Anti-Oxidative Defences Are Modulated Differentially in Three Freshwater Teleosts in Response to Ammonia-Induced Oxidative Stress

Abstract

Oxidative stress and the antioxidant response induced by high environmental ammonia (HEA) were investigated in the liver and gills of three freshwater teleosts differing in their sensitivities to ammonia. The highly ammonia-sensitive salmonid Oncorhynchus mykiss (rainbow trout), the less ammonia sensitive cyprinid Cyprinus carpio (common carp) and the highly ammonia-resistant cyprinid Carassius auratus (goldfish) were exposed to 1 mM ammonia (as NH4HCO3) for 0 h (control), 3 h, 12 h, 24 h, 48 h, 84 h and 180 h. Results show that HEA exposure increased ammonia accumulation significantly in the liver of all the three fish species from 24 h–48 h onwards which was associated with an increment in oxidative stress, evidenced by elevation of xanthine oxidase activity and levels of hydrogen peroxide (H2O2) and malondialdehyde (MDA). Unlike in trout, H2O2 and MDA accumulation in carp and goldfish liver was restored to control levels (84 h–180 h); which was accompanied by a concomitant increase in superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase activity and reduced ascorbate content. Many of these defence parameters remained unaffected in trout liver, while components of the glutathione redox cycle (reduced glutathione, glutathione peroxidase and glutathione reductase) enhanced to a greater extent. The present findings suggest that trout rely mainly on glutathione dependent defensive mechanism while carp utilize SOD, CAT and ascorbate as anti-oxidative sentinels. Hepatic cells of goldfish appear to utilize each of these protective systems, and showed more effective anti-oxidative compensatory responses towards HEA than carp, while trout were least effective. The present work also indicates that HEA exposure resulted in a relatively mild oxidative stress in the gills of all three species. This probably explains the almost complete lack of anti-oxidative responses in branchial tissue. This research suggests that oxidative stress, as well as the antioxidant potential clearly differ between salmonid and cyprinid species.

High environmental ammonia elicits differential oxidative stress and antioxidant responses in five different organs of a model estuarine teleost ( Dicentrarchus labrax )

“…Similarly, Hegazi et al (2010) observed substantial LPO increment in liver and white muscle of Nile tilapia (Oreochromis niloticus) juveniles chronically exposed to 5 mg/L ammonia. Also, Sinha et al (2014b) reported augmented MDA and H 2 O 2 level in liver of ammonia exposed goldfish (Carassius auratus), common carp (Cyprinus carpio) and rainbow trout (Oncorhynchus mykiss). Ammonia is a potent neurotoxin that predominantly affects brain tissue.…”

“…Reduced glutathione (GSH) and reduced ascorbate (ASC) were quantified by high-performance liquid chromatography (ReversedPhase HPLC of Shimadzu, Hai Zhonglu, Shanghai) following the methodology described by Sinha et al (2014b). The concentrations of reduced glutathione (GSH), total glutathione (tGSH), reduced ascorbate (ASC) and total ascorbate (tASC) were calculated using a standard curve created by known concentrations of GSH and ASC.…”

“…These include-minimize the ammonia production by suppression of amino acid catabolism, conversion of accumulated ammonia into free amino acids particularly glutamine, detoxification of ammonia to the less toxic urea, and augmentation of ammonia excretion by up-regulation of 'Na +/ NH 4 + exchange complex' involving the Rh glycoproteins (Wright and Wood, 2009). Furthermore, some studies suggest that ammonia exerts the (cyto)toxic effects in fish by the production of reactive oxygen species (ROS) such as superoxide (O 2 2010;Hegazi, 2011;Sun et al, 2011Sun et al, , 2012Sinha et al, 2014b). ROS are generated as by-products of oxidative metabolism, and high production and accumulation of ROS could result in build-up of oxidized and damaged lipids and proteins in the cellular compartments, eventually inducing oxidative damage (Droge, 2003).…”

Dietary choline regulates antibacterial activity, inflammatory response and barrier function in the gills of grass carp (Ctenopharyngodon idella)

“…Moreover, ROS also caused oxidative damage and disruption of barrier function of human brain endothelial [31]. To scavenge ROS, fish have developed antioxidant systems, which are composed of non-enzymatic compounds (GSH) and antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), glutathione-S-transferase (GST) and glutathione reductase (GR) [32]. It was demonstrated that dietary choline could reduce the oxidative damage [33] and improve the GPx activity [34] in rats.…”

Responses of Takifugu obscurus fertilized eggs and larvae to increased ammonia exposure

“…Antioxidant processes occur in organisms to avoid the damage caused by ammonia accumulation . Sinha et al (2014) compared three freshwater teleosts in response to ammonia-induced oxidative stress and found that defensive strategies associated with an anti-oxidation system more effectively respond to ammonia challenge in goldfish than in carp and trout. The effect of high environmental ammonia concentration was more evident in the liver compared with the gills.…”