Plasma markers of oxidative stress are uncorrelated in a wild mammal.

Louise L Christensen,Daniel H Nussey,Jonathan D Blount,Josephine M Pemberton,Kathryn A Watt,Jane M Reid,Colin Selman,Jill G Pilkington

doi:10.1002/ece3.1771

Abstract

Oxidative stress, which results from an imbalance between the production of potentially damaging reactive oxygen species versus antioxidant defenses and repair mechanisms, has been proposed as an important mediator of life-history trade-offs. A plethora of biomarkers associated with oxidative stress exist, but few ecological studies have examined the relationships among different markers in organisms experiencing natural conditions or tested whether those relationships are stable across different environments and demographic groups. It is therefore not clear to what extent studies of different markers can be compared, or whether studies that focus on a single marker can draw general conclusions regarding oxidative stress. We measured widely used markers of oxidative damage (protein carbonyls and malondialdehyde) and antioxidant defense (superoxide dismutase and total antioxidant capacity) from 706 plasma samples collected over a 4-year period in a wild population of Soay sheep on St Kilda. We quantified the correlation structure among these four markers across the entire sample set and also within separate years, age groups (lambs and adults), and sexes. We found some moderately strong correlations between some pairs of markers when data from all 4years were pooled. However, these correlations were caused by considerable among-year variation in mean marker values; correlation coefficients were small and not significantly different from zero after accounting for among-year variation. Furthermore, within each year, age, and sex subgroup, the pairwise correlation coefficients among the four markers were weak, nonsignificant, and distributed around zero. In addition, principal component analysis confirmed that the four markers represented four independent axes of variation. Our results suggest that plasma markers of oxidative stress may vary dramatically among years, presumably due to environmental conditions, and that this variation can induce population-level correlations among markers even in the absence of any correlations within contemporaneous subgroups. The absence of any consistent correlations within years or demographic subgroups implies that care must be taken when generalizing from observed relationships with oxidative stress markers, as each marker may reflect different and potentially uncoupled biochemical processes.

Highlights

The balance between production of potentially damaging reactive oxygen species (ROS) and the mobilization of antioxidant (AOX) defenses and repair systems that prevent damage is of fundamental importance to cellular and organismal function (Balaban et al 2005; Monaghan et al 2009)
An important question still remains: Can we draw general conclusions about patterns of variation in Oxidative stress (OS) and their consequences for life histories from just one or a few markers, or Are the findings of any one study of OS likely to be specific to the markers selected and the context in which they are measured? Our findings support the latter conclusion
Considering all data pooled across years, we found unexpected negative correlations between our two oxidative damage markers (PC and MDA) which in turn had opposing correlations with one (SOD) but not the other (TAC) of our antioxidant markers

Summary

Introduction

The balance between production of potentially damaging reactive oxygen species (ROS) and the mobilization of antioxidant (AOX) defenses and repair systems that prevent damage is of fundamental importance to cellular and organismal function (Balaban et al 2005; Monaghan et al 2009). Correlations Among Oxidative Stress Markers during aerobic metabolism within the mitochondria They are important components of cellular signaling (e.g., Nemoto et al 2000) and immune function (Babior et al 1973; Forman and Torres 2002), but in excess can cause DNA, lipid, and protein damage and disrupt cellular function (Harman 1956; Beckman and Ames 1998; Buffenstein et al 2008). Oxidative stress (OS) has been defined as “an imbalance between oxidants and AOX in favor of the oxidants” (Sies and Jones 2007) This arises when ROS production exceeds the capacity of AOX defenses, potentially leading to disruption of redox signaling and cellular damage and dysfunction (Sies 1991; Sies and Jones 2007; Limon-Pacheco and Gonsebatt 2009)

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