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Developmental competence of cat (Felis domesticus) oocytes and embryos after parthenogenetic stimulation using different methods

Published online by Cambridge University Press:  22 February 2018

Joanna Kochan ,
Agnieszka Nowak ,
Wojciech Niżański ,
Sylwia Prochowska ,
Anna Migdał ,
Wiesława Młodawska ,
Agnieszka Partyka  and
Maciej Witkowski
Joanna Kochan
Affiliation:
University of Agriculture in Krakow, Faculty of Animal Sciences, Institute of Veterinary Sciences, Krakow, Poland.
Agnieszka Nowak*
Affiliation:
University of Agriculture in Krakow, Faculty of Animal Sciences, Institut of Veterinary Sciences, al. Mickiewicza 21, 30–120 Krakow, Poland.
Wojciech Niżański
Affiliation:
Wroclaw University of Environmental and Life Sciences, Department of Reproduction and Clinic of Farm Animals, Wroclaw, Poland.
Sylwia Prochowska
Affiliation:
Wroclaw University of Environmental and Life Sciences, Department of Reproduction and Clinic of Farm Animals, Wroclaw, Poland.
Anna Migdał
Affiliation:
University of Agriculture in Krakow, Faculty of Animal Sciences, Institute of Veterinary Sciences, Krakow, Poland.
Wiesława Młodawska
Affiliation:
University of Agriculture in Krakow, Faculty of Animal Sciences, Institute of Veterinary Sciences, Krakow, Poland.
Agnieszka Partyka
Affiliation:
Wroclaw University of Environmental and Life Sciences, Department of Reproduction and Clinic of Farm Animals, Wroclaw, Poland.
Maciej Witkowski
Affiliation:
University of Agriculture in Krakow, Faculty of Animal Sciences, Institute of Veterinary Sciences, Krakow, Poland.
*
All correspondence to: Agnieszka Nowak. University of Agriculture in Krakow, Faculty of Animal Sciences, Institut of Veterinary Sciences, al. Mickiewicza 21, 30–120 Krakow, Poland. E-mail [email protected]
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Summary

The aim of this study was to compare the effects of various activating factors on feline oocytes. The study included activation within the ovary (natural), activation during in vitro maturation (spontaneous activation), chemical activation (ionomycin + 6-DMAP), activation by spermatozoa and injection (ICSI) and mechanical activation (sham ICSI). According to our results, parthenogenetic embryos could emerge at every step of in vitro embryo production (IVP) procedures. After oocyte collection, 6% of parthenogenetic embryos were observed, mainly at the 2–4-blastomere stages. After 24 h of in vitro maturation, parthenogenetic activation was observed in 7% of oocytes. Using ionomycin and 6-DMAP to artificially activate oocytes, 53% of cleaved embryos were obtained. The results after ICSI (54% cleaved embryos) were not significantly different from the results in Group III using chemical activation (53% cleaved embryos). But only after ICSI were blastocysts obtained (5/73.7%) as a result of in vitro culture. Moreover, embryos after ICSI were of the best morphological quality with minor levels of fragmentation evident in the embryos. After sham mechanical activation, ‘sham ICSI’, 8% of cleaved embryos were noted. Therefore, it is advised to maintain a negative control in parallel with each step of IVP techniques, to avoid misleading results. Chemical methods for artificial activation of feline oocytes are the most promising for application to the cloning and production of parthenogenetic embryos for experimental studies.

Keywords

Feline oocytesICSIOocyte activationParthenogenesis
Type
Research Article
Information
Zygote , Volume 26 , Issue 2 , April 2018 , pp. 119 - 126
Copyright
Copyright © Cambridge University Press 2018 

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References

Barlow, D.P. (1995). Gametic imprinting in mammals. Science 270 (5242), 1610–13.CrossRefGoogle ScholarPubMed
Bogliolo, L., Leoni, G., Ledda, S., Zedda, M.T., Bonelli, P., Madau, L., Santucciu, C., Naitana, S. & Pau, S. (2004). M-Phase promoting factor (MPF) and mitogen activated protein kinases (MAPK) activities of domestic cat oocytes matured in vitro and in vivo. Cloning Stem Cells 6, 15–23.CrossRefGoogle ScholarPubMed
Chung, J.T., Keefer, C.L. & Downey, B.R. (2000). Activation of bovine oocytes following intracytoplasmic sperm injection (ICSI). Theriogenology 53, 1273–84.CrossRefGoogle ScholarPubMed
Combelles, C.H.M., Cekleniak, N.A., Racowsky, C. & Albertini, D.F. (2002). Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum. Reprod. 17, 1006–16.CrossRefGoogle ScholarPubMed
Comizzoli, P., Wildt, D.E. & Pukazhenthi, B.S. (2003). Overcoming poor in vitro nuclear maturation and developmental competence of domestic cat oocytes during the non-breeding season. Reproduction 126, 809–16.CrossRefGoogle ScholarPubMed
Comizzoli, P., Wildt, D.E. & Pukazhenthi, B.S. (2006). Poor centrosomal function of cat testicular spermatozoa impairs embryo development in vitro after intracytoplasmic sperm injection. Biol. Reprod. 75, 252–60.CrossRefGoogle ScholarPubMed
Cuellar, O. (1977). Animal parthenogenesis. Science 197 (4306), 837–43.CrossRefGoogle ScholarPubMed
Fernandez-Gonzalez, L., Hribal, R., Stagegaard, J., Zahmel, J. & Jewgenow, K. (2015). Production of lion (Panthera leo) blastocysts after in vitro maturation of oocytes and intracytoplasmic sperm injection. Theriogenology 83, 995–9.CrossRefGoogle ScholarPubMed
Gómez, M.C., Catt, J.W., Evans, G. & Maxwell, W.M. (1998). Sheep oocyte activation after intracytoplasmic sperm injection (ICSI). Reprod. Fertil. Dev. 10, 197–205.CrossRefGoogle ScholarPubMed
Gómez, M.C., Pope, C.E., Giraldo, A., Lyons, L.A., Harris, R.F., King, A.L., Cole, A., Godke, R.A. & Dresser, B.L. (2004). Birth of African Wildcat cloned kittens born from domestic cats. Cloning Stem Cells 6, 247–58.CrossRefGoogle ScholarPubMed
Goodrowe, K.L., Wall, R.J., O'Brien, S.J., Schmidt, P.M. & Wildt, D.E. (1988). Developmental competence of domestic cat follicular oocytes after fertilization in vitro. Biol. Reprod. 39, 355–72.CrossRefGoogle ScholarPubMed
Grabiec, A., Max, A. & Tischner, M. (2007). Parthenogenetic activation of domestic cat oocytes using ethanol, calcium ionophore, cycloheximide and a magnetic field. Theriogenology 67, 795–800.CrossRefGoogle ScholarPubMed
Herrick, J.R., Bond, J.B., Magarey, G.M., Bateman, H.L., Krisher, R.L., Dunford, S. & Swanson, W.F. (2007). Toward a feline-optimized culture medium: effect of ions, carbohydrates, essential amino acids, vitamins, and serum on development and metabolism of in vitro fertilization-derived feline embryos relative to embryos grown in vivo. Biol. Reprod. 76, 858–70.CrossRefGoogle Scholar
Hoffert, K.A., Anderson, G.B., Wildt, D.E. & Roth, T.L. (1997). Transition from maternal to embryonic control of development in IVM/IVF domestic cat embryos. Mol. Reprod. Dev. 48, 208–15.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Hribal, R., Braun, BC., Ringleb, J. & Jewgenow, K. (2012). Capabilities and challenges of examination of gene expression for quality assessment of domestic cat embryos. Reprod. Domest. Anim. 47, 147–51.CrossRefGoogle ScholarPubMed
Jewgenow, K., Blottner, S., Lengwinat, T. & Meyer, H.H. (1997). New methods for gamete rescue from gonads of nondomestic felids. J. Reprod. Fertil. 51 (Suppl.), 33–9.Google ScholarPubMed
Johnston, L.A., O'Brien, S.J. & Wildt, D.E. (1989). In vitro maturation and fertilization of domestic cat follicular oocytes. Gamete Res. 24, 343–56.CrossRefGoogle ScholarPubMed
Johnston, L., Donoghue, A., O'Brien, S. & Wildt, D. (1991). Culture medium and protein supplementation influence in vitro fertilization and embryo development in the domestic cat. J. Exp. Zool. 257, 350–9.CrossRefGoogle ScholarPubMed
Karja, N.W., Otoi, T., Murakami, M., Wongsrikeao, P., Budiyanto, A., Fahrudin, M. & Nagai, T. (2005). Effect of cycloheximide on in vitro development of electrically activated feline oocytes. J. Reprod. Dev. 51, 783–6.CrossRefGoogle ScholarPubMed
Keefer, C.L. & Schuetz, A.W. (1982). Spontaneous activation of ovulated rat oocytes during in vitro culture. J. Exp. Zool. 224, 371–7.CrossRefGoogle ScholarPubMed
Kharche, S.D. & Birade, H.S. (2013). Parthenogenesis and activation of mammalian oocytes for in vitro embryo production. Adv. Biosci. Biotechnol. 4, 170–82.CrossRefGoogle Scholar
Kitiyanant, Y., Saikhun, J. & Pavasuthipaisit, K. (2003). Somatic cell nuclear transfer in domestic cat oocytes treated with IGF-I for in vitro maturation. Theriogenology 59, 1775–86.CrossRefGoogle ScholarPubMed
Lechniak, D., Cieślak, D. & Sosnowski, J. (1998). Cytogenetic analysis of bovine parthenotes after spontaneus activation in vitro. Theriogenology 49, 779–85.CrossRefGoogle Scholar
Loi, P., Branca, A., Dattena, M., Gallus, M., Ledda, S., Naitana, S. & Cappai, P. (1996). Parthenogenetic development of sheep oocytes after activation with ionomycin and 6-dimethylaminopurine. Int. Congr. Anim. Reprod. AI Sydney 2, 8–4.Google Scholar
Merlo, B., Iacono, E., Regazzini, M. & Zambelli, D. (2008). Cat blastocysts produced in vitro from oocytes vitrified using the cryoloop technique and cryopreserved electroejaculated semen. Theriogenology 70, 126–30.CrossRefGoogle ScholarPubMed
Moro, L.N., Sestelo, A.J. & 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.CrossRefGoogle ScholarPubMed
Murakami, O., Otoi, T., Karja, N.W., Ooka, A. & Suzuki, T. (2002). Effects of serum-free culture medium on in vitro development of domestic cat embryos following in vitro maturation and fertilization. Reprod. Domest. Anim. 37, 352–6.CrossRefGoogle ScholarPubMed
Nagano, M., Uchikura, K., Takahashi, Y. & Hishinuma, M. (2008). Effect of duration of in vitro maturation on nuclear maturation and fertilizability of feline oocytes. Theriogenology 69, 231–6.CrossRefGoogle ScholarPubMed
Penfold, L.M., Jost, L., Evenson, D.P. & Wildt, D.E. (2003). Normospermic versus teratospermic domestic cat sperm chromatin integrity evaluated by flow cytometry and intracytoplasmic sperm injection. Biol. Reprod. 69, 1730–5.CrossRefGoogle ScholarPubMed
Pincus, G. & Enzmann, E.V. (1935). The comparative behaviour of mammalian eggs in vivo and in vitro I. The activation of ovarian eggs. J. Exp. Med. 62, 665–75.CrossRefGoogle ScholarPubMed
Pope, C.E. (2014). Aspects of in vivo oocyte production., blastocyst development and embryo transfer in the cat. Theriogenology 81, 126–37.CrossRefGoogle ScholarPubMed
Pope, C., Keller, G. & Dresser, B. (1993). In vitro fertilization in domestic and non-domestic cats including sequences of early nuclear events., development in vitro, cryopreservation and successful intra- and interspecies embryo transfer. J. Reprod. Fertil. Suppl. 47, 189–201.Google ScholarPubMed
Pope, C.E., Johnson, C.A., McRae, M.A., Keller, G.L. & Dresser, B.L. (1998). Development of embryos produced by intracytoplasmic sperm injection of cat oocytes. Anim. Reprod. Sci. 53 (1–4), 221–36.CrossRefGoogle ScholarPubMed
Pope, C., Schmid, R. & Dresser, BL. (1999). In vitro development of cat embryos produced by in vitro fertilization is enhanced by addition of cysteine to the maturation medium and a reduced O2 atmosphere. Theriogenology 51, 291.CrossRefGoogle Scholar
Pushett, D.A., Gunn, I.M. & Trounson, A.O. (1997). Retrieval of partheno-like embryos from the ovaries of domestic cats. Theriogenology 47, 404.CrossRefGoogle Scholar
Rascado, T.S., Martins, L.R., Minto, B.W., de Sá Lorena, S.E. & Landim-Alvarenga, F.C. (2010). Parthenogenetic development of domestic cat oocytes treated with ionomycin., cycloheximide., roscovitine and strontium. Theriogenology 74, 596–601.CrossRefGoogle ScholarPubMed
Ringleb, J., Rohleder, M. & Jewgenow, K. (2004). Impact of feline zona pellucida glycoprotein B-derived synthetic peptides on in vitro fertilization of cat oocytes. Reproduction 127, 179–86.CrossRefGoogle ScholarPubMed
Shin, T., Kraemer, D., Pryor, J., Liu, L., Rugila, J., Howe, L., Buck, S., Murphy, K., Lyons, L. & Westhusin, M.A. (2002). Cat cloned by nuclear transplantation. Nature 415 (6874), 859.CrossRefGoogle ScholarPubMed
Suttner, R., Zakhartchenko, V., Stojkovic, P., Muller, S., Alberio, R., Medjugorac, I., Brem, G., Wolf, E. & Stojkovic, M. (2000). Intracytoplasmic sperm injection in bovine effects of oocyte activation., sperm pretreatment and injection technique. Theriogenology 54, 935–48.CrossRefGoogle ScholarPubMed
Thuwanut, P., Arya, N., Comizzoli, P. & Chatdarong, K. (2015). Effect of extracellular adenosine 5´-triphosphate on cryopreserved epididymal cat sperm intracellular ATP concentration., sperm quality., and in vitro fertilizing ability. Theriogenology 84, 702–9.CrossRefGoogle ScholarPubMed
Vick, M.M., Bateman, H.L., Lambo, C.A. & Swanson, W.F. (2012). Improved cryopreservation of domestic cat sperm in a chemically defined medium. Theriogenology 78, 2120–8.CrossRefGoogle Scholar
Vrana, K.E., Hipp, J.D., Gross, A.M., McCoo, B.A. & Riddle, D.R. (2003). Nonhuman primate parthenogenetic stem cells. Proc. Natl. Acad. Sci. USA 30 (Suppl.), 100.Google Scholar
Wang, C., Swanson, W.F., Herrick, J.R., Lee, K. & Machaty, Z. (2009). Analysis of cat oocyte activation methods for the generation of feline disease models by nuclear transfer. Reprod. Biol. Endocrinol. 11, 148.CrossRefGoogle Scholar
Waurich, R., Ringleb, J., Braun, BC. & Jewgenow, K. (2010). Embryonic gene activation in in vitro produced embryos of the domestic cat (Felis catus). Reproduction 140, 531–40.CrossRefGoogle ScholarPubMed
Zambelli, D., Raccagni, R., Cunto, M., Andreani, G. & Isani, G. (2010). Sperm evaluation and biochemical characterization of cat seminal plasma collected by electroejaculation and urethral catheterization. Theriogenology 74, 1396–402CrossRefGoogle ScholarPubMed