The effects of glial cell line‐derived neurotrophic factor on the in vitro matured porcine oocyte transcriptome

Toms, Derek; Tsoi, Stephen; Dobrinsky, J.R.; Dyck, Michael K.; Li, Julang

doi:10.1002/mrd.22288

Cited by 10 publications

(11 citation statements)

References 43 publications

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“…Our results are in line with previously published reports in pig, which implied a stimulating effect of EGF on oocyte maturation (Prochazka et al , 2000; Mao et al , 2012). These results are also in agreement with previous reports in pig, indicating that supplementation of maturation medium with GDNF enhances oocyte maturation (Linher et al , 2007; Toms et al , 2014).…”

Section: Discussionsupporting

confidence: 94%

“…Moreover, EGF-like growth factors have also been reported to be involved in the regulation of maternal mRNA translation in mouse oocytes by activation of the PI(3)K–AKT–mTOR pathway (Chen et al , 2013). GDNF has also been shown not only to induce the level of cyclin B1 (CCNB1) protein expression, a proxy for oocyte cytoplasmic maturation (Linher et al , 2007), but also to decrease the meiosis inhibitor WEE1 homolog 2 (WEE1B/WEE2) transcript levels in pig oocytes (Toms et al , 2014). Furthermore, treatment of granulosa cells with GDNF was shown to induce increased expression of both miR-378-3p and miR-378-5p; which are proposed to be actively involved in the regulation of porcine follicle maturation (Toms, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Accordingly, in the last few years, various cellular growth factors have received a great deal of attention as regulators of ovarian cell function (Sun & Nagai, 2003). Among the numerous ovarian factors, epidermal growth factor (EGF) and glial cell line-derived neurotrophic factor (GDNF) ligands have received increasing attention in recent years because of their roles in many aspects of oocyte maturation and ovulation in several mammals including mouse, pig and human (Linher et al , 2007; Kawamura et al , 2008; Zhao et al , 2011; Toms et al , 2014; Ritter et al , 2015; Sugimura et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

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Optimal doses of EGF and GDNF act as biological response modifiers to improve porcine oocyte maturation and quality

Valleh

Zandi

Rasmussen

et al. 2017

Zygote

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It is well documented that both epidermal growth factor (EGF) and glial cell line-derived neurotrophic factor (GDNF) are critical for porcine oocyte maturation, however, little information is known about their mechanism of action in vitro. To gain insight into the mechanisms of action of the optimum doses of EGF and GDNF on porcine oocyte maturation, porcine cumulus-oocyte complexes (COCs) were matured in defined porcine oocyte medium supplemented with EGF, GDNF or a combination of both at varying concentrations (0-100 ng/ml) for 44 h. Nuclear and cytoplasmic maturation were determined in terms of nuclear stage after DNA staining with Hoechst and cortical granule distribution after lectin labeling, respectively. Mature oocytes were subsequently collected for gene expression analysis or subjected to in vitro fertilization and cultured for 7 days. The results showed that EGF and/or GDNF, when administered in a certain dose (50 ng/μl) to the maturation medium, not only effectively improved the synchronization of nuclear and cytoplasmic maturation processes within the oocyte, but enhanced expression of their corresponding receptors in mature oocytes (P < 0.05). Moreover, supplementation with an optimal combination of EGF + GDNF resulted in elevation of TFAM transcripts as well as a decrease of caspase-3 transcripts compared with the other studied groups (P < 0.05). Collectively, our results indicate that treatment of porcine oocytes with specific-dose combinations of EGF and GDNF stimulates oocyte quality and competence by transcriptional modulation of genes involved in oocyte survival and competence.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Optimal doses of EGF and GDNF act as biological response modifiers to improve porcine oocyte maturation and quality

Valleh

Zandi

Rasmussen

et al. 2017

Zygote

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“…Following IVM, denuded oocytes were washed and underwent in vitro fertilization (IVF), as described previously without modification (53). On day 7 after fertilization, oocytes were examined under a light microscope to determine cleavage and blastocyst rates.…”

Section: Methodsmentioning

confidence: 99%

MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells

Pan

Toms

Shen

et al. 2015

American Journal of Physiology-Endocrinology and Metabolism

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Pan B, Toms D, Shen W, Li J. MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells. Am J Physiol Endocrinol Metab 308: E525-E534, 2015. First published January 27, 2015; doi:10.1152/ajpendo.00480.2014.-We sought to investigate whether miR-378 plays a role in cumulus cells and whether the manipulation of miRNA levels in cumulus cells influences oocyte maturation in vitro. Cumulus-oocyte complexes (COCs) from ovarian follicles had significantly lower levels of precursor and mature miR-378 in cumulus cells surrounding metaphase II (MII) oocytes than cumulus cells surrounding germinal vesicle (GV) oocytes, suggesting a possible role of miR-378 during COC maturation. Overexpression of miR-378 in cumulus cells impaired expansion and decreased expression of genes associated with expansion (HAS2, PTGS2) and oocyte maturation (CX43, ADAMTS1, PGR). Cumulus cell expression of miR-378 also suppressed oocyte progression from the GV to MII stage (from 54 Ϯ 2.7 to 31 Ϯ 5.1%), accompanied by a decrease of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), zona pellucida 3 (ZP3), and CX37 in the oocytes. Subsequent in vitro fertilization resulted in fewer oocytes from COCs overexpressing miR-378 reaching the blastocyst stage (7.3 Ϯ 0.7 vs. 16.6 Ϯ 0.5%). miR-378 knockdown led to increased cumulus expansion and oocyte progression to MII, confirming a specific effect of miR-378 in suppressing COC maturation. Aromatase (CYP19A1) expression in cumulus cells was also inhibited by miR-378, leading to a significant decrease in estradiol production. The addition of estradiol to IVM culture medium reversed the effect of miR-378 on cumulus expansion and oocyte meiotic progression, suggesting that decreased estradiol production via suppression of aromatase may be one of the mechanisms by which miR-378 regulates the maturation of COCs. Our data suggest that miR-378 alters gene expression and function in cumulus cells and influences oocyte maturation, possibly via oocyte-cumulus interaction and paracrine regulation.

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“…Based on our data, we cannot explain the principles of observed synergism between GDNF and EGF on oocyte competency, but it could be attributed to their roles in regulation of different aspects of oocyte maturation. Specifically, GDNF has been shown not only to induce the level of cyclin B1 (CCNB1) protein expression, a proxy for oocyte cytoplasmic maturation (Linher et al , 2007), but also to decrease the meiosis inhibitor WEE1 homolog 2 (WEE1B/WEE2) transcript levels in pig oocytes (Toms et al , 2014). In contrast, the stimulating effects of EGF on oocyte maturation are thought to be mediated through different mechanisms including activation of PI3 kinase and MAPK in cumulus cells (Li et al , 2008) as well as increasing the activity of the hexosamine biosynthesis pathway (HBP) rate-limiting enzyme gene in the oocyte (Richani et al , 2014).…”

Section: Discussionmentioning

confidence: 99%

Combination effects of epidermal growth factor and glial cell line-derived neurotrophic factor on the in vitro developmental potential of porcine oocytes

Valleh

Rasmussen

Hyttel

2015

Zygote

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The developmental potential of in vitro matured porcine oocytes is still lower than that of oocytes matured and fertilized in vivo. Major problems that account for the lower efficiency of in vitro production include the improper nuclear and cytoplasmic maturation of oocytes. With the aim of improving this issue, the single and combined effects of epidermal growth factor (EGF) and glial cell line-derived neurotrophic factor (GDNF) on oocyte developmental competence were investigated. Porcine cumulus-oocyte cell complexes (COCs) were matured in serum-free medium supplemented with EGF (0, 10 or 50 ng/ml) and/or GDNF (0, 10 or 50 ng/ml) for 44 h, and subsequently subjected to fertilization and cultured for 7 days in vitro. The in vitro-formed blastocysts derived from selected growth factor groups (i.e. EGF = 50 ng/ml; GDNF = 50 ng/ml; EGF = 50 ng/ml + GDNF = 50 ng/ml) were also used for mRNA expression analysis, or were subjected to Hoechst staining. The results showed that the addition of EGF and/or GDNF during oocyte maturation dose dependently enhanced oocyte developmental competence. Compared with the embryos obtained from control or single growth factor-treated oocytes, treatment with the combination of EGF and GDNF was shown to significantly improve oocyte competence in terms of blastocyst formation, blastocyst cell number and blastocyst hatching rate (P < 0.05), and also simultaneously induced the expression of BCL-xL and TERT and suppressed the expression of caspase-3 in resulting blastocysts (P < 0.05). These results suggest that both GDNF and EGF may play an important role in the regulation of porcine in vitro oocyte maturation and the combination of these growth factors could promote oocyte competency and blastocyst quality.

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The effects of glial cell line‐derived neurotrophic factor on the in vitro matured porcine oocyte transcriptome

Cited by 10 publications

References 43 publications

Optimal doses of EGF and GDNF act as biological response modifiers to improve porcine oocyte maturation and quality

Optimal doses of EGF and GDNF act as biological response modifiers to improve porcine oocyte maturation and quality

MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells

Combination effects of epidermal growth factor and glial cell line-derived neurotrophic factor on the in vitro developmental potential of porcine oocytes

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