Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-27T21:18:34.204Z Has data issue: false hasContentIssue false
  • English
  • Français

Toxic effects of Hoechst staining and UV irradiation on preimplantation development of parthenogenetically activated mouse oocytes

Published online by Cambridge University Press:  12 July 2012

Karen Versieren ,
Björn Heindryckx ,
Chen Qian ,
Jan Gerris  and
Petra De Sutter
Karen Versieren*
Affiliation:
Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium.
Björn Heindryckx
Affiliation:
Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium.
Chen Qian
Affiliation:
Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium.
Jan Gerris
Affiliation:
Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium.
Petra De Sutter
Affiliation:
Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium.
*
All correspondence to: Karen Versieren. Department of Reproductive Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Ghent, Belgium. Tel: +32 9 332 4748. Fax: +32 9 332 4972. e-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

Parthenogenetic activation of oocytes is a helpful tool to obtain blastocysts, of which the inner cell mass may be used for derivation of embryonic stem cells. In order to improve activation and embryonic development after parthenogenesis, we tried to use sperm injection and subsequent removal of the sperm head to mimic the natural Ca2+ increases by release of the oocyte activating factor. Visualization of the sperm could be accomplished by Hoechst staining and ultraviolet (UV) light irradiation. To exclude negative effects of this treatment, we examined toxicity on activated mouse oocytes. After activation, oocytes were incubated in Hoechst 33342 or 33258 stain and exposed to UV irradiation. The effects on embryonic development were evaluated. Our results showed that both types of Hoechst combined with UV irradiation have toxic effects on parthenogenetically activated mouse oocytes. Although activation and cleavage rate were not affected, blastocyst formation was significantly reduced. Secondly, we used MitoTracker staining for removal of the sperm. Sperm heads were stained before injection and removed again after 1 h. However, staining was not visible anymore in all oocytes after intracytoplasmic sperm injection. In case the sperm could be removed, most oocytes died after 1 day. As MitoTracker was also not successful, alternative methods for sperm identification should be investigated.

Keywords

Artificial activationHoechstParthenogenesisPreimplantation developmentUV irradiation
Type
Research Article
Information
Zygote , Volume 22 , Issue 1 , February 2014 , pp. 32 - 40
Copyright
Copyright © Cambridge University Press 2012 

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

Alberio, R., Zakhartchenko, V., Motlik, J. & Wolf, E. (2001). Mammalian oocyte activation: lessons from the sperm and implications for nuclear transfer. Int. J. Dev. Biol. 45, 797–809.Google Scholar
Athar, M., Chaudhury, N.K., Hussain, M.E. & Varshney, R. (2010). Hoechst 33342 induces radiosensitization in malignant glioma cells via increase in mitochondrial reactive oxygen species. Free Radic. Res. 44, 936–49.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Swann, K. & Whittingham, D.G. (1995). Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes. Mol. Reprod. Dev. 41, 84–90.Google Scholar
Brevini, T.A., Pennarossa, G., Antonini, S. & Ganfolfi, F. (2008). Parthenogenesis as an approach to pluripotency: advantages and limitations involved. Stem Cell Rev. 4, 127–35.CrossRefGoogle ScholarPubMed
Bussalleu, E., Pinart, E., Yeste, M., Briz, M., Sancho, S., Garcia-Gil, N., Badia, E., Bassols, J., Pruneda, A., Casa, I. & Bonet, S. (2005). Development of a protocol for multiple staining with fluorochromes to assess the functional status of boar spermatozoa. Microsc. Res. Tech. 68, 277–83.CrossRefGoogle ScholarPubMed
Byrne, J.A., Pedersen, D.A., Clepper, L.L., Nelson, M., Sanger, W.G., Gokhale, S., Wolf, D.P. & Mitalipov, S.M. (2007). Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature 450, 497–502.Google Scholar
Cibelli, J.B., Kiessling, A.A., Cunniff, K., Richards, C., Lanza, R.P. & West, M.D. (2001). Somatic cell nuclear transfer in humans: pronuclear and early embryonic development. J. Regen. Med. 2, 25–31.Google Scholar
Critser, E.S. & First, N.L. (1986). Use of a fluorescent stain for visualization of nuclear material in living oocytes and early embryos. Stain Technol. 61, 1–5.CrossRefGoogle ScholarPubMed
de Fried, E.P., Ross, P., Zang, G., Divita, A., Cunniff, K., Denaday, F., Salamone, D., Kiessling, A. & Cibelli, J. (2008). Human parthenogenetic blastocysts derived from noninseminated cryopreserved human oocytes. Fertil. Steril. 89, 943–7.CrossRefGoogle ScholarPubMed
De Sutter, P., Dozortsev, D., Cieslak, J., Wolf, G., Verlinsky, Y. & Dyban, A. (1992). Parthenogenetic activation of human oocytes by puromycin. J. Assist. Reprod. Genet. 9, 328–37.CrossRefGoogle ScholarPubMed
De Sutter, P., Dozortsev, D., Vrijens, P., Desmet, R. & Dhont, M. (1994). Cytogenetic analysis of human oocytes parthenogenetically activated by puromycin. J. Assist. Reprod. Genet. 11, 382–8.Google Scholar
Dozortsev, D., Qian, C., Ermilov, A., Rybouchkin, A., De Sutter, P. & Dhont, M. (1997). Sperm-associated oocyte-activating factor is released from the spermatozoon within 30 minutes after injection as a result of the sperm–oocyte interaction. Hum. Reprod. 12, 2792–6.CrossRefGoogle ScholarPubMed
Ducibella, T., Huneau, D., Angelichio, E., Xu, Z., Schultz, R.M., Kopf, G.S., Fissore, R., Madoux, S. & Ozil, J.P. (2002). Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Dev. Biol. 250, 280–91.CrossRefGoogle ScholarPubMed
Durand, R.E. & Olive, P.L. (1982). Cytotoxicity, Mutagenicity and DNA damage by Hoechst 33342. J. Histochem. Cytochem. 30, 111–6.Google Scholar
Forsberg, E.J., Strelchenko, N.S., Augenstein, M.L., Betthauser, J.M., Childs, L.A., Eilertsen, K.J.et al. (2002). Production of cloned cattle from in vitro systems. Biol. Reprod. 67, 327–33.Google Scholar
French, A.J., Adams, C.A., Anderson, L.S., Kitchen, J.R., Hughes, M.R. & Wood, S.H. (2008). Development of human cloned blastocysts following somatic cell nuclear transfer with adult fibroblasts. Stem Cells 26, 485–93.CrossRefGoogle ScholarPubMed
Goddard, M.J. & Pratt, H.P. (1983). Control of events during early cleavage of the mouse embryo: an analysis of the ‘2-cell block.’ J. Embryol. Exp. Morphol. 73, 111–33.Google ScholarPubMed
Hamdoun, A. & Epel, D. (2007). Embryo stability and vulnerability in an always changing world. Proc. Natl. Acad. Sci. USA 6, 1745–50.Google Scholar
Hao, J., Zhu, W., Sheng, C., Yu, Y. & Zhou, Q. (2009). Human parthenogenetic embryonic stem cells: one potential resource for cell therapy. Sci. China C Life Sci. 52, 599–602.Google Scholar
Heindryckx, B., De Sutter, P. & Gerris, J. (2009). Somatic nuclear transfer to in vitro-matured human germinal vesicle oocytes. In: Stem Cells in Human Reproduction (eds Simon, C. & Pellicer, E.) Informa, London, pp. 227–43.Google Scholar
Heindryckx, B., De Sutter, P., Gerris, J., Dhont, M. & Van der Elst, J. (2007). Embryo development after successful somatic cell nuclear transfer to in vitro matured human germinal vesicle oocytes. Hum. Reprod. 22, 1982–90.Google Scholar
Heindryckx, B., Rybouchkin, A., Van Der Elst, J. & Dhont, M. (2002). Serial pronuclear transfer increases the developmental potential of in vitro-matured oocytes in mouse cloning. Biol. Reprod. 67, 1790–5.CrossRefGoogle ScholarPubMed
Heytens, E., Parrington, J., Coward, K., Young, C., Lambrecht, S., Yoon, S.Y.et al. (2009). Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum. Reprod. 24, 2417–28.Google Scholar
Hikichi, T., Kishigami, S., Thuan, N.V., Ohta, H., Mizutani, E., Wakayama, S. & Wakayama, T. (2005). Round spermatids stained with MitoTracker can be used to produce offspring more simple. Zygote 13, 55–61.CrossRefGoogle Scholar
Joshi, N.V., Medina, H., Colasante, C. & Osuna, A. (2000). Ultrastructural investigation of human sperm using atomic force microscopy. Arch. Androl. 44, 51–7.Google Scholar
Keefe, D., Liu, L., Wang, W. & Silva, C. (2003). Imaging meiotic spindles by polarization light microscopy: principles and applications to IVF. Reprod. BioMed. Online 7, 24–9.Google Scholar
Kline, D. & Kline, J.T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80–9.CrossRefGoogle ScholarPubMed
Kyono, K., Kumagai, S., Nishinaka, C., Nakajo, Y., Uto, H., Toya, M., Sugawara, J. & Araki, Y. (2008). Birth and follow-up of babies born following ICSI using SrCl2 oocyte activation. Reprod. BioMed. Online 17, 53–8.Google Scholar
Lawitts, J.A. & Biggers, J.D. (1991). Optimization of mouse embryo culture media using simplex methods. J. Reprod. Fertil. 91, 543–56.Google Scholar
Li, G.P., White, K.L. & Bunch, T.D. (2004). Review of enucleation methods and procedures used in animal cloning: state of the art. Cloning Stem Cells 6, 5–13.Google Scholar
Lin, H., Lei, J., Wininger, D., Nguyen, M.T., Khanna, R., Hartmann, C., Yan, W.L. & Huang, S.C. (2003). Multilineage potential of homozygous stem cells derived from metaphase II oocytes. Stem Cells 21, 152–61.CrossRefGoogle ScholarPubMed
Liu, S.Z., Jiang, M.X., Yan, L.Y., Jiang, Y., Ouyang, Y.C., Sun, Q.Y. & Chen, D.Y. (2005). Parthenogenetic and nuclear transfer rabbit embryo development and apoptosis after activation treatments. Mol. Reprod. Dev. 72, 48–53.Google Scholar
Ma, S.F., Liu, X.Y., Miao, D.Q., Han, Z.B., Zhang, X., Miao, Y.L., Yanagimachi, R. & Tan, J.H. (2005). Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology 64, 1142–57.Google Scholar
Mai, Q., Yu, Y., Li, T., Wang, L., Chen, M.J., Huang, S.Z., Zhou, C. & Zhou, Q. (2007). Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Res. 17, 1008–19.Google Scholar
McElroy, S.L., Kee, K., Tran, N., Menses, J., Giudice, L.C. & Reijo Pera, R.A. (2008). Developmental competence of immature and failed abnormally fertilized human oocytes in nuclear transfer. Reprod. BioMed. Online 16, 684–93.CrossRefGoogle ScholarPubMed
Mitalipov, S.M., Yeoman, R.R., Nusser, K.D. & Wolf, D.P. (2002). Rhesus monkey embryos produced by nuclear transfer from embryonic blastomeres or somatic cells. Biol. Reprod. 66, 1367–73.Google Scholar
Montag, M. & van der Ven, H. (2008). Symposium: innovative techniques in human embryo viability assessment. Oocyte assessment and embryo viability prediction: birefringence imaging. Reprod. BioMed. Online 17, 454–60.Google Scholar
Nandedkar, P., Chohan, P., Patwardhan, A., Gaikwad, S. & Bhartiva, D. (2009). Parthenogenesis and somatic cell nuclear transfer in sheep oocytes using Polscope. Indian J. Exp. Biol. 47, 550–8.Google Scholar
Paffoni, A., Brevini, T.A., Somigliana, E., Restelli, L., Gandolfi, F. & Ragni, G. (2007). In vitro development of human oocytes after parthenogenetic activation or intracytoplasmic sperm injection. Fertil. Steril. 87, 77–82.CrossRefGoogle ScholarPubMed
Parrington, J., Jones, M.L., Tunwell, R., Devader, C., Katan, M. & Swann, K. (2002). Phospholipase C isoforms in mammalian spermatozoa: potential components of the sperm factor that causes Ca2+ release in eggs. Reproduction 123, 31–9.CrossRefGoogle ScholarPubMed
Portugal, J. & Waring, M.J. (1988). Assignment of DNA binding sites for 4′,6-diamidine-2-phenylindole and bisbenzimide (Hoechst 33258). A comparative footprinting study. Biochim. Biophys. Acta 949, 158168.Google Scholar
Revazova, E.S., Turovets, N.A., Kochetkova, O.D., Kindarova, L.B., Kuzmichev, L.N., Janus, J.D. & Pryzhkova, M.V. (2007). Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9, 432–49.Google Scholar
Rinaudo, P., Pepperell, J.R., Buradgunta, S., Massobrio, M. & Keefe, D.L. (1997). Dissociation between intracellular calcium elevation and development of human oocytes treated with calcium ionophore. Fertil. Steril. 68, 1086–92.Google Scholar
Rogers, N.T., Hobson, E., Pickering, S., Lai, F.A., Braude, P. & Swann, K. (2004). Phospholipase C zeta causes Ca2+ oscillations and parthenogenetic activation of human oocytes. Reproduction 128, 697–702.CrossRefGoogle Scholar
Rybouchkin, A., Heindryckx, B., Van der Elst, J. & Dhont, M. (2002). Developmental potential of cloned mouse embryos reconstructed by a conventional technique of nuclear injection. Reproduction 124, 197–207.Google Scholar
Saunders, C.M., Larman, M.G., Parrington, J., Cox, L.J., Royse, J., Blayney, L.M., Swann, K. & Lai, F.A. (2002). PLC zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–44.CrossRefGoogle ScholarPubMed
Singh, S., Dwarakanath, B.S. & Mathew, T.L. (2004). DNA ligand Hoechst-33342 enhances UV induced cytotoxicity in human glioma cell lines. J. Photochem. Photobiol. B 7, 45–54.Google Scholar
Smith, L.C. (1993). Membrane and intracellular effects of ultraviolet irradiation with Hoechst 33342 on bovine secondary oocytes matured in vitro. J. Reprod. Fertil. 99, 39–44.CrossRefGoogle ScholarPubMed
Soderlind, K.J., Gorodetsky, B., Singh, A.K., Bachur, N.R., Miller, G.G. & Lown, J.W. (1999). Bis-benzimidazole anticancer agents: targeting human tumour helicases. Anticancer Drug Des. 14, 19–36.Google Scholar
Stojkovic, M., Stojkovic, P., Leary, C., Hall, V.J., Armstrong, L., Herbert, M., Nesbitt, M., Lako, M. & Murdoch, A. (2005). Derivation of a human blastocyst after heterologous nuclear transfer to donated oocytes. Reprod. BioMed. Online 11, 226–31.Google Scholar
Swann, K. & Parrington, J. (1999). Mechanism of Ca2+ release at fertilization in mammals. J. Exp. Zool. 285, 267–75.Google Scholar
Swann, K., Larman, M.G., Saunders, C.M. & Lai, F.A. (2004). The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLC zeta. Reproduction 127, 431–9.CrossRefGoogle Scholar
Swann, K., Saunders, C.M., Rogers, N.T. & Lai, F.A. (2006). PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin. Cell Dev. Biol. 17, 264–73.CrossRefGoogle ScholarPubMed
Taylor, A.S. & Braude, P.R. (1994). The early development and DNA content of activated human oocytes and parthenogenetic human embryos. Hum. Reprod. 9, 2389–97.Google Scholar
Thouas, G.A., Korfiatis, N.A., French, A.J., Jones, G.M. & Trounson, A.O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. BioMed. Online 3, 25–9.Google Scholar
Toth, S., Huneau, D., Banrezes, B. & Ozil, J.P. (2006). Egg activation is the result of calcium signal summation in the mouse. Reproduction 131, 27–34.Google Scholar
Tsunoda, Y., Shioda, Y., Onodera, M., Nakamura, K. & Uchida, T. (1988). Differential sensitivity of mouse pronuclei and zygote cytoplasm to Hoechst staining and ultraviolet irradiation. J. Reprod. Fertil. 82, 173–8.Google Scholar
Velilla, E., López-Béjar, M., Rodríguez-González, E., Vidal, F. & Paramio, M.T. (2002). Effect of Hoechst 33342 staining on developmental competence of prepubertal goat oocytes. Zygote 10, 201–8.Google Scholar
Versieren, K., Heindryckx, B., Lierman, S., Gerris, J. & De Sutter, P. (2010). Developmental competence of parthenogenetic mouse and human embryos after chemical or electrical activation. Reprod. Biomed. Online 21, 769–75.Google Scholar
Westhusin, M.E., Levanduski, M.J., Scarborough, R., Looney, C.R. & Bondioli, K.R. (1992). Viable embryos and normal calves after nuclear transfer into Hoechst stained enucleated demi-oocytes of cows. J. Reprod. Fertil. 95, 475–80.Google Scholar
Whittingham, D.G. & Siracusa, G. (1978). The involvement of calcium in the activation of mammalian oocytes. Exp. Cell Res. 113, 311–7.Google Scholar
Winston, N., Johnson, M., Pickering, S. & Braude, P. (1991). Parthenogenetic activation and development of fresh and aged human oocytes. Fertil. Steril. 56, 904–12.Google Scholar
Yanagida, K., Morozumi, K., Katayose, H., Hayashi, S. & Sato, A. (2006). Successful pregnancy after ICSI with strontium oocytes activation in low rates of fertilization. Reprod. BioMed. Online 13, 801–6.Google Scholar
Yang, X., Zhang, L., Kovács, A., Tobback, C. & Foote, R.H. (1990). Potential of hypertonic medium treatment on embryo micromanipulation: II. Assessment of nuclear transplantation methodology, isolation, subzona insertion, and electrofusion of blastomeres to intact or functionally enucleated oocytes in rabbits. Mol. Reprod. Dev. 27, 118–29.Google Scholar
Yu, Y., Mai, Q., Chen, X., Wang, L., Gao, L., Zhou, C. & Zhou, Q. (2009). Assessment of the developmental competence of human somatic cell nuclear transfer embryos by oocyte morphology classification. Hum. Reprod. 24, 649–57.Google Scholar
Yu, Y., Saunders, C.M., Lai, F.A. & Swann, K. (2008). Preimplantation development of mouse oocytes activated by different levels of human phospholipase C zeta. Hum. Reprod. 23, 365–73.Google Scholar
Zhang, J., Wang, C.W., Blaszcyzk, A., Grifo, J.A., Ozil, J., Haberman, E., Adler, A. & Krey, L.C. (1999). Electrical activation and in vitro development of human oocytes that fail to fertilize after intracytoplasmic sperm injection. Fertil. Steril. 72, 509–12.Google Scholar
Zhang, X. & Kiechle, F.L. (2003). Hoechst 33342 alters luciferase gene expression in transfected BC3H-1 myocytes. Arch. Pathol. Lab. Med. 127, 1124–32.Google Scholar