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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Production of inbred offspring by intracytoplasmic sperm injection of oocytes from juvenile female mice

Jie Zhu A , Wei Cui B and Yan-Feng Dai A C
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, The University of Inner Mongolia, University West Road, Huhehot, 010021, China.

B Institute of Reproductive and Developmental Biology, Faculty of Medicine, Imperial College London, W12 0NN, UK.

C Corresponding author. Email: daiyf@life.imu.edu.cn

Reproduction, Fertility and Development 30(3) 451-458 https://doi.org/10.1071/RD16399
Submitted: 6 October 2016  Accepted: 12 July 2017   Published: 25 August 2017

Abstract

The aim of the present study was to determine whether the use of oocytes from juvenile female mice would improve the efficiency of intracytoplasmic sperm injection (ICSI). In the present study, 15 adult and 14 juvenile C57BL6/J female mice were superovulated, with 17.8 oocytes per mouse harvested from adults, significantly lower than the 40.2 harvested from juveniles (P < 0.01). Sixty and 233 oocytes were harvested from C57BL/6J adult and juvenile mice respectively, activated in 10 mM SrCl2 + 5 μg mL−1 cytochalasin B for 5–6 h and cultured in potassium simplex optimisation medium (KSOM) for 3.5 days, with no differences in morula and blastocyst rates between groups (91.7% vs 96.6%; P > 0.05). Twelve hours after injection of human chorionic gonadotrophin, oocytes were harvested from C57BL/6J juvenile mice into KSOM, randomly divided into groups and activated with the same method mentioned above at 0, 2, 4 or 6 h and then cultured in KSOM for 3.5 days. There was no significant difference in morula and blastocyst rates among the different groups (P > 0.05). Oocytes from juvenile mice activated in 10 mM SrCl2 for 2 h were subjected to ICSI and the rates of pronuclear formation and Day 1 cleavage were significantly improved compared with the control group (P < 0.01). ICSI combined with activation of oocytes from inbred mouse strains (C57BL/6J, C57BL/6N and 129Svev) successfully produced pups. The fertility of some these mice resulting from ICSI was tested, and the animals proved fertile. In conclusion, superovulated juvenile mice can yield more useable oocytes than adult mice, but additional activation is essential for full development of ICSI oocytes harvested from juvenile inbred mice.

Additional keywords: human chorionic gonadotrophin, oocyte activation, pregnant mare’s serum gonadotropin, superovulation.


References

Ajduk, A., Tamauchi, Y., and Ward, M. A. (2006). Sperm chromatin remodelling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biol. Reprod. 75, 442–451.
Sperm chromatin remodelling after intracytoplasmic sperm injection differs from that of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWmuro%3D&md5=e828beacd2d5ce8141e1eca06117d25eCAS |

Armstrong, D. T. (2001). Effects of maternal age on oocyte 541 developmental competence. Theriogenology 55, 1303–1322.
Effects of maternal age on oocyte 541 developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSis78%3D&md5=008097b7bf4f49287a60b4a5873b57b4CAS |

Avendaño, C., and Oehninger, S. (2011). DNA fragmentation in morphological normal spermatozoa: how much should we be concerned in the ICSI era? J. Androl. 32, 356–363.
DNA fragmentation in morphological normal spermatozoa: how much should we be concerned in the ICSI era?Crossref | GoogleScholarGoogle Scholar |

Boni, R., Gualtieri, R., Talevi, R., and Tosti, E. (2007). Calcium and other ion dynamics during gamete maturation and fertilization. Theriogenology 68, S156–S164.
Calcium and other ion dynamics during gamete maturation and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitb4%3D&md5=26806fee0e098a3bee1ed6c983aec781CAS |

Cozzi, J., Monier-Gavelle, F., Lievre, N., and Bomsel, M. (2001). Mouse offspring after microinjection of heated spermatozoa. Biol. Reprod. 65, 1518–1521.
Mouse offspring after microinjection of heated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVersL4%3D&md5=475977f41e92e9e4ee2fa07b5936a162CAS |

de Waal, E., Yamazaki, Y., Ingale, P., Bartolomei, M. S., Yanagimachi, R., and McCarrey, J. R. (2012). Gonadotropin stimulation contributes to an increased incidence of epimutations in ICSI-derived mice. Hum. Mol. Genet. 21, 4460–4472.
Gonadotropin stimulation contributes to an increased incidence of epimutations in ICSI-derived mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVart7%2FI&md5=118429e2f3f407426b8562d3c79bed7cCAS |

Han, D., Cao, X. Y., Wang, H. L., Li, J. J., Wang, Y.-B., and Tan, J.-H. (2010). Effects of puberty and gonadotropins on the molecular events controlling meiotic resumption of mouse oocytes. Reproduction 139, 959–969.
Effects of puberty and gonadotropins on the molecular events controlling meiotic resumption of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns12qsLg%3D&md5=afd8273c124ce8fcc0c6d3ddcb78ded2CAS |

Heindryckx, B., Van der Elst, J., De Sutter, P., and Dhont, M. (2005). Treatment option for sperm- or oocyte-related fertilization failure: assisted oocyte activation following diagnostic heterologous ICSI. Hum. Reprod. 20, 2237–2241.
Treatment option for sperm- or oocyte-related fertilization failure: assisted oocyte activation following diagnostic heterologous ICSI.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mzms1CrtQ%3D%3D&md5=06ff184010a3d559ae2eea226d3f12fbCAS |

Jiménez-Macedo, A.-R., Anguita, B., Izquierdo, D., Mogas, T., and Paramio, M.-T. (2006). Embryo development of prepubertal goat oocytes fertilised by intracytoplasmic sperm injection (ICSI) according to oocyte diameter. Theriogenology 66, 1065–1072.
Embryo development of prepubertal goat oocytes fertilised by intracytoplasmic sperm injection (ICSI) according to oocyte diameter.Crossref | GoogleScholarGoogle Scholar |

Kaneko, T., and Ohno, R. (2011). Improvement in the development of oocytes from C57BL/6 mice after sperm injection. J. Am. Assoc. Lab. Anim. Sci. 50, 33–36.

Kawase, Y., Iwata, T., Toyoda, Y., Wakayama, T., Yanagimachi, R., and Suzuki, H. (2001). Comparison of intracytoplasmic sperm injection for inbred and hybrid mice. Mol. Reprod. Dev. 60, 74–78.
Comparison of intracytoplasmic sperm injection for inbred and hybrid mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFWis78%3D&md5=3058ac611d084420255fb4e2c813bd0aCAS |

Kimura, Y., and Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–720.
Intracytoplasmic sperm injection in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksFWhtrk%3D&md5=954a56a36620ef9edcde7395987afb87CAS |

Kuretake, S., Kimura, Y., Hoshi, K., and Yanagimachi, R. (1996). Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789–795.
Fertilization and development of mouse oocytes injected with isolated sperm heads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xls1Gkt7c%3D&md5=3c11ca4d89571ce3ff651acb45e9bf7cCAS |

Kusakabe, H., Szczygiel, M. A., Whittingham, D. G., and Yanagimachi, R. (2001). Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc. Natl Acad. Sci. USA 98, 13501–13506.
Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVynsrs%3D&md5=495802c9a06cd7ecdf0f4b6090c25874CAS |

Lacham-Kaplan, O., Shaw, J., Gabriel Sanchez-Partida, L., and Trounson, A. (2003). Oocyte activation after intracytoplasmic injection with sperm frozen without cryoprotectants results in live offspring from inbred and hybrid mouse strains. Biol. Reprod. 69, 1683–1689.
Oocyte activation after intracytoplasmic injection with sperm frozen without cryoprotectants results in live offspring from inbred and hybrid mouse strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosV2rs74%3D&md5=638f1de5f88f9b3c2d113935f9b706b4CAS |

Li, C., Mizutani, F., Ono, T., and Wakayama, T. (2010). An efficient method for generating transgenic mice using NaOH-treated spermatozoa. Biol. Reprod. 82, 331–340.
An efficient method for generating transgenic mice using NaOH-treated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSnsLY%3D&md5=51d3b2fae09ce44c772dbef89ce1fd39CAS |

Li, C., Mizutani, F., Ono, T., Terashita, Y., Jia, X.-F., Shi, H., and Wakayama, T. (2011). Intracytoplasmic sperm injection with mouse spermatozoa preserved without freezing for six months can lead to full term development. Biol. Reprod. 85, 1183–1190.
Intracytoplasmic sperm injection with mouse spermatozoa preserved without freezing for six months can lead to full term development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1ShsLbL&md5=f7afbe6fc74e812f8ea6da57560cc475CAS |

Liu, J., Lee, G. Y., Lawitts, J. A., Toner, M., and Biggers, J. D. (2014). Live pups from evaporatively dried mouse sperm stored at ambient temperature for up to years. PLoS One 9, e99809.
Live pups from evaporatively dried mouse sperm stored at ambient temperature for up to years.Crossref | GoogleScholarGoogle Scholar |

Luo, C., Zuniga, J., Ediso, E., Palla, S., Dong, W., and Parker-Thornburg, J. (2011). Superovulation strategies for 6 commonly used mouse strains. J. Am. Assoc. Lab. Anim. Sci. 50, 471–478.
| 1:CAS:528:DC%2BC3MXhtVCntLrN&md5=6020b35c268f625684f5cf8aa7b7cf32CAS |

Markoulaki, S., Meissner, A., and Jaenisch, R. (2008). Somatic cell nuclear transfer and derivation of embryonic stem cells in the mouse. Methods 45, 101–114.
Somatic cell nuclear transfer and derivation of embryonic stem cells in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVGit7c%3D&md5=4e3645806228bcc2e0db9559549e8e5aCAS |

Morozumi, K., Shikano, T., Miyazaki, S., and Yanagimachi, R. (2006). Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development. Proc. Natl Acad. Sci. USA 103, 17661–17666.
Simultaneous removal of sperm plasma membrane and acrosome before intracytoplasmic sperm injection improves oocyte activation/embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Klur7N&md5=fec810f36df26e6bc9e8bd01064a0e18CAS |

Morton, K. M. (2008). Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes. Reprod. Domest. Anim. 43, 137–143.
Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes.Crossref | GoogleScholarGoogle Scholar |

Nakagata, N. (2011) Cryopreservation of mouse spermatozoa and in vitro fertilization. In ‘Transgenic Mouse Methods and Protocols, Methods in Molecular Biology’. Vol. 693 (Eds M. H. Marten and J. M. van Deursen.) pp. 57–72. (Humana Press, Springer: New York.)

Nishizono, H., Shioda, M., Takeo, T., Irie, T., and Nakagata, N. (2004). Decrease of fertilizing ability of mouse spermatozoa after freezing and thawing is related to cellular injury. Biol. Reprod. 71, 973–978.
Decrease of fertilizing ability of mouse spermatozoa after freezing and thawing is related to cellular injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntFeju7k%3D&md5=ab27fb6f91e1915ab2a4b1d7e7581023CAS |

Ogonuki, N., Mochida, K., Miki, H., Inoue, K., Fray, M., Iwaki, T., Moriwaki, K., Obata, Y., Morozumi, K., Yanagimachi, R., and Ogura, A. (2006). Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring. Proc. Natl Acad. Sci. USA 103, 13098–13103.
Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xptlemu7g%3D&md5=ab4075046bbb57fe01756231c2ac4f32CAS |

Piotrowska-Nitsche, K., and Chan, A. W. S. (2013). Effect of sperm entry on blastocyst development after in vitro fertilization and intracytoplasmic sperm injection – mouse model. J. Assist. Reprod. Genet. 30, 81–89.
Effect of sperm entry on blastocyst development after in vitro fertilization and intracytoplasmic sperm injection – mouse model.Crossref | GoogleScholarGoogle Scholar |

Stein, P., and Schultz, R. M. (2010). ICSI in the mouse. Methods Enzymol. 476, 251–262.
ICSI in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Kis7nE&md5=3dff148189109c32a0b423a836cd8f15CAS |

Sugawara, A., and Ward, M. A. (2013). Biopsy of embryos produced by in vitro fertilization affects development in C57BL/6 mouse strain. Theriogenology 79, 234–241.
Biopsy of embryos produced by in vitro fertilization affects development in C57BL/6 mouse strain.Crossref | GoogleScholarGoogle Scholar |

Szczygiel, M. A., Kusakabe, H., Yanagimachi, R., and Whittingham, D. G. (2002a). Separation of motile populations of spermatozoa prior to freezing is beneficial for subsequent fertilization in vitro: a study with various mouse strains. Biol. Reprod. 67, 287–292.
Separation of motile populations of spermatozoa prior to freezing is beneficial for subsequent fertilization in vitro: a study with various mouse strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2iur4%3D&md5=3939551b449e2ed41742bc461b959d3fCAS |

Szczygiel, M. A., Kusakabe, H., Yanagimachi, R., and Whittingham, D. G. (2002b). Intracytoplasmic sperm injection is more efficient than in vitro fertilization for generating mouse embryos from cryopreserved spermatozoa. Biol. Reprod. 67, 1278–1284.
Intracytoplasmic sperm injection is more efficient than in vitro fertilization for generating mouse embryos from cryopreserved spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2rtLw%3D&md5=3aa3fb72a32493b95662424bb0c8da91CAS |

Wakayama, T., and Yanagimachi, R. (1998). Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nat. Biotechnol. 16, 639–641.
Development of normal mice from oocytes injected with freeze-dried spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkt1Gns7k%3D&md5=694b6d55edc2b2088d24aa31b92995efCAS |

Wakayama, T., Whittingham, D. G., and Yanagimachi, R. (1998). Production of normal offspring from mouse oocytes injected with spermatozoa cryopreserved with or without cryoprotection. J. Reprod. Fertil. 112, 11–17.
Production of normal offspring from mouse oocytes injected with spermatozoa cryopreserved with or without cryoprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqsbg%3D&md5=10fa8ed8a0eeae7107b916319e1a1982CAS |

Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in human and animals. Reprod. Biomed. Online 10, 247–288.
Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in human and animals.Crossref | GoogleScholarGoogle Scholar |

Yanagimachi, R., Wakayama, T., Kishikawa, H., Fimia, G. M., Monaco, L., and Sassone-Corsi, P. (2004). Production of fertile offspring from genetically infertile male mice. Proc. Natl Acad. Sci. USA 101, 1691–1695.
Production of fertile offspring from genetically infertile male mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFaqtL0%3D&md5=4f7abd36a9959f78d4a93995ac8d4fafCAS |

Yoshida, N., and Perry, A. C. F. (2007). Piezo-actuated mouse intracytoplasmic sperm injection (ICSI) Nat. Protoc. 2, 296–304.
Piezo-actuated mouse intracytoplasmic sperm injection (ICSI)Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGntbvM&md5=45cf46e72d2af04285e904e4b6b14232CAS |