Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T07:03:41.293Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression and cellular distribution of zona pellucida glycoproteins in canine oocytes before and after in vitro maturation

Published online by Cambridge University Press:  15 October 2014

Bartosz Kempisty ,
Hanna Piotrowska ,
Dorota Bukowska ,
Magdalena Woźna ,
Sylwia Ciesiółka ,
Katarzyna Wojtanowicz-Markiewicz ,
Renata Włodarczyk ,
Karol Jopek ,
Michal Jeseta  and
Małgorzata Bruska
...Show all authors
Bartosz Kempisty*
Affiliation:
Department of Histology and Embryology, Department of Anatomy, Poznan University of Medical Sciences, 6 Święcickiego St., 60–781 Poznań, Poland. Department of Histology and Embryology, Poznan University of Medical Sciences, Poznan, Poland. Department of Anatomy, Poznan University of Medical Sciences, Poznan, Poland.
Hanna Piotrowska
Affiliation:
Department of Toxicology, Poznan University of Medical Sciences, Poznan, Poland.
Dorota Bukowska
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, Poznan, Poland.
Magdalena Woźna
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, Poznan, Poland.
Sylwia Ciesiółka
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, Poznan, Poland.
Katarzyna Wojtanowicz-Markiewicz
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, Poznan, Poland.
Renata Włodarczyk
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, Poznan, Poland.
Karol Jopek
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, Poznan, Poland.
Michal Jeseta
Affiliation:
Department of Genetics and Reproduction, Veterinary Research Institute, Brno, Czech Republic.
Małgorzata Bruska
Affiliation:
Department of Anatomy, Poznan University of Medical Sciences, Poznan, Poland.
Michał Nowicki
Affiliation:
Department of Histology and Embryology, Poznan University of Medical Sciences, Poznan, Poland.
Jędrzej M. Jaśkowski
Affiliation:
Institute of Veterinary Sciences, Poznan University of Life Sciences, Poznan, Poland.
Klaus-Peter Brüssow
Affiliation:
Institute of Reproductive Biology, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany.
Maciej Zabel
Affiliation:
Department of Histology and Embryology, Wroclaw Medical University, Wroclaw, Poland.
*
All correspondence to: Bartosz Kempisty. Department of Histology and Embryology, Department of Anatomy, Poznan University of Medical Sciences, 6 Święcickiego St., 60–781 Poznań, Poland. Tel: +48 61 8546419. Fax: +48 61 8546455. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study was aimed at investigating zona pellucida glycoproteins (ZP) ZP2, ZP3 mRNA expression as well as ZP3, ZP4 (ZPB) protein distribution before and after in vitro maturation (IVM) in canine oocytes. The cumulus–oocyte complexes (COCs) were recovered from 27 anoestrous mongrel bitches and matured for 72 h in TCM199 medium. The canine COCs were analysed before and after IVM. Using real-time quantitative polymerase chain reaction (RQ-PCR), both groups of oocytes were analysed for detection of ZP2 and ZP3 mRNA profiles as well as using confocal microscopic analysis for observation of ZP3 and ZP4 protein distribution. In post-IVM canine oocytes an increase in transcript content of ZP2 and ZP3 genes as well as a decrease in ZP3 and ZP4 protein levels were observed when compared with pre-IVM oocytes. Moreover, the ZP4 protein before IVM was significantly distributed in the peripheral area of cytoplasm, whereas after IVM it was localized rather than in the entire cytoplasm. In contrast, the ZP3 protein was found both before and after IVM was distributed in the peripheral area of the cytoplasm. In conclusion, we suggest that the expression of ZP2 and ZP3 genes is associated with the maturation stage of canine oocytes, as higher mRNAs levels were found after IVM. However, a decreased expression of ZP3 and ZP4 proteins after IVM suggests maturation-dependent down-regulation of these protein translations, which may result in disturbed fertilization.

Keywords

BitchGlycoproteinsOocyteSubcellular protein distributionZona pellucida
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 863 - 873
Copyright
Copyright © Cambridge University Press 2014 

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

Abe, H. & Hoshi, H. (2003). Evaluation of bovine embryos produced in high performance serum-free media. J. Reprod. Dev. 49, 193–202.Google Scholar
Antosik, P., Kempisty, B., Jackowska, M., Bukowska, D., Lianeri, M., Brüssow, K.P., Woźna, M. & Jaśkowski, J.M. (2010). The morphology of porcine oocytes is associated with zona pellucida glycoprotein 3 and integrin beta 2 protein levels. Vet. Med. (Praha) 55, 154–62.Google Scholar
Blackmore, D.G., Baillie, L.R., Holt, J.E., Dierkx, L., Aitken, R.J. & McLaughlin, E.A. (2004). Biosynthesis of the canine zona pellucida requires the integrated participation of both oocytes and granulosa cells. Biol. Reprod. 71, 661–8.CrossRefGoogle ScholarPubMed
Chiu, P.C., Wong, B.S., Chung, M.K., Lam, K.K., Pang, R.T., Lee, K.F., Sumitro, S.B., Gupta, S.K. & Yeung, W.S. (2008). Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa. Biol. Reprod. 799, 869–77.Google Scholar
Chiu, P.C., Wong, B.S., Lee, C.L., Lam, K.K., Chung, M.K., Lee, K.F., Koistinen, R., Koistinen, H., Gupta, S.K., Seppälä, M. & Yeung, W.S. (2010). Zona pellucida-induced acrosome reaction in human spermatozoa is potentiated by glycodelin-A via down-regulation of extracellular signal-regulated kinases and up-regulation of zona pellucida-induced calcium influx. Hum. Reprod. 25, 2721–33.Google Scholar
Concannon, P.W. (2011). Reproductive cycles of the domestic bitch. Anim. Reprod. Sci. 124, 200–10.Google Scholar
de Avila Rodrigues, B. & Rodrigues, J.L. (2003). Influence of reproductive status on in vitro oocyte maturation in dogs. Theriogenology 60, 59–66.CrossRefGoogle ScholarPubMed
Diederich, M., Hansmann, T., Heinzmann, J., Barg-Kues, B., Herrmann, D., Aldag, P., Baulain, U., Reinhard, R., Kues, W., Weissgerber, C., Haaf, T. & Niemann, H. (2012). DNA methylation and mRNA expression profiles in bovine oocytes derived from prepubertal and adult donors. Reproduction 144, 319–30.Google Scholar
Duranthon, V. & Renard, J.P. (2001). The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. Theriogenology 55, 1277–89.Google Scholar
El-Mestrah, M., Castle, P.E., Borossa, G. & Kan, F.W. (2002). Subcellular distribution of ZP1, ZP2, and ZP3 glycoproteins during folliculogenesis and demonstration of their topographical disposition within the zona matrix of mouse ovarian oocytes. Biol. Reprod. 66, 866–76.Google Scholar
Gupta, S.K., Bhandari, B., Shrestha, A., Biswal, B.K., Palaniappan, C., Malhotra, S.S. & Gupta, N. (2012). Mammalian zona pellucida glycoproteins: structure and function during fertilization. Cell Tissue Res. 349, 665–78.CrossRefGoogle ScholarPubMed
Hewitt, D.A. & England, G.C. (1997). Effect of preovulatory endocrine events upon maturation of oocytes of domestic bitches. J. Reprod. Fertil. 51, 83–91.Google ScholarPubMed
Hidalgo, C.O., Gómez, E., Prieto, L., Duque, P., Goyache, F., Fernández, L., Fernández, I., Facal, N. & Díez, C. (2004). Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer. Theriogenology 62, 664–76.Google Scholar
Hirao, Y. (2011). Conditions affecting growth and developmental competence of mammalian oocytes in vitro . Anim. Sci. J. 82, 187–97.Google Scholar
Ikawa, M., Inoue, N., Benham, A.M. & Okabe, M. (2010). Fertilization: a sperm's journey to and interaction with the oocyte. J. Clin. Invest. 120, 984–94.Google Scholar
Jackowska, M., Kempisty, B., Antosik, P., Bukowska, D., Budna, J., Lianeri, M., Rosińska, E., Woźna, M., Jagodziński, P.P. & Jaśkowski, J.M. (2009). The morphology of porcine oocytes is associated with zona pellucida glycoprotein transcript contents. Reprod. Biol. 9, 79–85.CrossRefGoogle ScholarPubMed
Kempisty, B., Jackowska, M., Piotrowska, H., Antosik, P., Woźna, M., Bukowska, D., Brüssow, K.P. & Jaśkowski, J.M. (2011). Zona pellucida glycoprotein 3 (pZP3) and integrin β2 (ITGB2) mRNA and protein expression in porcine oocytes after single and double exposure to brilliant cresyl blue test. Theriogenology 75, 1525–35.Google Scholar
Kempisty, B., Woźna, M., Piotrowska, H., Bukowska, D., Jackowska, M., Antosik, P., Jaśkowski, J.M. & Brüssow, K.P. (2012). The expression of genes encoding zona pellucida glycoproteins in canine cumulus–oocyte complexes cultured in vitro in media supplemented with progesterone and estradiol. Theriogenology 77, 684–93.Google Scholar
Kölle, S., Dubois, C.S., Caillaud, M., Lahuec, C., Sinowatz, F. & Goudet, G. (2007). Equine zona protein synthesis and ZP structure during folliculogenesis, oocyte maturation, and embryogenesis. Mol. Reprod. Dev. 74, 851–9.Google Scholar
Krisher, R.L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82 E-Suppl., E14–23.Google ScholarPubMed
Luvoni, G.C., Luciano, A.M., Modina, S. & Gandolfi, F. (2001). Influence of different stages of the oestrous cycle on cumulus-oocyte communications in canine oocytes: effects on the efficiency of in vitro maturation. J. Reprod. Fertil. Suppl. 57, 141–6.Google ScholarPubMed
Martinova, Y., Petrov, M., Mollova, M., Rashev, P. & Ivanova, M. (2008). Ultrastructural study of cat zona pellucida during oocyte maturation and fertilization. Anim. Reprod. Sci. 108, 425–34.Google Scholar
Michelmann, H.W., Rath, D., Töpfer-Petersen, E. & Schwartz, P. (2007). Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis. Reprod. Domest. Anim. 42, 594–602.Google Scholar
Nickson, D.A., Boyd, J.S., Eckersall, P.D., Ferguson, J.M., Harvey, M.J. & Renton, J.P. (1993). Molecular biological methods for monitoring oocyte maturation and in vitro fertilization in bitches. J. Reprod. Fertil. Suppl. 47, 231–40.Google Scholar
Otoi, T., Murakami, M., Fujii, M., Tanaka, M., Ooka, A., Une, S. & Suzuki, T. (2000). Development of canine oocytes matured and fertilized in vitro . Vet. Rec. 146, 52–3.Google Scholar
Otoi, T., Willingham, L., Shin, T., Kraemer, D.C. & Westhusin, M. (2002). Effects of oocyte culture density on meiotic competence of canine oocytes. Reproduction 124, 775–81.Google Scholar
Otoi, T., Shin, T., Kraemer, D. & Westhusin, M.E. (2004). Influence of maturation culture period on the development of canine oocytes after in vitro maturation and fertilization. Reprod. Nutr. Dev. 44, 631–7.Google Scholar
Parillo, F. & Verini Supplizi, A. (1999). Glycohistochemical investigation of canine and feline zonae pellucidae of preantral and antral oocytes. Acta Histochem. 101, 127–46.Google Scholar
Parillo, F., Zelli, R., Verini Supplizi, A., Fagioli, O. & Gargiulo, A.M. (2005). Topographical localisation of glucidic residues and their variations in the canine zona pellucida during folliculogenesis. J. Mol. Histol. 36, 131–7.CrossRefGoogle ScholarPubMed
Rankin, T.L., O’Brien, M., Lee, E., Wigglesworth, K., Eppig, J. & Dean, J. (2001). Defective zonae pellucidae in ZP2-null mice disrupt folliculogenesis, fertility and development. Development 128, 1119–26.Google Scholar
Rath, D., Töpfer-Petersen, E., Michelmann, H.W., Schwartz, P., von Witzendorff, D., Ebeling, S., Ekhlasi-Hundrieser, M., Piehler, E., Petrunkina, A. & Romar, R. (2006). Structural, biochemical and functional aspects of sperm-oocyte interactions in pigs. Soc. Reprod. Fertil. Suppl. 62, 317–30.Google ScholarPubMed
Reynaud, K., Fontbonne, A., Marseloo, N., Viaris de Lesegno, C., Saint-Dizier, M. & Chastant-Maillard, S. (2006). In vivo canine oocyte maturation, fertilization and early embryogenesis: a review. Theriogenology 66,1685–93.Google Scholar
Rodrigues, B.A. & Rodrigues, J.L. (2010). In vitro maturation of canine oocytes: a unique conundrum. Anim. Reprod. 7, 3–15.Google Scholar
Rodrigues Bde, A., dos Santos, L.C. & Rodrigues, J.L. (2004). Embryonic development of in vitro matured and in vitro fertilized dog oocytes. Mol. Reprod. Dev. 67, 215–23.Google Scholar
Schwartz, P., Magerkurth, C. & Michelmann, H.W. (1996). Scanning electron microscopy of the zona pellucida of human oocytes during intracytoplasmic sperm injection (ICSI). Hum. Reprod. 11, 2693–6.Google Scholar
Sirard, M.A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.CrossRefGoogle ScholarPubMed
Songsasen, N. & Wildt, D.E. (2007). Oocyte biology and challenges in developing in vitro maturation systems in the domestic dog. Anim. Reprod. Sci. 98, 2–22.Google Scholar
St John, J.C. (2002). The transmission of mitochondrial DNA following assisted reproductive techniques. Theriogenology 57, 109–23.Google Scholar
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A. & Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68, S131–7.Google Scholar
von Witzendorff, D., Ekhlasi-Hundrieser, M., Dostalova, Z., Resch, M., Rath, D., Michelmann, H.W. & Töpfer-Petersen, E. (2005). Analysis of N-linked glycans of porcine zona pellucida glycoprotein ZPA by MALDI-TOF MS: a contribution to understanding zona pellucida structure. Glycobiology 15, 475–88.CrossRefGoogle Scholar
Willingham-Rocky, L.A., Hinrichs, K., Westhusin, M.E. & Kraemer, D.C. (2003). Effects of stage of oestrous cycle and progesterone supplementation during culture on maturation of canine oocytes in vitro . Reproduction 126, 501–8.Google Scholar
Yuan, Y. & Krisher, R.L. (2012). In vitro maturation (IVM) of porcine oocytes. Methods Mol. Biol. 825, 183–98.Google Scholar
Yuan, Y.Q., Van Soom, A., Leroy, J.L., Dewulf, J., Van Zeveren, A., de Kruif, A. & Peelman, L.J. (2005). Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63, 2147–63.Google Scholar