Abstract
Lipid metabolism in ovarian follicular cells supports the preparation of an enclosed oocyte to ovulation. We aimed to compare lipid composition of a dominant large follicle (LF) and subordinated small follicles (SFs) within the same ovaries. Mass spectrometry imaging displayed the differences in the distribution of several lipid features between the different follicles. Comparison of lipid fingerprints between LF and SF by Matrix Assisted Laser Desorption/Ionisation Time-Of-Flight (MALDI-TOF) mass spectrometry revealed that in the oocytes, only 8 out of 468 detected lipids (1.7%) significantly changed their abundance (p < 0.05, fold change > 2). In contrast, follicular fluid (FF), granulosa, theca and cumulus cells demonstrated 55.5%, 14.9%, 5.3% and 9.8% of significantly varied features between LF and SF, respectively. In total, 25.2% of differential lipids were identified and indicated potential changes in membrane and signaling lipids. Tremendous changes in FF lipid composition were likely due to the stage specific secretions from somatic follicular cells that was in line with the differences observed from FF extracellular vesicles and gene expression of candidate genes in granulosa and theca cells between LF and SF. In addition, lipid storage in granulosa and theca cells varied in relation to follicular size and atresia. Differences in follicular cells lipid profiles between LF and SF may probably reflect follicle atresia degree and/or accumulation of appropriate lipids for post-ovulation processes as formation of corpus luteum. In contrast, the enclosed oocyte seems to be protected during final follicular growth, likely due in part to significant lipid transformations in surrounding cumulus cells. Therefore, the enclosed oocyte could likely keep lipid building blocks and energy resources to support further maturation and early embryo development.
Highlights
In mammals, an oocyte develops inside of ovarian follicle until an ovulation in tight communications with somatic follicular cells [1], notably surrounding cumulus cells (CCs), mural granulosa cells (GCs) and theca cell layers (THs)
Along the ovarian follicle growth, GC increase estradiol production by converting TH-derived androgens into estrogens [11] and become highly steroidogenic within the weeks leading up to ovulation [12]. Both GC and TH layers express specific genes involved in steroidogenesis and lipid metabolism [13], and transcriptomic patterns of GC and TH changed along final follicular growth in bovine [14,15,16]
The different colors in Mass Spectrometry Imaging (MSI) segmentation map represent the differences in lipid composition between the different zones throughout ovarian sections, and between the different follicles
Summary
An oocyte develops inside of ovarian follicle until an ovulation in tight communications with somatic follicular cells [1], notably surrounding cumulus cells (CCs), mural granulosa cells (GCs) and theca cell layers (THs). Along the ovarian follicle growth, GC increase estradiol production by converting TH-derived androgens into estrogens [11] and become highly steroidogenic within the weeks leading up to ovulation [12] Both GC and TH layers express specific genes involved in steroidogenesis and lipid metabolism [13], and transcriptomic patterns of GC and TH changed along final follicular growth in bovine [14,15,16]. Analysis of lipids in bovine ovarian follicular cells and fluid using Matrix Assisted Laser Desorption/Ionisation Time-Of-Flight Mass spectrometry (MALDI MS) revealed very specific lipid fingerprints in GC, TH, CC, oocyte and FF [13] These differences in lipid composition corroborate with specific expression patterns of lipid metabolism-related genes in somatic follicular cells [13,17] and oocyte–cumulus complex [18,19,20,21]. Each follicle possesses molecular machinery to uptake and transform lipids to assure energy requirement, membrane synthesis and signaling to maintain follicular homeostasis and [13] and provide to oocyte the necessary building blocks for the first steps of embryo development [5,22]
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