Abstract
Assisted reproductive technology (ART) has been applied in various procedures as an effective breeding method in experimental, domestic, and wild animals, and for the treatment of human infertility. Micro-insemination techniques such as intracytoplasmic injection of spermatozoa and spermatids are now routinely used ART tools. With these techniques, even immotile and immature sperm cells can be employed as donors for producing the next generation. Gamete preservation, another ART tool, has contributed to reproductive regulation, worldwide transportation, and disease protection of animal strains, and the preserved gametes have been effectively used for the production of offspring. ART is now an indispensable tool in mammalian reproduction. This review covers the latest ART tools, with a particular emphasis on micro-insemination and gamete preservation, and discusses the future direction of mammalian artificial reproductive technology.
Similar content being viewed by others
References
Steptoe PC, Edwards RG. Birth after the reimplantation of a human embryo. Lancet. 1978;2:366.
Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 1951;168:697–8.
Austin CR. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B. 1951;4:581–96.
Chang MC. Fertilization of rabbit ova in vitro. Nature. 1959;184:466–7.
Yanagimachi R, Chang MC. Fertilization of hamster eggs in vitro. Nature. 1963;200:281–2.
Iwamatsu T, Chang MC. In vitro fertilization of mouse eggs in the presence of bovine follicular fluid. Nature. 1969;224:919–20.
Miyamoto H, Chang MC. In vitro fertilization of rat eggs. Nature. 1973;241:50–2.
Toyoda Y, Chang MC. Fertilization of rat eggs in vitro by epididymal spermatozoa and the development of eggs following transfer. J Reprod Fertil. 1974;36:9–22.
Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology. 2006;65:1716–26.
Agca Y. Genome resource banking of biomedically important laboratory animals. Theriogenology. 2012;78:1653–65.
Nakagata N. Cryopreservation of mouse spermatozoa. Mamm Genome. 2000;11:572–6.
Landel CP. Archiving mouse strains by cryopreservation. Lab Anim NY. 2005;34:50–7.
Kaenko T, Yamamura A, Ide Y, Ogi M, Yanagita T, Nakagata N. Long-term cryopreservation of mouse sperm. Theriogenology. 2006;66:1098–101.
Critser JK, Mobraaten LE. Cryopreservation of murine spermatozoa. ILAR J. 2000;41:197–206.
Malter HE, Cohen J. Partial zona dissection of the human oocyte: a nontraumatic method using micromanipulation to assist zona pellucida penetration. Fertil Steril. 1989;51:139–48.
Nakagata N, Okamoto M, Ueda O, Suzuki H. Positive effect of partial zona-pellucida dissection on the in vitro fertilizing capacity of cryopreserved C57BL/6 J transgenic mouse spermatozoa of low motility. Biol Reprod. 1997;57:1050–5.
Kawase Y, Iwata T, Ueda O, Kamada N, Tachibe T, Aoki Y, Jishage K, Suzuki H. 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. 2002;66:381–5.
Kaneko T, Yanagi M, Nakashima T, Nakagata N. The improvement in fertilizing ability of cryopreserved mouse spermatozoa using laser-microdissected oocytes. Reprod Med Biol. 2006;5:249–53.
Anzai M, Nishiwaki M, Yanagi M, Nakashima T, Kaneko T, Taguchi Y, Tokoro M, Shin S, Mitani T, Kato H, Matsumoto K, Nakagata N, Iritani A. Application of laser-assisted zona drilling to in vitro fertilization of cryopreserved mouse oocytes with spermatozoa from a subfertile transgenic mouse. J Reprod Dev. 2006;52:601–6.
Kaneko T, Fukumoto K, Haruguchi Y, Kondo T, Machida H, Koga M, Nakagawa Y, Tsuchiyama S, Saiki K, Noshiba S, Nakagata N. Fertilization of C57BL/6 mouse sperm collected from cauda epididymides after preservation or transportation at 4 degrees C using laser-microdissected oocytes. Cryobiology. 2009;59:59–62.
Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod Biomed Online. 2005;10:247–88.
Goto K, Kinoshita A, Takuma Y, Ogawa K. Fertilisation of bovine oocytes by the injection of immobilised, killed spermatozoa. Vet Rec. 1990;127:517–20.
Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121:2397–405.
Uehara T, Yanagimachi R. Microsurgical injection of spermatozoa into hamster eggs with subsequent transformation of sperm nuclei into male pronuclei. Biol Reprod. 1976;15:467–70.
Uehara T, Yanagimachi R. Behavior of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs. Biol Reprod. 1977;16:315–21.
Kimura Y, Yanagimachi R. Intracytoplasmic sperm injection in the mouse. Biol Reprod. 1995;52:709–20.
Palermo G, Joris H, Devroey P, Van Steirteghem AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet. 1992;340:17–8.
Kawase Y, Iwata T, Toyoda Y, Wakayama T, Yanagimachi R, Suzuki H. Comparison of intracytoplasmic sperm injection for inbred and hybrid mice. Mol Reprod Dev. 2001;60:74–8.
Sakamoto W, Kaneko T, Nakagata N. Use of frozen-thawed oocytes for efficient production of normal offspring from cryopreserved mouse spermatozoa showing low fertility. Comp Med. 2005;55:136–9.
Kaneko T, Ohno R. Improvement in the development of oocytes from C57BL/6 mice after sperm injection. J Am Assoc Lab Anim Sci. 2011;50:33–6.
Miki H, Lee J, Inoue K, Ogonuki N, Noguchi Y, Mochida K, Kohda T, Nagashima H, Ishino F, Ogura A. Microinsemination with first-wave round spermatids from immature male mice. J Reprod Dev. 2004;50:131–7.
Ogonuki N, Inoue K, Hirose M, Miura I, Mochida K, Sato T, Mise N, Mekada K, Yoshiki A, Abe K, Kurihara H, Wakana S, Ogura A. A high-speed congenic strategy using first-wave male germ cells. PLoS One. 2009;4:e4943.
Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471:504–7.
Yokonishi T, Sato T, Komeya M, Katagiri K, Kubota Y, Nakabayashi K, Hata K, Inoue K, Ogonuki N, Ogura A, Ogawa T. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014;5:4320.
Kishikawa H, Tateno H, Yanagimachi R. Fertility of mouse spermatozoa retrieved from cadavers and maintained at 4 degrees C. J Reprod Fertil. 1999;116:217–22.
Ogonuki N, Mochida K, Miki H, Inoue K, Fray M, Iwaki T, Moriwaki K, Obata Y, Morozumi K, Yanagimachi R, Ogura A. Spermatozoa and spermatids retrieved from frozen reproductive organs or frozen whole bodies of male mice can produce normal offspring. Proc Natl Acad Sci USA. 2006;103:13098–103.
Van Thuan N, Wakayama S, Kishigami S, Wakayama T. New preservation method for mouse spermatozoa without freezing. Biol Reprod. 2005;72:444–50.
Wakayama T, Whittingham DG, Yanagimachi R. Production of normal offspring from mouse oocytes injected with spermatozoa cryopreserved with or without cryoprotection. J Reprod Fertil. 1998;112:11–7.
Ward MA, Kaneko T, Kusakabe H, Biggers JD, Whittingham DG, Yanagimachi R. Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection. Biol Reprod. 2003;69:2100–8.
Kaneko T, Kimura S, Nakagata N. Offspring derived from oocytes injected with rat sperm, frozen or freeze-dried without cryoprotection. Theriogenology. 2007;68:1017–21.
Wakayama T, Yanagimachi R. Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nat Biotechnol. 1998;16:639–41.
Kusakabe H, Szczygiel MA, Whittingham DG, Yanagimachi R. Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc Natl Acad Sci USA. 2001;98:13501–6.
Kaneko T, Whittingham DG, Yanagimachi R. Effect of pH value of freeze-drying solution on the chromosome integrity and developmental ability of mouse spermatozoa. Biol Reprod. 2003;68:136–9.
Kaneko T, Whittingham DG, Overstreet JW, Yanagimachi R. Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulfide status. Biol Reprod. 2003;69:1859–62.
Kaneko T, Nakagata N. Improvement in the long-term stability of freeze-dried mouse spermatozoa by adding of a chelating agent. Cryobiology. 2006;53:279–82.
Kaneko T, Kimura S, Nakagata N. Importance of primary culture conditions for the development of rat ICSI embryos and long-term preservation of freeze-dried sperm. Cryobiology. 2009;58:293–7.
Kaneko T, Nakagata N. Relation between storage temperature and fertilizing ability of freeze-dried mouse spermatozoa. Comp Med. 2005;55:140–4.
Kaneko T, Serikawa T. Successful long-term preservation of rat sperm by freeze-drying. PLoS One. 2012;7:e35043.
Kaneko T, Serikawa T. Long-term preservation of freeze-dried mouse spermatozoa. Cryobiology. 2012;64:211–4.
Li MW, Willis BJ, Griffey SM, Spearow JL, Lloyd KC. Assessment of three generations of mice derived by ICSI using freeze-dried sperm. Zygote. 2009;17:239–51.
Kaneko T. Mouse molecular embryology, methods and protocols, methods in molecular biology 1092. In: Lewandoski M, editor. The latest improvements in the mouse sperm preservation. New York: Springer; 2014. p. 357–65.
Bhowmick S, Zhu L, McGinnis L, Lawitts J, Nath BD, Toner M, Biggers J. Desiccation tolerance of spermatozoa dried at ambient temperature: production of fetal mice. Biol Reprod. 2003;68:1779–86.
Biggers JD. Evaporative drying of mouse spermatozoa. Reprod Biomed Online. 2009;19:4338.
Kaneko T. Chromosomal mutagenesis 2nd ed., methods in molecular biology 1239. In: Shondra M, editor. Simple sperm preservation by freeze-drying for conserving animal strains. Newyork: Springer; 2015. p. 317–29.
Leibo SP, Songsasen N. Cryopreservation of gametes and embryos of non-domestic species. Theriogenology. 2002;57:303–26.
Comizzoli P, Mermillod P, Mauget R. Reproductive biotechnologies for endangered mammalian species. Reprod Nutr Dev. 2000;40:493–504.
Liu JL, Kusakabe H, Chang CC, Suzuki H, Schmidt DW, Julian M, Pfeffer R, Bormann CL, Tian XC, Yanagimachi R, Yang X. Freeze-dried sperm fertilization leads to full-term development in rabbits. Biol Reprod. 2004;70:1776–81.
Muneto T, Horiuchi T. Full-term development of hamster embryos produced by injecting freeze-dried spermatozoa into oocytes. J Mamm Ova Res. 2011;28:32–9.
Kaneko T, Ito H, Sakamoto H, Onuma M, Inoue-Murayama M. Sperm preservation by freeze-drying for the conservation of wild animals. PLoS One. 2014;9:e113381.
Dickey RP, Lu PY, Sartor BM, Dunaway HE Jr, Pyrzak R, Klumpp AM. Steps taken to protect and rescue cryopreserved embryos during hurricane Katrina. Fertil Steril. 2006;86:732–4.
Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, 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 GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R. Knockout rats via embryo microinjection of zinc-finger nucleases. Science. 2009;325:433.
Tesson L, Usal C, Ménoret S, Leung E, Niles BJ, Remy S, Santiago Y, Vincent AI, Meng X, Zhang L, Gregory PD, Anegon I, Cost GJ. Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol. 2011;29:695–6.
Mashimo T, Kaneko T, Sakuma T, Kobayashi J, Kunihiro Y, Voigt B, Yamamoto T, Serikawa T. Efficient gene targeting by TAL effector nucleases coinjected with exonucleases in zygotes. Sci Rep. 2013;3:1253.
Sakuma T, Ochiai H, Kaneko T, Mashimo T, Tokumasu D, Sakane Y, Suzuki K, Miyamoto T, Sakamoto N, Matsuura S, Yamamoto T. Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci Rep. 2013;3:3379.
Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell. 2013;154:1370–9.
Yoshimi K, Kaneko T, Voigt B, Mashimo T. Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR-Cas platform. Nat Comm. 2014;5:4240.
Kaneko T, Mashimo T. Chromosomal mutagenesis 2nd ed., methods in molecular biology 1239. In: Shondra M, editor. Creating knockout and knockin rodents using engineered endonucleases via direct embryo injection. Newyork: Springer; 2015. p. 307–15.
Perry AC, Wakayama T, Kishikawa H, Kasai T, Okabe M, Toyoda Y, Yanagimachi R. Mammalian transgenesis by intracytoplasmic sperm injection. Science. 1999;284:1180–3.
Kaneko T, Moisyadi S, Suganuma R, Hohn B, Yanagimachi R, Pelczar P. Recombinase-mediated mouse transgenesis by intracytoplasmic sperm injection. Theriogenology. 2005;64:1704–15.
Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997;385:810–3.
Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 1998;394:369–74.
Kono T, Obata Y, Wu Q, Niwa K, Ono Y, Yamamoto Y, Park ES, Seo JS, Ogawa H. Birth of parthenogenetic mice that can develop to adulthood. Nature. 2004;428:860–4.
Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146:519–32.
Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338:971–5.
Hosoi Y, Miyake M, Utsumi K, Iritani A. In: Development of rabbit oocytes after microinjection of spermatozoa. Proceeding of the 11th international congress on animal reproduction. 1988. abstract 331.
Iritani A, Hosoi Y. Microfertilization by various methods in mammalian species. Prog Clin Biol Res. 1989;294:145–9.
Catt SL, Catt JW, Gomez MC, Maxwell WM, Evans G. Birth of a male lamb derived from an in vitro matured oocyte fertilised by intracytoplasmic injection of a single presumptive male sperm. Vet Rec. 1996;139:494–5.
Pope CE, Johnson CA, McRae MA, Keller GL, Dresser BL. Development of embryos produced by intracytoplasmic sperm injection of cat oocytes. Anim Reprod Sci. 1998;53:221–36.
Cochran R, Meintjes M, Reggio B, Hylan D, Carter J, Pinto C, Paccamonti D, Godke RA. Live foals produced from sperm-injected oocytes derived from pregnant mares. J Equine Vet Sci. 1998;18:736–40.
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, Schatten G. Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nat Med. 1999;5:431–3.
Martin MJ. Development of in vivo-matured porcine oocytes following intracytoplasmic sperm injection. Biol Reprod. 2000;63:109–12.
Miyata T, Okada H, Hashizume R, Ito M. The offspring of intracytoplasmic sperm injection in the rat. J Mamm Ova Res. 2000;17:S24.
Hirabayash M, Kato M, Aoto T, Sekimoto A, Ueda M, Miyoshi I, Kasai N, Hochi S. Offspring derived from intracytoplasmic injection of transgenic rat sperm. Transgenic Res. 2002;11:221–8.
Yamauchi Y, Yanagimachi R, Horiuchi T. Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection. Biol Reprod. 2002;67:534–9.
Wang B, Baldassarre H, Pierson J, Cote F, Rao KM, Karatzas CN. The in vitro and in vivo development of goat embryos produced by intracytoplasmic sperm injection using tail-cut spermatozoa. Zygote. 2003;11:219–27.
Choi YH, Varner DD, Love CC, Hartman DL, Hinrichs K. Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. Reproduction. 2011;142:529–38.
Keskintepe L, Pacholczyk G, Machnicka A, Norris K, Curuk MA, Khan I, Brackett BG. Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol Reprod. 2002;67:409–15.
Martins CF, Báo SN, Dode MN, Correa GA, Rumpf R. Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm. Theriogenology. 2007;67:1307–15.
Kwon IK, Park KE, Niwa K. Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biol Reprod. 2004;71:1430–6.
Sánchez-Partida LG, Simerly CR, Ramalho-Santos J. Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection. Fertil Steril. 2008;89:742–5.
Disclosures
Conflict of interest
The author declares no conflict of interest.
Human rights and informed consent
This article does not contain any studies with human subjects.
Animal studies
All institutional and national guidelines for the care and use of animals were followed.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Kaneko, T. Simple gamete preservation and artificial reproduction of mammals using micro-insemination techniques. Reprod Med Biol 14, 99–105 (2015). https://doi.org/10.1007/s12522-014-0202-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12522-014-0202-4