Abstract
Ovarian follicle provides a favorable environment for enclosed oocytes, which acquire their competence in supporting embryo development in tight communications with somatic follicular cells and follicular fluid (FF). Although steroidogenesis in theca (TH) and granulosa cells (GC) is largely studied, and the molecular mechanisms of fatty acid (FA) metabolism in cumulus cells (CC) and oocytes are emerging, little data is available regarding lipid metabolism regulation within ovarian follicles. In this study, we investigated lipid composition and the transcriptional regulation of FA metabolism in 3–8 mm ovarian follicles in bovine. Using liquid chromatography and mass spectrometry (MS), 438 and 439 lipids were identified in FF and follicular cells, respectively. From the MALDI-TOF MS lipid fingerprints of FF, TH, GC, CC, and oocytes, and the MS imaging of ovarian sections, we identified 197 peaks and determined more abundant lipids in each compartment. Transcriptomics revealed lipid metabolism-related genes, which were expressed constitutively or more specifically in TH, GC, CC, or oocytes. Coupled with differential lipid composition, these data suggest that the ovarian follicle contains the metabolic machinery that is potentially capable of metabolizing FA from nutrient uptake, degrading and producing lipoproteins, performing de novo lipogenesis, and accumulating lipid reserves, thus assuring oocyte energy supply, membrane synthesis, and lipid-mediated signaling to maintain follicular homeostasis.
Highlights
In dairy cows, lipid metabolism is crucial to maintain proper reproductive function, which is affected by negative energy balance (NEB) occurring during the early postpartum period, due to the elevated mobilization of fat reserves to liberate the energy that is required for milk production [1,2]
TH cell layers are transpierced by blood microvessels, and since antrum appearance, the follicle is filled with a fluid that is rich in proteins, steroids, and lipids, coming from the blood and secretory activity of follicular somatic cells—TH, granulosa cells (GC), and cumulus cells (CC), too [11,12]
Nile red fluorescence (NRF) was more intensive in the cellular compartments of ovarian follicles than in follicular fluid (FF) (Figure 1A)
Summary
Lipid metabolism is crucial to maintain proper reproductive function, which is affected by negative energy balance (NEB) occurring during the early postpartum period, due to the elevated mobilization of fat reserves to liberate the energy that is required for milk production [1,2]. Oocyte competence or capacity to support embryo development after fertilization is one of the key factors affected by misbalanced fatty acid (FA) metabolism during the NEB period [3]. The impaired lipid composition of FF, which is rich in saturated free FA (C18:0 stearic and C16:0 palmitic acids) in lactating cows, may explain their lower fertility as compared to heifers [5], as well as the seasonal variations of oocyte developmental competence in dairy cows [6]. Oocytes develop and acquire their developmental competence in the ovarian follicle through tight bidirectional communication with follicular somatic cells, with each compartment secreting specific regulation factors [7,8,9,10]. The closest follicular environment of the oocyte, including FF, GC, and especially CC, has a crucial impact on the acquisition of oocyte developmental competence [12,14,15,16] and possesses molecular factors that are predictive of oocyte developmental potential [17,18,19]
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