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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Sperm capacitation combined with removal of the sperm acrosome and plasma membrane enhances paternal nucleus remodelling and early development of bovine androgenetic embryos

Yao Xiao A B , Hualin Zhang A , Sibtain Ahmad A C , Liya Bai A , Xiaomin Wang A , Lijun Huo A , Xin Zhang A , Wengong Li A , Xiang Li A and Liguo Yang A D
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, Huazhong Agricultural University, Wuhan, Hubei, 430070, PR China.

B Department of Animal Sciences, University of Arizona, Tucson, AZ 85721, USA.

C Department of Livestock Management, University of Agriculture, Faisalabad 38040, Pakistan.

D Corresponding author. Email: yangliguo2006@yahoo.com.cn

Reproduction, Fertility and Development 25(4) 624-638 https://doi.org/10.1071/RD12075
Submitted: 11 March 2012  Accepted: 17 May 2012   Published: 17 July 2012

Abstract

The androgenetic embryo is a useful model for functional analysis of the paternal genome during embryogenesis. However, few studies have focused on the factors involved in the suppressed developmental competence of such embryos or why sperm cloning-derived androgenetic embryos fail to develop beyond the morula stage in large domestic animals. To overcome this developmental failure, we tried to improve sperm decondensation, as well as to enhance embryonic development by sperm capacitation and removal of the acrosome and plasma membrane before injection of the spermatozoa. Before injection of the spermatozoa, we quantified the effects of sperm capacitation combined with sperm pretreatment on the acrosome and plasma membrane status. We also evaluated sperm decondensation potential, sperm viability and chromatin integrity. Immunostaining data showed that the sperm acrosome and plasma membrane could be more efficiently removed after capacitation. Dithiothreitol-induced sperm decondensation potential was improved with capacitation and removal of the acrosome and plasma membrane. Although most spermatozoa lost viability after pretreatment, their chromatin remained integrated. The patterns of paternal chromatin remodelling within uncleaved androgenetic embryos and the nucleus morphology of cleaved embryos indicated that capacitation combined with membrane disruption could make injected spermatozoa decondense synchronously not only with each other, but also with the developmental pace of the ooplasm. We successfully produced androgenetic blastocysts, and efficiency increased with sperm pretreatment. In conclusion, sperm decondensation and the early development of androgenetic embryos were enhanced with sperm capacitation and removal of the acrosome and plasma membrane prior to sperm injection.

Additional keywords: mammals, sperm decondensation, sperm pretreatment, uniparental development.


References

Aitken, R. J. (2011). The capacitation–apoptosis highway: oxysterols and mammalian sperm function. Biol. Reprod. 85, 9–12.
The capacitation–apoptosis highway: oxysterols and mammalian sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOlsro%3D&md5=27e4668c0da921d46e773a09eda5eb09CAS | 21490245PubMed |

Ajduk, A., Yamauchi, Y., and Ward, M. A. (2006). Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biol. Reprod. 75, 442–451.
Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWmuro%3D&md5=3d7e6df4e1d6be5e54c29fc5e05b9cfbCAS | 16775225PubMed |

Barton, S. C., Surani, M. A., and Norris, M. L. (1984). Role of paternal and maternal genomes in mouse development. Nature 311, 374–376.
Role of paternal and maternal genomes in mouse development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M%2Fht1Kkug%3D%3D&md5=ec065741888e7a2efc308a70dfdb515bCAS | 6482961PubMed |

Bedford, S. J., Kurokawa, M., Hinrichs, K., and Fissore, R. A. (2004). Patterns of intracellular calcium oscillations in horse oocytes fertilized by intracytoplasmic sperm injection: possible explanations for the low success of this assisted reproduction technique in the horse. Biol. Reprod. 70, 936–944.
Patterns of intracellular calcium oscillations in horse oocytes fertilized by intracytoplasmic sperm injection: possible explanations for the low success of this assisted reproduction technique in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1Sitbk%3D&md5=d9a1b886b260658eebda529e31c50da7CAS | 14656727PubMed |

Brouwers, J. F., Boerke, A., Silva, P. F., Garcia-Gil, N., van Gestel, R. A., Helms, J. B., van de Lest, C. H., and Gadella, B. M. (2011). Mass spectrometric detection of cholesterol oxidation in bovine sperm. Biol. Reprod. 85, 128–136.
Mass spectrometric detection of cholesterol oxidation in bovine sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOls7Y%3D&md5=5e6bad04a6be34c7a60fc193f8e19aaeCAS | 21415139PubMed |

Bui, H. T., Wakayama, S., Mizutani, E., Park, K. K., Kim, J. H., Van Thuan, N., and Wakayama, T. (2011). Essential role of paternal chromatin in the regulation of transcriptional activity during mouse preimplantation development. Reproduction 141, 67–77.
Essential role of paternal chromatin in the regulation of transcriptional activity during mouse preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7o%3D&md5=fc49dfc8afc619263b532f9db69d179aCAS | 20974742PubMed |

Carambula, S. F., Oliveira, L. J., and Hansen, P. J. (2009). Repression of induced apoptosis in the 2-cell bovine embryo involves DNA methylation and histone deacetylation. Biochem. Biophys. Res. Commun. 388, 418–421.
Repression of induced apoptosis in the 2-cell bovine embryo involves DNA methylation and histone deacetylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVOisrnK&md5=057d2cd7d8c8bb7d8be8f01f3b25c307CAS | 19665989PubMed |

Chamberland, A., Fournier, V., Tardif, S., Sirard, M. A., Sullivan, R., and Bailey, J. L. (2001). The effect of heparin on motility parameters and protein phosphorylation during bovine sperm capacitation. Theriogenology 55, 823–835.
The effect of heparin on motility parameters and protein phosphorylation during bovine sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1emur8%3D&md5=6d2301664bea79046396da3da7b37a28CAS | 11245268PubMed |

Chung, J. T., Keefer, C. L., and Downey, B. R. (2000). Activation of bovine oocytes following intracytoplasmic sperm injection (ICSI). Theriogenology 53, 1273–1284.
Activation of bovine oocytes following intracytoplasmic sperm injection (ICSI).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktVOmsb8%3D&md5=111cf1d0c0103ca91fd6b67dd8a0681eCAS | 10832752PubMed |

Davis, B. K. (1976). Influence of serum albumin on the fertilizing ability in vitro of rat spermatozoa. Proc. Soc. Exp. Biol. Med. 151, 240–243.
| 1:CAS:528:DyaE28XhtFKgu70%3D&md5=eb37a20cb0d7710eabc916efc14d74c5CAS | 1250865PubMed |

de Lamirande, E., Leclerc, P., and Gagnon, C. (1997). Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod. 3, 175–194.
Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjt1arsr0%3D&md5=8f102c8611b73663ec3d3805804fbc2bCAS | 9237244PubMed |

Fischer-Brown, A., Monson, R., Parrish, J., and Rutledge, J. (2002). Cell allocation in bovine embryos cultured in two media under two oxygen concentrations. Zygote 10, 341–348.
Cell allocation in bovine embryos cultured in two media under two oxygen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVSg&md5=a6b590bc2d47fc58232da42899fff75dCAS | 12463530PubMed |

Flesch, F. M., Voorhout, W. F., Colenbrander, B., van Golde, L. M., and Gadella, B. M. (1998). Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biol. Reprod. 59, 1530–1539.
Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVOgs78%3D&md5=dfa6b892744af2eb0fa7e715705ff842CAS | 9828202PubMed |

Galantino-Homer, H. L., Florman, H. M., Storey, B. T., Dobrinski, I., and Kopf, G. S. (2004). Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Mol. Reprod. Dev. 67, 487–500.
Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWnurk%3D&md5=680079ecd7e8dd16ed73f53abc4818adCAS | 14991741PubMed |

Galli, C., Vassiliev, I., Lagutina, I., Galli, A., and Lazzari, G. (2003). Bovine embryo development following ICSI: effect of activation, sperm capacitation and pre-treatment with dithiothreitol. Theriogenology 60, 1467–1480.
Bovine embryo development following ICSI: effect of activation, sperm capacitation and pre-treatment with dithiothreitol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns12kt7s%3D&md5=c8e9c9dd9354e6da497343f8485485cbCAS | 14519468PubMed |

Gao, G., Yi, J., Zhang, M., Xiong, J., Geng, L., Mu, C., and Yang, L. (2007). Effects of iron and copper in culture medium on bovine oocyte maturation, preimplantation embryo development, and apoptosis of blastocysts in vitro. J. Reprod. Dev. 53, 777–784.
Effects of iron and copper in culture medium on bovine oocyte maturation, preimplantation embryo development, and apoptosis of blastocysts in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGgsL7J&md5=29d645d29395783eb94dd5ab40c59426CAS | 17420621PubMed |

Garcia-Rosello, E., Matas, C., Canovas, S., Moreira, P. N., Gadea, J., and Coy, P. (2006). Influence of sperm pretreatment on the efficiency of intracytoplasmic sperm injection in pigs. J. Androl. 27, 268–275.
Influence of sperm pretreatment on the efficiency of intracytoplasmic sperm injection in pigs.Crossref | GoogleScholarGoogle Scholar | 16304206PubMed |

Horiuchi, T. (2006). Application study of intracytoplasmic sperm injection for golden hamster and cattle production. J. Reprod. Dev. 52, 13–21.
Application study of intracytoplasmic sperm injection for golden hamster and cattle production.Crossref | GoogleScholarGoogle Scholar | 16538031PubMed |

Jaiswal, B. S., Cohen-Dayag, A., Tur-Kaspa, I., and Eisenbach, M. (1998). Sperm capacitation is, after all, a prerequisite for both partial and complete acrosome reaction. FEBS Lett. 427, 309–313.
Sperm capacitation is, after all, a prerequisite for both partial and complete acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVKisLs%3D&md5=3e8b66e4bdab7c400731f443a12fea0dCAS | 9607335PubMed |

Jin, M., Fujiwara, E., Kakiuchi, Y., Okabe, M., Satouh, Y., Baba, S. A., Chiba, K., and Hirohashi, N. (2011). Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl Acad. Sci. USA 108, 4892–4896.
Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktValt7s%3D&md5=8a9ed79d4cf669976b2d0b87c0843fc7CAS | 21383182PubMed |

Katayama, M., Sutovsky, P., Yang, B. S., Cantley, T., Rieke, A., Farwell, R., Oko, R., and Day, B. N. (2005). Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs. Reproduction 130, 907–916.
Increased disruption of sperm plasma membrane at sperm immobilization promotes dissociation of perinuclear theca from sperm chromatin after intracytoplasmic sperm injection in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt12msw%3D%3D&md5=299027e515054f798eb0276cd1cc663eCAS | 16322550PubMed |

Katayose, H., Yanagida, K., Hashimoto, S., Yamada, H., and Sato, A. (2003). Use of diamide-acridine orange fluorescence staining to detect aberrant protamination of human-ejaculated sperm nuclei. Fertil. Steril. 79, 670–676.
Use of diamide-acridine orange fluorescence staining to detect aberrant protamination of human-ejaculated sperm nuclei.Crossref | GoogleScholarGoogle Scholar | 12620475PubMed |

Keskintepe, L., Pacholczyk, G., Machnicka, A., Norris, K., Curuk, M. A., Khan, I., and Brackett, B. G. (2002). Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol. Reprod. 67, 409–415.
Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFKqtro%3D&md5=4c00d32b270862102d934460779a6e6fCAS | 12135874PubMed |

Kim, K., Lerou, P., Yabuuchi, A., Lengerke, C., Ng, K., West, J., Kirby, A., Daly, M. J., and Daley, G. Q. (2007). Histocompatible embryonic stem cells by parthenogenesis. Science 315, 482–486.
Histocompatible embryonic stem cells by parthenogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotFCiuw%3D%3D&md5=7999ada725f48b2d6c6bd18a236fe0e8CAS | 17170255PubMed |

King, W. A. (1991). Embryo-mediated pregnancy failure in cattle. Can. Vet. J. 32, 99–103.
| 1:STN:280:DC%2BC3crpsV2gtw%3D%3D&md5=fae3ea49c1a10ce2626fdd48429738e9CAS | 17423747PubMed |

Lagutina, I., Lazzari, G., Duchi, R., and Galli, C. (2004). Developmental potential of bovine androgenetic and parthenogenetic embryos: a comparative study. Biol. Reprod. 70, 400–405.
Developmental potential of bovine androgenetic and parthenogenetic embryos: a comparative study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsl2jsg%3D%3D&md5=3e271d5f4d245a0319a8a582201c1d78CAS | 14561645PubMed |

Lessig, J., Glander, H. J., Schiller, J., Petkovic, M., Paasch, U., and Arnhold, J. (2006). Destabilization of the acrosome results in release of phospholipase A2 from human spermatozoa and subsequent formation of lysophospholipids. Andrologia 38, 69–75.
Destabilization of the acrosome results in release of phospholipase A2 from human spermatozoa and subsequent formation of lysophospholipids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFWnsLk%3D&md5=1df47e78a9c5c4f54680249cee09157eCAS | 16529578PubMed |

Li, C., Mizutani, E., Ono, T., and Wakayama, T. (2009). Production of normal mice from spermatozoa denatured with high alkali treatment before ICSI. Reproduction 137, 779–792.
Production of normal mice from spermatozoa denatured with high alkali treatment before ICSI.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgtLs%3D&md5=4a5f23c80762db302ed29f8ddbabb99bCAS | 19251742PubMed |

Li, C., Mizutani, E., 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=a472cfd8284f5cb9554f2397332aa832CAS | 19812303PubMed |

Long, C. R., Damiani, P., Pinto-Correia, C., MacLean, R. A., Duby, R. T., and Robl, J. M. (1994). Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization. J. Reprod. Fertil. 102, 361–369.
| 1:CAS:528:DyaK2MXjtFyns7w%3D&md5=578f5171a57736a58e65aea275893c1eCAS | 7861389PubMed |

Malcuit, C., Maserati, M., Takahashi, Y., Page, R., and Fissore, R. A. (2006). Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation. Reprod. Fertil. Dev. 18, 39–51.
Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlanu7vK&md5=8c270dd606ec44b307ae7894a129df47CAS | 16478601PubMed |

Markette, K. L., Seidel, G. E., and Elsden, R. P. (1985). Estimation of embryonic losses in bovine embryo transfer recipients from progesterone profiles and returns to estrus. Theriogenology 23, 45–62.
Estimation of embryonic losses in bovine embryo transfer recipients from progesterone profiles and returns to estrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1GktL0%3D&md5=f884af7c34260147f271424f13a4f686CAS |

McGrath, J., and Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–183.
Completion of mouse embryogenesis requires both the maternal and paternal genomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3gsFKguw%3D%3D&md5=595cbe4f8ffa74ce805a091f15539497CAS | 6722870PubMed |

Miki, H., Hirose, M., Ogonuki, N., Inoue, K., Kezuka, F., Honda, A., Mekada, K., Hanaki, K., Iwafune, H., Yoshiki, A., Ishino, F., and Ogura, A. (2009). Efficient production of androgenetic embryos by round spermatid injection. Genesis 47, 155–160.
Efficient production of androgenetic embryos by round spermatid injection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVWrt7o%3D&md5=94e6979d2957c15723b257f58c40bbfcCAS | 19241381PubMed |

Miranda, P. V., Allaire, A., Sosnik, J., and Visconti, P. E. (2009). Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm. Biol. Reprod. 80, 897–904.
Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVWqu70%3D&md5=0a1ff3204cf1ce8eafbff93c8987e18fCAS | 19144954PubMed |

Morozumi, K., and Yanagimachi, R. (2005). Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development. Proc. Natl Acad. Sci. USA 102, 14 209–14 214.
Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFChu7bJ&md5=32d463a3ddef4cc7d335774f9d2266b6CAS |

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, 17 661–17 666.
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=a3062ab03a6df28d1f79d4451505dabfCAS |

Nakai, M., Ito, J., Sato, K., Noguchi, J., Kaneko, H., Kashiwazaki, N., and Kikuchi, K. (2011). Pre-treatment of sperm reduces success of ICSI in the pig. Reproduction 142, 285–293.
Pre-treatment of sperm reduces success of ICSI in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2gs73N&md5=8876f7d30bcaeef23617edb3924fd8f4CAS | 21610169PubMed |

Ogawa, H., Shindo, N., Kumagai, T., Usami, Y., Shikanai, M., Jonwn, K., Fukuda, A., Kawahara, M., Sotomaru, Y., Tanaka, S., Arima, T., and Kono, T. (2009). Developmental ability of trophoblast stem cells in uniparental mouse embryos. Placenta 30, 448–456.
Developmental ability of trophoblast stem cells in uniparental mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFels74%3D&md5=e2d18a0dea6321311276568f07f4a092CAS | 19345411PubMed |

Oikawa, T., Takada, N., Kikuchi, T., Numabe, T., Takenaka, M., and Horiuchi, T. (2005). Evaluation of activation treatments for blastocyst production and birth of viable calves following bovine intracytoplasmic sperm injection. Anim. Reprod. Sci. 86, 187–194.
Evaluation of activation treatments for blastocyst production and birth of viable calves following bovine intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1CjtLc%3D&md5=beeba2335e0b27273ac8533abcd98128CAS | 15766799PubMed |

Parrish, J. J., Susko-Parrish, J., Winer, M. A., and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
Capacitation of bovine sperm by heparin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkslWit7g%3D&md5=f45cbc9d70f88613dedbf00729038d72CAS | 3408784PubMed |

Paula-Lopes, F. F., de Moraes, A. A., Edwards, J. L., Justice, J. E., and Hansen, P. J. (1998). Regulation of preimplantation development of bovine embryos by interleukin-1beta. Biol. Reprod. 59, 1406–1412.
Regulation of preimplantation development of bovine embryos by interleukin-1beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVKqu7c%3D&md5=03e60845286d1b6112e6b3d178372192CAS | 9828185PubMed |

Rho, G. J., Kawarsky, S., Johnson, W. H., Kochhar, K., and Betteridge, K. J. (1998a). Sperm and oocyte treatments to improve the formation of male and female pronuclei and subsequent development following intracytoplasmic sperm injection into bovine oocytes. Biol. Reprod. 59, 918–924.
Sperm and oocyte treatments to improve the formation of male and female pronuclei and subsequent development following intracytoplasmic sperm injection into bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVGrtr0%3D&md5=5df31616e2133d2a0d3d06e39f7cc7beCAS | 9746744PubMed |

Rho, G. J., Wu, B., Kawarsky, S., Leibo, S. P., and Betteridge, K. J. (1998b). Activation regimens to prepare bovine oocytes for intracytoplasmic sperm injection. Mol. Reprod. Dev. 50, 485–492.
Activation regimens to prepare bovine oocytes for intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlKrurk%3D&md5=4b4daaaac9b0f232286ab87596e207ccCAS | 9669532PubMed |

Roldan, E. R. (1998). Role of phospholipases during sperm acrosomal exocytosis. Front. Biosci. 3, D1109–D1119.
| 1:CAS:528:DyaK1cXntlKgu70%3D&md5=c201d8c3f27510f418c96602ba155852CAS | 9792902PubMed |

Roldan, E. R. (2006). Better intracytoplasmic sperm injection without sperm membranes and acrosome. Proc. Natl Acad. Sci. USA 103, 17 585–17 586.
Better intracytoplasmic sperm injection without sperm membranes and acrosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1KltbfL&md5=4b9bdcdebe5db9a6a89717ee94b4312cCAS |

Sathananthan, A. H., Szell, A., Ng, S. C., Kausche, A., Lacham-Kaplan, O., and Trounson, A. (1997). Is the acrosome reaction a prerequisite for sperm incorporation after intra-cytoplasmic sperm injection (ICSI)? Reprod. Fertil. Dev. 9, 703–709.
Is the acrosome reaction a prerequisite for sperm incorporation after intra-cytoplasmic sperm injection (ICSI)?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3osV2nug%3D%3D&md5=9b9e23e677409c890b593ead01b3dbd1CAS | 9623490PubMed |

Seita, Y., Ito, J., and Kashiwazaki, N. (2009). Removal of acrosomal membrane from sperm head improves development of rat zygotes derived from intracytoplasmic sperm injection. J. Reprod. Dev. 55, 475–479.
Removal of acrosomal membrane from sperm head improves development of rat zygotes derived from intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 19444004PubMed |

Shadan, S., James, P. S., Howes, E. A., and Jones, R. (2004). Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol. Reprod. 71, 253–265.
Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKku78%3D&md5=3dead901403e72cf6ae86c99d7c90bb0CAS | 15028630PubMed |

Shirazi, A., Derakhshan-Horeh, M., Pilvarian, A. A., Ahmadi, E., Nazari, H., and Heidari, B. (2011). Effect of pre-treatment of ovine sperm on male pronuclear formation and subsequent embryo development following intracytoplasmic sperm injection. Reprod. Domest. Anim. 46, 87–94.
Effect of pre-treatment of ovine sperm on male pronuclear formation and subsequent embryo development following intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itlyjsA%3D%3D&md5=cf7cf49507e73ca5f6578e21abcde4b4CAS | 20456664PubMed |

Surani, M. A., Barton, S. C., and Norris, M. L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548–550.
Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7mvVWltg%3D%3D&md5=0d12686af2148d15001f952edcdc9551CAS | 6709062PubMed |

Susko-Parrish, J. L., Leibfried-Rutledge, M. L., Northey, D. L., Schutzkus, V., and First, N. L. (1994). Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Dev. Biol. 166, 729–739.
Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVWkur4%3D&md5=3184afd79ca02137fa17e8c3a9de29c9CAS | 7813790PubMed |

Suzuki, J., Therrien, J., Filion, F., Lefebvre, R., Goff, A. K., Perecin, F., Meirelles, F. V., and Smith, L. C. (2011). Loss of methylation at H19 DMD is associated with biallelic expression and reduced development in cattle derived by somatic cell nuclear transfer. Biol. Reprod. 84, 947–956.
Loss of methylation at H19 DMD is associated with biallelic expression and reduced development in cattle derived by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGisrg%3D&md5=7ed1a9d1a2e2e4788f0e3c07ea6392b6CAS | 21248292PubMed |

Szczygiel, M. A., and Ward, W. S. (2002). Combination of dithiothreitol and detergent treatment of spermatozoa causes paternal chromosomal damage. Biol. Reprod. 67, 1532–1537.
Combination of dithiothreitol and detergent treatment of spermatozoa causes paternal chromosomal damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1Kjs7c%3D&md5=100f5e5ce6da6aa74bee0312f876cbecCAS | 12390885PubMed |

Tardif, S., Sirard, M. A., Sullivan, R., and Bailey, J. L. (1999). Identification of capacitation-associated phosphoproteins in porcine sperm electroporated with ATP-gamma-(32)P. Mol. Reprod. Dev. 54, 292–302.
Identification of capacitation-associated phosphoproteins in porcine sperm electroporated with ATP-gamma-(32)P.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsVCjt7s%3D&md5=915832327d42d573bac55f63dd5e2278CAS | 10497351PubMed |

Tejada, R. I., Mitchell, J. C., Norman, A., Marik, J. J., and Friedman, S. (1984). A test for the practical evaluation of male fertility by acridine orange (AO) fluorescence. Fertil. Steril. 42, 87–91.
| 1:STN:280:DyaL2c3gvV2quw%3D%3D&md5=c8358a71e9697ba9759d9f4cccc1c098CAS | 6724015PubMed |

Teramura, T., Onodera, Y., Murakami, H., Ito, S., Mihara, T., Takehara, T., Kato, H., Mitani, T., Anzai, M., Matsumoto, K., Saeki, K., Fukuda, K., Sagawa, N., and Hosoi, Y. (2009). Mouse androgenetic embryonic stem cells differentiated to multiple cell lineages in three embryonic germ layers in vitro. J. Reprod. Dev. 55, 283–292.
Mouse androgenetic embryonic stem cells differentiated to multiple cell lineages in three embryonic germ layers in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFehtbg%3D&md5=e1fde158f067540c91751677e69e1b23CAS | 19305126PubMed |

Therien, I., and Manjunath, P. (2003). Effect of progesterone on bovine sperm capacitation and acrosome reaction. Biol. Reprod. 69, 1408–1415.
Effect of progesterone on bovine sperm capacitation and acrosome reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2ntr4%3D&md5=580ca697d836620990ec335996a7eb97CAS | 12826580PubMed |

Tian, J. H., Wu, Z. H., Liu, L., Cai, Y., Zeng, S. M., Zhu, S. E., Liu, G. S., Li, Y., and Wu, C. X. (2006). Effects of oocyte activation and sperm preparation on the development of porcine embryos derived from in vitro-matured oocytes and intracytoplasmic sperm injection. Theriogenology 66, 439–448.
Effects of oocyte activation and sperm preparation on the development of porcine embryos derived from in vitro-matured oocytes and intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1Gktr0%3D&md5=d16ece879e1a4568217e25ddb2bcaeecCAS | 16426671PubMed |

Van Cleeff, J., Drost, M., and Thatcher, W. W. (1991). Effects of postinsemination progesterone supplementation on fertility and subsequent estrous responses of dairy heifers. Theriogenology 36, 795–807.
Effects of postinsemination progesterone supplementation on fertility and subsequent estrous responses of dairy heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XjsVOntw%3D%3D&md5=c64a20512944545042a077f4922372d2CAS | 16727048PubMed |

Vichera, G., Olivera, R., Sipowicz, P., Radrizzani, M., and Salamone, D. (2011). Sperm genome cloning used in biparental bovine embryo reconstruction. Reprod. Fertil. Dev. 23, 769–779.
| 21791178PubMed |

Visconti, P. E., Krapf, D., de la Vega-Beltran, J. L., Acevedo, J. J., and Darszon, A. (2011). Ion channels, phosphorylation and mammalian sperm capacitation. Asian J. Androl. 13, 395–405.
Ion channels, phosphorylation and mammalian sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFGrtrc%3D&md5=350479cb352f00b6dc43353c3ba0228bCAS | 21540868PubMed |

Ward, W. S., and Coffey, D. S. (1991). DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44, 569–574.
DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhvVamt7c%3D&md5=37b35cde2633dfaa30421d66cb19a478CAS | 2043729PubMed |

Ward, W. S., Partin, A. W., and Coffey, D. S. (1989). DNA loop domains in mammalian spermatozoa. Chromosoma 98, 153–159.
DNA loop domains in mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXmtFSltb8%3D&md5=4d698fabd3b0a05e84879fcfc159ee81CAS | 2582896PubMed |

Watanabe, H., and Fukui, Y. (2006). Effects of dithiothreitol and boar on pronuclear formation and embryonic development following intracytoplasmic sperm injection in pigs. Theriogenology 65, 528–539.
Effects of dithiothreitol and boar on pronuclear formation and embryonic development following intracytoplasmic sperm injection in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvFGruw%3D%3D&md5=6e1200cd76c2b8edd39a84c2398c55e4CAS | 16009412PubMed |

Watanabe, H., Suzuki, H., and Fukui, Y. (2010). Fertilizability, developmental competence, and chromosomal integrity of oocytes microinjected with pre-treated spermatozoa in mice. Reproduction 139, 513–521.
Fertilizability, developmental competence, and chromosomal integrity of oocytes microinjected with pre-treated spermatozoa in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtV2lsbw%3D&md5=0c61c97033942e3c9044fec0bd29ed3aCAS | 19955207PubMed |

Yan, W., Morozumi, K., Zhang, J., Ro, S., Park, C., and Yanagimachi, R. (2008). Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and microRNAs in the sperm nuclei. Biol. Reprod. 78, 896–902.
Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and microRNAs in the sperm nuclei.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltVOnsrk%3D&md5=103643c2ff0c279786908050f94904e0CAS | 18256326PubMed |

Yanagimachi, R. (1994). Mammalian fertilizaiton. In ‘The Physiology of Reproduction.’ 2nd edn. (Eds E. Knobil and J. D. Neill.) pp. 189–317. (Raven Press: New York.)

Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod. Biomed. Online 10, 247–288.
Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals.Crossref | GoogleScholarGoogle Scholar | 15823233PubMed |

Yanagimachi, R. (2011). Problems of sperm fertility: a reproductive biologist’s view. Syst. Biol. Reprod. Med. 57, 102–114.
Problems of sperm fertility: a reproductive biologist’s view.Crossref | GoogleScholarGoogle Scholar | 21208150PubMed |

Yang, H., Shi, L., Wang, B. A., Liang, D., Zhong, C., Liu, W., Nie, Y., Liu, J., Zhao, J., Gao, X., Xu, G. L., and Li, J. (2012). Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell 149, 605–617.
Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1KjsL4%3D&md5=25bb0fbd7315e1c7a2dcd3db28db6709CAS | 22541431PubMed |

Zhao, Q., Wang, J., Zhang, Y., Kou, Z., Liu, S., and Gao, S. (2010). Generation of histocompatible androgenetic embryonic stem cells using spermatogenic cells. Stem Cells 28, 229–239.
| 1:CAS:528:DC%2BC3cXktF2qtbg%3D&md5=d60d6e4a1321b9d1db750d61a1686eddCAS | 20020425PubMed |