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Maternally derived yolk antioxidants buffer the developing avian embryo against oxidative stress induced by hyperoxia

Watson, Hannah LU ; Salmón, Pablo LU and Isaksson, Caroline LU (2018) In Journal of Experimental Biology 221(13).
Abstract

In oviparous animals, maternally transferred antioxidants protect the embryo from oxidative damage from high rates of reactive oxygen species (ROS) production incurred by rapid growth. Elevated ROS exposure, beyond that incurred by normal growth, can occur as a result of exposure to exogenous factors (e.g. pollutants, toxins, radiation), increasing the risk of oxidative damage, with potentially adverse consequences for embryonic development and long-term fitness. The capacity of the avian embryo’s antioxidant protection system to counter an increased exogenous oxidative threat is poorly understood. We induced an external oxidative challenge via experimental increase in ambient oxygen concentration throughout incubation of wild great tit... (More)

In oviparous animals, maternally transferred antioxidants protect the embryo from oxidative damage from high rates of reactive oxygen species (ROS) production incurred by rapid growth. Elevated ROS exposure, beyond that incurred by normal growth, can occur as a result of exposure to exogenous factors (e.g. pollutants, toxins, radiation), increasing the risk of oxidative damage, with potentially adverse consequences for embryonic development and long-term fitness. The capacity of the avian embryo’s antioxidant protection system to counter an increased exogenous oxidative threat is poorly understood. We induced an external oxidative challenge via experimental increase in ambient oxygen concentration throughout incubation of wild great tit Parus major eggs in the laboratory. At day 11 of incubation, brain tissue revealed no consistent differences in oxidative stress status [as measured by antioxidant levels (superoxide dismutase and total glutathione), lipid peroxidation and telomere length] between control (21% oxygen) and hyperoxic (40% oxygen) embryos. However, the level of vitamin E was significantly lower and lipid peroxidation was significantly higher in yolks of eggs reared under elevated oxygen concentrations. The results suggest that maternally derived yolk antioxidants successfully buffer developing embryonic tissues against an increased exogenous oxidative threat. Furthermore, vitamin E plays a more important role in protecting the embryo than carotenoids. However, the depletion of antioxidants and increased peroxidation of lipids in the yolk could have negative consequences for embryonic development, in particular for the brain and heart that require highly unsaturated fatty acids, and protection against the oxidative burst following hatching.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Antioxidant, Hyperoxia, Lipid peroxidation, Oxidative stress, Prenatal development, Vitamin E
in
Journal of Experimental Biology
volume
221
issue
13
publisher
The Company of Biologists Ltd
external identifiers
  • scopus:85049678763
ISSN
0022-0949
DOI
10.1242/jeb.179465
language
English
LU publication?
yes
id
89e02c90-466b-4e74-9e81-6636f85d3a0f
date added to LUP
2018-07-30 14:11:39
date last changed
2019-02-20 11:23:14
@article{89e02c90-466b-4e74-9e81-6636f85d3a0f,
  abstract     = {<p>In oviparous animals, maternally transferred antioxidants protect the embryo from oxidative damage from high rates of reactive oxygen species (ROS) production incurred by rapid growth. Elevated ROS exposure, beyond that incurred by normal growth, can occur as a result of exposure to exogenous factors (e.g. pollutants, toxins, radiation), increasing the risk of oxidative damage, with potentially adverse consequences for embryonic development and long-term fitness. The capacity of the avian embryo’s antioxidant protection system to counter an increased exogenous oxidative threat is poorly understood. We induced an external oxidative challenge via experimental increase in ambient oxygen concentration throughout incubation of wild great tit Parus major eggs in the laboratory. At day 11 of incubation, brain tissue revealed no consistent differences in oxidative stress status [as measured by antioxidant levels (superoxide dismutase and total glutathione), lipid peroxidation and telomere length] between control (21% oxygen) and hyperoxic (40% oxygen) embryos. However, the level of vitamin E was significantly lower and lipid peroxidation was significantly higher in yolks of eggs reared under elevated oxygen concentrations. The results suggest that maternally derived yolk antioxidants successfully buffer developing embryonic tissues against an increased exogenous oxidative threat. Furthermore, vitamin E plays a more important role in protecting the embryo than carotenoids. However, the depletion of antioxidants and increased peroxidation of lipids in the yolk could have negative consequences for embryonic development, in particular for the brain and heart that require highly unsaturated fatty acids, and protection against the oxidative burst following hatching.</p>},
  articleno    = {jeb179465},
  author       = {Watson, Hannah and Salmón, Pablo and Isaksson, Caroline},
  issn         = {0022-0949},
  keyword      = {Antioxidant,Hyperoxia,Lipid peroxidation,Oxidative stress,Prenatal development,Vitamin E},
  language     = {eng},
  month        = {07},
  number       = {13},
  publisher    = {The Company of Biologists Ltd},
  series       = {Journal of Experimental Biology},
  title        = {Maternally derived yolk antioxidants buffer the developing avian embryo against oxidative stress induced by hyperoxia},
  url          = {http://dx.doi.org/10.1242/jeb.179465},
  volume       = {221},
  year         = {2018},
}