Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-19T00:36:03.805Z Has data issue: false hasContentIssue false
  • English
  • Français

Propensity in low-grade oocytes for delayed germinal vesicle breakdown compromises the developmental ability of sub-optimal grade Bubalus bubalis oocytes

Published online by Cambridge University Press:  05 October 2018

Manish Kumar ,
Mona Faraji ,
Parul Sarwalia ,
Sandeep Kumar ,
Moloya Gohain ,
Sachinandan De ,
Rakesh Kumar Open the ORCID record for Rakesh Kumar [Opens in a new window]  and
T K Datta
Manish Kumar
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
Mona Faraji
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
Parul Sarwalia
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
Sandeep Kumar
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
Moloya Gohain
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia Institute of Plant and Microbial Biology (IPMB) Sec 128, Academia Road, Nangang District, Taipei City – 11529Taiwan
Sachinandan De
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
Rakesh Kumar
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
T K Datta*
Affiliation:
Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal – 132001HaryanaIndia
*
*Author for correspondence: T K Datta. Animal Genomics Laboratory, Animal Biotechnology Centre, National Dairy Research Institute, Karnal 132001 Haryana India. Tel: +91 184 2259506. Fax: +91 184 2250042. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Maturing oocytes have diverse developmental potential and good quality oocytes exhibit a better ability to attain physiological milestones in a time-dependent manner. This situation necessitates the confirmation of oocyte developmental status more precisely under an in vitro embryo production (IVEP) regime. The aim of this study was to explain timely events in germinal vesicle breakdown (GVBD), an important milestone of oocyte nuclear maturation, to delineate the developmental capacity of Bubalus bubalis oocytes. In addition, the expression profile of genes responsible for GVBD was assessed in order to understand the molecular context responsible for GVBD. The chronology of GVBD events at different time intervals during in vitro maturation (IVM) suggests that the rate at which oocytes undergo GVBD was strikingly different in the brilliant cresyl blue (BCB)+ and BCB− groups. The expression of AKT and CDC25B genes for BCB+ oocytes was maximum at 8 h of IVM, and CCNB (cyclin B) peaked at around 10 h, which suggested that GVBD was finished after 10 h in BCB+ oocytes, whereas the expression of AKT and CDC25B was found to peak at around 12–14 h of IVM. This difference consequently delays the GVBD event by 2–4 h in BCB− oocytes. Poor abundance of gene transcripts was mainly implicated in delay and lower rate of GVBD in BCB− oocytes which in turn strongly affected the translational ability of oocytes to blastocysts. The findings of this study support the idea that there is a propensity in sub-optimal grade oocytes for delayed GVBD that compromises the developmental ability of low grade buffalo oocytes. The study highlights the very small, but importantly vital and separate, time window of the GVBD event during which the competence levels of buffalo oocytes are altered along with their translational ability to develop into the prospective embryos.

Keywords

Aceto-orcein stainingBrilliant cresyl blueGVBDOocyte competence
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 359 - 365
Copyright
© Cambridge University Press 2018 

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

*

These authors contributed equally to this work.

References

Alm, H, Torner, H, Loehrke, B, Viergutz, T, Ghoneim, IM Kanitz, W (2005) Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brilliant cresyl blue staining before IVM as indicator for glucose 6-phosphate dehydrogenase activity. Theriogenology 63, 2194–2205.Google Scholar
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, 341–345.Google Scholar
Brackett, BG Zuelke, KA (1993) Analysis of factors involved in the in vitro production of bovine embryos. Theriogenology 39, 43–64.Google Scholar
Brevini-Gandolfi, TA Gandolfi, F (2001) The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–1276.Google Scholar
Catala, MG, Izquierdo, D, Uzbekova, S, Morato, R, Roura, M, Romaguera, R, Papillier, P Paramio, T (2011) Brilliant cresyl blue (BCB) stain selects largest oocytes with highest mitochondria activity MPF activity and embryo development competence in prepubertal sheep. Reproduction 10, 528.Google Scholar
Chian, RC, Buckett, WM Tan, SL (2004) In-vitro maturation of human oocytes. Reprod Biomed Online 8, 148–166.Google Scholar
Eppig, JJ, Schultz, RM, O’Brien, M Chesnel, F (1994) Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev Biol 164, 1–9.Google Scholar
Gui, L Homer, H (2013) Hec1-dependent cyclin B2 stabilization regulates the G2–M, transition and early prometaphase in mouse oocytes. Dev Cell 25, 43–54.Google Scholar
Holm, P, Shukri, NN, Vajta, G, Booth, P, Bendixen, C Callesen, H (1998) Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology 50, 1285–1299.Google Scholar
Kalous, J, Solc, P, Baran, V, Kubelka, M, Schultz, RM Motlik, J (2006) PKB/Akt is involved in resumption of meiosis in mouse oocytes. Biol Cell 98, 111–123.Google Scholar
Karlsson, S, Burman, LG Akerlund, T (1999) Suppression of toxin production in Clostridium difficile VPI 10463 by amino acids. Microbiology 145, 1683–1693.Google Scholar
Kuroda, T, NaitoK Sugiura, K, Yamashita, M, Takakura, I Tojo, H (2004) Analysis of the roles of cyclin B1 and cyclin B2 in porcine oocyte maturation by inhibiting synthesis with antisense RNA injection. Biol Reprod 70, 154–159.Google Scholar
Levesque, JT Sirard, MA (1996) Resumption of meiosis is initiated by the accumulation of cyclin B in bovine oocytes. Biol Reprod 55, 1427–1436.Google Scholar
Livak, KJ Schmittgen, TD (2001) Analysis of relative gene expression data using real- time quantitative PCR and the 2−ΔΔCT method. Science 25, 402–408.Google Scholar
Lonergan, P, Monaghan, P, Rizos, D, Boland, MP Gordon, I (1994) Effect of follicle size on bovine oocyte quality and developmental competence following maturation fertilization and culture in vitro . Mol Reprod Dev 37, 48–53.Google Scholar
Manjunatha, BM, Gupta, PS, Devaraj, M, Ravindra, JP Nandi, S (2007) Selection of developmentally competent buffalo oocytes by brilliant cresyl blue staining before IVM. Theriogenology 68, 1299–1304.Google Scholar
Manjunatha, BM, Ravindra, JP, Gupta, PSP, Devaraj, M Nandi, S (2009) Effect of breeding season on in vitro oocyte recovery and embryo production in non-descriptive Indian river buffaloes (Bubalus bubalis). Anim Reprod Sci 111, 376–383.Google Scholar
Moor, RM, Dai, Y, Lee, C Fulka, J (1998) Oocyte maturation and embryonic failure. Hum Reprod Update 4, 223–226.Google Scholar
Oh, JS, Han, SJ Conti, M (2010) Wee1B Myt1 and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. J Cell Biol 188, 199–207.Google Scholar
Pavlok, A, Lucas‐Hahn, A Niemann, H (1992) Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol Reprod Dev 31, 63–67.Google Scholar
Prentice, JR Anzar, M (2011) Cryopreservation of mammalian oocyte for conservation of animal genetics. Vet Med Int ID 146405, doi:104061/2011/146405.Google Scholar
Presicce, GA (2007) Reproduction in the water buffalo. Reprod Domest Anim 42, 24–32.Google Scholar
Telford, NA, Watson, AJ Schultz, GA (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26, 90–100.Google Scholar
Torner, H, Ghanem, N, Ambros, C, Holker, M, Tomek, W, Phatsara, C, Alm, H, Sirard, MA, Kanitz, W, Schellander, K Tesfaye, D (2007) Molecular and subcellular characterization of oocytes screened for their developmental competence based on glucose-6 phosphate dehydrogenase activity. Reproduction 135, 197–212.Google Scholar
Westergaard, L, Byskov, AG, Andersen, CY, Grinsted, J McNatty, KP (1984) Is resumption of meiosis in the human preovulatory oocyte triggered by a meiosis-inducing substance (MIS) in the follicular fluid? Fertil Steril 41, 377–384.Google Scholar
Wu, YG, Liu, Y, Zhou, P, Lan, GC, Han, D, Miao, DQ Tan, JH (2007) Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: a study using the mouse model. Cell Res 17, 722–731.Google Scholar