Antioxidant defense system is altered by dietary oxidized lipid in
first-feeding rainbow trout (Oncorhynchus mykiss)
Stéphanie Fontagné-Dicharry ⁎, Emilie Lataillade, Anne Surget, Laurence Larroquet,
Marianne Cluzeaud, Sadasivam Kaushik
INRA, UR 1067 Nutrition, Métabolisme et Aquaculture, F-64310 Saint Pée-sur-Nivelle, France
abstract article info
Article history:
Received 19 October 2013
Received in revised form 9 January 2014
Accepted 13 January 2014
Available online 23 January 2014
Keywords:
Antioxidant enzymes
Lipid peroxidation
Oxidized lipids
Phospholipids
Larval development
Rainbow trout
High concentrations of n-3 polyunsaturated fatty acids (PUFA) that are readily susceptible to lipid peroxidative
damage are found in fish feeds and in the tissues of fish, especially in early developmental stages. A dietary phos-
pholipid (PL) supply has been shown to be beneficial during these critical stages. The objective of the study was to
characterize the response of the antioxidant defense system under dietary prooxidant conditions in presence or
absence of dietary PL during early development of rainbow trout. Rainbow trout (Oncorhynchus mykiss) at the
first-feeding fry stage (mean weight: 66 ± 2 mg) or at the fingerling stage (mean weight: 1.5 ± 0.4 g) were
fed 4 semi-purified diets supplemented with 12% fresh fish oil or 12% oxidized fish oil and 6% soybean lecithin
or 6% soybean oil for 4 weeks at 17 °C. At fry stages, rainbow trout fry fed the PL-supplemented diets had a sig-
nificantly higher final body weight than fry fed the PL-free diets (0.37 ± 0.07 vs. 0.27 ± 0.03 g, respectively). Di-
etary inclusion of oxidized lipid reduced growth (0.19 ± 0.02 vs. 0.45 ± 0.07 and 2.5 ± 0.6 vs. 4.8 ± 0.6 g,
respectively) and increased the mRNA expression of antioxidant enzymes such as glutathione reductase and glu-
tathione S-transferase at both developmental stages. However, dietary control of antioxidant enzyme activities
and vitamins was low in rainbow trout fry whereas increased activities of antioxidant enzymes and decreased
tocopherol contents were noticed in rainbow trout fingerlings fed oxidized lipid compared to rainbow trout fry
fed fresh oil. This resulted in higher content of lipid peroxidation products in rainbow trout fry fed oxidized
lipid compared to fish fed fresh lipid whereas this difference was reduced at the fingerling stage. The present
study demonstrates that rainbow trout fry are more susceptible to oxidative stress induced by dietary oxidized
lipid than rainbow trout fingerlings, possibly due to delayed response or lack of complete development of endog-
enous antioxidant defense system.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
High concentrations of n -3 polyunsaturated fatty acids (PUFA), in
particular docosahexaenoic acid (DHA, 22:6n -3) and eicosapentaenoic
acid (EPA, 20:5n -3), that have potential benefits for human health
(Ruxton et al., 2005) are found in the tissues of fish, right from early on-
togeny (Tocher, 2010). In the absence of suitable antioxidant protection,
due to the high degree of unsaturation, the long-chain n -3 PUFA are
prone to in vivo lipid peroxidation within the fish tissues leading to
pathologies, including muscular dystrophy (Boglione et al., 2013). In the
feeds also, these fatty acids are readily susceptible to autoxidation when
exposed to atmospheric oxygen and if adequate care is not taken in the
preparation and storage of feeds, the positive nutritional value of long-
chain n -3 PUFA derived from fish oils and meals can become a negative
factor for fish (Hsieh and Kinsella, 1989).
To limit lipid peroxidation, all aerobic organisms possess two types of
antioxidant defense system: free radical scavengers, generally of low
molecular weight, and antioxidant enzymes (Halliwell and Gutteridge,
2007). These antioxidant enzymes have been shown to be active all
through the development of rainbow trout and to be modulated by feed-
ing moderate levels of oxidized lipid (Fontagné et al., 2008). Early devel-
opmental stages of fish appear to be particularly sensitive to oxidative
stress due to the overpowering effects of prooxidants on antioxidant
defenses of cells that can cause alteration in development (Boglione
et al., 2013; Fontagné et al., 2006; Hata and Kaneda, 1980; Lewis-
McCrea and Lall, 2007, 2010). At a molecular level, some of the genes cod-
ing for antioxidant enzymes, such as superoxide dismutase (SOD), cata-
lase (CAT), glutathione peroxidase (GPX), glutathione reductase (GR)
and glutathione S-transferase (GST), contain binding sites for oxidative
stress-sensitive transcription factors, such as the nuclear factor
erythroid-2 related factor 2 (Nrf2) and the nuclear factor kappa-light-
chain-enhancer of activated B cells (NF-κB), in their regulatory region
(Thimmulappa et al., 2002; Zhou et al., 2001). Early life stages of fish
also need a dietary phospholipid (PL) supply for good development
(Boglione et al., 2013; Cahu et al., 2009; Tocher et al., 2008). Dietary PL
Aquaculture 424–425 (2014) 220–227
⁎ Corresponding author. Tel.: +33 559 515 951; fax: +33 559 545 152.
E-mail address: fontagne@st-pee.inra.fr (S. Fontagné-Dicharry).
0044-8486/$ – see front matter © 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquaculture.2014.01.009
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