Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidative responses of marine mussels, Perna viridis
Introduction
Although the sale and use of polychlorinated biphenyls (PCBs) have been banned in many countries for almost 20 years, PCB congeners and related polyhalogenated hydrocarbons still pose a serious threat to aquatic organisms. Besides causing reproductive failures in mammals (Addison, 1989) and birds (Kubiak, 1989), PCBs have been found to induce alternations in the metabolism of hormones and lipids.
Chlorinated hydrocarbons like PCBs and chlorinated pesticides (CPs) are ubiquitously distributed and are major environmental pollutants. Environmental risks associated with chlorinated hydrocarbons in a densely populated coastal city like Hong Kong have previously been reviewed and evaluated by Connell et al., 1998a, Connell et al., 1998b, and the conclusion was that PCBs, total DDTs and total HCHs were likely to pose significant risks to the local marine ecosystem.
Antioxidative responses of mammals exposed to xenobiotics (typically induction of antioxidants and antioxidant enzymes) have been extensively studied during the past 10 years. Numerous reports have demonstrated that these responses can be induced in a dose–response manner by free radicals and free radical generating agents, and thus can be used as biomarkers for these substances. Examples of these antioxidant enzymes include superoxide dismutase (SOD), glutathione peroxidase (GPx), catalase (CAT), glutathione reductase (GR) and glutathione S-transferase (GST). Vitamin E and glutathione (GSH) are examples of “non-enzymatic” antioxidants.
In recent years, investigations have been concentrated on the use of antioxidative responses as biomarkers to reflect the pollution level of trace organics. Most of these studies revealed that the antioxidative responses of indigenous animals such as fishes and mussels from polluted areas generally had greater responses than did control populations. For example, Roberts et al. (1987) reported a greater SOD activity in the liver of spot (Leiostomus xanthurus) from a PAH-contaminated site. Similarly, CAT activity was found to increase in channel catfish (Ictalurus punctatus) exposed to mill effluent (Mather-Mihaich and DiGiulio, 1991) and SOD, GPx and CAT were all elevated in the liver of gray mullet collected from contaminated sites (Rodriguez-Ariza et al., 1993).
Recently, several studies have demonstrated the ability of PCBs to induce the production of reactive oxygen species (Palace et al., 1996; Schlezinger et al., 2000; Beyer et al., 1997). It was reported that PCBs with fewer halogens might lead to increased cytochrome P450 activity, which accounted for the majority of PCB metabolism (Mills et al., 1985). However, the inducibility of antioxidant enzymes by PCBs has not been unequivocally demonstrated. In addition, variable responses in the activity of antioxidant enzymes have been observed in silver carp (Hypothalmichthys molitrix) exposed to the herbicide paraquat depending on the level of exposure (Matkovics et al., 1984).
A field-based study was undertaken in Hong Kong waters to investigate the relationship between antioxidative responses and tissue concentrations of common trace organic contaminants [including polycyclic aromatic hydrocarbons (PAHs), PCBs and CPs] using a local mussel, Perna viridis, as the experimental animal. In the field experiment, mussels were transplanted from a relatively clean site to various polluted sites in Hong Kong. After a 30-day field exposure, different antioxidant parameters including GST, SOD, CAT, GPx, GR, NADPH DT-diaphorase (DT-d), GSH and lipid peroxidation were quantified, and tissue concentrations of PAHs, PCBs, and CPs were determined for individual mussels. The relationships between tissue PAH concentrations and antioxidative responses of P. viridis have been reported earlier by Cheung et al. (2001). This paper reports the relationships between tissue concentrations of organochlorines (PCBs and CPs) and antioxidative responses of P. viridis, and attempts to examine the usefulness and adequacy of antioxidative responses in mussels as a general exposure biomarker for trace organics in the subtropical waters of Hong Kong.
Section snippets
Chemicals and reagents
GR, GSH, GSSG and NADPH were purchased from Roche Molecular Biochemicals. Ascorbic acid, bovine serum albumin (BSA), 1-chloro-2,4-dinitrobenzene (CDNB), cumene hydroperoxide, 5,5′-dithiobis (2-nitrobenzoic acid) (DTNB), 2,6-dichlorophenol-indophenol (DCPIP), iron sulfate, potassium thiocyanate, pyrogallol, thiobarbituric acid, trichloroacetic acid (TCA) were obtained from Sigma (St. Louis, MO, USA). Dicumarol, dipotassium hydrogen phosphate, hydrogen peroxide, potassium dihydrogen phosphate,
Results
Tissue burdens of total PCBs and CPs are given in Table 1. Levels of PCBs and CPs appeared to be higher at Tsim Sha Tsui as compared to the other sites, although the Kruskal–Wallis test revealed no inter-site differences (Table 1).
Antioxidant parameters of the two target organs (gill and hepatopancreas) and tissue concentrations of PCBs and CPs for individual mussels are summarized in Table 2.
GST activity was greater in the gills than in the hepatopancreas, while the levels of the oxyradical
Discussion
Many environmental pollutants can cause oxidative damage to biological systems. For example, chlorinated biphenyls and pesticides may produce superoxide anion radicals by redox cycling, while transition metals such as iron catalyze the reaction of superoxide anion radicals with hydrogen peroxide to produce hydroxyl radicals by Fenton reactions (Aust et al., 1985; Sies, 1988; Winston and DiGiulio, 1991). Thus, mussels inhabiting environments contaminated with these xenobiotics may be exposed to
Acknowledgements
The work described in this paper was partially supported by grants from the Hong Kong Research Grants Council (Project No.: 8730011 and 9040550), and a grant from CityU (Project No.: 7001030). This project was undertaken during tenure of City University Postgraduate Studentships to C.C.C. Cheung. The authors are grateful for most useful comments by Prof. J.P. Giesy.
References (51)
Determination of glutathione and glutathione disulfide in biological samples
Methods of Enzymology
(1985)- et al.
Role of metals in oxygen radical reactions
Free Radical Biology and Medicine
(1985) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Analytical Biochemistry
(1976)- et al.
Effects of chemical contaminants on subcellular changes in digestive cells of the marine bivalve, Mytilus edulis, from Puget Sound, Washington
Marine Environmental Research
(1996) - et al.
Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis
Aquatic Toxicology
(2001) - et al.
Fate and risk evaluation of persistent organic contaminants and related compounds in Victoria Harbour, Hong Kong
Chemosphere
(1998) - et al.
Occurrence of persistent organic contaminants and related substances in Hong Kong marine areas: an overview
Marine Pollution Bulletin
(1998) Lipid peroxidation: mechanism, analysis, enzymology and biological relevance
- et al.
Glutathione peroxidase activity in selenium-deficient rat liver
Biochemistry and Biophysics Research Communication
(1976) - et al.
Assessment of the impact of organic pollutants on Goby (Zosterisessor ophiocephalus) and Mussel (Mytilus galloprovincialis) from the Venice Lagoon, Italy: biochemical studies
Marine Environmental Research
(1995)
Apparent induction of cytochrome P450 with immunochemical similarities to CYP1A in digestive gland of the common mussel (Mytilus galloprovincialis L.) with exposure to 2,2′3,4,4′5′-hexachlorobiphenyl and Arochlor 1254
Aquatic Toxicology
Development of hepatic CYP1A and blood vitellogenin in eel (Anguilla anguilla) for use as biomarkers in the Thames Estuary, UK
Marine Environmental Research
Effects of benzo(a)pyrene, 3,3′,4,4′-tetrachlorobiphenyl and 2,2′,4,4′,5,5′-hexachlorobiphenyl on the xenobiotic-metabolizing enzymes in the (Mytilus galloprovincialis)
Aquatic Toxicology
Studies of ascorbate-dependent, iron-catalyzed lipid peroxidation
Archives of Biochemistry and Biophysics
Studies on the structure activity relationships for the metabolism of polybrominated biphenyls by rat liver microsomes
Toxicology and Applied Pharmacology
Variation in levels of cytochrome P450 1A, 2B, 2E, and 4A-immunopositive protein in digestive gland of indigenous and transplanted mussel, Mytilus galloprovincialis in Venice Lagoon, Italy
Marine Environmental Research
The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW Spain)
Environmental Pollution
Chlorinated hydrocarbon contaminants in Hong Kong surficial sediments
Chemosphere
Temporal changes in AHH and SOD activities in feral spot from the Elizabeth River, a polluted sub-estuary
Marine Environmental Research
3,3′,4,4′-tertachlorobiphenyl oxidation in fish, bird and reptile species: relationship to cytochrome P450 1A inactivation and reactive oxygen production
Comparative Biochemistry and Physiology Part C
Effects of the Aegean Sea oil spill on biotransformation enzymes, oxidative stress and DNA adducts in digestive gland of the mussel (Mytilus edulis) L
Comparative Biochemistry and Physiology
Assessment of the results of chemical analyses combined with biological effects of organic pollution on mussels
Trends in Analytical Chemistry
Prooxidant and antioxidant mechanisms in aquatic organisms
Aquatic Toxicology
Concentrations of persistent organic pollutants in surface sediments of the mudflat and mangroves at Mai Po Marshes Nature Reserve, Hong Kong
Marine Pollution Bulletin
Organochlorines and marine mammal reproduction
Canadian Journal of Fisheries and Aquatic Science
Cited by (90)
Immunotoxicity of microplastics and polychlorinated biphenyls alone or in combination to Crassostrea gigas
2024, Marine Pollution BulletinMulti-biomarker approach in Mytilus galloprovincialis and Ruditapes decussatus as a predictor of pelago-benthic responses after exposure to Benzo[a]Pyrene
2021, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyEnzymatic assays for the assessment of toxic effects of halogenated organic contaminants in water and food. A review
2020, Food and Chemical ToxicologyBaseline levels of antioxidant activities in Mytilus galloprovincialis along the coast of Cape Town, South Africa
2019, Marine Pollution BulletinThe detoxification responses, damage effects and bioaccumulation in the scallop Chlamys farreri exposed to single and mixtures of benzo[a]pyrene and chrysene
2017, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyCitation Excerpt :It was conceivable that GSH could be a sensitive biomarker evaluating PAHs pollution. Increases in levels of GSH have been reported in catfish exposed to sediments contaminated by aromatic hydrocarbons (Di Giulio et al., 1993), in mussels exposed to PAHs in a laboratory study (Cheung et al., 2002), in scallop C. farreri exposed to TBBPA (Hu et al., 2015b), similar trends were found in current study (days 3, 6, 10 and 15) (Fig. 5D). In addition, BaP1 + CHR1 significantly increased the content of GSH showing synergistic effect indicated the effects of the combination can be different from those of single contaminant independently (Song et al., 2016; Oliveira et al., 2015).