Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM
Christopher G. Grupen A C and David T. Armstrong BA Faculty of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.
B Research Centre for Reproductive Health, School of Paediatrics and Reproductive Health, The University of Adelaide, Adelaide, SA 5005, Australia.
C Corresponding author. Email: cgrupen@vetsci.usyd.edu.au
Reproduction, Fertility and Development 22(7) 1100-1109 https://doi.org/10.1071/RD09307
Submitted: 16 December 2009 Accepted: 22 February 2010 Published: 20 August 2010
Abstract
The objective of the present study was to determine the temporal effects of sow follicular fluid (FF) in vitro on cumulus cell viability and function, as well as oocyte nuclear and cytoplasmic maturation. Cumulus–oocyte complexes (COCs) recovered from the ovaries of prepubertal pigs were matured in medium with (+FF) or without (–FF) follicular fluid for the first 22 h of IVM. At 22 h of IVM, each group of COCs was then transferred to medium with or without FF and matured for another 22 h, forming four treatment groups (–FF/–FF, –FF/+FF, +FF/–FF and +FF/+FF). The concentration of progesterone in spent IVM medium and the incidence of cumulus cell apoptosis in individual COCs were determined at 22 and 44 h of IVM. Cumulus expansion was also recorded at 44 h of IVM. Finally, the ability of oocytes to complete meiosis to the MII stage and form blastocysts after IVF and embryo culture was assessed. Maturation with FF for part or the whole of IVM increased cumulus expansion and progesterone production and decreased the incidence of cumulus cell apoptosis compared with the –FF/–FF group (P < 0.05). The changes were greatest for the +FF/+FF group and intermediate for the –FF/+FF and +FF/–FF groups. Regression analysis revealed a negative association between cumulus cell progesterone production and the incidence of cumulus cell apoptosis (P < 0.001). Meiotic maturation was enhanced when FF was present during the first half of IVM. Oocytes matured in the presence of FF during the first and/or second half of IVM displayed an increased ability to form blastocysts compared with the –FF/–FF group (P < 0.05). The extent of the increase was similar for all FF-supplemented groups. The results show that FF exerts several beneficial effects at different times during IVM and suggest that a major role of FF is to provide protection from oxidative stress. We propose that the incidence of cumulus cell apoptosis in COCs must be kept below a certain threshold to ensure adequate functionality, including steroidogenic activity, is maintained for the acquisition of oocyte developmental competence.
Additional keywords: blastocyst, cumulus expansion, embryo development, fertilisation, meiosis.
Acknowledgements
The authors gratefully acknowledge Tamer Hussein for assessment of cumulus cell apoptosis, Samantha Schulz for technical assistance and Glyn Naylor for the collection of ovaries. The authors also thank the staff of Big River Pork (Murray Bridge, SA, Australia) for supplying the ovaries. This work was funded by grants from the National Health and Medical Research Council of Australia and the Canadian Institutes for Health Research (grant no. MT-14400).
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