Role of extracellular vesicles during oocyte maturation and early embryo development

The follicle is a dynamic microenvironment in the ovary where the oocyte develops. Intercellular communication between somatic cells and the oocyte inside the follicle is essential to generate a competent gamete. Extracellular vesicles are nanoparticles secreted by cells that mediate cell-to-cell communication in the follicle microenvironment and can be obtained from the follicular fluid. These extracellular vesicles have been studied as biomarkers and supplementation tools to mimic physiological conditions during assisted reproductive techniques because they are vehicles of bioactive molecules. Therefore, this paper reviews the importance of changes in the ovarian follicle and the effects of extracellular vesicles from follicular fluid during oocyte maturation and early embryo development. Finally, we propose that is important to consider the source of the extracellular vesicles to improve diagnostic methods and to increase invitro embryo production.

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Bovine Follicular Fluid and Extracellular Vesicles Derived from Follicular Fluid Alter the Bovine Oviductal Epithelial Cells Transcriptome

International Journal of Molecular Sciences ◽

10.3390/ijms21155365 ◽

2020 ◽

Vol 21 (15) ◽

pp. 5365 ◽

Cited By ~ 2

Author(s):

Mohammad Mehedi Hasan ◽

Janeli Viil ◽

Freddy Lättekivi ◽

James Ord ◽

Qurat Ul Ain Reshi ◽

...

Keyword(s):

Gene Expression ◽

Epithelial Cells ◽

Embryo Development ◽

Extracellular Vesicles ◽

Follicular Fluid ◽

Early Embryo ◽

Transcriptional Responses ◽

Early Embryo Development ◽

Sperm Survival

While follicular fluid (FF) is well known to provide an optimal environment for oogenesis, its functional roles following its release into the oviduct during ovulation are currently elusive. We hypothesized that FF and FF-derived extracellular vesicles (EVs) may be conveyors of signals capable of inducing functionally-relevant transcriptional responses in oviductal cells. The aim of this study was, therefore, to evaluate the effect of FF and FF-derived EVs on the transcriptome of primary bovine oviductal epithelial cells (BOECs). We examined the gene expression of BOECs in three conditions: BOECs cultured with FF, FF-derived EVs, and without supplementations. For each condition, cells were cultured for 6 and 24 h. RNA sequencing results revealed that FF had a stronger effect on BOECs gene expression compared to EVs. We detected 488 and 1998 differentially expressed genes (DEGs) with FF treatment in 6 and 24 h, respectively, whereas only 41 DEGs were detected at 6 h following EV treatment. Pathway analysis of the FF-induced DEGs showed that several pathways were highly enriched, notably oxidative phosphorylation, thermogenesis, arachidonic acid metabolism, and steroid hormone biosynthesis. Some of these pathways have a role in sperm survival, fertilization, and early embryo development. In conclusion, the findings of our study demonstrate for the first time that bovine FF and FF-derived EVs can induce changes in the gene expression of the bovine oviductal cells which, although observed in vitro, may be reflective of in vivo responses which may contribute to a favorable periconceptional microenvironment for sperm survival, fertilization, and early embryo development.

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Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows

Reproduction ◽

10.1530/rep-10-0068 ◽

2010 ◽

Vol 139 (6) ◽

pp. 1047-1055 ◽

Cited By ~ 83

Author(s):

K Bender ◽

S Walsh ◽

A C O Evans ◽

T Fair ◽

L Brennan

Keyword(s):

Fatty Acids ◽

Embryo Development ◽

Oocyte Maturation ◽

Follicular Fluid ◽

Negative Impact ◽

Saturated Fatty Acids ◽

Early Embryo ◽

Gas Chromatography Mass Spectrometry ◽

Early Embryo Development ◽

Lactating Cows

There has been a marked decline in the fertility of dairy cows over the past decades, and metabolomic analysis offers a potential to investigate the underlying causes. Metabolite composition of the follicular fluid, which presents the intrafollicular environment, may be an important factor affecting oocyte maturation and subsequent early embryo development. The aim of the present study was to investigate the metabolic differences between follicular fluid from the dominant follicle of lactating cows and heifers using gas chromatography mass spectrometry (GC–MS)-based metabolomics. Follicular fluid and serum were collected from cows and heifers over three phases of follicle development: newly selected dominant follicles, preovulatory follicles prior to oestrus and post-LH surge follicles. Analysis of the fatty acids revealed that there were 24 fatty acids and 9 aqueous metabolites significantly different between cows and heifers. Of particular interest were the higher concentrations of saturated fatty acids (palmitic acid, P=0.001; stearic acid, P=0.005) in follicular fluid from cows and higher docosahexaenoic acid levels (P=0.022) in follicular fluid from heifers. Analysis of the metabolite composition of serum revealed that follicular fluid had a unique lipid composition. The higher concentrations of detrimental saturated fatty in cows will have a negative impact on oocyte maturation and early embryo development. Overall, the results suggest that the follicle microenvironment in cows potentially places their oocytes at a developmental disadvantage compared with heifers, and that this may contribute to well-characterised differences in fertility.

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Impact of linoleic acid on bovine oocyte maturation and embryo development

Reproduction ◽

10.1530/rep-09-0503 ◽

2010 ◽

Vol 139 (6) ◽

pp. 979-988 ◽

Cited By ~ 93

Author(s):

Waleed F Marei ◽

D Claire Wathes ◽

Ali A Fouladi-Nashta

Keyword(s):

Linoleic Acid ◽

Embryo Development ◽

Oocyte Maturation ◽

Follicular Fluid ◽

Early Embryo ◽

Farm Animals ◽

Lower Percentage ◽

Prostaglandin E ◽

Bovine Oocyte ◽

Early Embryo Development

Linoleic acid (LA; 18:2 n-6) is the most abundant fatty acid in bovine follicular fluid, and it was previously reported that LA concentration significantly decreases when follicle size increases. This suggests that LA may have a role in the regulation of oocyte maturation. The present study investigated the effect of LA supplementation on bovine oocyte maturation and early embryo development in vitro. Treatment of cumulus–oocyte complexes (COCs) with LA significantly inhibited cumulus cell expansion and retarded development of the oocytes to the metaphase II (MII) stage in a dose-dependent manner. This effect was reversible, and the oocytes developed to the MII stage after extended culture in the absence of LA. Treatment of COCs with LA also resulted in a significantly lower percentage of cleaved embryos and blastocyst yield. Furthermore, COCs treated with LA had significant effects compared with controls in i) increasing prostaglandin E2 concentration in the medium, ii) decreasing intracellular cAMP at 6 and 24 h of maturation and iii) decreasing phosphorylation of the MAPK1 and 3 at 24 h, and AKT at 6 h of maturation. In conclusion, LA supplementation to bovine oocytes during maturation altered the molecular mechanisms regulating oocyte maturation and resulted in decreased percentage of oocytes at MII stage and inhibition of the subsequent early embryo development. These data provide evidence for adverse effects of LA on oocyte development, which can be associated with dietary increased level of LA in the follicular fluid and the decline in fertility in farm animals and human.

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