Bovine Cumulus Cells Protect Maturing Oocytes from Increased Fatty Acid Levels by Massive Intracellular Lipid Storage

Abstract

Metabolic conditions characterized by elevated free fatty acid concentrations in blood and follicular fluid are often associated with impaired female fertility. Especially elevated saturated fatty acid levels can be lipotoxic for several somatic cell types. The aim of this study was to determine the impact of elevated free fatty acid concentrations in follicular fluid on neutral lipids (fatty acids stored in lipid droplets) inside cumulus cells and oocytes and their developmental competence. To this end, cows were exposed to a short-term fasting period during final oocyte maturation. This resulted in elevated, but distinct, free fatty acid concentrations in blood and follicular fluid and a rise in the concentrations of in particular fatty acids with a chain length of 14-18 carbon atoms. Interestingly, elevated free fatty acid concentrations in follicular fluid resulted in a massive increase in the level of neutral lipids in cumulus cells, whereas the level of neutral lipid in oocytes was hardly affected. Furthermore, competence of oocytes to develop to the blastocyst stage after fertilization and culture of cumulus-oocyte-complexes of the experimental and control group was not different. In conclusion these data suggest that short-term elevated free fatty acid concentrations in follicular fluid do not harm oocyte developmental competence. We propose that the involvement of high levels of mobilized oleic acid in follicular fluid in combination with the induced lipid storage in cumulus cells serves to prevent harmful saturated fatty acid exposure to the oocyte.

Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation

“…Heifers with moderate body condition score had less fatty acids in aspirated COCs than heifers with low body condition score; and the inclusion of a lipid supplement in the diet for 35 days increased the total fatty acid content of whole COCs (Adamiak et al 2006). In contrast to experiments that increased or altered fat in the diet, cows that were fasted for 4 days also exhibited increased NEFA in both plasma and follicular fluid (Jorritsma et al 2003, Aardema et al 2013. Interestingly, there are also seasonal changes in the fatty acid composition of bovine ovarian follicles.…”

“…increased oocyte droplet size and number (Aardema et al 2011). However, when bovine COCs were treated with a mixture of these three NEFAs (palmitic/stearic/ oleic acids) during IVM, oocyte lipid content was not affected even though cumulus cells exhibited lipid accumulation (Aardema et al 2013). Addition of conjugated linoleic acid (t10,c12CLA) to bovine COCs during maturation increased t10,c12CLA content in both cumulus cells and oocytes, but did not alter total fatty acid levels (Lapa et al 2011).…”

Correlations among oocyte quality, hepatic triacylglycerols, and some blood metabolites in Carora breed cows during early postpartum

“…Furthermore, higher total lipid levels, and in particular TAG presenting acylation with oleic and palmitic acids, are observed in cumulus-enclosed than in denuded oocytes (5). Stored neutral lipids may be very important energy sources to be used through β-oxidation as well as precursors for de novo membrane synthesis during embryo development (28).…”

“…Moreover, the composition and balance of saturated and unsaturated NEFAs in follicular fluid may distinctly modify these potential toxic effects of NEFAs on oocyte developmental competence. As recently demonstrated both in vivo and in vitro, exposure of maturing oocytes to elevated NEFAs can affect either β-oxidation or lipogenesis, crucial mechanisms for postfertilization developmental competence (4,5).…”

The effect of nutrition and metabolic status on the development of follicles, oocytes and embryos in ruminants

“…The same laboratory suggests that these negative effects of NEFAs on the embryo could be a consequence of modified energy metabolism and particularly, mitochondrial β-oxidation of fatty acids in the oocyte (Van Hoeck et al, 2013). A recent study has shown that bovine cumulus cells are able to protect maturing oocytes from potential harmful effects of increased local concentrations of fatty acids by intracellular storage of lipids (Aardema et al, 2013).…”