Mitochondrial-related consequences of heat stress exposure during bovine oocyte maturation persist in early embryo development

Abstract

Hyperthermia during estrus has direct consequences on the maturing oocyte that carries over to the resultant embryo to compromise its ability to continue in development. Because early embryonic development is reliant upon maternal transcripts and other ooplasmic components, we examined impact of heat stress on bovine oocyte transcripts using microarray. Oocytes were matured at 38.5ºC for 24 h or 41.0ºC for the first 12 h of in vitro maturation; 38.5ºC thereafter. Transcriptome profile was performed on total (adenylated + deadenylated) RNA and polyadenylated mRNA populations. Heat stress exposure altered the abundance of several transcripts important for mitochondrial function. The extent to which transcript differences are coincident with functional changes was evaluated by examining reactive oxygen species, ATP content, and glutathione levels. Mitochondrial reactive oxygen species levels were increased by 6 h exposure to 41.0ºC while cytoplasmic levels were reduced compared to controls (P < 0.0001). Exposure to 41.0ºC for 12 h increased total and reduced glutathione levels in oocytes at 12 h but reduced them by 24 h (time × temperature P < 0.001). ATP content was higher in heat-stressed oocytes at 24 h (P < 0.0001). Heat-induced increases in ATP content of matured oocytes persisted in early cleavage-stage embryos (8- to 16-cell embryos; P < 0.05) but were no longer apparent in blastocysts (P > 0.05). Collectively, results indicate that direct exposure of maturing oocytes to heat stress may alter oocyte mitochondrial processes/function, which is inherited by the early embryo after fertilization.

Heat stress, a serious threat to reproductive function in animals and humans

“…In bovine oocytes, exposing oocytes to high temperature (41°C) during the first 6 hr of IVM increased mitochondrial ROS levels, whereas cytoplasmic ROS levels decreased compared with controls (Payton et al, ). After 12 hr of high thermal exposure, oocyte developmental competence is compromised and apoptosis increases within the inner cell mass (ICM) cells of the blastocysts obtained from HS oocytes (Ascari et al, ).…”

Stress‐induced alterations in oocyte transcripts are further expressed in the developing blastocyst

“…Rearrangement of the mitochondria during maturation is associated with increased mitochondrial polarity and activity, and these have been found to be altered by seasonal thermal stress and associated with reduced embryonic development (Gendelman & Roth, ). Recently, Payton et al () reported that exposing bovine oocytes to heat shock (41°C) during in vitro maturation impairs mitochondrial reactive oxygen species, glutathione and ATP contents in the oocyte. Interestingly, the oocyte ATP content increased upon exposure to heat stress (41°C for 24 hr) and persisted in 8‐ to 16‐cell embryos, but not in the blastocyst, suggesting a long‐lasting effect on mitochondrial function through the early cleavage stages of embryonic development.…”

“…Recent studies have provided new insight into the molecular alterations induced by heat shock, including impairments in both maternal and mitochondrial transcripts (Ferreira et al, ; Gendelman & Roth, , ; Payton et al, , ). These observations could clarify, in part, the mechanism underlying the response of the oocyte to heat stress and the further consequences in the developing embryo.…”

“…A recent study in which bovine oocyte transcripts were examined by microarray revealed that heat stress alters the relative abundance of transcripts related to mitochondrial function (Payton et al, ), in particular those involved in electron chain transport and oxidative‐phosphorylation reactions ( ATP5O , COQ3 , and NDUFC2 ). These alterations were associated with a temporal increase in mitochondrial reactive oxygen species and changes in total glutathione content.…”

“…Furthermore, ATP content was higher in heat‐stressed oocytes and in embryos that developed from those oocytes. Increased ATP content persisted throughout the early stages (two cells and 8–16 cells) of embryonic development, but not in the formed blastocysts (Payton et al, ).…”