A Comparative Analysis of Oocyte Development in Mammals

Dalbiès-Tran, Rozenn; Cadoret, Véronique; Desmarchais, Alice; Elis, Sébastien; Maillard, Virginie; Monget, Philippe; Monniaux, Danielle; Reynaud, Karine; Saint‐Dizier, Marie; Uzbekova, Svetlana

doi:10.3390/cells9041002

Cited by 46 publications

(30 citation statements)

References 231 publications

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“…Interestingly, numerous genes were more highly expressed in oocytes compared with the other follicular cell types (cluster 1). Because mRNA and correspondent protein abundances did not correlate in the oocyte ( 2 , 69 – 71 ), overexpression in the oocyte suggests that these transcripts may be stored as maternal RNAs for translation during oocyte maturation and/or the first rounds of embryonic cleavage ( 72 ). An increased abundance of these transcripts in oocyte and presence of their corresponding proteins in ffEVs are of particular importance to oocyte maturation and further embryonic development.…”

Section: Discussionmentioning

confidence: 99%

“…In mammals, the antral ovarian follicle is filled with follicular fluid (FF), which provides an optimal environment for oocyte growth, meiotic maturation, and the acquisition of oocyte competence for embryonic development ( 1 , 2 ). The FF is derived from both blood plasma and the secretions of different types of somatic follicular cells (cumulus, granulosa, and thecal layers).…”

Section: Introductionmentioning

confidence: 99%

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Protein Cargo of Extracellular Vesicles From Bovine Follicular Fluid and Analysis of Their Origin From Different Ovarian Cells

et al. 2020

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Follicular fluid (FF) fills the interior portion of the ovarian antral follicle and provides a suitable microenvironment for the growth of the enclosed oocyte through molecular factors that originate from plasma and the secretions of follicular cells. FF contains extracellular nanovesicles (ffEVs), including 30–100-nm membrane-coated exosomes, which carry different types of RNA, proteins, and lipids and directly influence oocyte competence to develop embryo. In the present study, we aimed to characterize the protein cargo of EVs from the FF of 3–6-mm follicles and uncover the origins of ffEVs by assessing expression levels of corresponding mRNAs in bovine follicular cells and oocyte and cell proteomes. Isolated exosome-like ffEVs were 53.6 + 23.3 nm in size and could be internalized by cumulus-oocyte complex. Proteomes of ffEVs and granulosa cells (GC) were assessed using nanoflow liquid chromatography coupled with high-resolution tandem mass spectrometry after the gel fractionation of total proteins. In total, 460 protein isoforms corresponding to 322 unique proteins were identified in ffEVs; among them, 190 were also identified via GC. Gene Ontology terms related to the ribosome, protein and RNA folding, molecular transport, endocytosis, signal transduction, complement and coagulation cascades, apoptosis, and developmental biology pathways, including PI3K-Akt signaling, were significantly enriched features of ffEV proteins. FfEVs contain numerous ribosome and RNA-binding proteins, which may serve to compact different RNAs to regulate gene expression and RNA degradation, and might transfer ribosomal constituents to the oocyte. Majority of genes encoding ffEV proteins expressed at different levels in follicular cells and oocyte, corroborating with numerous proteins, which were reported in bovine oocyte and cumulus cells in other studies thus indicating possible origin of ffEV proteins. The limited abundance of several mRNAs within follicular cells indicated that corresponding ffEV proteins likely originated from circulating exosomes released by other tissues. Analysis of bovine ffEV transcriptome revealed that mRNAs present in ffEV accounted for only 18.3% of detected ffEV proteins. In conclusion, our study revealed numerous proteins within ffEVs, which originated from follicular and other cells. These proteins are likely involved in the maintenance of follicular homeostasis and may affect oocyte competence.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Protein Cargo of Extracellular Vesicles From Bovine Follicular Fluid and Analysis of Their Origin From Different Ovarian Cells

et al. 2020

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“…The basic plan of the early development is mostly similar, however, the intervening events differ among species. For instance, the pig and ruminant oocytes depend more on lipid metabolism, whereas, rodent and human oocytes mostly depend on glucose and pyruvate metabolism ( Dalbies-Tran et al, 2020 ). Due to the procedural and ethical barriers in using human oocytes, still there is need to define the best animal model for translational studies of oocyte lipidomics.…”

Section: Current Challenges and Future Directionsmentioning

confidence: 99%

Role of Lipid Metabolism and Signaling in Mammalian Oocyte Maturation, Quality, and Acquisition of Competence

Khan

Jiang

Hameed

et al. 2021

Front. Cell Dev. Biol.

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It has been found that the quality of oocytes from obese women has been compromised and subsequent embryos displayed arrested development. The compromised quality may be either due to the poor or rich metabolic conditions such as imbalance or excession of lipids during oocyte development. Generally, lipids are mainly stored in the form of lipid droplets and are an important source of energy metabolism. Similarly, lipids are also essential signaling molecules involved in various biological cascades of oocyte maturation, growth and oocyte competence acquisition. To understand the role of lipids in controlling the oocyte development, we have comprehensively and concisely reviewed the literature and described the role of lipid metabolism in oocyte quality and maturation. Moreover, we have also presented a simplified model of fatty acid metabolism along with its implication on determining the oocyte quality and cryopreservation for fertilization.

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“…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 follicular growth, antral cavity fills with follicular fluid (FF), coming from plasma and secretions from follicular cells.…”

Section: Introductionmentioning

confidence: 99%

MALDI-TOF Mass Spectrometry Revealed Significant Lipid Variations in Follicular Fluid and Somatic Follicular Cells but Not in Enclosed Oocytes between the Large Dominant and Small Subordinate Follicles in Bovine Ovary

Bertevello

Teixeira-Gomes

Labas

et al. 2020

IJMS

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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.

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A Comparative Analysis of Oocyte Development in Mammals

Cited by 46 publications

References 231 publications

Protein Cargo of Extracellular Vesicles From Bovine Follicular Fluid and Analysis of Their Origin From Different Ovarian Cells

Protein Cargo of Extracellular Vesicles From Bovine Follicular Fluid and Analysis of Their Origin From Different Ovarian Cells

Role of Lipid Metabolism and Signaling in Mammalian Oocyte Maturation, Quality, and Acquisition of Competence

MALDI-TOF Mass Spectrometry Revealed Significant Lipid Variations in Follicular Fluid and Somatic Follicular Cells but Not in Enclosed Oocytes between the Large Dominant and Small Subordinate Follicles in Bovine Ovary

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