Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review

Abstract

Toxic metals and metalloid are being rapidly added from multiple pathways to aquatic ecosystem and causing severe threats to inhabiting fauna including fish. Being common in all the type of aquatic ecosystems such as freshwater, marine and brackish water fish are the first to get prone to toxic metals and metalloids. In addition to a number of physiological/biochemical alterations, toxic metals and metalloids cause enhanced generation of varied reactive oxygen species (ROS) ultimately leading to a situation called oxidative stress. However, as an important component of antioxidant defence system in fish, the tripeptide glutathione (GSH) directly or indirectly regulates the scavenging of ROS and their reaction products. Additionally, several other GSH-associated enzymes such as GSH reductase (GR, EC 1.6.4.2), GSH peroxidase (EC 1.11.1.9), and GSH sulfotransferase (glutathione-S-transferase (GST), EC 2.5.1.18) cumulatively protect fish against ROS and their reaction products accrued anomalies under toxic metals and metalloids stress conditions. The current review highlights recent research findings on the modulation of GSH, its redox couple (reduced glutathione/oxidised glutathione), and other GSH-related enzymes (GR, glutathione peroxidase, GST) involved in the detoxification of harmful ROS and their reaction products in toxic metals and metalloids-exposed fish.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Abbas HHH, Authman MMN (2009) Effects of accumulated selenium on some physiological parameters and oxidative stress indicators in tilapia fish (Oreochromis spp.). Am-Eurasian J of Agric Environ Sci 5:219–225

  2. Ahmad I, Mohmood I, Coelho JP, Pacheco M, Santos MA, Duarte AC, Pereira E (2012) Role of non-enzymatic antioxidants on the bivalves’ adaptation to environmental mercury: organ-specificities and age effect in Scrobicularia plana inhabiting a contaminated lagoon. Environ Pollut 163:218–225

  3. Ahmad I, Maria VL, Oliveira M, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2008) DNA damage and lipid peroxidation vs. protection responses in the gill of Dicentrarchus labrax L. from a contaminated coastal lagoon (Ria de Aveiro, Portugal). Sci Total Environ 406:298–307

  4. Ahmad I, Maria VL, Oliveira M, Pacheco M, Santos MA (2006) Oxidative stress and genotoxic effects in gill and kidney of Anguilla anguilla L. exposed to chromium with or without pre-exposure to β-naphthoflavone. Mutat Res 1:16–28

  5. Ahmad I, Oliveira M, Pacheco M, Santos MA (2005) Anguilla anguilla L. oxidative stress biomarkers responses to copper exposure with or without β-naphthoflavone pre-exposure. Chemosphere 61:267–275

  6. Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1523:37–48

  7. Ali M, Parvez S, Pandey S, Atif F, Kaur M, Rehman H, Raisuddin S (2004) Fly ash leachate induces oxidative stress in freshwater fish Channa punctata (Bloch). Environ Int 30:933–938

  8. Allen T, Rana S (2004) Effect of arsenic (AsIII) on glutathione-dependent enzymes in liver and kidney of the freshwater fish Channa punctatus. Biol Trace Elem Res 100:39–48

  9. Almeida JA, Diniz YS, Marques SFG, Faine LA, Ribas BO, Burneiko RC, Novelli ELB (2002) The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679

  10. Almeida JA, Barreto RE, Novelli ELB, Castro FJ, Moron SE (2009) Oxidative stress biomarkers and aggressive behavior in fish exposed to aquatic cadmium contamination. Neotrop Ichthyol 7:103–108

  11. Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

  12. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

  13. Ates B, Orun I, Talas Z, Durmaz G, Yilmaz I (2008) Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+. Fish Physiol Biochem 34:53–59

  14. Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Safety 73:1884–1889

  15. Atli G, Canli M (2008) Responses of metallothionein and reduced glutathione in a freshwater fish Oreochromis niloticus following metal exposures. Environ Toxicol Pharmacol 25:33–38

  16. Atli G, Alptekin O, Tukel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of fresh water fish Oreochromis niloticus. Comp Biochem Physiol C 143:218–224

  17. Aureliano M, Joaquim N, Sousa A, Martins H, Coucelo JM (2002) Oxidative stress in toadfish (Halobactrachus didactylus) cardiac muscle: acute exposure to vanadate oligomers. Journal of Inorg Biochem 90:159–165

  18. Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 78:325–331

  19. Banaee M (2012) Insecticides basic and other apllications. In: Soloneski S, Larramendy M (eds). Adverse effect of insecticides on various aspects of fish’s applications. Intech, pp 102–126

  20. Banni M, Chouchene L, Said K, Kerkeni A, Messaoudi I (2011) Mechanisms underlying the protective effect of zinc and selenium against cadmium-induced oxidative stress in zebrafish Danio rerio. Bio Metals 24:981–992

  21. Barillet S, Adam-Guillermin C, Palluel O, Porcher J-M, Devaux A (2011) Uranium bioaccumulation and biological disorders induced in zebrafish (Danio rerio) after a depleted uranium waterborne exposure. Environ Pollut 159:495–502

  22. Basha PS, Rani AU (2003) Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (tilapia). Ecotoxicol Environ Safety 56:218–221

  23. Berntssen M, Lundebye A, Hamre K. (2000) Tissue lipid peroxidative responses in Atlantic salmon (Salmo salar L.) parr fed high levels of dietary copper and cadmium. Fish Physiol Biochem 23:35–48

  24. Berntssen MHG, Aatland A, Handy RD (2003) Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquat Toxicol 65:55–72

  25. Beyer J, Sandvik M, Skare J, Egaas E, Hylland K, Waagbo R, Goksoyr A (1997) Time- and dose-dependent biomarker responses in flounder (Platichthys flesus L.) exposed to benzo[a]pyrene, 2,3,3′,4,4′, 5-hexachlorobiphenyl (PCB-156) and cadmium. Biomarkers 2:35–44

  26. Bhattacharya A, Bhattacharya S (2007) Induction of oxidative stress by arsenic in Clarias batrachus: involvement of peroxisomes. Ecotoxicol Environ Safety 66:178–187

  27. Bocchetti R, Regoli F (2006) Seasonalvariabilityofoxidativebiomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65:913–921

  28. Branco V, Canário J, Lu J, Holmgren A, Carvalho C (2012) Mercury and selenium interaction in vivo: effects on thioredoxin reductase and glutathione peroxidase. Free Radical Biol Med 52:781–793

  29. Camargo MMP, Martinez CBR (2006) Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil. Environ Toxicol Pharmacol 21:61–69

  30. Canesi L, Viarengo A, Leonzio C, Filippelli M, Gallo G (1999) Heavy metals and glutathione metabolism in mussel tissues. Aquat Toxicol 46:67–76

  31. Cao L, Huang W, Shan X, Ye Z, Dou S (2012) Tissue-specific accumulation of cadmium and its effects on antioxidative responses in Japanese flounder juveniles. Environ Toxicol Pharmacol 33:16–25

  32. Cao L, Huang W, Liu J, Yin X, Dou S (2010) Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. Comp Biochem and Physiol Part C 151:386–392

  33. Chung MJ, Walker PA, Hogstrand C (2004) Metal physiology and biochemistry in fish cells: from toxicity to protection by zinc. Comp Biochem Physiol 100C:137–147

  34. Coelho JP, Pereira ME, Duarte AC, Pardal MA (2005) Macroalgae response to a mercury contamination gradient in a temperate coastal lagoon (Ria de Aveiro, Portugal). Estuar Coast Shelf Sci 65:492–500

  35. Comakli V, Ciftci M, Kufrevioglu O (2011) Purification of glutathione S-transferase enzyme from rainbow trout erythrocytes and examination of the effects of certain antibiotics on enzyme activity. Hacettepe J Biol Chem 39:413–419

  36. Cong M, Wu H, Liu X, Zhao J, Wang X, Lv J, Hou L(2012) Effects of heavy metals on the expression of a zinc-inducible metallothionein-III gene and antioxidant enzyme activities in Crassostrea gigas. Ecotoxicol 21:1928–1936

  37. Dabas A, Nagpure N, Kumar R, Kushwaha B, Kumar P, Lakra W (2012) Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiol Biochem 38:469–482

  38. Dafre AL, Medeiros ID, Muller IC, Ventura EC, Bainy ACD (2004) Antioxidant enzymes and SH /disulfide status in the digestive gland of the brown mussel Perna perna exposed to lead and paraquat. Chemico-Biol Interact 149:97–105

  39. de Almeida EA, Miyamoto S, Bainy AC, de Medeiros MH, Di Mascio P (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Mar Pollut Bull 49:386–92

  40. DeForest DK, Brix KV, Adams WJ (2007) Assessing metal bioaccumulation in aquatic environments: the inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration. Aquat Toxicol 84:236–246

  41. DeLeve LD, Kaplowitz N (1991) Glutathione metabolism and its role in hepatotoxicity. Pharmacol Ther 52:287–305

  42. Dorval J, Leblond V, Deblois C, Hontela A (2005) Oxidative stress and endocrine endpoints in white sucker (Catostomus commersoni) from a river impacted by agricultural chemicals. Environ Toxicol Chem 24:1273–1280

  43. Doyotte A, Cossu C, Jacquin MC, Babut M, Vasseur P (1997) Glutathione reductase, selenium-dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicol Environ Saf 38:122–31

  44. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

  45. Elia AC, Galarini R, Taticchi MI, Dörr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Safety 55:162–167

  46. Elumalai M, Antunes C, Guilhermino L (2007) Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NW Portugal) exposed to zinc and mercury. Chemosphere 66:1249–1255

  47. Falfushynska HI, Gnatyshyna LL, Stoliar OB, Nam YK (2011) Various responses to copper and manganese exposure of Carassius auratus gibelio from two populations. Comp Biochem Physiol Part C 154:242–253

  48. Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria ogun river. Int J Environ Res Publ Health 4:158–165

  49. Fernandes C, Fontaínhas-Fernandes A, Ferreira M, Salgado M (2008) Oxidative stress response in gill and liver of Liza saliens, from the Esmoriz–Paramos Coastal Lagoon, Portugal. Arch Environ Cont Toxicol 55:262–269

  50. Filho DW, Torres MA, Tribess TB, Pedrosa RC, Soares CHL (2001) Influence of season and pollution on the antioxidant defenses of the cichlid fish acara (Geophagus brasiliensis). Brazilian J Med Biol Res 34:719–726

  51. Firat Ö, Çogun HY, Aslanyavrusu S, Kargın F (2009) Antioxidant responses and metal accumulation in tissues of Nile tilapia Oreochromis niloticus under Zn, Cd and Zn + Cd exposures. J App Toxicol 29:295–301

  52. Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress and its possible reversal by chelation therapy. Indian J Med Res 128:501–523

  53. Foltinova J, Foltin V, Neu E (2007) Occurrence of lead in placenta important information for prenatal and postnatal development of child. Neuro Endocrinol Lett 28:335–340

  54. Fonseca VF, França S, Serafim A, Company R, Lopes B, Bebianno MJ, Cabral HN (2011) Multi-biomarker responses to estuarine habitat contamination in three fish species: Dicentrarchus labrax, Solea senegalensis and Pomatoschistus microps. Aquat Toxicol 102:216–227

  55. Geret F, Serafim A, Bebianno MJ (2003) Antioxidant enzyme activities, metallothioneins and lipid peroxidation as biomarkers in Ruditapes decussatus? Ecotoxicol 12:417–426

  56. Gil F, Pla A (2001) Biomarkers as biological indicators of xenobiotic exposure. J Appl Toxicol 21:245–255

  57. Goering PI, Waalkes MP, Klassen CD (1995) Toxicology of cadmium. In: Goyer RA, Cherian MG (eds) Toxicology of metal biochemical aspects: handbook of experimental pharmacology. Springer, New York, pp 189–213

  58. Griffith OW, Meister A (1985) Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci USA 82:4668–4672

  59. Guimaraes L, Gravato C, Santos J, Monteiro L, Guilhermino L (2009) Yellow eel (Anguilla anguilla ) development in NW Portuguese estuaries with different contamination levels. Ecotoxicol 18:385–402

  60. Gul M, Kutay FZ, Temocin S, Hanninen O (2000) Cellular and clinical implications of glutathione. Ind J Exp Biol 38:625–634

  61. Gunaratnam M, Grant MH (2001) The role of glutathione reductase in the cytotoxicity of chromium (VI) in isolated rat hepatocytes. Chem Biol Inter 134:191–202

  62. Gutteridge JM (1999) Does redox regulation of cell function explain why antioxidants perform so poorly as therapeutic agents? Redox report 4:129–131

  63. Hamed R, Maharem T, Guinidi R (2004) Glutathione and its related enzymes in the Nile fish. Fish Physiol Biochem 30:189–199

  64. Huang W, Cao L, Liu J, Lin L, Dou S (2010) Short-term mercury exposure affecting the development and antioxidant biomarkers of Japanese flounder embryos and larvae. Ecotoxicol Environ Safety 73:1875–1883

  65. Jia X, Zhang H, Liu X (2011) Low levels of cadmium exposure induce DNA damage and oxidative stress in the liver of Oujiang colored common carp Cyprinus carpio Var. color. Fish Physiol Biochem 37:97–103

  66. Jihen EH, Sonia S, Fatima H, Tahar SM, Abdelhamid K (2011) Interrelationships between cadmium, zinc and antioxidants in the liver of the rat exposed orally to relatively high doses of cadmium and zinc. Ecotoxicol Environ Saf 74:2099–2104

  67. Karaytug S, Sevgiler Y, Karayakar F (2011) Comparison of the protective effects of antioxidant compounds in the liver and kidney of Cd- and Cr-exposed common carp. Environ Toxicol. doi:10.1002/tox.20779

  68. Kock G, Triendl M, Hofer R (1996) Seasonal patterns of metal accumulation in Arctic char (Salvelinus alpinus) from an oligotrophic Alpine lake related to temperature. Can J Fisheries Aquat Sci 53:780–786

  69. Kohrle J, Jakob F, Contempré B, Dumont JE (2005) Selenium, the thyroid, and the endocrine system endocrine. Endocr Rev 26:944–984

  70. Kovacevic TB, Borkovic SS, Pavlovic SZ, Despotovic SG, Saicic ZS (2008) Glutathione as a suitable biomarker in hepatopancreas, gills and muscle of three freshwater cray fish species. Arch Biol Sci 60:59–66

  71. Kovarova J, Svobodova Z (2009) Can thiol compounds be used as biomarkers of aquatic ecosystem contamination by cadmium? InterdiscipToxicol 2:177–183

  72. Kovarova J, Celechovska O, Kizek R, Adam V, Harustiakova D, Svobodova Z (2009) Effect of metals, with special attention of Cd, content of the Svitava and Svratka rivers on levels of thiol compounds in fish liver and their use as biochemical markers. Neuro Endocrinol Lett 30:169–176

  73. Kubrak OI, Husak VV, Rovenko BM, Storey JM, Storey KB, Lushchak VI (2011) Cobalt-induced oxidative stress in brain, liver and kidney of goldfish Carassius auratus. Chemosphere 85:983–989

  74. Kudirat AO (2008) Bioconcentration of lead in the tissues of feral and laboratory exposed Clarias gariepinus. J Med Sci 8:281–286

  75. Lange A, Ausseil O, Segner H (2002) Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc. Comp Bioch Physiol Part C 131:231–243

  76. Larose C, Canuel R, Lucotte M, Di Giulio RT (2008) Toxicological effects of methylmercury on walleye (Sander vitreus) and perch (Perca flavescens) from lakes of the boreal forest. Comp Bioch Physiol Part C 147:139–149

  77. Leblanc GA (1994) Hepatic vectorial transport of xenobiotics. Chem Biol Interact 90:l0l–120

  78. Lenartova V, Holovska K, Pedrajas JR, Martinez-Lara E, Peinado J, Lopez-Barea J, Rosival I, Kosuth P (1997) Antioxidant and detoxifying fish enzymes as biomarkers of river pollution. Biomarkers 2:247–252

  79. Lerebours A, Gonzalez P, Adam C, Camilleri V, Bourdineaud JP, Garnier-Laplace J (2009) Comparative analysis of gene expression in brain, liver, skeletal muscles, and gills of zebrafish (Danio rerio) exposed to environmentally relevant waterborne uranium concentrations. Environ Toxicol Chem 28:1271–1278

  80. Li Z-H, Li P, Randak T (2010) Effect of a human pharmaceutical carbamazepine on antioxidant responses in brain of a model teleost in vitro: an efficient approach to biomonitoring. J App Toxicol 30:644–648

  81. Li ZH, Li P, Randak T (2011) Evaluating the toxicity of environmental concentrations of waterborne chromium (VI) to a model teleost, Oncorhynchus mykiss: a comparative study of in vivo and in vitro. Comp Biochem Physiol 153:402–407

  82. Li X, Liu Y, Song L, Liu J (2003) Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin–LR. Toxicon 42:85–89

  83. Lima PL, Benassi JC, Pedrosa RC, Dal Magro J, Oliveira TB, Wilhelm Filho D (2006) Time-course variations of DNA damage and biomarkers of oxidative stress in tilapia (Oreochromis niloticus) exposed to effluents from a swine industry. Arch Environ Contam Toxicol 50:23–30

  84. Liu H, Wang W, Zhang J, Wang X (2006) Effects of copper and its ethylenediaminetetraacetate complex on the antioxidant defenses of the goldfish, Carassius auratus. Ecotoxicol Environ Saf 65:350–354

  85. Lopes PA, Pinheiro T, Santos MC, da Luz MM, Collares-Pereira MJ, Viegas-Crespo AM (2001) Response of antioxidant enzymes in freshwater fish populations (Leuciscus alburnoides complex) to inorganic pollutants exposure. Sci Total Environ 280:153–163

  86. Luoma SN, Rainbow PS (2008) Sources and cycles of trace matals. In: Metal contamination in aquatic environments: science and lateral management. Cambridge University Press, Cambridge, pp 47–66

  87. Lushchak VI (2012) Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids. doi:10.1155/2012/736837

  88. Lushchak OV, Kubrak OI, Nykorak MZ, Storey KB, Lushchak VI (2008) The effect of potassium dichromate on free radical processes in goldfish: possible protective role of glutathione. Aquat Toxicol 87:108–114

  89. Mannervik B (1987) The enzymes of glutathione metabolism: an overview. Biochem Soc Trans 15:717–780

  90. Martensson J, Jain A, Meister A (1990) Glutathione is required for intestinal function. Proc Natl Acad Sci USA 87:1715–1719

  91. Martinez-Alvarez R, Morales A, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fisheries 15:75–88

  92. Meierjohann S, Walter RD, Müller S (2002) Regulation of intracellular glutathione levels in erythrocytes infected with chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochem J 368:761–768

  93. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760

  94. Messaoudi I, Barhoumi S, Saïd K, Kerken A (2009) Study on the sensitivity to cadmium of marine fish Salaria basilisca (Pisces: Blennidae). J Environ Sci (China) 21:1620–1624

  95. Mieiro CL, Pacheco M, Pereira ME, Duarte AC (2011a) Mercury organotropism in feral European sea bass (Dicentrarchus labrax). Arch Environ Contam Toxicol 61:135–143

  96. Mieiro CL, Pereira ME, Duarte AC, Pacheco M (2011b) Brain as a critical target of mercury in environmentally exposed fish (Dicentrarchus labrax)—bioaccumulation and oxidative stress profiles. Aquat Toxicol 103:233–240

  97. Miller LL, Wang F, Palace VP, Hontela A (2007) Effect of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout. Aquat Toxicol 83:263–271

  98. Mitchelmore CL, Ringwood AH, Weis VM (2003) Differential accumulation of heavy metals in the sea anemone Anthopleura elegantissima as a function of symbiotic state. Aquat Toxicol 20:317–29

  99. Monteiro D, Rantin F, Kalinin A (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicol 19:105–123

  100. Morel Y, Barouki R (1999) Repression of gene expression by oxidative stress. Biochem J 342:481–496

  101. Naganuma A, Anderson M, Meister A (1990) Cellular glutathione as a determinant of sensitivity to mercury chloride toxicity: prevention of toxicity by giving glutathione monoester. Biochem Pharmacol 40:693–697

  102. Navarro A, Quirós L, Casado M, Faria M, Carrasco L, Benejam L, Benito J, Díez S, Raldúa D, Barata C, Bayona JM, Piña B (2009) Physiological responses to mercury in feral carp populations inhabiting the low Ebro River (NE Spain), a historically contaminated site. Aquat Toxicol 93:150–157

  103. Nishida Y (2011) The chemical process of oxidative stress by copper(II) and iron(III) ions in several neurodegenerative disorders. Monatsh Chem 142:375–384

  104. Olafsdottir K, Reed DJ (1988) Retention of oxidized glutathione by isolated rat liver mitochondria during hydroperoxide treatment. Biochim Biophys Acta 964:377–382

  105. Oliva M, José Vicente J, Gravato C, Guilhermino L, Dolores Galindo-Riaño M (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotoxicol Environ Saf 75:151–162

  106. Orun I, Ates B, Selamoglu Z, Yazlak H, Ozturk E, Yilmaz I (2005) Effects of various sodium selenite concentrations on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss). Fresenius Environ Bull 14:18–22

  107. Padmini E (2010) Physiological adaptations of stressed fish to polluted environments: role of heat shock proteins. Rev Environ Contam Toxicol 206:1–27

  108. Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Int 174:183–192

  109. Paris-Palacios S, Biagianti-Risbourg S, Vernet G (2000) Biochemical and (ultra)structural hepatic perturbation of Brachydanio rerio (Teleostei, Cyprinidae) exposed to two sublethal concentrations of copper sulphate. Aquat Toxicol 50:109–124

  110. Parvez S, Sayeed I, Pandey S, Ahmad A, Bin-Hafeez B, Haque R, Ahmad I, Raisuddin S (2003) Modulatory effect of copper on nonenzymatic antioxidants in freshwater fish Channa punctatus (Bloch.). Biol Trace Elem Res 93:237–248

  111. Pena-Llopis S, Ferrando MD, Peña JB (2003) Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcysteine. Aquat Toxicol 65:337–360

  112. Pena-Llopis S, Pen JB, Rios C, Sancho E, Fernandez C, Ferrando MD (2000) Role of glutathione in thiobencarb resistance in the European eel Anguilla anguilla. Ecotoxicol Environ Saf 46:51–56

  113. Pereira P, Pablo HD, Vale C, Pacheco M (2010) Combined use of environmental data and biomarkers in fish (Liza aurata) inhabiting a eutrophic and metal-contaminated coastal system—gills reflect environmental contamination. Mar Environ Res 69:53–62

  114. Pretto A, Loro V, Baldisserotto B, Pavanato M, Moraes B, Menezes C, Cattaneo R, Clasen B, Finamor I, Dressler V (2011) Effects of water cadmium concentrations on bioaccumulation and various oxidative stress parameters in Rhamdia quelen. Arch Environ Cont Toxicol 60:309–318

  115. Rainbow PS (2007) Trace metal bioaccumulation: models, metabolic availability and toxicity. Review Environ Int 33:576–582

  116. Rajkumar JSI, John Milton MC (2011) Biochemical markers of oxidative stress in Mugil cephalus exposed to cadmium, copper, lead and zinc. Int J Pharma Bio Sci 2:41–50

  117. Ramos-Martinez JI, BartolomtTR PRV (1983) Purification and properties of glutathione reductase from hepatopancreas of Mytilus edulis L. Comp Biochem Physiol 75B:689–962

  118. Rana SVS, Singh R, Verma S (1995) Mercury-induced lipidperoxidation in the liver, kidney, brain and gills of a fresh water fish, Channa punctatus. Jap J Icthyol 42:255–259

  119. Regoli F, Principato G (1995) Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquat Toxicol 31:143–164

  120. Regoli F, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S, Winston GW (2002) Oxidative stress in ecotoxicology: from analysis of individual antioxidants to a more integrated approach. Mar Environ Res 54:419–423

  121. Romeo M, Gharbi-Bouraoui S, Gnassia-Barelli M, Dellali M, Aissa P (2006) Responses of Hexaplex (Murex) trunculus to selected pollutants. Sci Total Environ 239:135–144

  122. Saenz LA, Seibert EL, Zanette J, Fiedler HD, Curtius AJ, Ferreira JF, Alves de Almeida E, Marques MR, Bainy AC (2010) Biochemical biomarkers and metals in Perna perna mussels from mariculture zones of Santa Catarina, Brazil. Ecotoxicol Environ Saf 73:796–804

  123. Sanchez W, Palluel O, Meunier L, Coquery M, Porcher J-M, Ait-Aissa S (2005) Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183

  124. Sayeed I, Parvez S, Pandey S, Bin-Hafeez B, Haque R, Raisuddin S (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicol Environ Saf 56:295–301

  125. Segner H, Braunbeck T (1998) Chemical response profile to chemical stress. In: Schüürmann G, Markert B (eds) Ecotoxicology: ecological fundamentals, chemical exposure and biological effects. Wiley, New York, pp 521–557

  126. Sen A, Kirikbakan A (2004) Biochemical characterization and distribution of glutathione S-transferases in leaping mullet (Liza saliens). Biochem (Moscow) 69:993–1000

  127. Sevcikova M, Modra H, Slaninova A, Svobodova A (2011) Metals as a cause of oxidative stress in fish: a review. Veter Med 11:537–546

  128. Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27:916–921

  129. Slatinskf I, Smutna M, Havelkovi M, Svobodovi Z (2008) Biochemical markers of aquatic pollution in fish–glutathione S-transferase. Folia Vet Lat 52:129–134

  130. Soares SS, Martins H, Gutiérrez-Merino C, Aureliano M (2008) Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers. Comp Biochem Physiol Part C 147:168–178

  131. Song Y, Salbu B, Heier LS, Teien H-C, Lind O-C, Oughton D, Petersen K, Rosseland BO, Skipperud L, Tollefsen KE (2012) Early stress responses in Atlantic salmon (Salmo salar) exposed to environmentally relevant concentrations of uranium. Aquat Toxicol 112–113:62–71

  132. Stephensen E, Sturve J, Forlin L (2002) Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol Part C 133:435–442

  133. Stephensen E, Svavarsson J, Sturve J, Ericson G, Adolfsson-Erici M, Förlin L (2000) Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat Toxicol 48:431–442

  134. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

  135. Talas ZS, Orun I, Ozdemir L, Erdogan K, Alkan A, Yilmaz I (2008). Antioxidative role of selenium against the toxic effect of heavy metals (Cd2+, Cr3+) on liver of rainbow trout (Oncorhnchus mykiss). Fish Physiol Biochem 34:217–222

  136. Thomas P, Wofford HW (1984) Effects of metals and organic compounds on hepatic glutathione, cysteine, and acid-soluble thiol levels in mullet (Mugil cephalus L.). Toxicol App Pharmacol 76:172–182

  137. Torres MA, Testa CP, Gaspari C, Masutti MB, Panitz CMN, Curi-Pedrosa R, Almeida EA, Mascio PD, Filho DW (2002) Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar Pollut Bull 44:923–932

  138. Tort L, Gómez E, Montero D, Sunyer JO (1996) Serum haemolytic and agglutinating activity as indicators of fish immunocompetence: their suitability in stress and dietary studies. Aquacult Int 4:31–41

  139. Tsangaris C, Papathanasiou E, Cotou E (2007) Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotoxicol Environ Saf 66:232–243

  140. Tuvikene A, Huuskonen S, Koponen K, Ritola O, Mauer U, Lindström-Seppä P (1999) Oil shale processing as a source of aquatic pollution: monitoring of the biologic effects in caged and feral freshwater fish. Environ Health Persp 107:745–752

  141. van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

  142. Varo I, Nunes B, Amat F, Torreblanca A, Guilhermino L, Navarro JC (2007) Effect of sublethal concentrations of copper sulphate on seabream Sparus aurata fingerlings. Aquat Living Resour 20:263–270

  143. Velma V, Tchounwou PB (2011) Hexavalent chromium-induced multiple biomarker responses in liver and kidney of goldfish, Carassius auratus. Environ Toxicol 26:649–656

  144. Verlecar XN, Jena KB, Chainy GBN (2008) Modulation of antioxidant defences in digestive gland of Perna viridis (L.), on mercury exposures. Chemosphere 71:1977–1985

  145. Vieira LR, Gravato C, Soares AMVM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416–1427

  146. Vinodhini R, Narayanan M (2009) Biochemical changes of antioxidant enzymes in common carp (Cyprinus carpio L.) after heavy metal exposure. Turk J Veter Sci 33:273–278

  147. Watanabe T, Kiron V, Datoh S (1997) Trace minerals in fish nutrition. Aquacult 151:185–207

  148. Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol 100C:173–176

  149. Yamuna A, Bhavan PS, Geraldine P (2012) Glutathione S-transferase and metallothionein levels in the freshwater prawn Macrobrachium malcolmsonii exposed to mercury. J Environ Biol 33:133–137

  150. Zhang JF, Liu H, Sun YY, Wang XR, Wu JC, Xue YQ (2005) Responses of the antioxidant defenses of the goldfish Carassius auratus, exposed to 2,4-dichlorophenol. Environ Toxicol Pharmacol 19:185–190

  151. Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150

  152. Zitka O, Huska D, Adam V, Horna A, Beklova M, Svobodova Z, Kizek R (2010) Coul array detector as a tool for estimation of acute toxicity of silver(I) ions. Int J Electrochem Sci 5:1082–1089

Download references

Acknowledgments

K. Srikanth is thankful to the Portuguese Foundation of Science and Technology (FCT) (SFRH/BPD/79490/2011) and the Aveiro Research Institute/Centre for Environmental and Marine Studies (CESAM) for financial supports. We would like to thank the unknown reviewers whose precious comments have made the review article more outstanding.

Author information

Correspondence to I. Ahmad.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Srikanth, K., Pereira, E., Duarte, A.C. et al. Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review. Environ Sci Pollut Res 20, 2133–2149 (2013). https://doi.org/10.1007/s11356-012-1459-y

Download citation

Keywords

  • Fish
  • Metal
  • Metalloids
  • Oxidative stress
  • Glutathione metabolism