Cyclooxygenase-2-derived Prostaglandin E2 Directs Oocyte Maturation by Differentially Influencing Multiple Signaling Pathways

Takahashi, Toshifumi; Morrow, Jason D.; Wang, Haibin; Dey, Sudhansu K.

doi:10.1074/jbc.m608202200

Cited by 130 publications

(103 citation statements)

References 63 publications

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“…least in part, the Gn-induced oocyte maturation. These results are in accordance with data from Cox-2 À/À mice, where PGE 2 supplementation significantly increased GVBD and progress to MII only in the absence of Gn, but had no additive effect when supplied in the presence of FSH (Takahashi et al, 2006).…”

Section: Discussionsupporting

confidence: 92%

“…Immature COC collected from mice lacking the gene encoding PTGER2 failed to expand in vitro in response to FSH and PGE 2 (Hizaki et al, 1999). PTGS2 null mice exhibited impaired cumulus cell expansion, an effect which was mediated by down-regulation of tumour necrosis factor-induced protein-6 (TSG-6; which has HA-binding functions) and enhanced cumulus cell death (through AKT) (Takahashi et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Several studies have demonstrated that PTGS2-derived PGE 2 plays an important role in cumulus cell expansion and oocyte maturation in rodents (Eppig, 1981;Hizaki et al, 1999;Lim et al, 1997;Takahashi et al, 2006) but with fewer studies in cattle (Nuttinck et al, 2011), the role of PGE 2 in oocyte maturation is less characterized and it is not clear if PGE 2 can be used as an additive to improve oocyte competence. The present study examined the expression of genes involved in the synthesis of PGE 2 and PGF 2a in bovine COC and the role of exogenous PGE 2 supplementation during bovine oocyte maturation in the presence or absence of Gn.…”

Section: Introductionmentioning

confidence: 99%

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Role of PTGS2-generated PGE2 during gonadotrophin-induced bovine oocyte maturation and cumulus cell expansion

Marei

Abayasekara

Wathes

et al. 2014

Reproductive BioMedicine Online

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(AA Fouladi-Nashta).Waleed Fawzy A Marei is a veterinarian and graduated from Cairo University, Egypt in 2001. He started his academic career in theriogenology in 2002 and obtained his MSc degree in 2005. He joined the reproduction research group at the Royal Veterinary College, London, UK and investigated the effects of fatty acids on oocyte quality and early embryo development for his PhD, awarded in 2010. He then pursued post-doctoral research in the same group, working on early embryo development and implantation. Currently, he is a lecturer on theriogenology at Cairo University. His interests are clinical applications of assisted reproduction technologies and feed additives to improve reproductive performance in farm animals.Abstract Prostaglandin E 2 (PGE 2 ) is an autocrine/paracrine factor which mediates gonadotrophin (Gn) stimulation of cumulus expansion and oocyte maturation in rodents. Its role in bovine oocyte maturation is less characterized. This study detected PTGS2 (COX2) and PGE synthases (PTGES1, PTGES2 and PTGES3) in bovine cumulus-oocyte complexes (COC). Only PTGS2 and PTGES1 expression changed during maturation. In Gn-free media, no cumulus expansion and $45% nuclear maturation was achieved, while Gn-induced maturation showed full cumulus expansion (score 3) and $87% maturation. PGE 2 supplementation without Gn induced mild cumulus expansion (score 0.5-1) but increased nuclear maturation to levels similar to those obtained with Gn alone. In the presence of Gn, exogenous PGE 2 did not affect expansion or nuclear maturation and subsequent embryo development. Treatment with PTGS2 selective inhibitor (NS398), PTGS2-specific siRNA or PTGER2-receptor antagonist (AH6809) resulted in $20-25% reduction in nuclear maturation. NS398 and AH6809 did not affect cumulus expansion. Most oocytes not reaching metaphase of second meiosis (MII) following NS398, AH6809 and PTGS2-specific siRNA treatments were at MI. After longer maturation, NS398-treated oocytes had normal MII rate and uncompromised embryo development. PGE 2 has a limited role in cumulus expansion in bovine COC but is important for the timing of Gn-induced nuclear maturation. RBMOnline

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Role of PTGS2-generated PGE2 during gonadotrophin-induced bovine oocyte maturation and cumulus cell expansion

Marei

Abayasekara

Wathes

et al. 2014

Reproductive BioMedicine Online

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“…Next was PTX3, which was increased by FGF10 at 12 h, followed by TNFAIP6 expression, which was upregulated at 22 h of culture. TNFAIP6 was reported to be a target of PG action in mice and pigs, and either silencing of PTGS2 or disruption of PG signaling severely impaired TNFAIP6 expression (Ochsner et al 2003, Takahashi et al 2006, Yamashita et al 2011. Therefore, the effects of FGF10 on TNFAIP6 expression are probably mediated through increased PTGS2.…”

Section: Bmp15 and Fgf10 Regulate Cumulus Cell Behaviormentioning

confidence: 99%

Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus–oocyte complexes

et al. 2013

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Oocyte-secreted factors (OSFs) regulate differentiation of cumulus cells and are of pivotal relevance for fertility. Bone morphogenetic protein 15 (BMP15) and fibroblast growth factor 10 (FGF10) are OSFs and enhance oocyte competence by unknown mechanisms. We tested the hypothesis that BMP15 and FGF10, alone or combined in the maturation medium, enhance cumulus expansion and expression of genes in the preovulatory cascade and regulate glucose metabolism favouring hyaluronic acid production in bovine cumulus–oocyte complexes (COCs). BMP15 or FGF10 increased the percentage of fully expanded COCs, but the combination did not further stimulate it. BMP15 increased cumulus cell levels of mRNA encoding a disintegrin and metalloprotease 10 (ADAM10), ADAM17, amphiregulin (AREG), and epiregulin (EREG) at 12 h of culture and of prostaglandin (PG)-endoperoxide synthase 2 (PTGS2), pentraxin 3 (PTX3) and tumor necrosis factor alpha-induced protein 6 (TNFAIP6 (TSG6)) at 22 h of culture. FGF10 did not alter the expression of epidermal growth factor-like factors but enhanced the mRNA expression of PTGS2 at 4 h, PTX3 at 12 h, and TNFAIP6 at 22 h. FGF10 and BMP15 stimulated glucose consumption by cumulus cells but did not affect lactate production or levels of mRNA encoding glycolytic enzymes phosphofructokinase and lactate dehydrogenase A. Each growth factor increased mRNA encoding glucosamine:fructose-6-PO4 transaminases, key enzymes in the hexosamine pathway leading to hyaluronic acid production, and BMP15 also stimulated hyaluronan synthase 2 (HAS2) mRNA expression. This study provides evidence that BMP15 and FGF10 stimulate expansion of in vitro-matured bovine COCs by driving glucose metabolism toward hyaluronic acid production and controlling the expression of genes in the ovulatory cascade, the first acting upon ADAM10, ADAM17, AREG, and EREG and the second on downstream genes, particularly PTGS2.

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“…In contrast, COX‐2 is an inducible isoform that is responsive to many growth factors and to cytokine stimulation, especially to the factors that are produced during ovulation 11, 12. The ovulation rate is reduced by COX‐2 suppression13, 14 and this suppression can be inhibited by supplying prostaglandin E 2 or IL‐1 beta 13, 15…”

Section: Introductionmentioning

confidence: 99%

Expression of cytokine‐induced neutrophil chemoattractant suppresses tumor necrosis factor alpha expression and thereby prevents the follicles from undergoing atresia and apoptosis

Tanaka

Kuwahara

Ushigoe

et al. 2017

Reprod Medicine & Biology

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AimCytokine‐induced neutrophil chemoattractant (CINC/gro) is a CXC family chemokine, similar to interleukin‐8 in rats, and is one of the factors that regulates ovulation. However, the mechanism that regulates atresia of the ovaries postovulation is not clearly defined.MethodsWhether antibody‐blocking of CINC/gro can alter the number of ovulated oocytes and modulate neutrophil infiltration was investigated. The effect of the antibody on the level of inflammatory cytokine production and follicular atresia was examined. Apoptosis was measured by the terminal deoxynucleotidyl transferase‐mediated dUTP nick end labeling (TUNEL) method and via analysis of the messenger RNA expression of Bcl‐2 and Bcl2‐associated X (Bax).ResultsThe anti‐CINC/gro antibody treatment decreased the number of ovulated oocytes. The messenger RNA levels of cyclooxygenase‐2 and interleukin‐1 beta were decreased by the antibody treatment, whereas that of tumor necrosis factor (TNF) alpha was increased. The TUNEL analysis revealed a larger number of apoptotic cells in the antibody group, compared with those in the control group, as well as a significant increase in the Bax/Bcl‐2 ratio 24 hours after human chorionic gonadotropin administration.ConclusionThese findings suggest that ovulation is accelerated by neutrophil infiltration into the theca layer. The CINC/gro appears to synergize with interleukin‐1 beta for ovulation. By contrast, the data suggest that CINC/gro expression suppresses TNF alpha expression and that CINC/gro expression therefore prevents the follicles from undergoing atresia and apoptosis.

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Cyclooxygenase-2-derived Prostaglandin E2 Directs Oocyte Maturation by Differentially Influencing Multiple Signaling Pathways

Cited by 130 publications

References 63 publications

Role of PTGS2-generated PGE2 during gonadotrophin-induced bovine oocyte maturation and cumulus cell expansion

Role of PTGS2-generated PGE2 during gonadotrophin-induced bovine oocyte maturation and cumulus cell expansion

Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus–oocyte complexes

Expression of cytokine‐induced neutrophil chemoattractant suppresses tumor necrosis factor alpha expression and thereby prevents the follicles from undergoing atresia and apoptosis

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