Idebenone relieves the damage of heat stress on the maturation and developmental competence of porcine oocytes

Author(s):  
Xueying Shi ◽  
Xiaohu Jin ◽  
Jingyi Lin ◽  
Liangzhen Sun ◽  
Xue Liu ◽  
...  
Reproduction ◽  
2002 ◽  
pp. 683-689 ◽  
Author(s):  
M Ozawa ◽  
M Hirabayashi ◽  
Y Kanai

Mammalian preimplantation embryos are sensitive to maternal and direct heat stress. However, the mechanisms by which heat stress affects early embryonic development in vivo or in vitro are unknown. This study examined whether heat-stress-induced loss of developmental competence in mouse embryos was mediated by physiological changes in the maternal environment or by high temperatures alone. After fertilization, zygotes at the same stage were heat-stressed at 39.5 degrees C for 12 h either maternally (measured by maternal rectal temperature) or directly in culture. Zygotes in each group were cultured at 37.5 degrees C for a further 84 h to assess their developmental ability. Neither type of heat stress affected the first cleavage rate. However, the proportion of embryos that developed to morulae or blastocysts was significantly lower in the maternally heat-stressed group, but not in the directly heat-stressed group. Moreover, maternal heat stress significantly reduced intracellular glutathione concentrations and enhanced hydrogen peroxide concentrations in both zygotes and two-cell embryos that were recovered immediately after heat stress or 12 h later, respectively. In contrast, direct heat stress had little effect on concentrations of glutathione or hydrogen peroxide in cultured early embryos. These results demonstrate that maternal heat stress at the zygote stage reduces the developmental ability of mouse embryos via physiological changes in the maternal environment that lead to an increase in intracellular oxidative stress on the embryo.


2021 ◽  
Vol 33 (2) ◽  
pp. 66
Author(s):  
Zvi Roth

The ovarian pool of follicles, and their enclosed oocytes, is highly sensitive to hyperthermia. Heat-induced changes in small antral follicles can later manifest as impaired follicle development and compromised competence of the enclosed oocytes to undergo maturation, fertilisation and further development into an embryo. This review describes the main changes documented so far that underlie the oocyte damage. The review discusses some cellular and molecular mechanisms by which heat stress compromises oocyte developmental competence, such as impairment of nuclear and cytoplasmic maturation and mitochondrial function, changes in the expression of both nuclear and mitochondrial transcripts and the induction of apoptosis. The review emphasises that although the oocyte is exposed to heat stress, changes are also evident in the developed embryo. Moreover, the effect of heat stress is not limited to the summer; it carries over to the cold autumn, as manifest by impaired steroid production, low oocyte competence and reduced fertility. The spontaneous recovery of oocytes from the end of the summer through the autumn until the beginning of winter suggests that only subpopulations of follicles, rather than the entire ovarian reserve, are damaged upon heat exposure.


2009 ◽  
Vol 21 (1) ◽  
pp. 195 ◽  
Author(s):  
R. R. Payton ◽  
L. A. Rispoli ◽  
J. L. Edwards

It is well established that exposure of cumulus–oocyte complexes (COC) to heat stress during the first 12 h of maturation reduces blastocyst development by 42 to 65%. Previous research supports the notion that some of the effects of heat stress on oocyte competence may be cumulus-mediated. To determine the extent to which this may occur, COC were matured at 38.5°C for 24 h (control) or 41°C for the first 12 h of maturation followed by 38.5°C for remaining 12 h (heat stress). A subset of COC underwent IVF with Percoll-prepared sperm and then was cultured in KSOM containing 0.5% BSA to assess developmental competence. Remaining oocytes were denuded. Cumulus cells, kept separate by treatment, were stored in lysis buffer at –80°C until RNA extraction. Total RNA from cumulus was amplified prior to hybridization to bovine Affymetrix GeneChips (Affymetrix Inc., Santa Clara, CA, USA; n = 8 pools per treatment collected on 8 different occasions; n = 16 chips). Following pre-processing using the MAS5.0 algorithm, microarray data were subjected to linear modeling and empirical Bayes analyses (Bioconductor, Limma package). False discovery rate was controlled using the Benjamini and Hochberg method, and differentially expressed genes were selected by an adjusted P-value (P < 0.05). Functional annotation of selected genes was performed using NetAffx (Affymetrix Inc.) and Database for Annotation, Visualization and Integrated Discovery (DAVID; NIAID, NIH, Bethesda, MD, USA). Heat stress of COC reduced blastocyst development (27.2 v. 16.1% for control v. heat stress, respectively; SEM = 1.6; P < 0.002). Approximately 66 and 65% of 24 000 possible genes were called present (i.e. expressed) in RNA from cumulus of competent (control) v. challenged (heat-stressed) oocytes, respectively. In cumulus from developmentally challenged COC, increased abundance of 42 genes (36 currently annotated) was noted. Use of DAVID demonstrated enrichment of genes important for electron transport and energy generation (NOS2A, MAOB, CYP11A1, HSD11B1L, LTB4DH). Further examination of gene ontology identified genes associated with mitochondrial function (SLC25A10, MAOB, CYP11A1), cell signaling (similar to JAK-3, FSHR, CYP11A1, WNT2B), cytoskeleton (ACTA1), antioxidant activity (GSTA1), and extracellular region (FMOD). In contrast, cumulus from developmentally competent COC had increased expression of 22 genes (20 currently annotated), of which 15% were related to protein binding (CAV1, MMP9, TGFB2) according to DAVID. Further analysis using gene ontology revealed genes associated with extracellular matrix formation (MMP9, MMP19, PCOLCE2) and neural tissue (METRNL). In summary, alterations in cumulus gene expression were associated with differences in developmental competence of oocytes. Additional research is necessary to examine the extent to which identified genes account for functional differences in oocyte competence. This research was supported in part by National Research Initiative Competitive Grant no. 2004-35203-14772 from the USDA Cooperative State Research, Education, and Extension Service.


2017 ◽  
Vol 52 ◽  
pp. 48-51 ◽  
Author(s):  
M Vendrell-Flotats ◽  
N Arcarons ◽  
E Barau ◽  
M López-Béjar ◽  
T Mogas

2009 ◽  
Vol 21 (1) ◽  
pp. 226
Author(s):  
A. M. Ward ◽  
F. N. Schrick ◽  
R. R. Payton ◽  
E. Peixoto ◽  
J. L. Edwards

Studies in the literature have shown that cumulus–oocyte complexes produce PGF2α, that ova and cumulus cells have PGF2α receptors, and that PGF2α addition to maturing ova, above what would normally be produced, decreases blastocyst development. Because previous studies have shown elevated systemic and tissue levels of PGF2α as a consequence of heat stress, it was hypothesized that detrimental effects of exposing maturing ova to elevated temperatures may be mediated in part through heat-induced increases in PGF2α. To test this hypothesis, cumulus–oocyte complexes were matured at 38.5 or 41.0°C in the presence of a PGF2α receptor antagonist (AL-8810). Preattachment embryo development of AL-8810-treated ova was compared with development of ova matured in media with or without diluent (DMSO added at the same concentration as AL-8810; diluent and developmental controls, respectively), resulting in 6 total treatment combinations. Data were analyzed as a randomized block design (blocking on oocyte collection date) with fixed effects of maturation temperature, AL-8810, and the respective interaction included in the statistical model. In experimental replicates in which the effects of heat stress decreased blastocyst development greater than 10% (n = 14), a significant maturation temperature × AL-8810 interaction was noted when evaluating blastocyst development (P = 0.05). Specifically, when ova were heat stressed during the first 12 h of in vitro maturation, blastocyst development was reduced in developmental and diluent controls (26.2 v. 18.8 and 24.4 v. 19.9, respectively; SEM = 1.6). In contrast, when ova were matured under the same conditions but in the presence of a PGF2α receptor antagonist, the effects of heat stress to reduce blastocyst development after in vitro fertilization were no longer observed (22.5 v. 22.5; SEM = 1.6). When using abattoir-derived ovaries, it is not uncommon to collect, on occasion, ova that are developmentally challenged (i.e. blastocyst development is less than the 20 to 50% expected). In this experiment, this occurred on 5 occasions. Data from these experimental replicates were analyzed and reported separately because previous efforts had shown that the responsiveness of ova to changes in culture environment differs depending on the level of developmental competence. Relevant to this study, addition of AL-8810 to developmentally challenged ova matured under thermoneutral conditions increased cleavage (60.4 v. 55.4%, respectively; P = 0.06) and blastocyst development (17.7 v. 13.7%, respectively; P = 0.07). In summary, data illustrate that developmentally challenged ova, heat-stressed or otherwise, are susceptible to detrimental effects of PGF2α. The ability to increase blastocyst development approaching or exceeding the values expected for competent ova suggests the usefulness of a PGF2α receptor antagonist during in vitro maturation to improve the efficiency of in vitro production procedures.


Zygote ◽  
2011 ◽  
Vol 20 (3) ◽  
pp. 249-259 ◽  
Author(s):  
Hisashi Nabenishi ◽  
Hiroshi Ohta ◽  
Toshihumi Nishimoto ◽  
Tetsuo Morita ◽  
Koji Ashizawa ◽  
...  

SummaryIn the present study, we investigated the effects of various concentrations of cysteine (0.0, 0.6, 1.2 and 1.8 mM) added to the maturation medium on nuclear maturation and subsequent embryonic development of bovine oocytes exposed to heat stress (HS: set at 39.5 °C for 5 h, 40.0 °C for 5 h, 40.5 °C for 6 h, and 40.0 °C for 4 h versus 38.5 °C for 20 h as the control group). This regime mimicked the circadian rhythm of the vaginal temperature of lactating dairy cows during the summer season in southwestern Japan. Moreover, we also evaluated the oocyte's reactive oxygen species (ROS) and glutathione (GSH) levels and the apoptosis levels of the oocytes and cumulus cells in the presence or absence of 1.2 mM cysteine. As a result, HS in the without-cysteine group significantly suppressed (p < 0.05) both the nuclear maturation rate up to the metaphase (M)II stage and the blastocyst formation rate compared with that of the control group. In addition, this group showed significantly higher (p < 0.05) ROS levels and significantly lower (p < 0.05) GSH levels than those of the control group. Moreover, the level of TdT-mediated dUTP nick end labelling (TUNEL)-positive cumulus cells in the HS without-cysteine group was significantly higher (p < 0.05) than that of the control group. However, the addition of 1.2 mM cysteine to the maturation medium restored not only the nuclear maturation, blastocyst formation rates and GSH contents, but also increased the ROS and TUNEL-positive levels of the cumulus cells, but not oocytes, to that of the control group. These results indicate that the addition of 1.2 mM cysteine during in vitro maturation (IVM) may alleviate the influence of heat stress for oocyte developmental competence by increasing GSH content and inhibiting the production of oocyte ROS followed by apoptosis of cumulus cells.


2016 ◽  
Vol 28 (2) ◽  
pp. 228
Author(s):  
L. A. Rispoli ◽  
R. R. Payton ◽  
C. Gondro ◽  
A. M. Saxton ◽  
J. L. Edwards

Direct exposure of maturing oocytes to a physiologically relevant elevated temperature reduces embryo development after fertilisation and has been coincident with reduced de novo protein synthesis. Mechanisms responsible for heat-induced reductions in protein synthesis are unknown but may be related to alterations in the transcriptome of the maturing oocyte. To determine the extent to which this may occur, the impact of heat stress on the maternal pool of RNA in bovine oocytes was assessed using microarrays. After maturation for 24 h at 38.5°C (control) or 41°C (first 12 h only, 38.5°C thereafter; heat stress) oocytes were denuded from associated cumulus cells and lysed for RNA extraction or underwent IVF to assess developmental competence. Total RNA from oocytes was amplified by 3′-poly(A) priming or a combination of 3′-poly(A) and internal priming because oocyte transcripts may or may not have a polyadenylated tail. Amplified RNA was hybridised to GeneChip Bovine Genome Arrays (Affymetrix, Santa Clara, CA, USA; 8 oocyte pools per treatment were collected on 7 different occasions and amplified by 2 methods; n = 32 chips). Differential transcript abundance was determined using R and Bioconductor with only probes having a P < 0.01, a fold change of at least 1.3, and called present for at least half the arrays. Functional annotation of selected transcripts was performed using Gene Ontology and KEGG annotations (Bos taurus build 4.0) and DAVID (v 6.7) with significance level set at P < 0.10. Coincident with reduced blastocyst development (28.3 v. 15.2% for control v. heat stress, respectively; SEM = 3.6; P < 0.0003), heat stress altered the abundance of 159 transcripts (22 increased, 137 decreased); 130 of these were annotated. Use of DAVID demonstrated enrichment of genes important for mitochondrial function and RNA processing. Towards validating certain findings, the relative abundance of 3 mitochondrial transcripts (NDUFC2, COQ3, ATP5O) were assessed by quantitative PCR on non-amplified RNA from the oocyte samples used for the microarray study. Gene-specific primers were designed for 5′ and 3′ ends of transcripts when possible. Exposure to elevated temperature during the first 12 h of oocyte maturation reduced transcript levels of NDUFC2 at the 5′ and 3′ ends (P < 0.0001 and P = 0.003), COQ3 at the 3′ end (P = 0.02) and ATP5O at the 5′ end (P = 0.02). In conclusion, exposure of maturing cumulus-oocyte complexes to a physiologically-relevant elevated temperature altered the transcriptome in oocytes, especially certain transcripts important for mitochondrial function. This research was supported in part by USDA National Institute of Food and Agriculture, Hatch Project No. 227701, the state of Tennessee through University of Tennessee AgResearch, Department of Animal Science, and East Tennessee Research and Education Center.


2021 ◽  
Vol 33 (2) ◽  
pp. 153
Author(s):  
M. T. Moura ◽  
C. A. I. Carvalho ◽  
F. R. O. Barros ◽  
F. Mossa ◽  
D. Bebbere ◽  
...  

Heat stress (HS) is characterised by an elevation in body temperature that ultimately undermines organism physiology. Most livestock production occurs in tropical regions under potential HS conditions that diminish productive and reproductive potential. Despite extensive evidence of HS-mediated effects in cell function, stage-specific detrimental effects of HS during oogenesis remain elusive. Mouse models represent an attractive alternative for faster interrogation of stage-specific phenomena during oogenesis. Therefore, the aim of the study was to determine the effects of HS exposure during the major window of female mice germ-cell DNA methylation programming. CD1/Swiss female mice with litters (F0 progeny) at postnatal Day 10 (P10) were randomly allocated to HS (35°C/12-h light; 21°C/12-h dark) or control (CTL: 21°C/24h) for 11 days. The F0 progeny were weaned at P21 and superovulated after reaching puberty at P35. F0 females were superovulated by intraperitoneal injections with 5.0IU of equine chorionic gonadotrophin (PMSG) followed by 5.0IU of human chorionic gonadotrophin (hCG) within a 48-h interval. Pre-implantation embryos were harvested at Day E3.5 in M2 medium under a stereomicroscope. One F0 female per litter was randomly mated to control mice when it reached 6 weeks of age. Data were subjected to least-squares analysis of variance using the General Linear Models procedure of SAS (SAS Institute Inc.). The experiment was replicated twice (CTL: n=4 F0 females and HS: n=4 F0 females). Preliminary results are given as LSM±s.e.m. There was no effect of heat stress on the number of embryos collected per female (CTL: 9.75±4.87 vs. HS: 11.25±4.81) or the percentage of non-viable embryos (CTL: 25.0±0.23% vs. HS: 42.5±0.25%). However, heat stress tended (P=0.07) to reduce the percentage of embryos that reached the morula stage from 63.5±0.08% for CTL to 35.1±0.09% for HS. The percentage of blastocysts collected (CTL: 11.45±0.18% vs. HS: 22.32±0.19%) and litter size of F0 females (CTL: 7.47±1.76 vs. HS: 7.66±1.47) was not affected by treatment. In conclusion, exposure of female mice to 11-day HS during the major wave of de novo DNA methylation during oocyte growth tended to reduce subsequent pre-implantation embryonic development, although it did not affect full-term development after natural mating.


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