» Articles » PMID: 32182244

Granulosa Secreted Factors Improve the Developmental Competence of Cumulus Oocyte Complexes from Small Antral Follicles in Sheep

Overview
Journal PLoS One
Date 2020 Mar 18
PMID 32182244
Citations 11
Authors
Affiliations
Soon will be listed here.
Abstract

Oocyte in vitro maturation can be improved by mimicking the intra-follicular environment. Oocyte, cumulus cells, granulosa cells, and circulating factors act as meiotic regulators in follicles and maintain oocyte in the meiotic phase until oocyte becomes competent and ready to be ovulated. In a randomized experimental design, an ovine model was used to optimize the standard in vitro maturation media by Granulosa secreted factors. At first, the development capacity of oocyte derived from medium (>4 to 6 mm) and small (2 to ≤4 mm) size follicles was determined. Differential gene expression of granulosa secreted factors and their receptors were compared between the cumulus cells of the two groups. Then, the best time and concentration for arresting oocytes at the germinal vesicle stage by natriuretic peptide type C (CNP) were determined by nuclear staining in both groups. Oocyte quality was further confirmed by calcein uptake and gene expression. The developmental competence of cumulus oocyte complexes derived from small size follicles that were cultured in the presence of CNP in combination with amphiregulin (AREG) and prostaglandin E2 (PGE2) for 24 h was determined. Finally, embryo quality was specified by assessing expressions of NANOG, SOX2, CDX2, OCT4, and TET1. The cumulus oocyte complexes derived from small size follicles had a lower capacity to form blastocyst in comparison with cumulus oocyte complexes derived from medium size follicles. Prostaglandin E receptor 2 and prostaglandin-endoperoxide synthase 2 had significantly lower expression in cumulus cells derived from small size follicles in comparison with cumulus cells derived from medium size follicles. Natriuretic peptide type C increased the percentage of cumulus oocyte complexes arresting at the germinal vesicle stage in both oocytes derived from medium and small follicles. Gap junction communication was also improved in the presence of natriuretic peptide type C. In oocytes derived from small size follicles; best blastocyst rates were achieved by sequential exposure of cumulus oocyte complexes in [TCM+CNP (6 h), then cultured in TCM+AREG+PGE2 (18h)] and [TCM+CNP (6 h), then cultured in conventional IVM supplements+AREG+PGE2 (18h)]. Increased SOX2 expression was observed in [TCM+CNP (6 h), then cultured in TCM+AREG+PGE2 (18h)], while decreased OCT4 expression was observed in [TCM+CNP (6 h), then cultured in conventional IVM supplements+AREG+PGE2 (18h)]. It seems that the natriuretic peptide type C modulates meiotic progression, and oocyte development is probably mediated by amphiregulin and prostaglandin E2. These results may provide an alternative IVM method to optimize in vitro embryo production in sheep and subsequently for humans.

Citing Articles

ρ-Coumaric acid-zinc oxide nanoparticles improve post-thaw quality of goat spermatozoa and developmental competence of fertilized oocytes in vitro.

Akhtarshenas B, Kowsar R, Hajian M, Vash N, Soltani L, Mahdavi A Sci Rep. 2024; 14(1):31971.

PMID: 39738447 PMC: 11686304. DOI: 10.1038/s41598-024-83585-z.


Maturational competence of equine oocytes is associated with alterations in their 'cumulome'.

Walter J, Colleoni S, Lazzari G, Fortes C, Grossmann J, Roschitzki B Mol Hum Reprod. 2024; 30(9).

PMID: 39288330 PMC: 11444741. DOI: 10.1093/molehr/gaae033.


Meiotic and developmental competence of growing pig oocytes derived from small antral follicles is enhanced in culture medium containing FGF2, LIF, and IGF1 (FLI medium).

Bartkova A, Nemcova L, Kinterova V, Radova D, Strejcek F, Toralova T J Ovarian Res. 2024; 17(1):54.

PMID: 38431654 PMC: 10908066. DOI: 10.1186/s13048-024-01360-0.


Combination of CNP, MT and FLI during IVM Significantly Improved the Quality and Development Abilities of Bovine Oocytes and IVF-Derived Embryos.

Zhang P, Yang B, Xu X, Zhang H, Feng X, Hao H Antioxidants (Basel). 2023; 12(4).

PMID: 37107273 PMC: 10135536. DOI: 10.3390/antiox12040897.


Developmental competence of IVF and SCNT goat embryos is improved by inhibition of canonical WNT signaling.

Sadeghi M, Andani M, Hajian M, Sanei N, Moradi-Hajidavaloo R, Mahvash N PLoS One. 2023; 18(4):e0281331.

PMID: 37075045 PMC: 10115261. DOI: 10.1371/journal.pone.0281331.


References
1.
Takahashi T, Hagiwara A, Ogiwara K . Prostaglandins in teleost ovulation: A review of the roles with a view to comparison with prostaglandins in mammalian ovulation. Mol Cell Endocrinol. 2017; 461:236-247. DOI: 10.1016/j.mce.2017.09.019. View

2.
Habibi R, Hosseini S, Ghazvini Zadegan F, Hajian M, Ostadhosseini S, Vash N . Functional characterization of NANOG in goat pre-implantation embryonic development. Theriogenology. 2018; 120:33-39. DOI: 10.1016/j.theriogenology.2018.07.023. View

3.
HosseinNia P, Hajian M, Tahmoorespur M, Hosseini S, Ostadhosseini S, Nasiri M . Expression Profile of Developmentally Important Genes in preand peri-Implantation Goat Embryos Produced . Int J Fertil Steril. 2016; 10(3):310-319. PMC: 5023042. DOI: 10.22074/ijfs.2016.4659. View

4.
Siqueira L, Barreta M, Gasperin B, Bohrer R, Santos J, Buratini Jr J . Angiotensin II, progesterone, and prostaglandins are sequential steps in the pathway to bovine oocyte nuclear maturation. Theriogenology. 2012; 77(9):1779-87. DOI: 10.1016/j.theriogenology.2011.12.022. View

5.
Leoni G, Palmerini M, Satta V, Succu S, Pasciu V, Zinellu A . Differences in the Kinetic of the First Meiotic Division and in Active Mitochondrial Distribution between Prepubertal and Adult Oocytes Mirror Differences in their Developmental Competence in a Sheep Model. PLoS One. 2015; 10(4):e0124911. PMC: 4403920. DOI: 10.1371/journal.pone.0124911. View