Effects of paternal heat stress on the in vivo development of preimplantation embryos in the mouse

Abstract

-The objective of this study was to examine the effect of paternal heat stress on the in vivo development of preimplantation embryos in the mouse. Synchronised B6CBF1 female mice were mated either to a control male mouse or to one that had been exposed at 7, 21 or 35 days previously, for 24 h to an ambient temperature of 36 ± 0.3 °C and 66 ± 5.6% relative humidity. Embryos were collected from the oviducts of mice at 14-16 h, 34-39 h or 61-65 h after mating or from the uterus at 85-90 h after mating and their developmental status was evaluated morphologically. The number of cells within blastocysts was also determined using bisbenzimide-propidium iodide staining. Paternal heat stress 7 days before mating reduced the proportion of embryos developing from 4-cell (4-C) to morulae (M), hatched blastocysts, total blastocysts and the number of inner cell mass (ICM) and trophectoderm (TE) cells in the blastocyst. Paternal heat stress 21 days prior to mating reduced the proportion of 2-C and 4-C to M embryos with no embryos developing to blastocysts. There were also increases in the number of 1-C and abnormal embryos recorded at this time. Paternal heat stress 35 days before mating decreased the proportion of 2-C embryos, expanded blastocysts and ICM and TE cells in the blastocyst. These results support previous work demonstrating that both the sperm in the epididymis and germ cells in the testis are susceptible to damage by environmental heat stress, with spermatocytes being the most vulnerable. This study also demonstrates that subtle effects on the male such as a short exposure to elevated environmental temperatures can translate to quite profound paternal impacts on early embryo development.paternal heat stress / in vivo development / mouse preimplantation embryos

Whole-body heat exposure induces membrane changes in spermatozoa from the cauda epididymidis of laboratory mice

“…The possible effects of whole-body heating on spermatozoa are less clear. There is some 592 npg suggestive evidence that paternal heat stress of 36ºC for 24 h a day may result in abnormalities in early embryo development [7,8], but these studies did not show any observable changes to the spermatozoa that could have produced such defects.…”

Modulation of embryonic development due to mating with immunised males

“…The exposure of male individuals to environmental factors during the pre-fertilisation period impacts the pre-and postnatal development of the progeny (Hales et al 1986;Hales and Robaire 2001;Zhu and Setchell 2004;Curley et al 2011). This phenomenon, known as paternal effects, contributes significantly to phenotypic diversity (Chong et al 2007;Curley et al 2011).…”

Mild induced testicular and epididymal hyperthermia alters sperm chromatin integrity in men

“…In mice, a paternal effect on embryo development has been demonstrated after 24 hours' exposure to an ambient temperature of 36 C, resulting in impaired embryo development (32). In addition, local scrotal heating of male mice to a high temperature (40-42 C for 30 minutes) caused sperm DNA breakdown, reduced pregnancy rates, low placental weight and litter size, and arrested embryo development at blastocyst stage (33,34).…”