Reproduction in Domestic Animals

Follicular and Oocyte Competence under Heat Stress 241(Takami et al. 1999), whereas excessive ROS levelswithin the follicle are associated with increased cytoplasmicdefects and abnormal chromosomal segregation(Van Blerkom et al. 1997).Given the importance of the oxidative status of theoocyte, and the fact that bovine oocytes are rich in fattyacids (McEvoy et al. 2000), membrane fatty-acid compositionis considered a major factor in determining theoocyte’s fate (Matorras et al. 1998). Seasonally increasedvariation in the fatty-acid profiles of thefollicular fluid and oocytes is associated with reduceddevelopment of the oocyte (Zeron et al. 2001). In the hotsummer, the proportions of saturated fatty acids inoocyte and granulosa cells are higher than those ofmono- and polyunsaturated fatty acids, implyingreduced oxidative status of the oocyte. Thus, administrationof antioxidants to reduce fatty-acid oxidation isone suggested strategy to stabilize the oocyte membraneupon heat stress. A recent study in mice providesevidence that administration of the antioxidant epigallocatechingallate (EGCG; 100 mg ⁄ kg body weight)before induction of hyperthermia increases the proportionof in-vivo-derived zygotes that reach the blastocyststage (Aroyo et al. 2006). Similarly, in-vitro maturationwith polyphenols improved the production of bovineembryos (Wang et al. 2007). A beneficial effect was alsoachieved by feeding lactating cows the antioxidantb-carotene (400 mg ⁄ day) for 90 days before insemination(Arechiga et al. 1998). Apparently, unlike forembryos (Hansen 2007b), antioxidant administrationcan alleviate the effect of thermal stress on the ovarianpool of oocytes.Accumulating evidence suggests that fat supplementationinfluences reproductive processes that are notdirectly related to energy balance and has beneficialeffects on the follicle, oocyte, embryo, and uterus(Mattos et al. 2000; Thatcher et al. 2003). Alterationsin fatty-acid composition of the oocyte might improveits developmental capacity. Zeron et al. (2002) reportedthat feeding ewes a diet supplemented with Ca salt offish oil increases the proportion of polyunsaturated fattyacids in the plasma and cumulus cells and improvesoocyte quality, as determined by membrane integrity.Feeding cows a diet enriched in unsaturated fatty acidsduring the summer did not have a beneficial effect onoocyte quality (Bilby et al. 2006), whereas a high level offeeding (Adamiak et al. 2005) or a high level of fat in thediet (Fouladi-Nashta et al. 2007) improved oocytedevelopmental competence. Given the potential ofnutritional manipulation, further research is warrantedto identify specific fatty acids and fat levels in diets thatmay have a beneficial effect on the ovarian pool ofoocytes.Heat Stress and Early Embryonic DevelopmentStudies indicate that embryonic loss under heat stress isdue to the sensitivity of early embryos to elevatedtemperatures. Embryos at early developmental stagesare more susceptible to thermal stress and become moreresistant during later developmental phases (Hansen2007a,b). Exposure of cows to heat stress on day 1 (butnot on days 3, 5, or 7) after oestrus decreased thedevelopment and viability of embryos on day 8 (Ealyet al. 1993). Exposure of cows to elevated temperaturesbetween onset of oestrus and insemination (Putney et al.1988) decreased subsequent embryo development. Similarly,induction of heat shock in vitro blocked thedevelopment of two-cell-stage embryos but had only amoderate effect on four- to eight-cell-stage embryos anda limited effect on the morulae (Hansen 2007a). Nevertheless,the mechanism by which the developing embryoacquires heat resistance to cellular disruption caused byelevated temperatures is not known (for reviews, see Ju2005; Hansen 2007a).Given that oocytes and early embryos are particularlysensitive to heat stress, embryo-transfer procedures thatbypass the effects of heat stress on early embryonicdevelopment have been attempted (see review, Rutledge2001; Hansen 2007b). One major limitation of thisapproach is the poor survival of embryos followingfreezing. Transferring in-vivo-derived frozen-thawedembryos increased pregnancy rates for recipient cowsrelative to traditionally inseminated cows (Putney et al.1989). Similarly, the percentage of pregnancies duringthe hot season was greater for cows receiving in-vitroderivedfresh embryos but not for those receiving frozenembryos (Ambrose et al. 1999; Drost et al. 1999).Moreover, use of vitrification did not improve thesurvival of the transferred embryos (Al-Katanani et al.2002). There is thus a compelling need to optimizeprocedures for embryo cryopreservation.Currently, fresh or in-vivo-derived frozen embryos arethe main source for embryo-production programs.Therefore, treatments that protect the ovarian pool ofoocytes can increase the number of competent oocytesavailable for embryo transfer. A protective effect of S1Phas been reported for bovine oocytes exposed to heatshock during maturation (Roth and Hansen 2004b,2005), as reflected by the reduced proportion of oocytesthat undergo apoptosis and the increased number thatreach the MII stage and develop into blastocysts. Theseembryos seem to have a high potential for development,since embryos derived from heat-shocked and S1Pprotectedoocytes were of the same quality as those fromnon-stressed oocytes, as determined by their total cellnumber, the proportion of apoptotic cells, and theintensity of caspase activity (Roth and Hansen 2004b).Moreover, pups developed from heat-stressed mice didnot differ from control pups in their learning potentialor episodic memory, as determined by behavioural andrecognition tests (Aroyo et al. 2007a).SummaryHyperthermia can impair cellular function in varioustissues of the reproductive system. However, disruptionof the follicle and its enclosed oocyte seems to be apivotal factor in the complex mechanism via which heatstress impairs fertility. This includes alterations in theendocrine milieu and follicular microenvironment towhich the ovarian pool of oocytes is exposed, leading totheir decreased developmental competence. Hyperthermiacan directly disrupt follicular function, but a carryovereffect on the follicle and its enclosed oocyte is alsoevident.Ó 2008 The Author. Journal compilation Ó 2008 Blackwell Verlag