Hostname: page-component-7479d7b7d-qlrfm Total loading time: 0 Render date: 2024-07-12T00:52:30.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental competence of different quality bovine oocytes retrieved through ovum pick-up following in vitro maturation and fertilization

Published online by Cambridge University Press:  13 July 2015

N. Saini ,
M. K. Singh ,
S. M. Shah ,
K. P. Singh ,
R. Kaushik ,
R. S. Manik ,
S. K. Singla ,
P. Palta  and
M. S. Chauhan
N. Saini
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
M. K. Singh
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
S. M. Shah
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
K. P. Singh
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
R. Kaushik
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
R. S. Manik
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
S. K. Singla
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
P. Palta
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
M. S. Chauhan*
Affiliation:
Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001, Haryana, India
*
†E-mail: chauhanabtc@gmail.com
Get access

Abstract

In the present study, oocytes retrieved from cross bred Karan Fries cows by ovum pick-up technique were graded into Group 1 and Group 2, based on the morphological appearance of the individual cumulus–oocyte complexes (COCs). To analyze whether the developmental potential of the COCs bears a relation to morphological appearance, relative expression of a panel of genes associated with; (a) cumulus–oocyte interaction (Cx43, Cx37, GDF9 and BMP15), (b) fertilization (ZP2 and ZP3), (c) embryonic development (HSF1, ZAR1 and bFGF) and (d) apoptosis and survival (BAX, BID and BCL-XL, MCL-1, respectively) was studied at two stages: germinal vesicle (GV) stage and after in vitro maturation. The competence was further corroborated by evaluating the embryonic progression of the presumed zygotes obtained from fertilization of the graded COCs. The gene expression profile and development rate in pooled A and B grade (Group 1) COCs and pooled C and D grade (Group 2) COCs were determined and compared according to the original grades. The results of the study demonstrated that the morphologically characterized Group 2 COCs showed significantly (P<0.05) lower expression for most of the genes related to cumulus–oocyte interplay, fertilization and embryonic development, both at GV stage as well as after maturation. Group 1 COCs also showed greater expression of anti-apoptotic genes (BCL-XL and MCL1) both at GV stage and after maturation, while pro-apoptotic genes (BAX and BID) showed significantly (P<0.05) elevated expression in poor quality COCs at both the stages. The cleavage rate in Group 1 COCs was significantly higher than that of Group 2 (74.46±7.06 v. 31.57±5.32%). The development of the presumed zygotes in Group 2 oocytes proceeded up to 8- to 16-cell stages only, while in Group 1 it progressed up to morulae (35.38±7.11%) and blastocyst stages (9.70±3.15%), indicating their better developmental potential.

Keywords

ovum pick-upin vitro fertilizationdevelopmental competenceKaran friesbovinegene expression
Type
Research Article
Information
animal , Volume 9 , Supplement 12 , December 2015 , pp. 1979 - 1985
Copyright
© The Animal Consortium 2015 

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

Ackert, CL, Gittens, JE, O’Brien, MJ, Eppig, JJ and Kidder, GM 2001. Intercellular communication via connexin 43 gap junctions is required for ovarian folliculogenesis in the mouse. Developmental Biology 233, 258–270.CrossRefGoogle ScholarPubMed
Adona, PR, de Bem, T, Mesquita, L, Rochetti, R and Leal, C 2010. Embryonic development and gene expression in oocytes cultured in vitro in supplemented pre-maturation and maturation media. Reproduction in Domestic Animals 46, e31–38, doi:10.1111/j.1439-0531.2010.0168.x.Google Scholar
Bols, PEJ, Ysebaert, MT, Van Soom, A and de Kruif, A 1997. Effects of needle tip bevel and aspiration procedure on the morphology and developmental capacity of bovine compact cumulus oocyte complexes. Theriogenology 47, 1221–1236.CrossRefGoogle ScholarPubMed
Bols, PEJ, Van Soom, A, Ysebaert, MT, Vandenheede, JMM and de Kruif, A 1996. Effects of aspiration vacuum and needle diameter on cumulus oocyte complex morphology and developmental capacity of bovine oocytes. Theriogenology 45, 1001–1014.CrossRefGoogle ScholarPubMed
Bols, PEJ, Jorssen, EPA, Goovaerts, IGF, Langbeen, A and JLMR, Leroy 2012. High throughput non-invasive oocyte quality assessment: the search continues. Animal Reproduction 9, 420–425.Google Scholar
Chauhan, MS, Singla, SK, Palta, P, Manik, RS and Madan, ML 1998. In vitro maturation and fertilization, and subsequent development of buffalo (Bubalus bubalis) embryos: effects of oocyte quality and type of serum. Reproduction, Fertility and Development 10, 173–177.CrossRefGoogle ScholarPubMed
Chang, HY and Yang, X 2000. Proteases for cell suicide: functions and regulation of gcaspases. Microbiology and Molecular Biology Reviews 64, 821–846.CrossRefGoogle Scholar
Chen, S, Costa, Vania and Beja-Pereira, A 2011. Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species. BMC Evolutionary Biology 11, 24.CrossRefGoogle ScholarPubMed
Christians, E, Davis, A, Thomas, SD and Benjamin, IJ 2000. Embryonic development: maternal effect of Hsf1 on reproductive success. Nature 407, 693–694.CrossRefGoogle ScholarPubMed
Duszewska, AM and Reklewski, Z 2000. Reproduction of cattle using the OPU-IVF-ET. Prace i Materialy Zootechniczne 57, 111–120.Google Scholar
Elvin, JA, Clark, AT, Wang, P, Wolfman, NM and Matzuk, MM 1999. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Molecular Endocrinology 13, 1035–1048.CrossRefGoogle ScholarPubMed
Fair, T, Hulshof, S, Hyttel, P, Greve, T and Boland, M 1997. Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Molecular Reproduction and Development 46, 208–215.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Gittens, JE, Mhawi, AA, Lidington, D, Ouellette, Y and Kidder, GM 2003. Functional analysis of gap junctions in ovarian granulosa cells: distinct role for connexin 43 in early stages of folliculogenesis. American Journal of Physiology-Cell Physiology 284, 880–887.CrossRefGoogle ScholarPubMed
Goodenough, D, Goliger, J and Paul, D 1996. Connexins, connexons and intercellular communication. Annual Review of Biochemistry 65, 475–502.CrossRefGoogle ScholarPubMed
Goovaerts, IG, Leroya, JL, Rizos, D, Bermejo-Alvarez, P, Gutierrez-Adan, A, Jorssen, E and Bols, PE 2011. Single in vitro bovine embryo production: coculture with autologous cumulus cells, developmental competence, embryo quality and gene expression profiles. Theriogenology 76, 1293–1303.CrossRefGoogle ScholarPubMed
Gospodarowicz, D, Cheng, J, Lui, GM and Bohlen, P 1985. Corpus luteum angiogenic factor is related to fibroblast growth factor. Endocrinology 117, 201.CrossRefGoogle ScholarPubMed
Granot, I and Dekel, N 2002. The ovarian gap junction protein connexin 43: regulation by gonadotropins. Trends in Endocrinology and Metabolism 13, 310–313.CrossRefGoogle ScholarPubMed
Jin, Y, Li, J, Choi, S, Choi, S, Kim, T, Cui, X and Kim, N 2007. Heat shock inducing apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro. Animal Reproduction Science 100, 118–127.CrossRefGoogle ScholarPubMed
Kovanci, E, Rohozinski, J, Simpson, J, Michael, J, Colin, E, Bishop, P, Sandra, A and Carson, M 2006. Growth differentiating factor-9 mutations may be associated with premature ovarian failure. Fertility and Sterility 18, 143–146.Google Scholar
Leader, B, Lim, H, Carabatsos, M, Harrington, A, Ecsedy, J, Pellman, D, Mass, R and Leder, P 2002. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nature Cell Biology 4, 921–928.CrossRefGoogle ScholarPubMed
Liang, XW, Lu, YQ, Chen, MT, Zhang, XF, Lu, SS, Zhang, M, Pang, CY, Huang, FX and Lu, KH 2008. In vitro embryo production in buffalo (Bubalus bubalis) using sexed sperm and oocytes from ovum pick up. Theriogenology 69, 822–826.CrossRefGoogle ScholarPubMed
Manik, RS, Chauhan, MS, Singla, SK and Palta, P 2002. Transvaginal ultrasound-guided aspiration of follicles from Indian buffaloes (Bubalus bubalis) with reproductive problems. Veterinary Record 150, 22–24.CrossRefGoogle ScholarPubMed
Merton, J, Knijn, H, Flapper, H, Dotinga, F, Roelen, B, Vos, P and Mullaart, E 2013. Cysteamine supplementation during in vitro maturation of slaughterhouse- and OPU-derived bovine oocytes improves embryonic development without affecting cryotolerance, pregnancy rate, and calf characteristics. Theriogenology 80, 365–371.CrossRefGoogle ScholarPubMed
Moore, RK and Shimasaki, S 2005. Molecular biology and physiological role of the oocyte factor, BMP-15. Molecular and Cellular Endocrinology 234, 67–73.CrossRefGoogle ScholarPubMed
Nilsson, E, Parrott, JA and Skinner, MK 2001. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Molecular and Cellular Endocrinology 175, 123–130.CrossRefGoogle ScholarPubMed
Otsuka, F, Tavish, K and Shimasaki, S 2011. Integral role of GDF-9 and BMP-15 in ovarian function. Molecular Reproduction and Development 78, 9–21.CrossRefGoogle ScholarPubMed
Otsuka, F, Yao, Z, Lee, T, Yamamoto, S, Erickson, G and Shimasaki, S 2000. Bone morphogenetic protein-15. Identification of target cells and biological functions. The Journal of Biological Chemistry 275, 39523–39528.CrossRefGoogle ScholarPubMed
Pontes, J, Melo Sterza, F, Basso, A, Ferreira, C, Sanches, B, Rubin, K and Seneda, M 2011. Ovum pick up, in vitro embryo production, and pregnancy rates from a large-scale commercial program using Nelore cattle (Bos indicus) donors. Theriogenology 75, 1640–1646.CrossRefGoogle ScholarPubMed
Romar, R, Santis, T, Papillier, P, Perreau, C, Thelie, A, Dell Aquila, M, Mermillod, P and Dalbies-Tran, R 2011. Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reproduction in Domestic Animals 46, e23--30, doi:10.1111/j.1439-0531.2010.01617.x.CrossRefGoogle ScholarPubMed
Schmittgen, TD and Livak, KJ 2008. Analyzing real-time PCR data by the comparative C(t) method. Nature Protocols 3, 1101–1108.CrossRefGoogle ScholarPubMed
Shah, SM, Saini, N, Ashraf, S, Zandi, M, Manik, RS, Suresh, SK, Palta, P and Chauhan, MS 2015. Comparative expression analysis of gametogenesis associated genes in fetal and adult bubaline (Bubalus bubalis) ovaries and testes. Reproduction in Domestic Animals 50, 365–377.CrossRefGoogle ScholarPubMed
Simon, AM, Goodenough, DA, Li, E and Paul, DL 1997. Female infertility in mice lacking connexin 37. Nature 385, 525–529.CrossRefGoogle ScholarPubMed
Soyal, S, Amlech, A and Dean, J 2000. FIG-alpha, a germ cell specific transcription factor required for ovarian follicle formation. Development 127, 4645–4654.CrossRefGoogle ScholarPubMed
Su, L, Yang, S, He, X, Li, X, Ma, J, Wang, Y, Presicce, G and Ji, W 2012. Effect of donor age on the developmental competence of bovine oocytes retrieved by ovum pick up. Reproduction in Domestic Animals 47, 184–189.CrossRefGoogle ScholarPubMed
Tilly, JL, Billig, H, Kowalski, KI and Hsueh, AJ 1992. Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine kinase-dependent mechanism. Molecular Endocrinology 6, 1942–1950.Google ScholarPubMed
Tong, ZB, Gold, L, Pfeifer, KE, Dorward, H, Lee, E, Bondy, CA, Dean, J and Nelson, LM 2000. Mater, a maternal effect gene required for early embryonic development in mice. Nature Genetics 26, 267–268.CrossRefGoogle Scholar
Wu, X, Viveiros, MM, Eppig, JJ, Bai, Y, Fitzpatrick, SL and Matzuk, MM 2003. Zygote arrest1 (Zar1) is a novel maternal effect gene critical for the oocyte-to-embryo transition. Nature Genetics 33, 187–191.CrossRefGoogle Scholar
Supplementary material: File

Saini supplementary material

Table S1

Download Saini supplementary material(File)
File 13.9 KB