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

J Reprod Dev. 2018 Jun 22;64(3):243-251. doi: 10.1262/jrd.2017-160. Epub 2018 Mar 18.

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.

Keywords: ATP content; Glutathione; Heat stress; Oxidative phosphorylation; Transcriptome.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Cattle
  • Embryonic Development / physiology*
  • Female
  • Fertilization in Vitro / veterinary
  • Hot Temperature
  • In Vitro Oocyte Maturation Techniques / methods
  • In Vitro Oocyte Maturation Techniques / veterinary
  • Mitochondria / metabolism*
  • Oocytes / metabolism*
  • Oxidative Phosphorylation
  • Pregnancy
  • Reactive Oxygen Species / metabolism
  • Stress, Physiological / physiology*
  • Transcriptome

Substances

  • Reactive Oxygen Species
  • Adenosine Triphosphate