 503-510. 23. Seita Y, Okuda Y, Kato M, Kawakami Y, Inomata T, Ito J, Kashiwazaki N. Successful cryopreservation of rat pronuclear-stage embryos by rapid cooling. Cryobiology 2009; 59: 226-228. 29. Shaw JM, Kuleshova LL, MacFarlane DR, Trounson AO. Vitrification properties of solutions of ethylene glycol in saline containing PVP, Ficoll, or dextran. Cryobiology 1997; 35: 219-229. 10. Katayama KP, Stehlik J, Kuwayama M, Kato O, Stehlik E. High survival rate of vitrified human oocytes results in clinical pregnancy. Fertil Steril 2003; 80: 223-224. 18. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endoc 2002; 16: 1154-1167. 7. Chen C. Pregnancy after human oocyte cryopreservation. Lancet 1986; 1: 884-886. 27. Ho Y, Wigglesworth K, Eppig JJ, Schultz RM. Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol Reprod Dev 1995; 41: 232-238. 24. Ito J, Kuramochi M, Inoue A, Yabe K, Fujiwara K, Sonoki S, Masaoka T, Kashiwazaki N. Cryotop facilitates high developmental ability of re-vitrified mouse embryos. J Reprod Engineering 2010; 13: 21-26. 6. Whittingham DG. Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at -196 degrees C. J Reprod Fertil 1977; 49: 89-94. 2. Zhou GB, Li N. Cryopreservation of porcine oocytes: recent advances. Mol Hum Reprod 2009; 15: 279-285. 26. Takeshima T, Nakagata N, Ogawa S. Cryopreservation of mouse spermatozoa. Jikken Dobutsu 1991; 40: 493-497(In Japanese). 33. Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology 2007; 67: 73-80. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: 22. Whittingham DG. Culture of mouse ova. J Reprod Fertil Suppl 1971; 7-21. – reference: 3. Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at -196 degrees C by vitrification. Nature 1985; 313: 573-575. – reference: 19. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 2004; 131: 1577-1586. – reference: 31. Martino A, Pollard JW, Leibo SP. Effect of chilling bovine oocytes on their developmental competence. Mol Reprod Dev 1996; 45: 503-512. – reference: 33. Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology 2007; 67: 73-80. – reference: 2. Zhou GB, Li N. Cryopreservation of porcine oocytes: recent advances. Mol Hum Reprod 2009; 15: 279-285. – reference: 10. Katayama KP, Stehlik J, Kuwayama M, Kato O, Stehlik E. High survival rate of vitrified human oocytes results in clinical pregnancy. Fertil Steril 2003; 80: 223-224. – reference: 24. Ito J, Kuramochi M, Inoue A, Yabe K, Fujiwara K, Sonoki S, Masaoka T, Kashiwazaki N. Cryotop facilitates high developmental ability of re-vitrified mouse embryos. J Reprod Engineering 2010; 13: 21-26. – reference: 32. Dinnyés A, Dai Y, Jiang S, Yang X. High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer. Biol Reprod 2000; 63: 513-518. – reference: 14. Larman MG, Sheehan CB, Gardner DK. Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes. Reproduction 2006; 131: 53-61. – reference: 29. Shaw JM, Kuleshova LL, MacFarlane DR, Trounson AO. Vitrification properties of solutions of ethylene glycol in saline containing PVP, Ficoll, or dextran. Cryobiology 1997; 35: 219-229. – reference: 1. Mazur P, Leibo SP, Seidel GE Jr Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions. Biol Reprod 2008; 78: 2-12. – reference: 12. Endoh K, Mochida K, Ogonuki N, Ohkawa M, Shinmen A, Ito M, Kashiwazaki N, Ogura A. The developmental ability of vitrified oocytes from different mouse strains assessed by parthenogenetic activation and intracytoplasmic sperm injection. J Reprod Dev 2007; 53: 1199-1206. – reference: 25. Toyoda Y, Yokoyama M, Hosi T. Studies on the fertilization of mouse eggs in vitro. I. In vitro fertilization of eggs by fresh epididymal sperm. Jpn J Anim Reprod 1972; 16: 147-151. – reference: 16. Van Soom A, Tanghe S, De Pauw I, Maes D, de Kruif A. Function of the cumulus oophorus before and during mammalian fertilization. Reprod Domest Anim 2002; 37: 144-151. – reference: 6. Whittingham DG. Fertilization in vitro and development to term of unfertilized mouse oocytes previously stored at -196 degrees C. J Reprod Fertil 1977; 49: 89-94. – reference: 34. Hochi S, Terao T, Kamei M, Kato M, Hirabayashi M, Hirao M. Successful vitrification of pronuclear-stage rabbit zygotes by minimum volume cooling procedure. Theriogenology 2004; 61: 267-275. – reference: 4. Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes. Theriogenology 2007; 67: 73-80. – reference: 27. Ho Y, Wigglesworth K, Eppig JJ, Schultz RM. Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol Reprod Dev 1995; 41: 232-238. – reference: 11. Park SE, Chung HM, Cha KY, Hwang WS, Lee ES, Lim JM. Cryopreservation of ICR mouse oocytes: improved post-thawed preimplantation development after vitrification using Taxol, a cytoskeleton stabilizer. Fertil Steril 2001; 75: 1177-1184. – reference: 23. Seita Y, Okuda Y, Kato M, Kawakami Y, Inomata T, Ito J, Kashiwazaki N. Successful cryopreservation of rat pronuclear-stage embryos by rapid cooling. Cryobiology 2009; 59: 226-228. – reference: 30. Songsasen N, Buckrell BC, Plante C, Leibo SP. In vitro and in vivo survival of cryopreserved sheep embryos. Cryobiology 1995; 32: 78-91. – reference: 8. al-Hasani S, Kirsch J, Diedrich K, Blanke S, van der Ven H, Krebs D. Successful embryo transfer of cryopreserved and in-vitro fertilized rabbit oocytes. Hum Reprod 1989; 4: 77-79. – reference: 9. Fuku E, Kojima T, Shioya Y, Marcus GJ, Downey BR. In vitro fertilization and development of frozen-thawed bovine oocytes. Cryobiology 1992; 29: 485-492. – reference: 5. Parkening TA, Chang MC. Effects of cooling rates and maturity of the animal on the recovery and fertilization of frozen-thawed rodent eggs. Biol Reprod 1977; 17: 527-531. – reference: 18. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endoc 2002; 16: 1154-1167. – reference: 21. Tamba S, Yodoi R, Segi-Nishida E, Ichikawa A, Narumiya S, Sugimoto Y. Timely interaction between prostaglandin and chemokine signaling is a prerequisite for successful fertilization. Proc Nat Acad Sci USA 2008; 105: 14539-14544. – reference: 17. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 2002; 61: 414-424. – reference: 13. Eroglu A, Bailey SE, Toner M, Toth TL. Successful cryopreservation of mouse oocytes by using low concentrations of trehalose and dimethylsulfoxide. Biol Reprod 2009; 80: 70-78. – reference: 7. Chen C. Pregnancy after human oocyte cryopreservation. Lancet 1986; 1: 884-886. – reference: 26. Takeshima T, Nakagata N, Ogawa S. Cryopreservation of mouse spermatozoa. Jikken Dobutsu 1991; 40: 493-497(In Japanese). – reference: 20. Shimada M, Yanai Y, Okazaki T, Noma N, Kawashima I, Mori T, Richards JS. Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 2008; 135: 2001-2011. – reference: 28. Seita Y, Sugio S, Ito J, Kashiwazaki N. Generation of live rats produced by in vitro fertilization using cryopreserved spermatozoa. Biol Reprod 2009; 80: 503-510. – reference: 15. Ito J, Yoshida T, Kasai Y, Wakai T, Parys JB, Fissore RA, Kashiwazaki N. Phosphorylation of inositol 1,4,5-triphosphate receptor 1 during in vitro maturation of porcine oocytes. 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| SubjectTerms | Animals Blastocyst - drug effects Calcium - pharmacology Cryopreservation - methods Cryoprotective Agents - pharmacology Cumulus Cells - drug effects Dimethyl Sulfoxide - pharmacology Ethylene Glycol - pharmacology Female In vitro fertilization Mice Mouse Oocyte Oocytes - cytology Oocytes - drug effects Oocytes - physiology Vitrification Vitrification - drug effects |
| Title | High Developmental Rates of Mouse Oocytes Cryopreserved by an Optimized Vitrification Protocol: The Effects of Cryoprotectants, Calcium and Cumulus Cells |
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