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Prediction of maturational competence of feline oocytes using supravital staining of cumulus cells by propidium iodide

Published online by Cambridge University Press:  18 May 2011

Kenzo Uchikura
Affiliation:
Department of Theriogenology, School of Veterinary Medicine, Faculty of Agriculture, Tottori University, 4–101 Koyama-Minami, Tottori 680–8553, Japan. The United Graduate School of Veterinary Science, Yamaguchi University, 1677–1 Yoshida, Yamaguchi 753–8515, Japan; 1 Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060–0818, Japan.
Masashi Nagano*
Affiliation:
Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060–0818, Japan.
Mitsugu Hishinuma
Affiliation:
Department of Theriogenology, School of Veterinary Medicine, Faculty of Agriculture, Tottori University, 4–101 Koyama-Minami, Tottori 680–8553, Japan.
*
All correspondence to: Masashi Nagano. Laboratory of Theriogenology, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060–0818, Japan. Tel:/Fax: +81 11 706 5232. e-mail: mnaga@vetmed.hokudai.ac.jp

Summary

We examined the relationship between integrity of cumulus cells and nuclear maturation rate after in vitro culture to determine a non-invasive prediction of the maturational competence of feline oocytes. Feline cumulus–oocyte complexes (COCs) were collected from either small (400–800 μm) or large (≥800 μm) follicles. Immediately after collection, cumulus cells were evaluated morphologically (thickness of cumulus cell layers) and stained with propidium iodide (PI), which penetrates only non-viable cells. Cumulus cells without PI staining were judged as having good membrane integrity. After evaluation, COCs were cultured for 30 h and their nuclear maturation rate was determined. The nuclear maturation rate of oocytes derived from large follicles (89.8%) was higher (p < 0.05) than that from small follicles (60.8%). There was no difference in the maturation rate of oocytes from follicles with the same size regardless of cumulus morphology. In contrast, oocytes that had cumulus cells with good membrane integrity showed a higher maturation rate (93.8%) than oocytes with poor cumulus integrity (76.9%) in large follicles (p < 0.05). We conclude that evaluation of membrane integrity of cumulus cells by propidium iodide staining can be used to predict the maturational competence of oocytes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

Anderson, R.A., Sciorio, R., Kinnell, H., Bayne, R.A., Thong, K.J., de Sousa, P.A. & Pickering, S. (2009). Cumulus gene expression as a predictor of human oocyte fertilisation, embryo development and competence to establish a pregnancy. Reproduction 138, 629637.CrossRefGoogle ScholarPubMed
Arlotto, T., Schwartz, J.L., First, N.L. & Leibfried-Rutledge, M.L. (1996). Aspects of follicle and oocyte stage that affect in vitro maturation and development of bovine oocytes. Theriogenology 45, 943956.CrossRefGoogle ScholarPubMed
Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S. & Sirard, M.A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209222.CrossRefGoogle ScholarPubMed
Assou, S., Haouzi, D., Mahmoud, K., Aouacheria, A., Guillemin, Y., Pantesco, V., Reme, T., Dechaud, H., De Vos, J. & Hamamah, S. (2008). A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol. Hum. Reprod. 14, 711719.CrossRefGoogle ScholarPubMed
Assou, S., Haouzi, D., De Vos, J. & Hamamah, S. (2010). Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol. Hum. Reprod. 16, 531538.CrossRefGoogle ScholarPubMed
Bettegowda, A., Patel, O.V., Lee, K.B., Park, K.E., Salem, M., Yao, J., Ireland, J.J. & Smith, G.W. (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol. Reprod. 79, 301309.CrossRefGoogle ScholarPubMed
Fair, T., Hyttel, P. & Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437442.CrossRefGoogle ScholarPubMed
Freistedt, P., Stojkovic, M. & Wolf, E. (2001). Efficient in vitro production of cat embryos in modified synthetic oviduct fluid medium: effects of season and ovarian status. Biol. Reprod. 65, 913.CrossRefGoogle ScholarPubMed
Harada, M., Miyano, T., Matsumura, K., Osaki, S., Miyake, M. & Kato, S. (1997). Bovine oocytes from early antral follicles grow to meiotic competence in vitro: effect of FSH and hypoxanthine. Theriogenology 48, 743755.CrossRefGoogle 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, 343356.CrossRefGoogle ScholarPubMed
Karja, N.W., Otoi, T., Murakami, M., Fahrudin, M. & Suzuki, T. (2002). In vitro maturation, fertilization and development of domestic cat oocytes recovered from ovaries collected at three stages of the reproductive cycle. Theriogenology 57, 22892298.CrossRefGoogle ScholarPubMed
Katska-Ksiazkiewicz, L., Rynska, B., Kania, G., Smorag, Z., Gajda, B. & Pienkowski, M. (2003). Timing of nuclear maturation of nonstored and stored domestic cat oocytes. Theriogenology 59, 15671574.CrossRefGoogle ScholarPubMed
Ledda, S., Bogliolo, L., Leoni, G. & Naitana, S. (1999). Follicular size affects the meiotic competence of in vitro matured prepubertal and adult oocytes in sheep. Reprod. Nutr. Dev. 39, 503508.CrossRefGoogle ScholarPubMed
Madison, V., Avery, B. & Greve, T. (1992). Selection of immature bovine oocytes for developmental potential in vitro. Anim. Reprod. Sci. 27, 111.CrossRefGoogle Scholar
Momozawa, K. & Fukuda, Y. (1995). In vitro maturation and in vitro fertilization of bovine oocytes with heterogeneous ooplasm. Anim. Sci. Technol. 66, 605609.Google Scholar
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, 231236.CrossRefGoogle ScholarPubMed
Naoi, H., Agung, B., Karja, N.W., Wongsrikeao, P., Shimizu, R., Taniguchi, M. & Otoi, T. (2008). Effects of the reproductive status on morphological oocyte quality and developmental competence of oocytes after in vitro fertilization and somatic cell nuclear transfer in cat. Reprod. Domest. Anim. 43, 157161.CrossRefGoogle ScholarPubMed
Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S. & Suzuki, T. (1997). Bovine oocyte diameter in relation to developmental competence. Theriogenology 48, 769774.CrossRefGoogle ScholarPubMed
Otoi, T., Murakami, M., Ooka, A., Karja, N.W. & Suzuki, T. (2001). Effects of size and storage temperature on meiotic competence of domestic cat oocytes. Vet. Rec. 148, 116118.CrossRefGoogle ScholarPubMed
Pope, C.E. (2000). Embryo technology in conservation efforts for endangered felids. Theriogenology 53, 163174.CrossRefGoogle ScholarPubMed
Pope, C.E., McRae, M.A., Plair, B.L., Keller, G.L. & Dresser, B.L. (1997). In vitro and in vivo development of embryos produced by in vitro maturation and in vitro fertilization of cat oocytes. J. Reprod. Fertil. Suppl. 51, 6982.Google ScholarPubMed
Pope, C.E., Gomez, M.C. & Dresser, B.L. (2006). In vitro production and transfer of cat embryos in the 21st century. Theriogenology 66, 5971.CrossRefGoogle Scholar
Pope, C.E., Crichton, E.G., Gomez, M.C., Dumas, C. & Dresser, B.L. (2009). Birth of domestic cat kittens of predetermined sex after transfer of embryos produced by in vitro fertilization of oocytes with flow-sorted sperm. Theriogenology 71, 864871.CrossRefGoogle ScholarPubMed
Ruppert-Lingham, C.J., Paynter, S.J., Godfrey, J., Fuller, B.J. & Shaw, R.W. (2006). Membrane integrity and development of immature murine cumulus–oocyte complexes following slow cooling to −60°C: the effect of immediate rewarming, plunging into LN2 and two-controlled-rate-stage cooling. Cryobiology 52, 219227.CrossRefGoogle Scholar
Saint-Dizier, M., Malandain, E., Thoumire, S., Remy, B. & Chastant-Maillard, S. (2007). Expression of follicle stimulating hormone and luteinizing hormone receptors during follicular growth in the domestic cat ovary. Mol. Reprod. Dev. 74, 989996.CrossRefGoogle ScholarPubMed
Sato, E., Matsuo, M. & Miyamoto, H. (1990). Meiotic maturation of bovine oocytes in vitro: improvement of meiotic competence by dibutyryl cyclic adenosine 3′,5′-monophosphate. J. Anim. Sci. 68, 11821187.CrossRefGoogle ScholarPubMed
Shioya, Y., Kuwayama, M., Fukushima, M., Iwasaki, S. & Hanada, A. (1988). In vitro fertilization and cleavage capability of bovine follicular oocytes classified by cumulus cells and matured in vitro. Theriogenology 30, 489496.CrossRefGoogle ScholarPubMed
Spinaci, M., Merlo, B., Zannoni, A., Iacono, E., De Ambrogi, M., Turba, M.E. & Zambelli, D. (2007). In vitro production of cat blastocysts of predetermined sex using flow cytometrically sorted semen. Theriogenology 67, 872877.CrossRefGoogle ScholarPubMed
Spindler, R.E. & Wildt, D.E. (1999). Circannual variations in intraovarian oocyte but not epididymal sperm quality in the domestic Cat. Biol. Reprod. 61, 188194.CrossRefGoogle Scholar
Stojkovic, M., Machado, S.A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P.B. & Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904909.CrossRefGoogle ScholarPubMed
Tanghe, S., Van Soom, A., Nauwynck, H., Coryn, M. & de Kruif, A. (2002). Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414424.CrossRefGoogle ScholarPubMed
Uchikura, K., Nagano, M. & Hishinuma, M. (2010). Evaluation of follicular development and oocyte quality in pre-pubertal cats. Reprod. Domest. Anim. 45, e405e411.CrossRefGoogle ScholarPubMed
Wood, T.C. & Wildt, D.E. (1997). Effect of the quality of the cumulus–oocyte complex in the domestic cat on the ability of oocytes to mature, fertilize and develop into blastocysts in vitro. J. Reprod. Fertil. 110, 355360.CrossRefGoogle ScholarPubMed
Xu, K.P., Greve, T., Smith, S. & Hyttel, P. (1986). Chronological changes of bovine follicular oocyte maturation in vitro. Acta Vet. Scand. 27, 505519.CrossRefGoogle ScholarPubMed
Yang, Y.B. & Lu, K.H. (1990). The influence of bovine oocyte type on in vitro fertilization and subsequent development in vitro. Theriogenology 33, 355.CrossRefGoogle Scholar