Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-19T04:47:11.770Z Has data issue: false hasContentIssue false

Assessment of three generations of mice derived by ICSI using freeze-dried sperm

Published online by Cambridge University Press:  01 August 2009

Ming-Wen Li
Affiliation:
Mouse Biology Program, School of Veterinary Medicine, University of California, Davis, California, USA. Center for Comparative Medicine, School of Veterinary Medicine, University of California, Davis, California, USA.
Brandon J. Willis
Affiliation:
Mouse Biology Program, School of Veterinary Medicine, University of California, Davis, California, USA.
Stephen M. Griffey
Affiliation:
Comparative Pathology Laboratory, School of Veterinary Medicine, University of California, Davis, California, USA.
Jimmy L. Spearow
Affiliation:
Section of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California, USA.
K. C. Kent Lloyd*
Affiliation:
Center for Comparative Medicine, School of Veterinary Medicine, University of California, Davis, California 95616, USA. Mouse Biology Program, School of Veterinary Medicine, University of California, Davis, California, USA. Center for Comparative Medicine, School of Veterinary Medicine, University of California, Davis, California, USA.
*
All correspondence to: K.C. Kent Lloyd, Center for Comparative Medicine, School of Veterinary Medicine, University of California, Davis, California 95616, USA. Tel: +1 530 752–6865. Fax: +1 530 752 7914. e-mail: kclloyd@ucdavis.edu

Summary

Although the derivation of mice by intracytoplasmic sperm injection (ICSI) using freeze-dried sperm has been demonstrated previously, a comprehensive analysis of their viability, health, and fertility has not. The purpose of the present study was to determine the extent to which ICSI using freeze-dried sperm stored at 4 °C for 1–2 months from mice on either an inbred (C57BL/6J) or hybrid (B6D2F1/J) genetic background results in genomic instability and/or phenotypic abnormality in mice and two generations of their progeny. Fertilization rates (number of 2-cells per injected oocytes) using ICSI of fresh and freeze-dried sperm were similar within and between mouse strains, although fewer freeze-dried sperm-derived embryos than fresh sperm-derived embryos developed to blastocysts in vitro (C57BL/6J and B6D2F1/J) and liveborn pups in vivo (B6D2F1/J only). Nevertheless, once born, mice derived by ICSI using freeze-dried sperm in both mouse strains were healthy and reproductively sound. No major differences in litter size, weaning rate, and sex ratio were noted in the two generations of progeny (F2 and F3) of ICSI-derived offspring using freeze-dried sperm compared with that in the natural mating (control) group. Further, there was no evidence that either ICSI or freeze drying induced genomic instability, as determined by microsatellite analysis of the derived mice and subsequent generations when compared with both parental genotypes, nor were there differences in the number or types of pathological changes in any of the three generations of progeny. We conclude that viable, healthy and genomically stable mice can be derived by ICSI using freeze-dried mouse sperm stored in the refrigerator for at least 2 months. Further, because freeze drying is a simpler and more economical technique compared with embryo and sperm cryopreservation, the results of this study justify additional research to continue to develop and enhance the technique for the preservation, storage, and sharing of genetically altered mice.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agarwal, A. (2007). Current and future perspectives on intracytoplasmic sperm injection: a critical commentary. Reprod. Biomed. Online 15, 719–27.Google Scholar
Ahmadi, A. & Ng, S.C. (1999). Fertilizing ability of DNA-damaged spermatozoa. J. Exp. Zool. 284, 696704.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Aitken, R.J. & De Iuliis, G.N. (2007). Origins and consequences of DNA damage in male germ cells. Reprod. Biomed. Online 14, 727–33.CrossRefGoogle ScholarPubMed
Barber, R.C. & Dubrova, Y.E. (2006). The offspring of irradiated parents, are they stable? Mut. Res. 598, 5060.CrossRefGoogle ScholarPubMed
Betts, D.H. & Madan, P. (2008). Permanent embryo arrest: molecular and cellular concepts. Mol. Hum. Reprod. 14, 445–53.CrossRefGoogle ScholarPubMed
Bhowmick, S., Zhu, L., McGinnis, L., Lawitts, J., Nath, B.D., Mehmet, T. & Biggers, J.D. (2003). Desiccation tolerance of spermatozoa dried at ambient temperature: production of fetal mice. Biol. Reprod. 68, 1779–86.CrossRefGoogle ScholarPubMed
Biggers, J.D., McGinnis, L.K. & Raffin, M. (2000). Amino acids and preimplantation development of the mouse in protein-free potassium simplex optimized medium. Biol. Reprod. 63, 281–93.CrossRefGoogle ScholarPubMed
Boland, C.R., Thibodeau, S.N., Hamilton, S.R., Sidransky, D., Eshleman, J.R., Burt, R.W., Meltzer, S.J., Rodriguez-Bigas, M.A., Fodde, R., Ranzani, G.N. & Srivastava, S. (1998). A National Cancer Institute Workshop on microsatellite instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res. 58, 5248–57.Google ScholarPubMed
Caperton, L., Murphey, P., Yamazaki, Y., McMahan, C.A., Walter, C.A., Yanagimachi, R. & McCarrey, J.R. (2007). Assisted reproductive technologies do not alter mutation frequency or spectrum. PNAS 104, 5085–90.CrossRefGoogle ScholarPubMed
Chatot, C.L., Lewis, J.L., Torres, I. & Ziomek, C.A. (1990). Development of 1-cell embryos from different strains of mice in CZB medium. Biol. Reprod. 42, 432–40.CrossRefGoogle ScholarPubMed
Chatterjee, S. & Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing and thawing. Mol. Reprod. Dev. 59, 451–8.CrossRefGoogle ScholarPubMed
Clementini, E., Palka, C., Iezzi, I., Stuppia, L., Guanciali-Franchi, P. & Tiboni, G.M. (2005). Prevalence of chromosomal abnormalities in 2078 infertile couples referred for assisted reproductive techniques. Hum. Reprod. 20, 437–42.CrossRefGoogle ScholarPubMed
Critser, J.K. & Mobraaten, L.E. (2000). Cryopreservation of murine spermatozoa. ILAR J. 41, 197206.CrossRefGoogle ScholarPubMed
Derijck, A., Van Der Heijden, G., Giele, M., Philippens, M. & de Boer, P. (2008). DNA double strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum. Mol. Genet. 17, 1922–37.CrossRefGoogle ScholarPubMed
Ecker, D.J., Stein, P., Xu, Z., Williams, C.J., Kopf, G.S., Bilker, W.B., Abel, T. & Schultz, R.M. (2004). Long-term effects of culture of preimplantation mouse embryos on behavior. PNAS 101, 1595–600.CrossRefGoogle ScholarPubMed
Fatehi, A.N., Bevers, M.M., Schoevers, E., Roelen, B.A., Colenbrander, B. & Gadella, B.M. (2006). DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages. J. Androl. 27, 176–88.CrossRefGoogle Scholar
Fernández-Gonzalez, R., Moreira, P.N., Pérez-Crespo, M., Sánchez-Martín, M., Ramirez, M.A., Pericuesta, E., Bilbao, A., Bermejo-Alvarez, P., Hourcade Jde, D., Fonseca, F.R. & Gutiérrez-Adán, A. (2008). Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol. Reprod. 78, 761–72.CrossRefGoogle ScholarPubMed
Gafà, R., Maestri, I., Matteuzzi, M., Santini, A., Ferretti, S., Cavazzini, L. & Lanza, G. (2000). Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer 89, 2025–37.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
González-García, I., Moreno, V., Navarro, M., Martí-Ragué, J., Marcuello, E., Benasco, C., Campos, O., Capellà, G. & Peinado, M.A. (2000). Standardized approach for microsatellite instability detection in colorectal carcinomas. J. Natl. Cancer Inst. 92, 544–9.CrossRefGoogle ScholarPubMed
Hansen, M., Bower, C., Milne, E., de Klerk, N. & Kurinczuk, J.J. (2005). Assisted reproductive technologies and the risk of birth defects—a systematic review. Hum. Reprod. 20, 328–38.CrossRefGoogle ScholarPubMed
Harvey, A.J., Kind, K.L., Pantaleon, M., Armstrong, D.T. & Thompson, J.G. (2004). Oxygen-regulated gene expression in bovine blastocysts. Biol. Reprod. 71, 1108–19.CrossRefGoogle ScholarPubMed
Harvey, A.J., Kind, K.L. & Thompson, J.G. (2007). Regulation of gene expression in bovine blastocysts in response to oxygen and the iron chelator desferrioxamine. Biol. Reprod. 77, 93101.CrossRefGoogle ScholarPubMed
Hirabayashi, M., Kato, M., Ito, J. & Hochi, S. (2005). Viable rat offspring derived from oocytes intracytoplasmically injected with freeze-dried sperm heads. Zygote 13, 7985.CrossRefGoogle ScholarPubMed
Hochi, S., Watanabe, K., Kato, M. & Hirabayashi, M. (2008). Live rats resulting from injection of oocytes with spermatozoa freeze-dried and stored for one year. Mol. Reprod. Dev. 75, 890–4.CrossRefGoogle ScholarPubMed
Huntriss, J. & Picton, H.M. (2008). Epigenetic consequences of assisted reproduction and infertility on the human preimplantation embryo. Hum. Fertil. (Camb.) 11, 8594.CrossRefGoogle ScholarPubMed
Islam, K.N. & Mendelson, C.R. (2006). Permissive effects of oxygen on cyclic AMP and interleukin-1 stimulation of surfactant protein A gene expression are mediated by epigenetic mechanisms. Mol. Cell Biol. 26, 2901–12.CrossRefGoogle ScholarPubMed
Kaneko, T. & Nakagata, N. (2005). Relation between storage temperature and fertilizing ability of freeze-dried mouse spermatozoa. Comp. Med. 55, 140–4.Google ScholarPubMed
Kaneko, T., Whittingham, D.G., Overstreet, J.W. & Yanagimachi, R. (2003). Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulfide status. Biol. Reprod. 69, 1859–62.CrossRefGoogle ScholarPubMed
Kawase, Y., Araya, H., Kamada, N., Jishage, K. & Suzuki, H. (2005). Possibility of long-term preservation of freeze-dried mouse spermatozoa. Biol. Reprod. 72, 568–73.CrossRefGoogle ScholarPubMed
Kawase, Y., Hani, T., Kamada, N., Jishage, K. & Suzuki, H. (2007). Effect of pressure at primary drying of freeze-drying mouse sperm reproduction ability and preservation potential. Reproduction 133, 841–6.CrossRefGoogle ScholarPubMed
Keskintepe, L., Pacholczyk, G., Machnicka, A., Norris, K., Curuk, M.A., Khan, I. & Brackett, B.G. (2002). Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol. Reprod. 67, 409–15.CrossRefGoogle ScholarPubMed
Kusakable, H., Szczygiel, M.A., Whittingham, D.G. & Yanagimach, R. (2001). Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. PNAS 98, 13501–6.CrossRefGoogle Scholar
Kusakabe, H., Yanagimachi, R. & Kamiguchi, Y. (2008). Mouse and human spermatozoa can be freeze-dried without damaging their chromosomes. Hum. Reprod. 23, 233–9.CrossRefGoogle ScholarPubMed
Kwon, I.K., Park, K.E. & Niwa, K. (2004). Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biol. Reprod. 71, 1430–6.CrossRefGoogle ScholarPubMed
Li, M.W. & Lloyd, K.C.K. (2006). Intracytoplasmic sperm injection (ICSI) in the mouse. In Principles and Practice: Mammalian and Avian Transgenesis – New Approaches, (eds Pease, S. & Lois, C.), pp. 2340. Berlin Heidelberg: Springer–Verlag.Google Scholar
Li, M.W., Meyers, S., Tollner, T.L. & Overstreet, J.W. (2007a). Damage to chromosomes and DNA of rhesus monkey sperm following cryopreservation. J. Androl. 28, 493501.CrossRefGoogle ScholarPubMed
Li, M.W., Biggers, J.D., Elmoazzen, H.Y., Toner, M. & Lloyd, K.C.K.. (2007b). Long term storage of mouse spermatozoa after evaporative drying. Reproduction 133, 919–29.CrossRefGoogle ScholarPubMed
Li, M.W., Biggers, J.D., Toner, M. & Lloyd, K.C.K.. (2007c). Phenotypic analysis of C57BL/6J and FVB/NJ mice generated using evaporatively dried sperm. Comp. Med. 7, 469–75.Google Scholar
Liu, C.H., Tsao, H.M., Cheng, T.C., Wu, H.M., Huang, C.C., Chen, C.I., Lin, D.P. & Lee, MS. (2004). DNA fragmentation, mitochondrial dysfunction and chromosomal aneuploidy in the spermatozoa of oligoasthenoteratozoospermic males. J. Assist. Reprod. Genet. 21, 119–26.CrossRefGoogle ScholarPubMed
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. & Yang, X. (2004). Freeze-dried sperm fertilization leads to full-term development in rabbits. Biol. Reprod. 70, 1776–81.CrossRefGoogle ScholarPubMed
Maione, B., Pittoggi, C., Achene, L., Lorenzini, R. & Spadafora, C. (1997). Activation of endogenous nucleases in mature sperm cells upon interaction with exogenous DNA. DNA Cell Biol. 16, 1087–97.CrossRefGoogle ScholarPubMed
Mansour, R. (1998). Intracytoplasmic sperm injection: a state of the art technique. Hum. Reprod. Update 4, 4356.CrossRefGoogle ScholarPubMed
Marchetti, F., Essers, J., Kanaar, R. & Wyrobek, A.J. (2007). Disruption of maternal DNA repair increases sperm-derived chromosomal aberrations. PNAS 104, 17725–9.CrossRefGoogle ScholarPubMed
Marschall, S. & Hrabé de Angelis, M. (1999). Cryopreservation of mouse spermatozoa: double your mouse space. Trends Genet. 15, 128–31.CrossRefGoogle ScholarPubMed
Martins, C.F., Báo, S.N., Dode, M.N., Correa, G.A. & Rumpf, R. (2007). Effects of freeze-drying on cytology, ultrastructure, DNA fragmentation, and fertilizing ability of bovine sperm. Theriogenology 67, 1307–15.CrossRefGoogle ScholarPubMed
Mazur, P., Leibo, S.P. & Seidel, G.E. (2008). Cryopreservation of the germplasm of animals used in biological and medical research: importance, impact, status, and future directions. Biol. Reprod. 78, 212.CrossRefGoogle ScholarPubMed
McGinnis, L., Zhu, L., Lawitts, J., Bhowmick, S., Mehmet, T. & Biggers, J.D. (2005). Mouse sperm desiccated and stored in trehalose medium without freezing. Biol. Reprod. 73, 627–33.CrossRefGoogle ScholarPubMed
Nakagata, N. (2000). Cryopreservation of mouse spermatozoa. Mamm. Genome 11, 572–6.CrossRefGoogle ScholarPubMed
Nakai, M., Kashiwazaki, N., Takizawa, A., Maedomari, N., Ozawa, M., Noguchi, J., Kaneko, H., Shino, M. & 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, 1524.CrossRefGoogle ScholarPubMed
Okuyama, M., Isogai, S., Saga, M., Hamada, H. & Ogawa, S. (1990). In vitro fertilization (IVF) and artificial insemination (AI) by cryopreserved spermatozoa in mouse. J. Fert. Implant (Tokyo) 7, 116–9.Google Scholar
Palermo, G., Joris, H., Devroey, P. & Van Steirteghem, A.C. (1992). Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340, 1718.CrossRefGoogle ScholarPubMed
Pang, M.G., Kim, Y.J., Lee, S.H., & Kim, C.K. (2005). The high incidence of meiotic errors increases with decreased sperm count in severe male factor infertilities. Hum. Reprod. 20, 1688–694.CrossRefGoogle ScholarPubMed
Pabst, T., Schwaller, J., Bellomo, M.J., Oestreicher, M., Mühlematter, D., Tichelli, A., Tobler, A. & Fey, M.F. (1996). Frequent clonal loss of heterozygosity but scarcity of microsatellite instability at chromosomal breakpoint cluster regions in adult leukemias. Blood 88, 1026–34.CrossRefGoogle ScholarPubMed
Pérez-Crespo, M., Moreira, P., Pintado, B. & Gutiérrez-Adán, A. (2008). Factors from damaged sperm affect its DNA integrity and its ability to promote embryo implantation in mice. J. Androl. 29, 4754.CrossRefGoogle ScholarPubMed
Peris, S.I., Morrier, A., Dufour, M. & Bailey, J.L. (2004). Cryopreservation of ram semen facilitates sperm DNA damage: relationship between sperm andrological parameters and the sperm chromatin structure assay. J. Androl. 25, 224–33.CrossRefGoogle ScholarPubMed
Seli, E., Gardner, D.K., Schoolcraft, W.B., Moffatt, O. & Sakkas, D. (2004). Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil. Steril. 82, 378–83.CrossRefGoogle ScholarPubMed
Silver, L.M. (1995). Mouse Genetics – Concepts and Applications, pp. 159–94. Oxford: Oxford University Press.Google Scholar
Sztein, J.M., Farley, J.S. & Mobraaten, L.E. (2000). In vitro fertilization with cryopreserved inbred mouse sperm. Biol. Reprod. 63, 1774–780.CrossRefGoogle ScholarPubMed
Tada, N., Sato, M., Yamonoi, J., Mizorgi, T., Kasai, K. & Ogawa, S. (1990). Cryopreservation of mouse spermatozoa in the presence of raffinose and glycerol. J. Reprod. Fertil. 89, 511–16.CrossRefGoogle ScholarPubMed
Tesarik, J., Greco, E. & Mendoza, C. (2004). Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum. Reprod. 19, 611–15.CrossRefGoogle Scholar
Twigg, J., Irvine, D.S., Houston, P., Fulton, N., Michael, L. & Aitken, R.J. (1998). Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol. Hum. Reprod. 4, 439–45.CrossRefGoogle ScholarPubMed
van Gent, D.C., Hoeijmakers, J.H. & Kanaar, R. (2001). Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2, 196206.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (1998). Development of normal nice from oocytes injected with freeze-dried spermatozoa. Nature Biotech. 16, 639–41.CrossRefGoogle Scholar
Ward, M.A., Kaneko, T., Kusakabe, H., Biggers, J.D., Whittingham, D.G. & Yanagimachi, R. (2003). Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection. Biol. Reprod. 69, 2100–8.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod. Biomed. Online 10, 247–88.CrossRefGoogle Scholar
Yildiz, C., Ottaviani, P., Law, N., Ayearst, R., Liu, L. & McKerlie, C. (2007). Effects of cryopreservation on sperm quality, nuclear DNA integrity, in vitro fertilization, and in vitro embryo development in the mouse. Reproduction 133, 585–95.CrossRefGoogle ScholarPubMed
Yokoyama, M., Akiba, H., Katsuki, M. & Nomura, T. (1990). Production of normal young following transfer of mouse embryos obtained by in vitro fertilization using cryopreserved spermatozoa. Exp. Anim. 39, 126–8.Google ScholarPubMed
Zorn, B., Vidmar, G. & Meden-Vrtovec, H. (2003). Seminal reactive oxygen species as predictors of fertilization, embryo quality and pregnancy rates after conventional in vitro fertilization and intracytoplasmic sperm injection. Int. J. Androl. 26, 279–85.CrossRefGoogle ScholarPubMed