Effects of Heat Stress on the Redox Status in the Oviduct and Early Embryonic Development in Mice

Abstract

Abstract. This study examined the association between redox status in the oviduct and early embryonic death in heat-stressed mice. In Experiment 1, non-pregnant mice were heat-stressed at 35 C with 60% relative humidity for 12, 24, or 36 h, and the maternal redox status was verified by measuring the levels of reactive oxygen species (ROS) and free radical scavenging activity (FRSA) in the oviduct, and thiobarbituric acid reactive substances (TBARS) and glutathione peroxidase (GSHPx) activity in the liver. In Experiment 2, zygotes were collected from mice heat-stressed for 12 h on the day of pregnancy, and their developmental abilities were assessed in vitro, along with the intensity of DNA damage at the 2-cell stage. The TBARS value and GSH-Px activity in the liver, and ROS level in the oviduct were significantly higher in heat-stressed mice, and this increase appeared to depend on the duration of the heat stress. Maternal heat stress significantly reduced the percentage of zygotes that developed to the morula and blastocyst and the total cell number in the blastocyst. In addition, DNA damage at the 2-cell stage was significantly higher in maternally heat-stressed embryos. These results suggest that heat stress induces systemic changes in redox status in the maternal body, and the resultant increase in oxidative stress in the oviduct is possibly involved in heat stress-induced early embryonic death . Key words: Early embryo death, Heat stress, Oxidative stress, Reactive oxygen species (J. Reprod. Dev. 51: [281][282][283][284][285][286][287] 2005) aternal hyperthermia during early pregnancy in heat-stressed animals often leads to preimplantation embryonic death. Although this is a common phenomenon in many mammalian species, e.g., in cattle [1], pigs [2], sheep [3], rats [4] and mice [5], the syndrome is more pronounced in high performance lactating cows because of their elevated metabolic heat production [6,7]. Hyperthermia-induced early embryonic death is generally ascribed to the high susceptibility of early embryos to elevated maternal body temperature [8,9]. However, recent studies have indicated that the disruption of embryonic development in heatstressed animals is connected with heat-stressassociated changes in the maternal body. Rivera and Hansen [10] have shown that in vitro exposure of bovine zygotes to a fluctuating high temperature (39.5-40.5 C), that carefully mimicked the rectal temperature of heat-stressed hyperthermic cows f or 2 4 h , d i d n ot c om p rom i s e s u bs e q ue nt development to the blastocyst stage. Similarly, we observed that the deleterious effects of maternal heat stress on mouse zygotes were not related to high body temperature alone, but were mediated

Effects of Seasonal Changes on In Vitro Developmental Competence of Porcine Oocytes

“…Additionally, heat stress was found to change the numbers of follicles and their diameters [6] and also to modify the fatty acid [6] and protein [18] composition of the porcine oocyte plasma membrane. Furthermore, heat stress induces reactive oxygen species and results in apoptosis of granulosa cells in mice and rats [19,20]. As reported in previous bovine studies [6][7][8], the present results clearly showed a negative relationship between developmental competence of porcine oocytes and atmospheric temperatures.…”

Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes

“…For example, exposing zygotes to heat shock has resulted in early embryonic loss, in association with increased hydrogen peroxide concentrations and reduced levels of GSH within the embryos (Ozawa et al 2002). Hyperthermia enhances the production of ROS in the mouse liver (Ozawa et al 2004) and oviduct (Matsuzuka et al 2005), shifting the redox status toward oxidative stress. In addition, in vitro supplementation of GSH or GSH ester reduced the effect of heat shock on viability of mouse embryos (Aréchiga et al 1995), while inhibition of GSH synthesis aggravated the deleterious effect of heat stress on the oocyte developmental capacity .…”

DL- -Tocopherol acetate mitigates maternal hyperthermia-induced pre-implantation embryonic death accompanied by a reduction of physiological oxidative stress in mice

“…For example, heat exposure of cattle on the day of artificial insemination compromises pre-implantation embryo development in vivo (Ealy et al 1993). Previous reports from our group have shown that maternal hyperthermia for 12 h soon after mating strongly disturbs normal embryonic development both in vitro (Ozawa et al 2002, Matsuzuka et al 2005a and in vivo (Ozawa et al 2003). The present results are consistent with those of previous studies, in that heat exposure of mated mice for 12 h severely compromised normal embryonic development, as determined by the blastocyst formation rate and the cell numbers in the blastocysts (Table 1).…”

“…In fact, recent reports have demonstrated that culturing zygotes at high temperatures, within the physiological range, in hyperthermic cows (40.5 8C) for 12 h did not alter subsequent development to the blastocyst stage (Ryan et al 1992. Our previous study has also indicated that in vitro exposure of zygotes to high temperature, mimicking the average rectal temperature of hyperthermic mice (39.5 8C), does not alter the blastocyst development rate, whereas maternal heat exposure for 12 h soon after mating drastically arrests subsequent embryonic development and is accompanied by increased H 2 O 2 levels, decreased GSH levels (Ozawa et al 2002) and damaged genomic DNA in the embryos, as assessed by elongation of the ladder tail in a comet assay, which is typical of ROS-mediated injury (Matsuzuka et al 2005a).…”

“…For example, Salo et al (1991) have reported that hyperthermia caused by exercise increases the generation of superoxide anion radicals and hydrogen peroxide in skeletal muscles and the heart. Similarly, heat stress-induced maternal hyperthermia enhances ROS production in the oviduct (Ozawa et al 2004, Matsuzuka et al 2005a, 2005b and lipid peroxidation in the liver (Matsuzuka et al 2005b). ROS are strongly reactive with cellular molecules and can cause serious dysfunction, such as enzyme inactivation (Halliwell & Gutteridge 1984), mitochondrial abnormalities (Kowaltowski & Vercesi 1999) and DNA fragmentation (Lopes et al 1998, Takahashi et al 1999.…”