Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T17:35:14.980Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental competence of Dromedary camel (Camelus dromedarius) oocytes selected using brilliant cresyl blue staining

Published online by Cambridge University Press:  11 July 2017

Mohamed Fathi ,
Mohamed Ashry ,
Ali Salama  and
Magdy R. Badr
Mohamed Fathi
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt.
Mohamed Ashry*
Affiliation:
B275 Anthony Hall, department of Animal Science, Michigan State University, East Lansing, MI 48824, USA. Laboratory of Mammalian Reproductive Biology, Department of Animal Science, Michigan State University, USA.
Ali Salama
Affiliation:
Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt.
Magdy R. Badr
Affiliation:
Department of Artificial Insemination and Embryo Transfer, Animal Reproduction Research Institute, Agriculture Research Centre, Giza, Egypt.
*
All correspondence to: M. Ashry: B275 Anthony Hall, department of Animal Science, Michigan State University, East Lansing, MI 48824, USA. E-mail: ashry@cu.edu.eg
Get access Rights & Permissions [Opens in a new window]

Summary

The objectives of the present studies were to investigate the developmental capacity of dromedary camel oocytes selected by brilliant cresyl blue (BCB) staining and to investigate the expression of select transcripts in germinal vesicle (GV) stage oocytes. These transcripts included BMP15 and GDF9 as important transcripts for folliculogenesis and oocyte development, Zar1 and Mater as maternal transcripts required for embryonic development, Cyclin B1 and CDK1 as cell cycle regulators and Oct4 and STAT3 as transcription factors. Dromedary camel oocytes were retrieved from ovaries collected at a local slaughterhouse. After exposure to BCB staining, cumulus–oocyte complexes (COCs) from BCB+, BCB− and control (selected based on morphological criteria) groups were subjected to in vitro maturation, in vitro fertilization and in vitro culture. For gene expression studies, after BCB staining cumulus cells were stripped off and the completely denuded GV stage oocytes were used for RT-PCR analysis of selected transcripts. BCB+ oocytes showed higher maturation, and fertilization rates compared with BCB− and control groups. Indices of early embryonic development, namely, cleavage at 48 hours post insemination (hpi), and development to morula at day 5 and day 7 blastocyst rates were also significantly higher in the BCB+ group. RT-PCR revealed a higher expression of BMP15, GDF9, Zar1, Mater, Cyclin B1, CDK1, OCT4 and STAT3 in good quality oocytes that stained positively for BCB (BCB+). Collectively, results provide novel information about the use of BCB screening for selecting good quality oocytes to improve in vitro embryo production in the dromedary camel.

Keywords

BCBBrilliant cresyl blueDromedary camelOocytesGene expression
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 529 - 536
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

5

These authors contributed equally to this work.

References

Alcoba, D. D., Conzatti, M., Ferreira, G. D., Pimentel, A. M., Kussler, A. P., Capp, E., von Eye Corleta, H. & Brum, I.S. (2016). Safety of brilliant cresyl blue staining protocols on human granulosa and cumulus cells. Zygote 24, 83–8.CrossRefGoogle ScholarPubMed
Alcoba, D. D., Schneider, J., Arruda, L., Martiny, P. B., Capp, E., von Eye Corleta, H. & Brum, I.S. (2017). Brilliant cresyl blue staining does not present cytotoxic effects on human luteinized follicular cells, according to gene/protein expression, as well as to cytotoxicity tests. Reprod. Biol. 17, 60–8.CrossRefGoogle Scholar
Alm, H., Torner, H., Lohrke, B., Viergutz, T., Ghoneim, I.M. & Kanitz, W. (2005). Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 63, 2194–205.CrossRefGoogle ScholarPubMed
Ashry, M., Lee, K., Mondal, M., Datta, T. K., Folger, J. K., Rajput, S. K., Zhang, K., Hemeida, N.A. & Smith, G.W. (2015). Expression of TGFbeta superfamily components and other markers of oocyte quality in oocytes selected by brilliant cresyl blue staining: Relevance to early embryonic development. Mol. Reprod. Dev. 82, 251–64.CrossRefGoogle ScholarPubMed
Ashry, M. & Smith, G.W. (2015). Application of embryo transfer using in vitro produced embryos: intrinsic factors affecting efficiency. Cattle Practice 23, 1–8.Google 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, 301–9.CrossRefGoogle ScholarPubMed
Bhojwani, S., Alm, H., Torner, H., Kanitz, W. & Poehland, R. (2007). Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer. Theriogenology 67, 341–5.CrossRefGoogle ScholarPubMed
Castedo, M., Perfettini, J. L., Roumier, T. & Kroemer, G. (2002). Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ. 9, 1287–93.CrossRefGoogle ScholarPubMed
Catalá, M. G., Izquierdo, D., Uzbekova, S., Morato, R., Roura, M., Romaguera, R., Papillier, P. & Paramio, M.T. (2011). Brilliant cresyl blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction 142, 517–27.CrossRefGoogle ScholarPubMed
Catalá, M. G., Roura, M., Izquierdo, D., Hammammi, S., Uzbekova, B.S. & Paramio, T.M. (2013). Relative mRNA expression of 4 candidates in lamb oocytes selected by brilliant cresyl blue staining. In 39th Annual Conference of the IETS (Reproduction Fertility and Development, 25). p. 46. Presented at 39th Annual Conference of the IETS, Hannover. Collingwood, AUS, CSIRO Publishing.Google Scholar
Chang, H., Brown, C.W. & Matzuk, M.M. (2002). Genetic analysis of the mammalian transforming growth factor-β superfamily. Endocrine Rev. 23, 787–823.CrossRefGoogle ScholarPubMed
El-Sayed, A. (2013). Comparative analysis of genes related to quality of oocyte in buffaloes (Bubalus bubalis) and camels (Camelus dromedarius) under in vitro conditions. Egyptian J. Anim. Prod. 50, 116–21.Google Scholar
El-Sayed, A. & Ghanem, N. (2015). Gene expression analysis of selected candidate genes in camel oocytes (Camelus dromedarius). with different quality based on morphological assessment. In Proceedings of the International Camel Conference, Al-Hasa, Saudi Arabia, 17–20 February 2013 Camel Publishing House, pp. 324–38.Google Scholar
El Shourbagy, S. H., Spikings, E. C., Freitas, M. & St John, J.C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–45.CrossRefGoogle ScholarPubMed
Ericsson, S., Boice, M., Funahashi, H. & Day, B. (1993). Assessment of porcine oocytes using brilliant cresyl blue. Theriogenology 39, 214.CrossRefGoogle Scholar
Fathi, M., Seida, A. A., Sobhy, R. R., Darwish, G. M., Badr, M.R. & Moawad, A.R. (2014). Caffeine supplementation during IVM improves frequencies of nuclear maturation and preimplantation development of dromedary camel oocytes following IVF. Theriogenology 81, 1286–92.CrossRefGoogle ScholarPubMed
Ishizaki, C., Watanabe, H., Bhuiyan, M.M. & Fukui, Y. (2009). Developmental competence of porcine oocytes selected by brilliant cresyl blue and matured individually in a chemically defined culture medium. Theriogenology 72, 72–80.CrossRefGoogle Scholar
Khatir, H., Anouassi, A. & Tibary, A. (2007). Quality and developmental ability of dromedary (Camelus dromedarius) embryos obtained by IVM/IVF, in vivo matured/IVF or in vivo matured/fertilized oocytes. Reprod. Domest. Anim. 42, 263–70.CrossRefGoogle ScholarPubMed
Li, Y., Li, R.-Q., Ou, S.-B., Zhang, N.-F., Ren, L., Wei, L.-N., Zhang, Q.-X. & Yang, D.-Z. (2014). Increased GDF9 and BMP15 mRNA levels in cumulus granulosa cells correlate with oocyte maturation, fertilization, and embryo quality in humans. Reprod. Biol. Endocrinol. 12, 81.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− Δ Δ C t method. Methods 25, 402–8.CrossRefGoogle ScholarPubMed
Mangia, F. & Epstein, C.J. (1975). Biochemical studies of growing mouse oocytes: preparation of oocytes and analysis of glucose-6-phosphate dehydrogenase and lactate dehydrogenase activities. Dev. Biol. 45, 211–20.CrossRefGoogle ScholarPubMed
Manjunatha, B. M., Gupta, P. S., Devaraj, M., Ravindra, J.P. & Nandi, S. (2007). Selection of developmentally competent buffalo oocytes by brilliant cresyl blue staining before IVM. Theriogenology 68, 1299–304.CrossRefGoogle ScholarPubMed
May-Panloup, P., Vignon, X., Chretien, M. F., Heyman, Y., Tamassia, M., Malthiery, Y. & Reynier, P. (2005). Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors. Reprod. Biol. Endocrinol. 3, 65.CrossRefGoogle ScholarPubMed
McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., Lawrence, S. B., Western, A., Meerasahib, M. F., Mottershead, D. G., Groome, N. P., Ritvos, O. & Laitinen, M.P. (2005). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129, 481–7.CrossRefGoogle ScholarPubMed
Moawad, A. R., Darwish, G. M., Badr, M.R. & El-Wishy, A.B. (2011). In vitro fertilization of dromedary camel (Camelus dromedarius) oocytes with epididymal spermatozoa. Reprod. Fertil. Dev. 24, 192–3.CrossRefGoogle Scholar
Opiela, J., Lipinski, D., Slomski, R. & Katska-Ksiazkiewicz, L. (2010). Transcript expression of mitochondria related genes is correlated with bovine oocyte selection by BCB test. Anim. Reprod. Sci. 118, 188–93.CrossRefGoogle Scholar
Pereira, G. R., Lorenzo, P. L., Carneiro, G. F., Bilodeau-Goeseels, S., Kastelic, J. P., Esteller-Vico, A., Lopez-Bejar, M. & Liu, I.K. (2014). Selection of developmentally competent immature equine oocytes with brilliant cresyl blue stain prior to in vitro maturation with equine growth hormone. Zygote 22, 500–4.CrossRefGoogle ScholarPubMed
Pujol, M., Lopez-Bejar, M. & Paramio, M.T. (2004). Developmental competence of heifer oocytes selected using the brilliant cresyl blue (BCB) test. Theriogenology 61, 735–44.CrossRefGoogle ScholarPubMed
Roca, J., Martinez, E., Vazquez, J.M. & Lucas, X. (1998). Selection of immature pig oocytes for homologous in vitro penetration assays with the brilliant cresyl blue test. Reprod. Fertil. Dev. 10, 479–85.CrossRefGoogle ScholarPubMed
Rodrigues, B. A., Rodriguez, P., Silva, A. E., Cavalcante, L. F., Feltrin, C. & Rodrigues, J.L. (2009). Preliminary study in immature canine oocytes stained with brilliant cresyl blue and obtained from bitches with low and high progesterone serum profiles. Reprod. Domest. Anim. 44 (Suppl. 2), 255–8.CrossRefGoogle ScholarPubMed
Rodriguez-Gonzalez, E., Lopez-Bejar, M., Velilla, E. & Paramio, M.T. (2002). Selection of prepubertal goat oocytes using the brilliant cresyl blue test. Theriogenology 57, 1397–409.CrossRefGoogle ScholarPubMed
Silva, D. S., Rodriguez, P., Galuppo, A., Arruda, N.S. & Rodrigues, J.L. (2013). Selection of bovine oocytes by brilliant cresyl blue staining: effect on meiosis progression, organelle distribution and embryo development. Zygote 21, 250–5.CrossRefGoogle ScholarPubMed
Spikings, E. C., Alderson, J. & St John, J.C. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biol. Reprod. 76, 327–35.CrossRefGoogle ScholarPubMed
Teng, C. B., Diao, H. L., Ma, X. H., Xu, L.B. & Yang, Z.M. (2004). Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol. Reprod. Dev. 69, 1–10.CrossRefGoogle ScholarPubMed
Tian, W. N., Braunstein, L. D., Pang, J., Stuhlmeier, K. M., Xi, Q. C., Tian, X. & Stanton, R.C. (1998). Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J. Biol. Chem. 273, 10609–17.CrossRefGoogle ScholarPubMed
Uzbekova, S., Roy-Sabau, M., Dalbies-Tran, R., Perreau, C., Papillier, P., Mompart, F., Thelie, A., Pennetier, S., Cognie, J., Cadoret, V., Royere, D., Monget, P. & Mermillod, P. (2006). Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.CrossRefGoogle ScholarPubMed
Wang, L., Lin, J., Huang, J., Wang, J., Zhao, Y. & Chen, T. (2012). Selection of ovine oocytes by brilliant cresyl blue staining. J. Biomed. Biotechnol. 2012, 161372.CrossRefGoogle ScholarPubMed
Wassarman, P.M. (1988). The mammalian ovum. In Knobil and Neill's Physiology of Reproduction vol. 3 (ed. Neill, J.D.), pp. 62–102. Elsevier. Academic Press.Google Scholar
Wu, G. & Scholer, H.R. (2014). Role of Oct4 in the early embryo development. Cell. Regen. (Lond), 3, 7.CrossRefGoogle ScholarPubMed
Wu, Y. G., Liu, Y., Zhou, P., Lan, G. C., Han, D., Miao, D.Q. & Tan, J.H. (2007a). Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: a study using the mouse model. Cell Res. 17, 722–31.CrossRefGoogle ScholarPubMed
Wu, Y. T., Tang, L., Cai, J., Lu, X. E., Xu, J., Zhu, X. M., Luo, Q. & Huang, H.F. (2007b). High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum. Reprod. 22, 1526–31.CrossRefGoogle ScholarPubMed