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Hypoglycosylated FSH enhances oocyte quality via increased cell-to-cell interaction during mouse follicle development

ABSTRACT: Differences in follicle-stimulating hormone (FSH) ß-subunit N-glycosylation results in distinct FSH glycoforms. Hypoglycosylated FSH21 is more bioactive and abundant in reproductively young women, whereas fully glycosylated FSH24 shows lower bioactivity and a relative increase with age. To investigate if the coinciding shift in FSH glycoform abundance contributes to the age-dependent decline in oocyte quality, an encapsulated in vitro follicle growth system was utilized to examine the direct effects of FSH glycoforms on folliculogenesis and resulting oocyte quality. Long-term culture (10-12 days) with FSH21 (10 ng/ml) enhanced follicle growth, estradiol secretion, and oocyte quality compared to equivalent FSH24 treatment. FSH21 exhibited enhanced capacity to establish transzonal projections, gap junctions, and cell-to-cell communication within 24 hrs in culture. Transient inhibition of FSH21-mediated bidirectional communication abrogated the positive effects of FSH21 on follicle growth, estradiol secretion and oocyte quality. These findings indicate FSH21 promotes folliculogenesis and oocyte quality in vitro through increasing cell-to-cell communication early in folliculogenesis and that the shift in abundance from FSH21 to FSH24 with reproductive aging could contribute to the age-dependent decline in oocyte quality.

ORGANISM(S): Mus musculus

PROVIDER: GSE236967 | GEO | 2023/07/15

REPOSITORIES: GEO

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Project description:Oocyte competence for early embryo development relies on intercellular communication between the maturing oocyte and preovulatory follicle. Preovulatory follicle maturity, as indicated by serum estradiol concentration or follicle diameter, has previously been linked to pregnancy, follicular fluid metabolites, cumulus-oocyte metabolism, and oocyte competency for embryo development. Such relationships indicate metabolic and developmental programming of the oocyte based on the preovulatory follicle’s physiological status, but downstream impacts on the molecular signature of blastocysts have not been examined. We hypothesized that supplementing maturing oocytes with follicular fluid originating from preovulatory follicles of greater or lesser maturity would impact the transcriptome of resulting blastocysts and indicate metabolic programming of the embryo that originated from the oocyte’s maturation environment. The objective was to investigate the effect of follicle maturity on metabolic preparation of the oocyte by examining the functional genome of blastocysts originating from oocytes matured in the presence of follicular fluid from preovulatory follicles of greater or lesser maturity. In vitro maturing oocytes were supplemented with follicular fluid collected from preovulatory follicles of greater or lesser maturity. Following identical embryo culture procedures, RNA-sequencing was performed on pools of 2 blastocysts (Greater, n = 12; Lesser, n = 15; all with stage code = 7 and quality code = 1). A total of 12,310 gene transcripts were identified in blastocysts after filtering to remove lowly abundant transcripts. There were 113 transcripts that differed in abundance between blastocysts originating from oocytes matured in greater versus lesser maturity follicular fluid (eFDR < 0.01). Although no pathways were significantly enriched with differentially abundant transcripts, transcriptome profiles suggested improved Wnt/β-catenin signaling, metabolism, and protection from oxidative stress in blastocysts derived from oocytes matured in greater maturity follicular fluid, while unregulated cell growth presented in blastocysts resulting from the lesser follicle maturity treatment.

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Hypoglycosylated FSH enhances oocyte quality via increased cell-to-cell interaction during mouse follicle development

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