Redox Regulation and Oxidative Stress in Mammalian Oocytes and Embryos Developed In Vivo and In Vitro

Madeleine L M Hardy, Margot L Day, Michael B Morris, Madeleine L M Hardy, Margot L Day, Michael B Morris

Abstract

Oocytes and preimplantation embryos require careful regulation of the redox environment for optimal development both in vivo and in vitro. Reactive oxygen species (ROS) are generated throughout development as a result of cellular metabolism and enzyme reactions. ROS production can result in (i) oxidative eustress, where ROS are helpful signalling molecules with beneficial physiological functions and where the redox state of the cell is maintained within homeostatic range by a closely coupled system of antioxidants and antioxidant enzymes, or (ii) oxidative distress, where excess ROS are deleterious and impair normal cellular function. in vitro culture of embryos exacerbates ROS production due to a range of issues including culture-medium composition and laboratory culture conditions. This increase in ROS can be detrimental not only to assisted reproductive success rates but can also result in epigenetic and genetic changes in the embryo, resulting in transgenerational effects. This review examines the effects of oxidative stress in the oocyte and preimplantation embryo in both the in vivo and in vitro environment, identifies mechanisms responsible for oxidative stress in the oocyte/embryo in culture and approaches to reduce these problems, and briefly examines the potential impacts on future generations.

Keywords: ROS; antioxidants; assisted reproductive technology; embryo; oocyte; redox; transgenerational effects.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 2
Figure 2
Cellular sources of ROS and antioxidants, and the effects of oxidative distress. Numerous cellular enzymes (yellow discs) produce ROS (shown in yellow sunbursts), whose homeostatic concentrations are controlled by a comprehensive system of antioxidants (only GSH is shown here) and antioxidant enzymes (blue discs) [37]. Principal sources are NOX, Complexes I–III of the mitochondrial electron transport chain due primarily to electron leakage [8,26], and to various enzymes (not shown), such as proline oxidase, which are coupled to Complex II [8,26]. The principal ROS signalling molecule is H2O2 (physiological concentration ≈1–10 nM [8,26]), which can penetrate membranes directly or (more efficiently) by transmembrane transporters (green disks). Oxidative distress occurs when the antioxidant system cannot maintain homeostatic concentrations of ROS, which can lead to a range of cellular dysfunctions (red boxes), frequently resulting in growth arrest and apoptosis. ACOX, acyl coenzyme A oxidase; AQP, aquaporin; CAT, catalase, CuZnSOD, copper–zinc superoxide dismutase; DAO, diamine oxidase; γ-GCS, γ-glutamylcysteine synthetase; GPx, glutathione peroxidase; GRx, glutathione reductase; GS, glutathione synthetase; MnSOD, manganese superoxide dismutase; NOX, NADPH oxidase; VDAC, voltage-dependent anion channel; XOR, xanthine oxidoreductase.
Figure 3
Figure 3
Sources of ROS and antioxidants during in vivo embryo development. The preimplantation embryo develops over 5 days in the mouse in vivo. The maternal reproductive tract is an environment low in oxygen, with an oxygen gradient of approximately 8% to 2% from the oviduct to the uterus. This, along with a number of antioxidants and antioxidant enzymes, supports redox homeostasis and helps prevent irreversible oxidative damage. During oocyte maturation and preimplantation embryo development, there are numerous oxidative stressors including at ovulation, fertilisation, cellular division, and hatching. Some examples of the control of the action of these stressors by redox enzymes (in black) and antioxidants (in blue) are shown. References are shown in square brackets.
Figure 4
Figure 4
Sources of ROS for in vitro cultured oocytes and embryos. Oxidative stress can be induced by a number of laboratory processes, as shown, and a number of antioxidants can be added to the culture medium to combat these excessive ROS levels.
Figure 1
Figure 1
Effects of ROS on cellular function. ROS production has a multitude of impacts on cellular function and can act in both a beneficial and deleterious manner. ROS are produced as a ‘by-product’ of cellular metabolism and as a result of various cell-signalling pathways, including many activated by growth factors. They can also directly affect the activity of signalling pathway components and metabolic enzymes, leading to changes in cellular metabolic profile and energy usage. In turn, these changes in metabolism and signalling can lead to changes in the epigenetic landscape and the activity of transcription factors, altering gene expression. Since these events directly and indirectly affect the reproductive system, transgenerational effects resulting from normal and aberrant ROS production can and do occur.

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