Skip to main content
Journal of Assisted Reproduction and Genetics logoLink to Journal of Assisted Reproduction and Genetics
. 1999 Jul;16(6):315–324. doi: 10.1023/A:1020406016312

Bypassing Spermiogenesis for Several Generations Does Not Have Detrimental Consequences on the Fertility and Neurobehavior of Offspring: A Study Using the Mouse

Kellie L K Tamashiro 1, Yasuyuki Kimura 2, Robert J Blanchard 1,, D Caroline Blanchard 1, Ryuzo Yanagimachi 2
PMCID: PMC3455532  PMID: 10394528

Abstract

Purpose:This study was conducted to determine whether the omission of spermiogenesis and all prefertilization events for five generations in mice affects the fertility or behavior of offspring.

Methods:Fifth-generation hybrid (C57BL/6 × DBA/2) mice were produced using round spermatid injection (ROSI). Control groups consisted of mice born after natural mating with and without sham operation. The growth, fertility, and behavior of offspring were compared. Behavior tests conducted assessed elementary reasoning (Krushinsky test), emotionality (Mouse Defense Test Battery), and spatial learning and memory (Morris water maze).

Results:There were no significant differences in the growth and fertility of fifth-generation ROSI mice compared to natural fertilization mice. We also found no evidence of significant learning or behavioral deficits of the fifth-generation ROSI mice.

Conclusions:In this study, we found no evidence that bypassing the natural biological processes involved in spermiogenesis produces adverse effects on the growth, fertility, or behavior of mouse offspring.

Keywords: round spermatid injection, spermatid, mouse, behavior

Full Text

The Full Text of this article is available as a PDF (695.5 KB).

REFERENCES

  • 1.Palermo G, Joris H, Devroey P, Van Steirteghem AC. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet. 1992;340:17–18. doi: 10.1016/0140-6736(92)92425-f. [DOI] [PubMed] [Google Scholar]
  • 2.Van Steirteghem AC, Nagy Z, Joris H, Liu J, Staessen C, Smitz J, Wisanto A, Devroey P. High fertilization and implantation rates after intracytoplasmic sperm injection. Hum Reprod. 1993;8:1061–1066. doi: 10.1093/oxfordjournals.humrep.a138192. [DOI] [PubMed] [Google Scholar]
  • 3.Fishel S, Timson J, Lisi F, Jacobson M, Rinaldi L, Gobetz L. Micro-assisted fertilization in patients who have failed subzonal insemination. Hum Reprod. 1994;9:501–505. doi: 10.1093/oxfordjournals.humrep.a138535. [DOI] [PubMed] [Google Scholar]
  • 4.Silber SJ, Van Steirteghem A, Nagy Z, Liu J, Tournaye H, Devroey P. Normal pregnancies resulting form testicular sperm extraction and intracytoplasmic sperm injection for azoospermia due to maturation arrest [see Comments] Fertil Steril. 1996;66:110–117. doi: 10.1016/s0015-0282(16)58396-4. [DOI] [PubMed] [Google Scholar]
  • 5.Devroey P, Liu J, Nagy Z, Tournaye H, Silber SJ, Van Steirteghem AC. Normal fertilization of human oocytes after testicular sperm extraction and intracytoplasmic sperm injection. Fertil Steril. 1994;62:639–641. doi: 10.1016/s0015-0282(16)56958-1. [DOI] [PubMed] [Google Scholar]
  • 6.Tucker MJ, Wright G, Morton PC, Mayer MP, Ingargiola PE, Jones AE. Practical evolution and application of direct intracytoplasmic sperm injection for male factor and idiopathic fertilization failure infertilities. Fertil Steril. 1995;63:820–827. doi: 10.1016/s0015-0282(16)57488-3. [DOI] [PubMed] [Google Scholar]
  • 7.Nagy Z, Silber S, Liu J, Devroey P, Cecile J, Van Steirteghem A. Using ejaculated, fresh, and frozen-thawed epididymal and testicular spermatozoa gives rise to comparable results after intracytoplasmic sperm injection. Fertil Steril. 1995;63:808–815. doi: 10.1016/s0015-0282(16)57486-x. [DOI] [PubMed] [Google Scholar]
  • 8.Meschede D, De Geyter C, Nieschlag E, Horst J. Genetic risk in micromanipulative assisted reproduction. Hum Reprod. 1995;10:2880–2886. doi: 10.1093/oxfordjournals.humrep.a135812. [DOI] [PubMed] [Google Scholar]
  • 9.Bonduelle M, Wilikens A, Buysse A, Van Assche E, Wisanto A, Devroey P, Van Steirteghem AC, Liebaers I. Prospective follow-up study of 877 children born after intracytoplasmic sperm injection (ICSI), with ejaculated epididymal and testicular spermatozoa and after replacement of cryopreserved embryos obtained after ICSI. Hum Reprod. 1996;11:131–155. doi: 10.1093/humrep/11.suppl_4.131. [DOI] [PubMed] [Google Scholar]
  • 10.Wisanto A, Bonduelle M, Camus M, Tournaye H, Magnus M, Liebaers I, Van Steirteghem A, Devroey P. Obstetric outcome of 904 pregnancies after intracytoplasmic sperm injection. Hum Reprod. 1996;11:121–129. doi: 10.1093/humrep/11.suppl_4.121. [DOI] [PubMed] [Google Scholar]
  • 11.Ogura A, Matsuda J, Yanagimachi R. Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proc Natl Acad Sci USA. 1994;91:7460–7462. doi: 10.1073/pnas.91.16.7460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Kimura Y, Yanagimachi R. Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring. Development. 1995;121:2397–2405. doi: 10.1242/dev.121.8.2397. [DOI] [PubMed] [Google Scholar]
  • 13.Tesarik J, Mendoza C. Spermatid injection into human oocytes. I. Laboratory techniques and special features of zygote development. Hum Reprod. 1996;11:772–779. doi: 10.1093/oxfordjournals.humrep.a019253. [DOI] [PubMed] [Google Scholar]
  • 14.Tesarik J, Rolet F, Brami C, Sedbon E, Thorel J, Tibi C, Thebault A. Spermatid injection into human oocytes. II. Clinical application in the treatment of infertility due to nonobstructive azoospermia. Hum Reprod. 1996;11:780–783. doi: 10.1093/oxfordjournals.humrep.a019254. [DOI] [PubMed] [Google Scholar]
  • 15.Antinori S, Versaci C, Dani G, Antinori M, Pozza D, Selman HA. Fertilization with human testicular spermatids: Four successful pregnancies. Hum Reprod. 1997;12:286–291. doi: 10.1093/humrep/12.2.286. [DOI] [PubMed] [Google Scholar]
  • 16.Kahraman S, Polat G, Samli M, Sozen E, Ozgun OD, Dirican K, Ozbicer T. Multiple pregnancies obtained by testicular spermatid injection in combination with intracytoplasmic sperm injection. Hum Reprod. 1998;13:104–110. doi: 10.1093/humrep/13.1.104. [DOI] [PubMed] [Google Scholar]
  • 17.Kimura Y, Yanagimachi R. Development of normal mice from oocytes injected with secondary spermatocyte nuclei. Biol Reprod. 1995;53:855–862. doi: 10.1095/biolreprod53.4.855. [DOI] [PubMed] [Google Scholar]
  • 18.Kuretake S, Maleszewski M, Tokumasu A, Fujimoto H, Yanagimachi R. Inadequate function of sterile tw5/tw32 spermatozoa overcome by intracytoplasmic sperm injection. Mol Reprod Dev. 1996;44:230–233. doi: 10.1002/(SICI)1098-2795(199606)44:2<230::AID-MRD12>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  • 19.Sasagawa I, Yanagimachi R. Spermatids from mice after cryptorchid and reversal operations can initiate normal embryo development. J Androl. 1997;18:203–209. [PubMed] [Google Scholar]
  • 20.Cummins JM, Wakayama T, Yanagimachi R. Fate of microinjected sperm components in the mouse oocyte and embryo. Zygote. 1997;5:301–308. doi: 10.1017/s0967199400003889. [DOI] [PubMed] [Google Scholar]
  • 21.Suzuki K, Yanagida K, Yanagimachi R. Comparison of the media for isolation and storage of round spermatid nuclei before intracytoplasmic injection. J Assist Reprod Genet. 1998;15:154–158. doi: 10.1023/A:1023013022295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Poletaeva II, Popova NV, Romanova LG. Genetic aspects of animal reasoning. Behav Genet. 1993;23:467–475. doi: 10.1007/BF01067982. [DOI] [PubMed] [Google Scholar]
  • 23.Dulioust E, Toyama K, Busnel M, Moutier R, Carlier M, Marchaland C, Ducot B, Roubertoux P, Auroux M. Long-term effects of embryo freezing in mice. Proc Natl Acad Sci USA. 1995;92:589–593. doi: 10.1073/pnas.92.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Griebel G, Blanchard DC, Jung A, Masuda CK, Blanchard RJ. 5-HT1A agonists modulate mouse antipredator defensive behavior differentiy from the 5-HT2A antagonist pirenperone. Pharmacol Biochem Behav. 1995;51:235–244. doi: 10.1016/0091-3057(94)00360-u. [DOI] [PubMed] [Google Scholar]
  • 25.Griebel G, Blanchard DC, Agnes RS, Blanchard RJ. Differential modulation of antipredator defensive behavior in Swiss-Webster mice following acute or chronic administration of imipramine and fluoxetine. Psychopharmacology. 1995;120:57–66. doi: 10.1007/BF02246145. [DOI] [PubMed] [Google Scholar]
  • 26.Griebel G, Sanger DJ, Perrault G. Genetic differences in the mouse defense test battery. Aggress Behav. 1997;23:19–31. [Google Scholar]
  • 27.Lamberty Y, Gower AJ. Spatial processing and emotionality in aged NMRI mice: A multivariate analysis. Physiol Behav. 1993;54:339–343. doi: 10.1016/0031-9384(93)90120-5. [DOI] [PubMed] [Google Scholar]
  • 28.Stenvers KL, Lund PK, Gallagher M. Increased expression of type I insulin-like growth factor receptor messenger RNA in rat hippocampal formation is associated with aging and behavioral impairment. Neuroscience. 1996;72:505–510. doi: 10.1016/0306-4522(95)00524-2. [DOI] [PubMed] [Google Scholar]
  • 29.Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297:681–683. doi: 10.1038/297681a0. [DOI] [PubMed] [Google Scholar]
  • 30.Wehner JM, Sleight S, Upchurch M. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res. 1990;523:181–187. doi: 10.1016/0006-8993(90)91485-y. [DOI] [PubMed] [Google Scholar]
  • 31.Upchurch M, Wehner JM. Effects of chronic diisopropylfluorophosphate treatment on spatial learning in mice. Pharmacol Biochem Behav. 1987;27:143–151. doi: 10.1016/0091-3057(87)90488-6. [DOI] [PubMed] [Google Scholar]
  • 32.Watanabe C, Satoh H. Effects of prolonged selenium deficiency on open field behavior and Morris water maze performance in mice. Pharmacol Biochem Behav. 1995;51:747–752. doi: 10.1016/0091-3057(95)00025-r. [DOI] [PubMed] [Google Scholar]
  • 33.Gower AJ, Lamberty Y. The aged mouse as a model of cognitive decline with special emphasis on studies in NMRI mice. Behav Brain Res. 1993;57:163–173. doi: 10.1016/0166-4328(93)90132-a. [DOI] [PubMed] [Google Scholar]
  • 34.Gallagher M, Nicolle MM. Animal models of normal aging: relationship between cognitive decline and markers in hippocampal circuitry. Behav Brain Res. 1993;57:155–162. doi: 10.1016/0166-4328(93)90131-9. [DOI] [PubMed] [Google Scholar]
  • 35.Upchurch M, Wehner JM. Differences between inbred strains of mice in Morris water maze performance. Behav Genet. 1988;18:55–68. doi: 10.1007/BF01067075. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Assisted Reproduction and Genetics are provided here courtesy of Springer Science+Business Media, LLC

RESOURCES