Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH FRONT

Sperm freeze-drying and micro-insemination for biobanking and maintenance of genetic diversity in mammals

Takehito Kaneko
+ Author Affiliations
- Author Affiliations

Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho, Sakyo-ku, Kyoto 606-8501, Japan. Email: tkaneko@anim.med.kyoto-u.ac.jp

Reproduction, Fertility and Development 28(8) 1079-1087 https://doi.org/10.1071/RD15386
Submitted: 29 September 2015  Accepted: 12 December 2015   Published: 29 February 2016

Abstract

Breeding by natural mating is ideal for maintaining animal populations. However, the lack of breeding space resulting from an increased number of strains and the decline in fertility caused by inbreeding inhibits the reproduction of subsequent generations. Reproductive technologies, such as gamete preservation and artificial fertilisation, have been developed to overcome these problems. These approaches efficiently produce offspring of laboratory, domestic and wild animals, and can also be used to treat human infertility. Gamete preservation using sperm contributes to improvements in reproductive systems and enables the use of smaller breeding spaces. Although cryopreservation with liquid nitrogen has been used to preserve spermatozoa, freeze-drying without liquid nitrogen, a novel method, facilitates long-term storage of spermatozoa. This method has recently been applied to maintain animal strains. Micro-insemination techniques, such as intracytoplasmic sperm injection (ICSI), are exceptional for improving assisted reproduction. ICSI can be used to fertilise oocytes, even with immotile and immature spermatozoa that are unsuitable for AI and IVF. Reproductive technologies provide a substantial advantage for biobanking and maintaining the genetic diversity of laboratory, domestic and wild animals. This review covers the latest method of sperm freeze-drying and micro-insemination, and future possibilities for maintaining animal strains and populations.

Additional keywords: conservation of wild animals, gamete preservation, intracytoplasmic sperm injection, reproductive technologies.


References

Agca, Y. (2012). Genome resource banking of biomedically important laboratory animals. Theriogenology 78, 1653–1665.
Genome resource banking of biomedically important laboratory animals.CrossRef | 22981880PubMed |

Andrabi, S. M., and Maxwell, W. M. (2007). A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim. Reprod. Sci. 99, 223–243.
A review on reproductive biotechnologies for conservation of endangered mammalian species.CrossRef | 1:CAS:528:DC%2BD2sXjslGktbc%3D&md5=b0ebbf63bbe9b3c8e357a8d4f3210c6bCAS | 16919407PubMed |

Anzai, M., Nishiwaki, M., Yanagi, M., Nakashima, T., Kaneko, T., Taguchi, Y., Tokoro, M., Shin, S., Mitani, T., Kato, H., Matsumoto, K., Nakagata, N., and Iritani, A. (2006). Application of laser-assisted zona drilling to in vitro fertilization of cryopreserved mouse oocytes with spermatozoa from a subfertile transgenic mouse. J. Reprod. Dev. 52, 601–606.
Application of laser-assisted zona drilling to in vitro fertilization of cryopreserved mouse oocytes with spermatozoa from a subfertile transgenic mouse.CrossRef | 16807506PubMed |

Balhorn, R. (1982). A model for the structure of chromatin in mammalian sperm. J. Cell Biol. 93, 298–305.
A model for the structure of chromatin in mammalian sperm.CrossRef | 1:CAS:528:DyaL38XktVamsbo%3D&md5=7b29db708cd3af48963c28060ef5ddefCAS | 7096440PubMed |

Bath, M. L. (2010). Inhibition of in vitro fertilizing capacity of cryopreserved mouse sperm by factors released by damaged sperm, and stimulation by glutathione. PLoS One 5, e9387.
Inhibition of in vitro fertilizing capacity of cryopreserved mouse sperm by factors released by damaged sperm, and stimulation by glutathione.CrossRef | 20195370PubMed |

Bedford, J. M., and Calvin, H. I. (1974). The occurrence and possible functional significance of -S-S- crosslinks in sperm heads, with particular reference to eutherian mammals. J. Exp. Zool. 188, 137–155.
The occurrence and possible functional significance of -S-S- crosslinks in sperm heads, with particular reference to eutherian mammals.CrossRef | 1:CAS:528:DyaE2cXkt1ensbw%3D&md5=e3481801119ea049cc8ce4e032fd0dd8CAS | 4207651PubMed |

Benson, J. D., Woods, E. J., Walters, E. M., and Critser, J. K. (2012). The cryobiology of spermatozoa. Theriogenology 78, 1682–1699.
The cryobiology of spermatozoa.CrossRef | 1:CAS:528:DC%2BC38XhsFSlt7vK&md5=39cfaae0c7c0f9872d4c710534ac16e0CAS | 23062722PubMed |

Bhowmick, S., Zhu, L., McGinnis, L., Lawitts, J., Nath, B. D., Toner, M., and Biggers, J. (2003). Desiccation tolerance of spermatozoa dried at ambient temperature: production of fetal mice. Biol. Reprod. 68, 1779–1786.
Desiccation tolerance of spermatozoa dried at ambient temperature: production of fetal mice.CrossRef | 1:CAS:528:DC%2BD3sXjt12ltL8%3D&md5=fba1e25f53cf27a8849229fcd1aee307CAS | 12606475PubMed |

Bialy, G., and Smith, V. R. (1957). Freeze-drying of bovine spermatozoa. J. Dairy Sci. 40, 739–745.
Freeze-drying of bovine spermatozoa.CrossRef |

Biggers, J. D. (2009). Evaporative drying of mouse spermatozoa. Reprod. Biomed. Online 19, 115–124.
Evaporative drying of mouse spermatozoa.CrossRef |

Bratton, R. W., Foote, R. H., and Cruthers, J. C. (1955). Preliminary fertility results with frozen bovine spermatozoa. J. Dairy Sci. 38, 40–46.
Preliminary fertility results with frozen bovine spermatozoa.CrossRef |

Byers, S. L., Payson, S. J., and Taft, R. A. (2006). Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 65, 1716–1726.
Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs).CrossRef | 16271754PubMed |

Carbery, I. D., Ji, D., Harrington, A., Brown, V., Weinstein, E. J., Liaw, L., and Cui, X. (2010). Targeted genome modification in mice using zinc-finger nucleases. Genetics 186, 451–459.
Targeted genome modification in mice using zinc-finger nucleases.CrossRef | 1:CAS:528:DC%2BC3cXhsFOnt7rI&md5=c6611d7cca90286853a640ffa44b740bCAS | 20628038PubMed |

Catt, S. L., Catt, J. W., Gomez, M. C., Maxwell, W. M., and Evans, G. (1996). Birth of a male lamb derived from an in vitro matured oocyte fertilised by intracytoplasmic injection of a single presumptive male sperm. Vet. Rec. 139, 494–495.
Birth of a male lamb derived from an in vitro matured oocyte fertilised by intracytoplasmic injection of a single presumptive male sperm.CrossRef | 1:STN:280:DyaK2s7gvVajtA%3D%3D&md5=69a95e0232a727efbd6ef1cb40d31aeaCAS | 8950820PubMed |

Choi, Y. H., Varner, D. D., Love, C. C., Hartman, D. L., and Hinrichs, K. (2011). Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. Reproduction 142, 529–538.
Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse.CrossRef | 1:CAS:528:DC%2BC3MXhtlyitb%2FJ&md5=3b4d584e41d1a43d2182f8dbf70640b0CAS | 21846810PubMed |

Cochran, R., Meintjes, M., Reggio, B., Hylan, D., Carter, J., Pinto, C., Paccamonti, D., and Godke, R. A. (1998). Live foals produced from sperm-injected oocytes derived from pregnant mares. J. Equine Vet. Sci. 18, 736–740.
Live foals produced from sperm-injected oocytes derived from pregnant mares.CrossRef |

Comizzoli, P., Mermillod, P., and Mauget, R. (2000). Reproductive biotechnologies for endangered mammalian species. Reprod. Nutr. Dev. 40, 493–504.
Reproductive biotechnologies for endangered mammalian species.CrossRef | 1:CAS:528:DC%2BD3MXmvFShsA%3D%3D&md5=c611536703e418ef049e9bb710586526CAS | 11140819PubMed |

Dickey, R. P., Lu, P. Y., Sartor, B. M., Dunaway, H. E., Pyrzak, R., and Klumpp, A. M. (2006). Steps taken to protect and rescue cryopreserved embryos during Hurricane Katrina. Fertil. Steril. 86, 732–734.
Steps taken to protect and rescue cryopreserved embryos during Hurricane Katrina.CrossRef | 16828479PubMed |

Dozortsev, D., Wakaiama, T., Ermilov, A., and Yanagimachi, R. (1998). Intracytoplasmic sperm injection in the rat. Zygote 6, 143–147.
Intracytoplasmic sperm injection in the rat.CrossRef | 1:STN:280:DyaK1cvktlOiug%3D%3D&md5=06dd8807d8aad4b3858175e1c077dd75CAS | 9770779PubMed |

Fernandez-Gonzalez, L., Hribal, R., Stagegaard, J., Zahmel, J., and Jewgenow, K. (2015). Production of lion (Panthera leo) blastocysts after in vitro maturation of oocytes and intracytoplasmic sperm injection. Theriogenology 83, 995–999.
Production of lion (Panthera leo) blastocysts after in vitro maturation of oocytes and intracytoplasmic sperm injection.CrossRef | 25586639PubMed |

Geurts, A. M., Cost, G. J., Freyvert, Y., Zeitler, B., Miller, J. C., Choi, V. M., Jenkins, S. S., Wood, A., Cui, X., Meng, X., Vincent, A., Lam, S., Michalkiewicz, M., Schilling, R., Foeckler, J., Kalloway, S., Weiler, H., Ménoret, S., Anegon, I., Davis, G. D., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., Jacob, H. J., and Buelow, R. (2009). Knockout rats produced via embryo pronuclear microinjection of designed zinc finger nucleases. Science 325, 433.
Knockout rats produced via embryo pronuclear microinjection of designed zinc finger nucleases.CrossRef | 1:CAS:528:DC%2BD1MXovVChtrY%3D&md5=50ec324b2da01508979e08a47984569dCAS | 19628861PubMed |

Goto, K., Kinoshita, A., Takuma, Y., and Ogawa, K. (1990). Fertilisation of bovine oocytes by the injection of immobilised, killed spermatozoa. Vet. Rec. 127, 517–520.
| 1:STN:280:DyaK3M7is12nsg%3D%3D&md5=ee40696c9bea4dd6bd162ea723cb729aCAS | 2281585PubMed |

Henkel, R., Kierspel, E., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Schill, W. B., and Kruger, T. F. (2003). DNA fragmentation of spermatozoa and assisted reproduction technology. Reprod. Biomed. Online 7, 477–484.
DNA fragmentation of spermatozoa and assisted reproduction technology.CrossRef | 14656411PubMed |

Henkel, R., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Gips, H., Schill, W. B., and Kruger, T. F. (2004). Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil. Steril. 81, 965–972.
Influence of deoxyribonucleic acid damage on fertilization and pregnancy.CrossRef | 1:CAS:528:DC%2BD2MXitFCrtrY%3D&md5=cec0379199030d14bb903cb83eb78eb3CAS | 15066449PubMed |

Hewitson, L., Dominko, T., Takahashi, D., Martinovich, C., Ramalho-Santos, J., Sutovsky, P., Fanton, J., Jacob, D., Monteith, D., Neuringer, M., Battaglia, D., Simerly, C., and Schatten, G. (1999). Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nat. Med. 5, 431–433.
Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys.CrossRef | 1:CAS:528:DyaK1MXisFOlt7g%3D&md5=843b9d9dd7c1587c31fef762785a4225CAS | 10202934PubMed |

Hirabayashi, M., Kato, M., Aoto, T., Sekimoto, A., Ueda, M., Miyoshi, I., Kasai, N., and Hochi, S. (2002). Offspring derived from intracytoplasmic injection of transgenic rat sperm. Transgenic Res. 11, 221–228.
Offspring derived from intracytoplasmic injection of transgenic rat sperm.CrossRef | 1:CAS:528:DC%2BD38Xkt1SqtLY%3D&md5=7ca03ce5ed860c8b906c0a7dbb07fff2CAS |

Hirabayashi, M., Kato, M., Ito, J., and Hochi, S. (2005). Viable rat offspring derived from oocytes intracytoplasmically injected with freeze-dried sperm heads. Zygote 13, 79–85.
Viable rat offspring derived from oocytes intracytoplasmically injected with freeze-dried sperm heads.CrossRef | 15984166PubMed |

Hochi, S., Watanabe, K., Kato, M., and Hirabayashi, M. (2008). Live rats resulting from injection of oocytes with spermatozoa freeze-dried and stored for one year. Mol. Reprod. Dev. 75, 890–894.
Live rats resulting from injection of oocytes with spermatozoa freeze-dried and stored for one year.CrossRef | 1:CAS:528:DC%2BD1cXktFGhtrk%3D&md5=7d6bdd5d36972ffe68f1993a5ebf3841CAS | 17926349PubMed |

Hosoi, Y., Miyake, M., Utsumi, K., and Iritani, A. (1988). Development of rabbit oocytes after microinjection of spermatozoa. In ‘Proceedings of the 11th International Congress on Animal Reproduction’, Abstract 331.

Iritani, A., and Hosoi, Y. (1989). Microfertilization by various methods in mammalian species. Prog. Clin. Biol. Res. 294, 145–149.
| 1:STN:280:DyaL1M3msVyqsA%3D%3D&md5=98f7d19eb79079dc02710c62362edc3fCAS | 2726959PubMed |

Kaneko, T. (2014). The latest improvements in the mouse sperm preservation. In ‘Methods in Molecular Biology 1092’. (Ed. M. Lewandoski.) pp. 357–365. (Springer: New York.)

Kaneko, T. (2015). Simple sperm preservation by freeze-drying for conserving animal strains. In ‘Methods in Molecular Biology 1239’. (Ed. M. Shondra.) pp. 317–329. (Springer: New York.)

Kaneko, T., and Mashimo, T. (2015a). Creating knockout and knockin rodents using engineered endonucleases via direct embryo injection. In ‘Methods in Molecular Biology 1239’. (Ed. M. Shondra.) pp. 307–315. (Springer: New York.)

Kaneko, T., and Mashimo, T. (2015b). Simple genome editing of rodent intact embryos by electroporation. PLoS One 10, e0142755.
Simple genome editing of rodent intact embryos by electroporation.CrossRef | 26556280PubMed |

Kaneko, T., and Nakagata, N. (2005). Relation between storage temperature and fertilizing ability of freeze-dried mouse spermatozoa. Comp. Med. 55, 140–144.
| 1:CAS:528:DC%2BD2MXhtFGju7%2FP&md5=8e3fd10cbe3cdf38c95f531db85e4b0cCAS | 15884775PubMed |

Kaneko, T., and Nakagata, N. (2006). Improvement in the long-term stability of freeze-dried mouse spermatozoa by adding of a chelating agent. Cryobiology 53, 279–282.
Improvement in the long-term stability of freeze-dried mouse spermatozoa by adding of a chelating agent.CrossRef | 1:CAS:528:DC%2BD28Xps1Omsbo%3D&md5=eefc564e4d2e6a075548b5fb837d9f4bCAS | 16870171PubMed |

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.
| 21333160PubMed |

Kaneko, T., and Serikawa, T. (2012a). Successful long-term preservation of rat sperm by freeze-drying. PLoS One 7, e35043.
Successful long-term preservation of rat sperm by freeze-drying.CrossRef | 1:CAS:528:DC%2BC38XlvV2isLc%3D&md5=b87edeb7dade6507076a6d387e336c6aCAS | 22496889PubMed |

Kaneko, T., and Serikawa, T. (2012b). Long-term preservation of freeze-dried mouse spermatozoa. Cryobiology 64, 211–214.
Long-term preservation of freeze-dried mouse spermatozoa.CrossRef | 1:CAS:528:DC%2BC38Xnt1Krurs%3D&md5=3c64eabc933e239dd5a0c3e132ec3a78CAS | 22326411PubMed |

Kaneko, T., Whittingham, D. G., Overstreet, J. W., and Yanagimachi, R. (2003a). Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulfide status. Biol. Reprod. 69, 1859–1862.
Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulfide status.CrossRef | 1:CAS:528:DC%2BD3sXpsVCns7w%3D&md5=eec1af8e0c655cee3c821eb6771305a9CAS | 12904320PubMed |

Kaneko, T., Whittingham, D. G., and Yanagimachi, R. (2003b). Effect of pH value of freeze-drying solution on the chromosome integrity and developmental ability of mouse spermatozoa. Biol. Reprod. 68, 136–139.
Effect of pH value of freeze-drying solution on the chromosome integrity and developmental ability of mouse spermatozoa.CrossRef | 1:CAS:528:DC%2BD3sXjtV2l&md5=7a88132f94a35254fa61b2338845e8bfCAS | 12493705PubMed |

Kaneko, T., Yamamura, A., Ide, Y., Ogi, M., Yanagita, T., and Nakagata, N. (2006a). Long-term cryopreservation of mouse sperm. Theriogenology 66, 1098–1101.
Long-term cryopreservation of mouse sperm.CrossRef | 1:CAS:528:DC%2BD28XotleqsLs%3D&md5=4db0fd5fb937b0d03d0346d5e00bf379CAS | 16620934PubMed |

Kaneko, T., Yanagi, M., Nakashima, T., and Nakagata, N. (2006b). The improvement in fertilizing ability of cryopreserved mouse spermatozoa using laser-microdissected oocytes. Reprod. Med. Biol. 5, 249–253.
The improvement in fertilizing ability of cryopreserved mouse spermatozoa using laser-microdissected oocytes.CrossRef |

Kaneko, T., Kimura, S., and Nakagata, N. (2007). Offspring derived from oocytes injected with rat sperm, frozen or freeze-dried without cryoprotection. Theriogenology 68, 1017–1021.
Offspring derived from oocytes injected with rat sperm, frozen or freeze-dried without cryoprotection.CrossRef | 1:STN:280:DC%2BD2srmslKlsg%3D%3D&md5=beda2e27644c1113ec3bf0e92158a339CAS | 17804050PubMed |

Kaneko, T., Fukumoto, K., Haruguchi, Y., Kondo, T., Machida, H., Koga, M., Nakagawa, Y., Tsuchiyama, S., Saiki, K., Noshiba, S., and Nakagata, N. (2009a). Fertilization of C57BL/6 mouse sperm collected from cauda epididymides after preservation or transportation at 4 degrees C using laser-microdissected oocytes. Cryobiology 59, 59–62.
Fertilization of C57BL/6 mouse sperm collected from cauda epididymides after preservation or transportation at 4 degrees C using laser-microdissected oocytes.CrossRef | 19394323PubMed |

Kaneko, T., Kimura, S., and Nakagata, N. (2009b). Importance of primary culture conditions for the development of rat ICSI embryos and longterm preservation of freeze-dried sperm. Cryobiology 58, 293–297.
Importance of primary culture conditions for the development of rat ICSI embryos and longterm preservation of freeze-dried sperm.CrossRef | 1:CAS:528:DC%2BD1MXlslWgt7Y%3D&md5=2f1de79dbc5440204412e7a20c8948cdCAS | 19236858PubMed |

Kaneko, T., Ito, H., Sakamoto, H., Onuma, M., and Inoue-Murayama, M. (2014a). Sperm preservation by freeze-drying for the conservation of wild animals. PLoS One 9, e113381.
Sperm preservation by freeze-drying for the conservation of wild animals.CrossRef | 25409172PubMed |

Kaneko, T., Sakuma, T., Yamamoto, T., and Mashimo, T. (2014b). Simple knockout by electroporation of engineered endonucleases into intact rat embryos. Sci. Rep. 4, 6382.
Simple knockout by electroporation of engineered endonucleases into intact rat embryos.CrossRef | 1:CAS:528:DC%2BC2MXksVymsbc%3D&md5=4592a4f98e6ff8c7d2d364b011d3646dCAS | 25269785PubMed |

Katayose, H., Matsuda, J., and Yanagimachi, R. (1992). The ability of dehydrated hamster and human sperm nuclei to develop into pronuclei. Biol. Reprod. 47, 277–284.
The ability of dehydrated hamster and human sperm nuclei to develop into pronuclei.CrossRef | 1:STN:280:DyaK3s%2Fgtl2jsA%3D%3D&md5=f277b2ed29da53a255ae0c6f0af2d5a3CAS | 1391332PubMed |

Kawase, Y., Iwata, T., Ueda, O., Kamada, N., Tachibe, T., Aoki, Y., Jishage, K., and Suzuki, H. (2002). Effect of partial incision of the zona pellucida by piezo-micromanipulator for in vitro fertilization using frozen thawed mouse spermatozoa on the developmental rate of embryos transferred at the 2-cell stage. Biol. Reprod. 66, 381–385.
Effect of partial incision of the zona pellucida by piezo-micromanipulator for in vitro fertilization using frozen thawed mouse spermatozoa on the developmental rate of embryos transferred at the 2-cell stage.CrossRef | 1:CAS:528:DC%2BD38XotVSltQ%3D%3D&md5=ba0d2b26d6176f217edddf796d3f5070CAS | 11804952PubMed |

Kawase, Y., Araya, H., Kamada, N., Jishage, K., and Suzuki, H. (2005). Possibility of long-term preservation of freeze-dried mouse spermatozoa. Biol. Reprod. 72, 568–573.
Possibility of long-term preservation of freeze-dried mouse spermatozoa.CrossRef | 1:CAS:528:DC%2BD2MXhvVeis70%3D&md5=8304626160fa2e20fc2539055164716dCAS | 15525816PubMed |

Kawase, Y., Tachibe, T., Jishage, K., and Suzuki, H. (2007). Transportation of freeze-dried mouse spermatozoa under different preservation conditions. J. Reprod. Dev. 53, 1169–1174.
Transportation of freeze-dried mouse spermatozoa under different preservation conditions.CrossRef | 17693699PubMed |

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 | 1:CAS:528:DC%2BD38XlsFKqtro%3D&md5=f9d81f40f9b61fa24c5f4f8e18efe9fcCAS | 12135874PubMed |

Kimura, Y., and Yanagimachi, R. (1995a). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–720.
Intracytoplasmic sperm injection in the mouse.CrossRef | 1:CAS:528:DyaK2MXksFWhtrk%3D&md5=65a6bf0316e5451c119e6a7f3e0c00d8CAS | 7779992PubMed |

Kimura, Y., and Yanagimachi, R. (1995b). Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development 121, 2397–2405.
| 1:CAS:528:DyaK2MXnsFSgsrw%3D&md5=24554a93358c3c7b884ebf218406b5ecCAS | 7671805PubMed |

Kishikawa, H., Tateno, H., and Yanagimachi, R. (1999). Fertility of mouse spermatozoa retrieved from cadavers and maintained at 4 degrees C. J. Reprod. Fertil. 116, 217–222.
Fertility of mouse spermatozoa retrieved from cadavers and maintained at 4 degrees C.CrossRef | 1:CAS:528:DyaK1MXkslOltL8%3D&md5=201dfe81c161ec9e854377d86f5d5510CAS | 10615245PubMed |

Kosower, N. S., Katayose, H., and Yanagimachi, R. (1992). Thiol-disulfide status and acridine orange fluorescence of mammalian sperm nuclei. J. Androl. 13, 342–348.
| 1:STN:280:DyaK3s%2FhsFanuw%3D%3D&md5=f010dfe1cc12f5f7248aa104c6e2240bCAS | 1399837PubMed |

Kusakabe, H., and Tateno, H. (2011). Characterization of chromosomal damage accumulated in freeze-dried mouse spermatozoa preserved under ambient and heat stress conditions. Mutagenesis 26, 447–453.
Characterization of chromosomal damage accumulated in freeze-dried mouse spermatozoa preserved under ambient and heat stress conditions.CrossRef | 1:CAS:528:DC%2BC3MXlt1Gktrc%3D&md5=2924802281b4fab5a2ac45dbb51313b2CAS | 21367815PubMed |

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, 13 501–13 506.
Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa.CrossRef | 1:CAS:528:DC%2BD3MXovVynsrs%3D&md5=9e5bdd09401fad6f8bc08d9ed96eee41CAS |

Kwon, I. K., Park, K. E., and Niwa, K. (2004). Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biol. Reprod. 71, 1430–1436.
Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa.CrossRef | 1:CAS:528:DC%2BD2cXpt1yis7o%3D&md5=7f272c4c18addea44cf7ecc070a74a0bCAS | 15215192PubMed |

Lee, K. B., and Niwa, K. (2006). Fertilization and development in vitro of bovine oocytes following intracytoplasmic injection of heat-dried sperm heads. Biol. Reprod. 74, 146–152.
Fertilization and development in vitro of bovine oocytes following intracytoplasmic injection of heat-dried sperm heads.CrossRef | 1:CAS:528:DC%2BD2MXhtlCjsrbE&md5=7af8d17cb5500998070d312916811b15CAS | 16192399PubMed |

Lee, J. D., Kamiguchi, Y., and Yanagimachi, R. (1996). Analysis of chromosome constitution of human spermatozoa with normal and aberrant head morphologies after injection into mouse oocytes. Hum. Reprod. 11, 1942–1946.
Analysis of chromosome constitution of human spermatozoa with normal and aberrant head morphologies after injection into mouse oocytes.CrossRef | 1:STN:280:DyaK2s%2FnvFegtA%3D%3D&md5=27cddf05b57cb70ff9aea2a1dc2631e9CAS | 8921068PubMed |

Lee, K. B., Park, K. E., Kwon, I. K., Tripurani, S. K., Kim, K. J., Lee, J. H., Niwa, K., and Kim, M. K. (2013). Develop to term rat oocytes injected with heat-dried sperm heads. PLoS One 8, e78260.
Develop to term rat oocytes injected with heat-dried sperm heads.CrossRef | 1:CAS:528:DC%2BC3sXhslGisLzE&md5=00d4ed0712db39a6f5ebbb163b490df9CAS | 24223784PubMed |

Leibo, S. P., and Songsasen, N. (2002). Cryopreservation of gametes and embryos of nondomestic species. Theriogenology 57, 303–326.
Cryopreservation of gametes and embryos of nondomestic species.CrossRef | 1:CAS:528:DC%2BD38XktFyltw%3D%3D&md5=75b48019e72dd75551f38db0cfde7695CAS | 11775977PubMed |

Li, M. W., Willis, B. J., Griffey, S. M., Spearow, J. L., and Lloyd, K. C. (2009). Assessment of three generations of mice derived by ICSI using freeze-dried sperm. Zygote 17, 239–251.
Assessment of three generations of mice derived by ICSI using freeze-dried sperm.CrossRef | 19416557PubMed |

Li, D., Qiu, Z., Shao, Y., Chen, Y., Guan, Y., Liu, M., Li, Y., Gao, N., Wang, L., Lu, X., Zhao, Y., and Liu, M. (2013a). Heritable gene targeting in the mouse and rat using a CRISPR–Cas system. Nat. Biotechnol. 31, 681–683.
Heritable gene targeting in the mouse and rat using a CRISPR–Cas system.CrossRef | 1:CAS:528:DC%2BC3sXht1Cgt73K&md5=e112eac648b0686866a4e1728191ffa6CAS | 23929336PubMed |

Li, W., Teng, F., Li, T., and Zhou, Q. (2013b). Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR–Cas systems. Nat. Biotechnol. 31, 684–686.
Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR–Cas systems.CrossRef | 1:CAS:528:DC%2BC3sXht1CgsbfJ&md5=f9166c728bf424e21d54b6af8de8052cCAS | 23929337PubMed |

Liu, J. L., Kusakabe, H., Chang, C. C., Suzuki, H., Schmidt, D. W., Julian, M., Pfeffer, R., Bormann, C. L., Tian, X. C., Yanagimachi, R., and Yang, X. (2004). Freeze-dried sperm fertilization leads to full-term development in rabbits. Biol. Reprod. 70, 1776–1781.
Freeze-dried sperm fertilization leads to full-term development in rabbits.CrossRef | 1:CAS:528:DC%2BD2cXktlOmt7Y%3D&md5=8cf361c42ca0a754b96245953a463824CAS | 14960482PubMed |

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 2 years. PLoS One 9, e99809.
Live pups from evaporatively dried mouse sperm stored at ambient temperature for up to 2 years.CrossRef | 24924588PubMed |

Malter, H. E., and Cohen, J. (1989). Partial zona dissection of the human oocyte: a nontraumatic method using micromanipulation to assist zona pellucida penetration. Fertil. Steril. 51, 139–148.
| 1:STN:280:DyaL1M%2FptFCltw%3D%3D&md5=0f3fc15aae2c57b70fff922b8898bb78CAS | 2910709PubMed |

Martin, M. J. (2000). Development of in vivo-matured porcine oocytes following intracytoplasmic sperm injection. Biol. Reprod. 63, 109–112.
Development of in vivo-matured porcine oocytes following intracytoplasmic sperm injection.CrossRef | 1:CAS:528:DC%2BD3cXktl2rs74%3D&md5=78bf27b1f32d39b9c44a3e59d6182756CAS | 10859248PubMed |

Martins, C. F., Báo, S. N., Dode, M. N., Correa, G. A., and Rumpf, R. (2007). Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm. Theriogenology 67, 1307–1315.
Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm.CrossRef | 1:CAS:528:DC%2BD2sXksVOms7s%3D&md5=d6f07e4fa96e49e5aeb4b9eb0a80c15fCAS | 17383718PubMed |

Marushige, Y., and Marushige, K. (1975). Transformation of sperm histone during formation and maturation of rat spermatozoa. J. Biol. Chem. 250, 39–45.
| 1:CAS:528:DyaE2MXht1anu7o%3D&md5=edda69d40673628308aaf6247afc331fCAS | 1141210PubMed |

Meistrich, M. L., Reid, B. O., and Barcellona, W. J. (1976). Changes sperm culei during sperimogensis and epidymal maturation. Exp. Cell Res. 99, 72–78.
Changes sperm culei during sperimogensis and epidymal maturation.CrossRef | 1:CAS:528:DyaE28XktVejurk%3D&md5=c49fd91c829d48430a89304454c5a673CAS | 1261617PubMed |

Men, N. T., Kikuchi, K., Nakai, M., Fukuda, A., Tanihara, F., Noguchi, J., Kaneko, H., Linh, N. V., Nguyen, B. X., Nagai, T., and Tajima, A. (2013). Effect of trehalose on DNA integrity of freeze-dried boar sperm, fertilization, and embryo development after intracytoplasmic sperm injection. Theriogenology 80, 1033–1044.
Effect of trehalose on DNA integrity of freeze-dried boar sperm, fertilization, and embryo development after intracytoplasmic sperm injection.CrossRef | 1:CAS:528:DC%2BC3sXhsVKktLvN&md5=99e3a797d2118a0a302e10d7a5392958CAS | 24041826PubMed |

Miyata, T., Okada, H., Hashizume, R., and Ito, M. (2000). The offspring of intracytoplasmic sperm injection in the rat. J. Mamm. Ova Res. 17, S–24.

Moro, L. N., Sestelo, A. J., and Salamone, D. F. (2014). Evaluation of cheetah and leopard spermatozoa developmental capability after interspecific ICSI with domestic cat oocytes. Reprod. Domest. Anim. 49, 693–700.
Evaluation of cheetah and leopard spermatozoa developmental capability after interspecific ICSI with domestic cat oocytes.CrossRef | 1:STN:280:DC%2BC2cfmslSrsg%3D%3D&md5=f105a3f169feb75e5d2c423d1834b028CAS | 24966115PubMed |

Muneto, T., and Horiuchi, T. (2011). Full-term development of hamster embryos produced by injecting freeze-dried spermatozoa into oocytes. J. Mamm. Ova Res. 28, 32–39.
Full-term development of hamster embryos produced by injecting freeze-dried spermatozoa into oocytes.CrossRef |

Nakai, M., Kashiwazaki, N., Takizawa, A., Maedomari, N., Ozawa, M., Noguchi, J., Kaneko, H., Shino, M., and Kikuchi, K. (2007). Effects of chelating agents during freeze-drying of boar spermatozoa on DNA fragmentation and on developmental ability in vitro and in vivo after intracytoplasmic sperm head injection. Zygote 15, 15–24.
Effects of chelating agents during freeze-drying of boar spermatozoa on DNA fragmentation and on developmental ability in vitro and in vivo after intracytoplasmic sperm head injection.CrossRef | 1:CAS:528:DC%2BD2sXhtVGis70%3D&md5=54d25abc0c4c941da5c7133bedde5b75CAS | 17391542PubMed |

Nei, T., and Nagase, H. (1961). Attempts to freeze-dry bull spermatozoa. Low Temp. Sci. 19, 107–115.

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, 13 098–13 103.
Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring.CrossRef | 1:CAS:528:DC%2BD28Xptlemu7g%3D&md5=483a0e0a5f88ba2f1c7a802388c190b4CAS |

Ostermeier, G. C., Wiles, M. V., Farley, J. S., and Taft, R. A. (2008). Conserving, distributing and managing genetically modified mouse lines by sperm cryopreservation. PLoS One 3, e2792.
Conserving, distributing and managing genetically modified mouse lines by sperm cryopreservation.CrossRef | 18665210PubMed |

Palermo, G., Joris, H., Devroey, P., and Van Steirteghem, A. C. (1992). Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340, 17–18.
Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte.CrossRef | 1:STN:280:DyaK38zgtFWrsA%3D%3D&md5=bb73a02f6fe32bd6029666e1b1d2f241CAS | 1351601PubMed |

Polge, C., Smith, A. U., and Parkes, A. S. (1949). Revival of spermatozoa after vitrification and dehydration at low temperatures. Nature 164, 666.
Revival of spermatozoa after vitrification and dehydration at low temperatures.CrossRef | 1:STN:280:DyaH1M%2FksV2gtQ%3D%3D&md5=3800b12b613a49c9520c06977928f00bCAS | 18143360PubMed |

Pope, C. E., Johnson, C. A., McRae, M. A., Keller, G. L., and Dresser, B. L. (1998). Development of embryos produced by intracytoplasmic sperm injection of cat oocytes. Anim. Reprod. Sci. 53, 221–236.
Development of embryos produced by intracytoplasmic sperm injection of cat oocytes.CrossRef | 1:STN:280:DyaK1M%2FltFSnsA%3D%3D&md5=c805d759aaf0568e3e7fb99eb92caad2CAS | 9835378PubMed |

Proudfoot, C., Carlson, D. F., Huddart, R., Long, C. R., Pryor, J. H., King, T. J., Lillico, S. G., Mileham, A. J., McLaren, D. G., Whitelaw, C. B., and Fahrenkrug, S. C. (2015). Genome edited sheep and cattle. Transgenic Res. 24, 147–153.
Genome edited sheep and cattle.CrossRef | 1:CAS:528:DC%2BC2cXhsFSgsLrF&md5=f3d7aa43e5eeaa88e71227ee26a7f714CAS | 25204701PubMed |

Ringleb, J., Waurich, R., Wibbelt, G., Streich, W. J., and Jewgenow, K. (2011). Prolonged storage of epididymal spermatozoa does not affect their capacity to fertilise in vitro-matured domestic cat (Felis catus) oocytes when using ICSI. Reprod. Fertil. Dev. 23, 818–825.
Prolonged storage of epididymal spermatozoa does not affect their capacity to fertilise in vitro-matured domestic cat (Felis catus) oocytes when using ICSI.CrossRef | 1:STN:280:DC%2BC3MjhsVCrtg%3D%3D&md5=3e057844fce211b5472ebc90f96047f2CAS | 21791183PubMed |

Sakamoto, W., Kaneko, T., and Nakagata, N. (2005). Use of frozen–thawed oocytes for efficient production of normal offspring from cryopreserved mouse spermatozoa showing low fertility. Comp. Med. 55, 136–139.
| 1:CAS:528:DC%2BD2MXhtFGju7%2FO&md5=c736bb33445c8ee0f165fa6f9c4ba971CAS | 15884774PubMed |

Sakuma, T., Ochiai, H., Kaneko, T., Mashimo, T., Tokumasu, D., Sakane, Y., Suzuki, K., Miyamoto, T., Sakamoto, N., Matsuura, S., and Yamamoto, T. (2013). Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci. Rep. 3, 3379.
Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity.CrossRef | 24287550PubMed |

Sánchez-Partida, L. G., Simerly, C. R., and Ramalho-Santos, J. (2008). Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection. Fertil. Steril. 89, 742–745.
Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection.CrossRef | 17562332PubMed |

Sherman, J. K. (1954). Freezing and freeze-drying of human spermatozoa. Fertil. Steril. 5, 357–371.
| 1:STN:280:DyaG2c7gtlelsQ%3D%3D&md5=8a82cdb2fad6ed27c2f4b4d43db7cb35CAS | 13183190PubMed |

Singh, S. G., and Roy, D. J. (1967). Freeze-drying of bovine semen. Indian J. Vet. Sci. 37, 1–7.

Sung, Y. H., Baek, I. J., Kim, D. H., Jeon, J., Lee, J., Lee, K., Jeong, D., Kim, J. S., and Lee, H. W. (2013). Knockout mice created by TALEN-mediated gene targeting. Nat. Biotechnol. 31, 23–24.
Knockout mice created by TALEN-mediated gene targeting.CrossRef | 1:CAS:528:DC%2BC3sXltVCksg%3D%3D&md5=a0d1792b0ac7504ec97db221647c43f4CAS | 23302927PubMed |

Takenaka, M., Horiuchi, T., and Yanagimachi, R. (2007). Effects of light on development of mammalian zygotes. Proc. Natl Acad. Sci. USA 104, 14 289–14 293.
Effects of light on development of mammalian zygotes.CrossRef | 1:CAS:528:DC%2BD2sXhtVGhtLzF&md5=1f7e3f926dc840c143e67107b0810c57CAS |

Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B. J., Remy, S., Santiago, Y., Vincent, A. I., Meng, X., Zhang, L., Gregory, P. D., Anegon, I., and Cost, G. J. (2011). Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 29, 695–696.
Knockout rats generated by embryo microinjection of TALENs.CrossRef | 1:CAS:528:DC%2BC3MXpvVOlurY%3D&md5=59fc39760e2eb4855393b2b3dffa50c3CAS | 21822240PubMed |

Uehara, T., and Yanagimachi, R. (1976). Microsurgical injection of spermatozoa into hamster eggs with subsequent transformation of sperm nuclei into male pronuclei. Biol. Reprod. 15, 467–470.
Microsurgical injection of spermatozoa into hamster eggs with subsequent transformation of sperm nuclei into male pronuclei.CrossRef | 1:STN:280:DyaE2s%2Fit1ektA%3D%3D&md5=422dc0a5943922310bb469dc51778186CAS | 974199PubMed |

Uehara, T., and Yanagimachi, R. (1977). Behavior of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs. Biol. Reprod. 16, 315–321.
Behavior of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs.CrossRef | 1:STN:280:DyaE2s7jsFWltw%3D%3D&md5=178a2140d097b182ac36ff7f87573504CAS | 843559PubMed |

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 | 1:CAS:528:DyaK1cXkt1Gns7k%3D&md5=8b653df5e60277d5058c42ebe325c747CAS | 9661196PubMed |

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 | 1:CAS:528:DyaK1cXitVKqsbg%3D&md5=0d43f6bfcdbdd3576d6ae47f5be25335CAS | 9538325PubMed |

Wang, B., Baldassarre, H., Pierson, J., Cote, F., Rao, K. M., and Karatzas, C. N. (2003). The in vitro and in vivo development of goat embryos produced by intracytoplasmic sperm injection using tail-cut spermatozoa. Zygote 11, 219–227.
The in vitro and in vivo development of goat embryos produced by intracytoplasmic sperm injection using tail-cut spermatozoa.CrossRef | 14640186PubMed |

Ward, M. A., Kaneko, T., Kusakabe, H., Biggers, J. D., Whittingham, D. G., and Yanagimachi, R. (2003). Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection. Biol. Reprod. 69, 2100–2108.
Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection.CrossRef | 1:CAS:528:DC%2BD3sXpsVCntr0%3D&md5=e2d55685e5393f85839b933b7f19a979CAS | 12930716PubMed |

Watanabe, H., Asano, T., Abe, Y., Fukui, Y., and Suzuki, H. (2009). Pronuclear formation of freeze-dried canine spermatozoa microinjected into mouse oocytes. J. Assist. Reprod. Genet. 26, 531–536.
Pronuclear formation of freeze-dried canine spermatozoa microinjected into mouse oocytes.CrossRef | 19856094PubMed |

Watanabe, H., Suzuki, H., Tateno, H., and Fukui, Y. (2010). A novel method for detection of chromosomal integrity in cryopreserved livestock spermatozoa using artificially fused mouse oocytes. J. Assist. Reprod. Genet. 27, 581–588.
A novel method for detection of chromosomal integrity in cryopreserved livestock spermatozoa using artificially fused mouse oocytes.CrossRef | 20521093PubMed |

Yamauchi, Y., Yanagimachi, R., and Horiuchi, T. (2002). Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection. Biol. Reprod. 67, 534–539.
Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection.CrossRef | 1:CAS:528:DC%2BD38XlsFKqtLw%3D&md5=11b1248c63eef119e498aa17bb507b02CAS | 12135892PubMed |

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 | 15823233PubMed |

Yoshimi, K., Kaneko, T., Voigt, B., and Mashimo, T. (2014). Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR–Cas platform. Nat. Commun. 5, 4240.
Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR–Cas platform.CrossRef | 1:CAS:528:DC%2BC2cXhvF2murfI&md5=4f1d0d731b5a250c8b80917c3d868b96CAS | 24967838PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (4)