Early-age changes in oxidative stress in brown trout, Salmo trutta
Bethanie Carney Almroth ⁎, Angelica Johansson, Lars Förlin, Joachim Sturve
Department of Zoology, University of Gothenburg, Göteborg, Sweden
abstract article info
Article history:
Received 22 October 2009
Received in revised form 21 January 2010
Accepted 23 January 2010
Available online 29 January 2010
Keywords:
Aging
Fish
Glutathione
Growth
Oxidative stress
Protein carbonyls
20S proteosome
Fish are often used as models for studies investigating the ability of xenobiotics to induce oxidative stress,
though age or developmental stage of the individuals studied has been given little attention. Oxidative stress
in other organisms is associated with aging as well as with periods of rapid growth, which occurs in young
brown trout. We measured protein carbonyls, 20S proteosome activity and glutathione (GSH) levels in
farmed Salmo trutta in four different age groups from 5 months to 3 years. We found an increase in protein
carbonyls and a decrease in 20S proteosome activity in both brain and liver tissues of the fish with increasing
size and age. Total GSH levels in liver tissue declined as fish aged and the GSSG:GSH ratio increased. Five
month and 1 year old trout were treated with paraquat (PQ) to induce oxidative stress. Five month old fish
showed no changes in the measured parameters while 1 year old fish had both an increase in protein
carbonylation in liver tissue and a decrease in 20S proteosome activity in brain tissue. These results indicate
that oxidative stress biomarkers are affected by age or rapid growth in brown trout, and that individuals of
different ages respond differently to oxidative stress induced by PQ.
© 2010 Elsevier Inc. All rights reserved.
1. Introduction
Fish have been proposed as ideal model animals for aging research
(Kishi et al. 2003; Gerhard 2007 and references therein). The three
different aging patterns described in teleost fishes lend themselves to
studies focusing on aging (Patnaik et al. 1994; Kishi et al. 2003; Kishi
2004). These three different types of senescence are as follows: rapid
(Pacific salmon exhibit rapid senescence and sudden death after
spawning), gradual (guppies and medaka which continue to grow,
though at decreased rates, throughout their life span), and negligible
(carp and rockfish show indeterminate growth with no increased
mortality as a function of age) (Patnaik et al. 1994; Kishi et al. 2003;
Kishi 2004). In this way, fish differ from mammals that have deter-
minate growth and gradual senescence (Patnaik et al. 1994; Kishi
et al. 2003; Kishi 2004). As teleosts represent the largest group of
vertebrate animals with an estimated 27,000 species (Nelson 2006), it
is even possible to find species within the same family displaying
different aging patterns. For example, within salmonids, one finds
Pacific salmon (genus Oncorhynchus) which undergo rapid senes-
cence and death after spawning, while Atlantic salmon (genus Salmo)
display gradual senescence. While fish have been proposed as models
for the study of aging (Gerhard 2007), this research focuses mainly on
small, short-lived species. Fish can also undergo periods of extremely
rapid growth (Elliot 1975; Metcalfe and Monaghan 2003), often at
early ages. Little is known about how rapid growth and aging in fish
affects parameters involved in oxidative stress, such as protein
carbonylation, 20S proteosome activity, and glutathione levels.
Aging has been defined as the progressive accumulation of
deleterious changes in the cells and tissues that increase the risk of
death and disease with increasing age (Harman 2001). These delete-
rious changes are effects of oxidative stress, which has been impli-
cated as one of the major causes of physiological aging (Harman 1957;
Harman 2003). Oxidative stress and ensuing damage is also tied to
rapid growth and attainment of a large body size (Rollo et al. 1996;
Alonso-Alvarez et al. 2007). Teleost species have also been used in
studies of oxidative stress, especially within the field of ecotoxicology.
Fish are often used as model animals to test effects of different
chemical contaminants on organisms and as sentinel species in
biomonitoring. As many pollutants released into the aquatic environ-
ment are prooxidants, owing at least part of their toxicity to the
production of reactive oxygen species (ROS), oxidative stress is an
important parameter to measure. Antioxidant enzymes as well as
several antioxidant molecules have been measured in fish in both
field and laboratory studies (see reviews van der Oost et al 2003;
Valavanidis et al. 2006) and are often used as biomarkers. Oxidative
damage, in the form of TBARS or protein carbonylation has also been
measured in fish (Carney Almroth et al 2005; Parvez and Raisuddin,
2005; Bagnyukova et al. 2006; Carney Almroth et al. 2008). However,
the age of the fish used in studies has been given little consideration,
particularly in field studies. This can be problematic, especially in light
of the fact that oxidative stress, both damage products and anti-
oxidant defences, enzymatic as well as molecular, have been shown to
be age-affected in a large number of organisms (Beckman and Ames
1998).
Comparative Biochemistry and Physiology, Part B 155 (2010) 442–448
⁎ Corresponding author. Department of Zoology, University of Gothenburg, Box 463,
SE-405 30, Göteborg, Sweden. Tel.: +46 31 786 3688; fax: +46 31 41 6729.
E-mail address: bethanie.carney@zool.gu.se (B. Carney Almroth).
1096-4959/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpb.2010.01.012
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