Peroxiredoxin 4 secreted by cumulus cells ameliorates the maturation of oocytes in vitro

Dai, Wangjuan; Zou, Xiaofei; Jia, Hongyan; Peng, Yawen; La, Boya; Yan, Zhenjie; Li, Gao; Qin, Lianju; Diao, Feiyang; Ma, Xiang; Meng, Yan; Cui, Yugui; Liu, Jiayin

doi:10.1016/j.bbrc.2022.10.073

Cited by 7 publications

(4 citation statements)

References 25 publications

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“…Proteins with ovarian roles that were altered by ZEN exposure included PRDX4, AKR1B1, and CDK2. In the ovary, PRDX4 is secreted by cumulus cells and protects the oocyte against oxidative stress ( Dai et al, 2022 ; Qian et al, 2022 ). There are reports of an association between PRDX4 and both polycystic ovary syndrome (PCOS; Meng et al, 2013 ; Gateva et al, 2019 ; Zhou et al, 2021 ) and ovarian aging ( Qian et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Zearalenone exposure differentially affects the ovarian proteome in pre-pubertal gilts during thermal neutral and heat stress conditions

Roach,

Mayorga,

Baumgard

et al. 2024

Journal of Animal Science

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Zearalenone (ZEN), a nonsteroidal estrogenic mycotoxin, causes endocrine disruption and porcine reproductive dysfunction. Heat stress (HS) occurs when exogenous and metabolic heat accumulation exceeds heat dissipation. Independently, HS and ZEN both compromise swine reproduction; thus, the hypothesis investigated was two-pronged: that ZEN exposure would alter the ovarian proteome and that these effects would differ in thermal neutral and HS pigs. Pre-pubertal gilts (n = 38) were fed ad libitum and assigned to either thermal neutral (TN: 21.0 ± 0.1°C) or HS (12 h cyclic temperatures of 35.0 ± 0.2°C and 32.2 ± 0.1°C). Within the TN group, a subset of pigs were pair-fed (PF) to the amount of feed that the HS gilts consumed to eliminate the confounding effects of dissimilar nutrient intake. All gilts orally received a vehicle control (CT) or ZEN (40 μg/kg/BW) resulting in six treatment groups: thermoneutral (TN) vehicle control (TC; n = 6); TN ZEN (TZ; n = 6); pair-fed (PF) vehicle control (PC; n = 6); PF ZEN (PZ; n = 6); HS vehicle control (HC; n = 7); or HS ZEN (HZ; n = 7) for 7 d. When compared to the TC pigs, TZ pigs had 45 increased and 39 decreased proteins (P ≤ 0.05). In the HZ pigs, 47 proteins were increased and 61 were decreased (P ≤ 0.05). Exposure to ZEN during TN conditions altered sec61 translocon complex (40%), rough endoplasmic reticulum membrane (8.2%), and proteasome complex (5.4%), asparagine metabolic process (0.60%), aspartate family amino acid metabolic process (0.14%), and cellular amide metabolic process (0.02%) pathways. During HS, ZEN affected cellular pathways associated with proteasome core complex alpha subunit complex (0.23%), fibrillar collagen trimer (0.14%), proteasome complex (0.05%), and spliceosomal complex (0.03%). Thus, these data identify ovarian pathways altered by ZEN exposure and suggest that the molecular targets of ZEN differ in TN and HS pigs.

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Section: Discussionmentioning

confidence: 99%

Zearalenone exposure differentially affects the ovarian proteome in pre-pubertal gilts during thermal neutral and heat stress conditions

Roach,

Mayorga,

Baumgard

et al. 2024

Journal of Animal Science

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“…In vitro maturation (IVM) has shown some promise in addressing this issue, although recent improvements in yields of mature oocytes have been rather modest. Some improvements to first polar body extrusion rates have been achieved by supplementation of IVM media with antioxidants melatonin, N-acetyl cysteine (NAC), mogroside V, putrecscine, β-cryptoxanthin, peroxiredoxin-4, and resveratrol [62][63][64][65][66][67][68]. Oocyte maturation rates in vitro were also improved by myostatin (alias GDF8) and bone morphogenic protein-15 (BMP-15), both of which are members of the TGFβ superfamily [69,70].…”

Section: Pathways and Therapeuticsmentioning

confidence: 99%

Gonadotropin elevation is ootoxic to ovulatory oocytes and inhibits oocyte maturation, and activin decoy receptor ActRIIB:Fc therapeutically restores maturation

Bernstein,

Mackenzie,

Chaffin

et al. 2024

Reprod Biol Endocrinol

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Background Elevated FSH often occurs in women of advanced maternal age (AMA, age ≥ 35) and in infertility patients undergoing controlled ovarian stimulation (COS). There is controversy on whether high endogenous FSH contributes to infertility and whether high exogenous FSH adversely impacts patient pregnancy rates. Methods The senescence-accelerated mouse-prone-8 (SAMP8) model of female reproductive aging was employed to assess the separate impacts of age and high FSH activity on the percentages (%) of viable and mature ovulated oocytes recovered after gonadotropin treatment. Young and midlife mice were treated with the FSH analog equine chorionic gonadotropin (eCG) to model both endogenous FSH elevation and exogenous FSH elevation. Previously we showed the activin inhibitor ActRIIB:Fc increases oocyte quality by preventing chromosome and spindle misalignments. Therefore, ActRIIB:Fc treatment was performed in an effort to increase % oocyte viability and % oocyte maturation. Results The high FSH activity of eCG is ootoxic to ovulatory oocytes, with greater decreases in % viable oocytes in midlife than young mice. High FSH activity of eCG potently inhibits oocyte maturation, decreasing the % of mature oocytes to similar degrees in young and midlife mice. ActRIIB:Fc treatment does not prevent eCG ootoxicity, but it restores most oocyte maturation impeded by eCG. Conclusions FSH ootoxicity to ovulatory oocytes and FSH maturation inhibition pose a paradox given the well-known pro-growth and pro-maturation activities of FSH in the earlier stages of oocyte growth. We propose the FOOT Hypothesis (“FSH OoToxicity Hypothesis), that FSH ootoxicity to ovulatory oocytes comprises a new driver of infertility and low pregnancy success rates in DOR women attempting spontaneous pregnancy and in COS/IUI patients, especially AMA women. We speculate that endogenous FSH elevation also contributes to reduced fecundity in these DOR and COS/IUI patients. Restoration of oocyte maturation by ActRIB:Fc suggests that activin suppresses oocyte maturation in vivo. This contrasts with prior studies showing activin A promotes oocyte maturation in vitro. Improved oocyte maturation with agents that decrease endogenous activin activity with high specificity may have therapeutic benefit for COS/IVF patients, COS/IUI patients, and DOR patients attempting spontaneous pregnancies.

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“…The MGCs differentiate into luteal cells and remain in the ovary after ovulation called corpus luteum, whereas CGCs transport the egg to the oviduct. Many reports and studies have shown that the quality of oocyte production and follicular maturation are both affected by the state of these cells [19]. There are several genes present within the follicles that are differently expressed between these two divisions of granulosa cells: MGCs and CGCs [20].…”

Section: Introductionmentioning

confidence: 99%

“…The examination of the enrichment of Gene Ontology for the Mural and Cumulus Granulosa Cells. The number of genes that are more prevalent in each biological process is represented along the vertical axis of the bar (hg-19)…”

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confidence: 99%

Genome-wide association study for single nucleotide polymorphism associated with mural and cumulus granulosa cells of PCOS (polycystic ovary syndrome) and non-PCOS patients

Pant

Chitme

Sircar³

et al. 2023

Futur J Pharm Sci

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Background The genetic make-up of local granulosa cells and their function in the pathophysiology of polycystic ovary syndrome (PCOS) is crucial to a full comprehension of the disorder. The major purpose of this study was to compare the Single Nucleotide Polymorphism (SNP) of cumulus granulosa cells (CGCs) and mural granulosa cells (MGCs) between healthy individuals and women with PCOS using genome-wide association analysis (GWA). A case–control study was conducted in a total of 24 women diagnosed with PCOS and 24 healthy non-PCOS women of reproductive age aggregated into 4 samples of 6 patients each. GWA studies entail several processes, such as cell separation, cellular DNA extraction, library preparation followed by interpretation using bioinformatics databases. SNP locations were identified by reference gene also involves the use of Matrix-assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) (MALDI-TOF-MS) for the first sorting. Hybridization with the gene chip was followed by reading the SNP genotypes according to the publications in the literature. TASSEL (Trait Analysis by aSSociation, Evolution and Linkage) program and methods were used for GWA studies. Results An aggregate of 21,039 SNP calls were obtained from our samples. Genes of autoimmune illnesses, obesity, inflammatory illnesses, nervous system diseases such as retinitis pigmentosa, autism, neural tube defects, and Alzheimer's disease; and various malignancies such as lung cancer, colorectal cancer, breast cancer were also identified in these cells. Gene ranking score reveals that granulosa cells carry key genes of neurological system and reproductive systems especially in brain and testis, respectively. Conclusions Mural and Cumulus Granulosa cells were shown to have the PCOS directly and indirectly related genes MMP9, PRKAA2, COMT and HP. We found that the expression of ARID4B, MUC5AC, NID2, CREBBP, GNB1, KIF2C, COL18A1, and HNRNPC by these cells may contribute to PCOS. Graphical abstract

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Peroxiredoxin 4 secreted by cumulus cells ameliorates the maturation of oocytes in vitro

Cited by 7 publications

References 25 publications

Zearalenone exposure differentially affects the ovarian proteome in pre-pubertal gilts during thermal neutral and heat stress conditions

Zearalenone exposure differentially affects the ovarian proteome in pre-pubertal gilts during thermal neutral and heat stress conditions

Gonadotropin elevation is ootoxic to ovulatory oocytes and inhibits oocyte maturation, and activin decoy receptor ActRIIB:Fc therapeutically restores maturation

Genome-wide association study for single nucleotide polymorphism associated with mural and cumulus granulosa cells of PCOS (polycystic ovary syndrome) and non-PCOS patients

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