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Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829)

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Abstract

Alterations in the antioxidant cellular system have often been proposed as biomarkers of pollutant-mediated toxicity. This study evaluated the effects of mercury on oxidative stress biomarkers and bioaccumulation in the liver, gills, white muscle and heart of the freshwater fish matrinxã, Brycon amazonicus, exposed to a nominal and sub-lethal concentration (~20% of 96 h-LC50) of 0.15 mg L−1 of mercury chloride (HgCl2) for 96 h in a static system. Increases in superoxide dismutase, catalase, glutathione peroxidase (GPx), glutathione S-transferase (GST) and glutathione reductase (GR) were observed in all tissues after HgCl2 exposure, except for white muscle GR activity and hepatic GPx. In the liver and gills, the exposure to HgCl2 also induced significant increases in reduced glutathione (GSH). Conversely, exposure to HgCl2 caused a significant decrease in the GSH levels and an increase in the oxidized glutathione (GSSG) content in the white muscle, while both GSH and GSSG levels increased significantly in the heart muscle. Metallothionein concentrations were significantly high after HgCl2 exposure in the liver, gills and heart, but remained at control values in the white muscle. HgCl2 exposure induced oxidative damage, increasing the lipid peroxidation and protein carbonyl content in all tissues. Mercury accumulated significantly in all the fish tissue. The pattern of accumulation follows the order gills > liver ≫ heart > white muscle. In conclusion, these data suggest that oxidative stress in response to inorganic mercury exposure could be the main pathway of toxicity induced by this metal in fish.

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References

  • Aebi H (1974) Catalase. In: Bergmayer HU (ed) Methods of enzymatic analysis. Academic Press, London, pp 671–684

    Google Scholar 

  • 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. doi:10.1016/S0304-4165(00)00098-2

    CAS  Google Scholar 

  • 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 608:16–28. doi:10.1016/j.mrgentox.2006.04.020

    CAS  Google Scholar 

  • Alam MK, Maughan OE (1992) The effect of malathion, diazinon, and various concentrations of zinc, copper, nickel, lead, iron, and mercury on fish. Biol Trace Elem Res 34:225–236. doi:10.1007/BF02783678

    CAS  Google Scholar 

  • Alam MK, Maughan OE (1995) Acute toxicity of heavy metals to common carp (Cyprinus carpio). J Environ Sci Health 30:1807–1816. doi:10.1080/10934529509376303

    Google Scholar 

  • Alho CJR, Vieira LM (1997) Fish and wildlife resources in the Pantanal wetlands of Brazil and potential disturbances from the release of environmental contaminants. Environ Toxicol Chem 16:71–74. doi:10.1897/1551-5028(1997)016<0071:FAWRIT>2.3.CO;2

    CAS  Google Scholar 

  • Alinnor IJ (2005) Assessment of elemental contaminants in water and fish samples from Aba River. Environ Monit Assess 102:15–25. doi:0.1007/s10661-005-1011-3

    CAS  Google Scholar 

  • Almeida JA, Diniz YS, Marques SFG, Faine LA, Ribas BO, Burneiko RC, Novelli ELB (2002) The use of oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679. doi:10.1016/S0160-4120(01)00127-1

    CAS  Google Scholar 

  • Almroth BC, Sturve J, Berglund A, Forlin L (2005) Oxidative damage in eelpout (Zoarces viviprus), measured as protein carbonyl and TBARS, as biomarkers. Aquat Toxicol 73:171–180. doi:10.1016/j.aquatox.2005.03.007

    CAS  Google Scholar 

  • Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbowd PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202. doi:10.1016/j.aquatox.2005.08.015

    CAS  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–555. doi:10.1016/S0076-6879(85)13073-9

    CAS  Google Scholar 

  • ANVISA (National Health Surveillance Agency) (1998) Decree No. 685, Brazil

  • Atli G, Canlia M (2008) Responses of metallothionein and reduced glutathione in a freshwater fish Oreochromis niloticus following metal exposures. Environ Toxicol Pharmacol 25:33–38. doi:10.1016/j.etap.2007.08.007

    CAS  Google Scholar 

  • Aureliano M, Joaquim N, Sousa A, Martins H, Coucelo JM (2002) Oxidative stress in toadfish (Halobatrachus didactylus) cardiac muscle: acute exposure to vanadate oligomers. J Inorg Biochem 90:159–165. doi:10.1016/S0162-0134(02)00414-2

    CAS  Google Scholar 

  • Bainy ACD (1996) Oxidative stress as biomarker of polluted aquatic sites. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA, Manaus, pp 101–110

    Google Scholar 

  • Balshaw S, Edwards JW, Ross KE, Daughtry BJ (2008) Mercury distribution in the muscular tissue of farmed southern bluefin tuna (Thunnus maccoyii) is inversely related to the lipid content of tissues. Food Chem 111:616–621. doi:10.1016/j.foodchem.2008.04.041

    CAS  Google Scholar 

  • Banerjee BD, Seth V, Bhattacharya A, Pasha ST, Chakraborty AK (1999) Biochemical effects of some pesticides on lipid peroxidation and free-radical scavengers. Toxicol Lett 107:33–47. doi:10.1016/S0378-4274(99)00029-6

    CAS  Google Scholar 

  • Bartling D, Radzio R, Steiner U, Weiler EW (1993) A glutathione S-transferase with glutathione peroxidase activity from Arabidopsis thaliana: molecular cloning and functional characterization. Eur J Biochem 216:579–586. doi:10.1111/j.1432-1033.1993.tb18177.x

    CAS  Google Scholar 

  • Berntssen MHG, Aatland A, Handy RD (2003) Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behavior in Atlantic salmon (Salmo salar) parr. Aquatic Toxicol 65:55–72. doi:10.1016/S0166-445X(03)00104-8

    CAS  Google Scholar 

  • Berntssen MHG, Hylland K, Julshamn K, Lundebye AK, Waagbø R (2004) Maximum limits of organic and inorganic mercury in fish fed. Aquac Nutr 10:83–97. doi:10.1046/j.1365-2095.2003.00282.x

    CAS  Google Scholar 

  • Bickham JW, Sandhu S, Hebert PDN, Chikhi L, Athwal R (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res 463:33–51. doi:10.1016/S1383-5742(00)00004-1

    CAS  Google Scholar 

  • Black FJ, Bruland KW, Flegal AR (2007) Competing ligand exchange-solid phase extraction method for the determination of the complexation of dissolved inorganic mercury (II) in natural waters. Anal Chim Acta 598:318–333. doi:10.1016/j.aca.2007.07.043

    CAS  Google Scholar 

  • Bleau H, Daniel C, Chevalier G, Von Tra H, Hontela A (1996) Effects of acute exposure to mercury chloride and methlymercury on plasma cortisol, T3, T4, glucose and liver glycogen in rainbow trout (Oncorhyncus mykiss). Aquatic Toxicol 34:221–235. doi:10.1016/0166-445X(95)00040-B

    CAS  Google Scholar 

  • Bollen A, Wenke A, Biester H (2008) Mercury speciation analyses in HgCl2—contaminated soils and groundwater—implications for risks assessment and remediation strategies. Water Res 42:91–100. doi:10.1016/j.watres.2007.07.011

    CAS  Google Scholar 

  • Bradford MMA (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:218–251. doi:10.1016/0003-2697(76)90527-3

    Google Scholar 

  • Bridges CM (1997) Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Environ Toxicol Chem 16:1935–1939. doi:10.1897/1551-5028(1997)016<1935:TSPAAA>2.3.CO;2

    CAS  Google Scholar 

  • Canesi L, Viarengo A, Leonzio C, Filippelli M, Gallo G (1999) Heavy metals and glutathione metabolism in mussel tissues. Aquat Toxicol 46:67–76. doi:10.1016/S0166-445X(98)00116-7

    CAS  Google Scholar 

  • Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480

    CAS  Google Scholar 

  • Carvalho GGA, de França JG, Dias DC, Lombardi JV, de Paiva MJR, Carvalho S, Sarrie GA, Ferreira JR (2009) Selenite and selenate effects on mercury (Hg2+) uptake and distribution in tilapia, Oreochromis niloticus L., assessed by chronic bioassay. Bull Environ Contam Toxicol 82:300–304. doi:10.1007/s00128-008-9617-0

    CAS  Google Scholar 

  • Choudhary G, Dudley SC Jr (2002) Heart failure, oxidative stress, and ion channel modulation. Congest Heart Fail 8:148–155. doi:10.1111/j.1527-5299.2002.00716.x

    CAS  Google Scholar 

  • CONAMA (Conselho Nacional do Meio Ambiente) (2005) Resolução CONAMA 357 de 17 de março de 2005. Diário Oficial da República Federativa do Brasil, Brasília, DF, 18 de março, seção 1, pp 58–63

  • Cunha Bastos VL, Salles JB, Valente RH, León IR, Perales J, Dantas RF, Albano RM, Bastos FF, Cunha Bastos J (2007) Cytosolic glutathione peroxidase from liver of pacu (Piaractus mesopotamicus), a hypoxia-tolerant fish of the pantanal. Biochimie 89:1332–1342. doi:10.1016/j.biochi.2007.04.003

    CAS  Google Scholar 

  • Cuvin-Aralar MLA, Furness R (1990) Tissue distribution of mercury and selenium in minnows, Phoxinus phoxinus. Bull Environ Contam Toxicol 45:775–782. doi:10.1007/BF01701000

    CAS  Google Scholar 

  • De Boeck G, Ngo TTH, Van Campenhout K, Blust R (2003) Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquat Toxicol 65:413–424. doi:10.1016/S0166-445X(03)00178-4

    Google Scholar 

  • Dórea JG, Barbosa AC, Silva GS (2006) Fish mercury bioaccumulation as a function of feeding behavior and hydrological cycles of the Rio Negro, Amazon. Comp Biochem Physiol C 142:275–283. doi:10.1016/j.cbpc.2005.10.014

    Google Scholar 

  • Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95. doi:10.1152/physrev.00018.2001

    CAS  Google Scholar 

  • Duncan DA, Klaverkamp JF (1983) Tolerance and resistance to cadmium in white suckers (Catostomus commersoni) previously exposed to cadmium, mercury, zinc or selenium. Can J Fish Aquat Sci 40:128–138. doi:10.1139/f83-022

    CAS  Google Scholar 

  • Eisler R, Hennekey RJ (1977) Acute toxicities of Cd2+, Cr6+, Hg2+, Ni2+, and Zn2+ to estuarine macrofauna. Arch Environ Contam Toxicol 6:315–323. doi:10.1007/BF02097772

    CAS  Google Scholar 

  • Elia AC, Galarini R, Taticchi MI, Dörra AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167. doi:10.1016/S0147-6513(02)00123-9

    CAS  Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal - induced oxidative damage. Curr Top Med Chem 1:529–539. doi:10.2174/1568026013394831

    CAS  Google Scholar 

  • Fabacher DL, Baumann PC (1985) Enlarged livers and hepatic microsomal mixed-function oxidase components in tumor-bearing brown bullheads from a chemically contaminated river. Environ Toxicol Chem 4:703–710. doi:10.1897/1552-8618(1985)4[703:ELAHMM]2.0.CO;2

    CAS  Google Scholar 

  • Fernandes C, Fontainhas-Fernandes A, Cabral D, Salgado MA (2007) Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz Paramos lagoon, Portugal. Environ Monit Assess 136:267–275. doi:10.1007/s10661-007-9682-6

    Google Scholar 

  • Fernandes D, Bebianno MJ, Porte C (2008) Hepatic levels of metals and metallothioneins in two commercial fish species of the Northern Iberian shelf. Sci Total Environ 391:159–167. doi:10.1016/j.scitotenv.2007.10.05

    CAS  Google Scholar 

  • Ferrat L, Bingert A, Roméo M, Gnassia-Barelli M, Pergent-Martini C (2002) Mercury uptake and enzymatic response of Posidonia oceanica after an experimental exposure to organic and inorganic forms. Environ Toxicol Chem 21:2365–2371. doi:10.1897/1551-5028(2002)021<2365:MUAERO>2.0.CO;2

    CAS  Google Scholar 

  • Figueiredo-Fernandes A, Fontaínhas-Fernandes A, Peixoto F, Rocha E, Reis-Henriques MA (2006) Effects of gender and temperature on oxidative stress enzymes in Nile tilapia Oreochromis niloticus exposed to paraquat. Pestic Biochem Physiol 85:97–103. doi:10.1016/j.pestbp.2005.11.001

    CAS  Google Scholar 

  • Flohé L, Ötting F (1984) Superoxide dismutase assays. Methods Enzymol 105:93–105. doi:10.1016/S0076-6879(84)05013-8

    Google Scholar 

  • Fournier D, Bride JM, Poirie M, Berge JB, Plapp FW Jr (1992) Insect glutathione S-transferase, biochemical characteristics of the major forms of houseflies susceptible and resistant to insecticides. J Biol Chem 267:1840–1845

    CAS  Google Scholar 

  • Gaikwad SA (1989) Acute toxicity of mercury, copper and selenium to the fish Etroplus maculates. Environ Ecol 7:694–696

    CAS  Google Scholar 

  • Gammons C, Slotton DG, Gerbrandt B, Weight W, Young CA, Mcnearny RL, Camac E, Calderon R, Tapia H (2006) Mercury concentrations of fish, river water, and sediment in the Río Ramis-Lake Titicaca watershed, Peru. Sci Total Environ 368:637–648. doi:10.1016/j.scitotenv.2005.09.076

    CAS  Google Scholar 

  • Giari L, Simoni E, Dezfuli BS (2008) Histo-cytological responses of Dicentrarchus labrax (L.) following mercury exposure. Ecotoxicol Environ Saf 70:400–410. doi:10.1016/j.ecoenv.2007.08.013

    CAS  Google Scholar 

  • Gobas FAPC, Morrison HA (2000) Bioconcentration and biomagnification in the aquatic environment. In: Boethling RS, Mackay D (eds) Handbook of property estimation methods for chemicals. CRC Press, Boca Raton, pp 189–231

    Google Scholar 

  • Grune T (2000) Oxidative stress, aging and the proteasomal system. Biogerontology 1:31–40. doi:10.1023/A:1010037908060

    CAS  Google Scholar 

  • Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Antioxidant and biotransformation responses in Liza aurata under environmental mercury exposure—relationship with mercury accumulation and implications for public health. Mar Pollut Bull 56:845–859. doi:10.1016/j.marpolbul.2008.02.003

    CAS  Google Scholar 

  • Gül A, Yilmaz M, Selvi M (2004) The study of the toxic effects of mercury-II-chloride to chub Leuciscus cephalus (L., 1758). G.U. J Sci 17:53–58

    Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JC (2000) Free radicals in biology and medicine, 3rd edn. Oxford University Press, UK

    Google Scholar 

  • Hamilton MA, Russo RC, Thurston RV (1977) Trimmed spearmam-karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719. doi:10.1021/es60130a004

    CAS  Google Scholar 

  • Hayes JD, Pulford DJ (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600. doi:10.3109/10409239509083491

    CAS  Google Scholar 

  • Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe(III) xilenol orange complex formation. Free Radic Biol Med 19:271–280. doi:10.1016/0891-5849(95)00020-x

    CAS  Google Scholar 

  • Hidaldo C, Donoso P (2008) Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid Redox Signal 10:1275–1312. doi:10.1089/ars.2007.1886

    Google Scholar 

  • Hinton DE, Baumann PC, Gardner GC, Hawkins WE, Hendricks JD, Murchelano MA, Okihiro MS (1992) Histopathologic biomarkers. In: Huggett RJ, Kimerly RA, Mehrle PM Jr, Bergman HL (eds) Biomarkers: biochemical, physiological and histological markers of anthropogenic stress. Lewis, Chelsea, MI, pp 155–210

    Google Scholar 

  • Hogstrand C, Haux C (1991) Binding and detoxification of heavy metals in lower vertebrates with reference to metallothionein. Comp Biochem Physiol C 100:137–141. doi:10.1016/0742-8413(91)90140-O

    CAS  Google Scholar 

  • Huang ZY, Zhang Q, Chen J, Zhuang ZX, Wang XR (2007) Bioaccumulation of metals and induction of metallothioneins in selected tissues of common carp (Cyprinus carpio L) co-exposed to cadmium, mercury and lead. Appl Organomet Chem 21:101–107. doi:10.1002/aoc.1167

    CAS  Google Scholar 

  • Hypolito R, Ferrer LM, Nascimento SC (2004) Comportamento de espécies de mercúrio no sistema sedimento-água do mangue no município de Cubatão, São Paulo. Águas Subterrâneas 19:15–24

    Google Scholar 

  • Jagoe CH, Shaw-Allen PL, Brundage S (1996) Gill Na+, K+-ATPase activity in largemouth bass (Micropterus salmoides) from three reservoirs with different levels of mercury contamination. Aquatic Toxicol 36:161–176. doi:10.1016/S0166-445X(96)00814-4

    CAS  Google Scholar 

  • Jezierska B, Witeska M (2007) The metal uptake and accumulation in fish living in polluted waters. Soil and water pollution monitoring. Prot Rem 69:107–114. doi:10.1007/s10661-007-9682-6

    Google Scholar 

  • Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low-density lipoprotein. Anal Biochem 202:384–389. doi:10.1016/0003-2697(92)90122-N

    CAS  Google Scholar 

  • Kane AS, Salierno JD, Brewer SK (2005) Fish models in behavioral toxicology: automated techniques, updates and perspectives. In: Ostrander GK (ed) Methods in aquatic toxicology, vol 2. Lewis, Boca Raton, pp 559–590

    Google Scholar 

  • Kehrer JP (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 34:21–48. doi:10.3109/10408449309104073

    Google Scholar 

  • Kehrig HA, Costa M, Moreira I, Malm O (2002) Total and methylmercury in a Brazilian estuary, Rio de Janeiro. Mar Pollut Bull 44:1018–1023. doi:10.1016/S0025-326X(02)00140-6

    CAS  Google Scholar 

  • Kirby MF, Neall P, Tylor T (1999) EROD activity measured in flatfish from the area of the Sea Empress oil spill. Chemosphere 38:2929–2949. doi:10.1016/S0045-6535(98)00484-6

    CAS  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantification. Methods Mol Biol 32:9–15. doi:10.1007/978-1-60327-259-9

    CAS  Google Scholar 

  • Lacerda LD (1997) Evolution of mercury contamination in Brazil. Water Air Soil Pollut 97:247–255. doi:10.1023/A:1018359023517

    CAS  Google Scholar 

  • Lacerda LD, Salomons W, Pfeiffer WC, Bastos WR (1991) Mercury distribution in sediment profiles from lakes of the high pantanal, Mato Grosso State, Brazil. Biogeochemistry 14:91–97. doi:10.1007/BF00002899

    Google Scholar 

  • 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 Biochem Physiol C 147:139–149. doi:10.1016/j.cbpc.2007.09.002

    Google Scholar 

  • Lopez PA, Pinheiro T, Santos MC, Mathias ML, Collares-Pereira MJ, Viesgas-Crespo AM (2001) Response of antioxidant enzymes in freshwater fish populations (Leucicus alburnoides complex) to inorganic pollutants exposure. Sci Total Environ 280:153–163. doi:10.1016/S0048-9697(01)00822-1

    Google Scholar 

  • Luo J, Xuan YT, Gu Y, Prabhu SD (2006) Prolonged oxidative stress inverts the cardiac force–frequency relation: role of altered calcium handling and myofilament calcium responsiveness. J Mol Cell Cardiol 40:64–75. doi:10.1016/j.yjmcc.2005.09.013

    CAS  Google Scholar 

  • Lushchak VL, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330. doi:10.1016/j.biocel.2005.01.006

    CAS  Google Scholar 

  • Mackay D, Fraser A (2000) Bioaccumulation of persistent organic chemicals: mechanisms and models. Environ Pollut 110:375–391. doi:10.1016/S0269-7491(00)00162-7

    CAS  Google Scholar 

  • Margarido VP, Galetti PM Jr (1996) Chromosome studies in fish of the genus Brycon (Characiformes, Characidae, Bryconinae). Cytobios 85:219–228

    Google Scholar 

  • Martin JK, Black MC (1998) Biomarker assessment of the effects of coal-strip mines contamination on channel fish. Ecotoxicol Environ Saf 41:307–320. doi:10.1006/eesa.1998.1714

    CAS  Google Scholar 

  • McFarland VA, Inouye LS, Lutz CH, Jarvis AS, Clarke JU, McCant DD (1999) Biomarkers of oxidative stress and genotoxicity in livers of field-collected brown bullhead, Ameiurus nebulosus. Arch Environ Contam Toxicol 37:236–241. doi:10.1007/s002449900510

    CAS  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760. doi:10.1146/annurev.bi.52.070183.003431

    CAS  Google Scholar 

  • Micaroni RCCM, Bueno MIMS, Jardim WF (2000) Composto de mercúrio. Revisão de métodos de determinação, tratamento e descarte. Quim Nova 23:487–495. doi:10.1590/S0100-40422000000400011

    Google Scholar 

  • Milaeva ER (2006) The role of radical reactions in organomercurials impact on lipid peroxidation. J Inorg Biochem 100:905–915. doi:10.1016/j.jinorgbio.2006.02.014

    CAS  Google Scholar 

  • Monteiro DA, Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C143:141–149. doi:10.1016/j.cbpc.2006.01.004

    Google Scholar 

  • Monteiro DA, Rantin FT, Kalinin AL (2009) The effects of selenium on oxidative stress biomarkers in the freshwater characid fish matrinxã, Brycon cephalus (Günther, 1869) exposed to organophosphate insecticide Folisuper 600 BR® (methyl parathion). Comp Biochem Physiol C 149:40–49. doi:10.1016/j.cbpc.2008.06.012

    Google Scholar 

  • Nakamura W, Hosoda S, Hayashi K (1974) Purification and properties of rat liver glutathione peroxidase. Biochim Biophys Acta 358:251–261

    CAS  Google Scholar 

  • Nordberg J, Arnér ESJ (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312. doi:10.1016/S0891-5849(01)00724-9

    CAS  Google Scholar 

  • OECD (Organization for Economic Cooperation and Development) (1992) OECD guideline for testing of chemicals no 203. Fish, Acute Toxicity Test

  • Oliveira Ribeiro CA, Gumarães JRD, Pfeiffer C (1996) Accumulation and distribution of inorganic mercury in a tropical fish (Trichomycterus zonatus). Ecotoxicol Environ Saf 34:190–195. doi:10.1006/eesa.1996.0063

    Google Scholar 

  • Oliveira Ribeiro CA, Pelletier E, Pfeiffer WC, Rouleau C (2000) Comparative uptake, bioaccumulation, and gill damages of inorganic mercury in tropical and nordic freshwater fish. Environ Res 83:286–292. doi:10.1006/enrs.2000.4056

    CAS  Google Scholar 

  • Oruç EO, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2, 4-D and azinphosmethyl. Comp Biochem Physiol C 137:43–51. doi:10.1016/j.cca.2003.11.006

    Google Scholar 

  • Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci Total Environ 309:105–115. doi:10.1016/S0048-9697(03)00006-8

    CAS  Google Scholar 

  • Pantke U, Volk T, Schmutzler M, Kox WJ, Sitte N, Grune T (1999) Oxidized proteins as a marker of oxidative stress during coronary heart surgery. Free Radic Biol Med 27:1080–1086. doi:10.1016/S0891-5849(99)00144-6

    CAS  Google Scholar 

  • Peña S, Peña JB, Ríos C, Sancho E, Fernández CM, Ferrando MD (2000) Role of glutathione in thiobencarb resistance in the european eel Anguilla anguilla. Ecotoxicol Environ Saf 46:51–56. doi:10.1006/eesa.1999.1882

    Google Scholar 

  • Peña-Llopis S, Peña JB, Sancho E, Fernández-Vega C, Ferrando MD (2001) Glutathione-dependent resistance of the European eel Anguilla anguilla to the herbicide molinate. Chemosphere 45:671–681. doi:10.1016/S0045-6535(00)00500-2

    Google Scholar 

  • Peña-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. Aquatic Toxicol 65:337–360. doi:10.1016/S0166-445X(03)00148-6

    Google Scholar 

  • Pfeiffer WC, Lacerda LD, Malm O, Souza CMM, Silveira EG, Bastos WR (1989) Mercury concentrations in inland waters of gold mining areas in Rondônia, Brazil. Sci Total Environ 87/88:233–240. doi:10.1016/0048-9697(89)90238-6

    Google Scholar 

  • Porter CM, Janz DM (2003) Treated municipal sewage discharge affects multiple levels of biological organization in fish. Ecotoxicol Environ Saf 54:199–206. doi:10.1016/S0147-6513(02)00056-8

    CAS  Google Scholar 

  • Ramamurthi R, Naidu KA, Subbiah MB, Balaji N, Rao MVR (1982) Toxicity of mercury to some freshwater organisms. Geobios 9:89–90

    Google Scholar 

  • Rana SVS, Singh R, Verma S (1995) Mercury-induced lipid peroxidation in the liver, kidney, brain and gills of a freshwater fish Channa punctatus. Jpn J Ichthyol 42:255–259

    Google Scholar 

  • Rao JV, Begum G, Pallela R, Usman PK, Rao RN (2005) Changes in behavior and brain acetylcholinesterase activity in mosquito fish, Gambusia affinis in response to the sub-lethal exposure to chlorpyrifos. Int J Environ Res Public Health 2:478–483. doi:10.3390/ijerph2005030013

    CAS  Google Scholar 

  • Reeder SW, Demago A, Taylor MC (1979) Mercury. In: Guidelines for surface water quality, vol. I: inorganic chemical substances. Water Quality Branch, Inland Waters Directorate, Environment Canada, Ottawa

  • Regoli F, Winston GW, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S (2003) Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environ Toxicol Chem 22:2120–2129. doi:10.1897/02-378

    CAS  Google Scholar 

  • Requena JR, Levine RL, Stadtman ER (2003) Recent advances in the analysis of oxidized proteins. Amino Acids 25:221–226. doi:10.1007/s00726-003-0012-1

    CAS  Google Scholar 

  • Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363. doi:10.1016/S0076-6879(94)33041-7

    CAS  Google Scholar 

  • Roesijadi G (1996) Metallothionein and its role in toxic metal regulation. Comp Biochem Physiol C 113:117–123. doi:10.1016/0742-8413(95)02077-2

    Google Scholar 

  • Roesijadi G, Robinson WE (1994) Metal regulation in aquatic animals: mechanisms of uptake, accumulation and release. In: Malins DC, Ostrander GK (eds) Aquatic toxicology; molecular, biochemical and cellular perspectives. Lewis Publishers, CRC press, Boca Raton, pp 387–420

    Google Scholar 

  • Rouleau K, Borg-Neczak K, Gottofrey J, Tjalve H (1999) Accumulation of waterborne mercury (II) in specific areas of fish brain. Environ Sci Technol 33:3384–3389. doi:10.1021/es990001v

    CAS  Google Scholar 

  • Satoh K (1978) Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta 90:37–43. doi:10.1016/0009-8981(78)90081-5

    CAS  Google Scholar 

  • 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. doi:10.1016/S0147-6513(03)00009-5

    CAS  Google Scholar 

  • Schlenk D, Zhang YS, Nix J (1995) Expression of hepatic metallothionein messenger RNA in feral and caged fish species correlates with muscle mercury levels. Ecotoxicol Environ Saf 31:282–286. doi:10.1006/eesa.1995.1075

    CAS  Google Scholar 

  • Scorvo-Filho JD, Martin NB, Ayrosa LMS (1998) Piscicultura em São Paulo: custos e retornos de diferentes sistemas de produção na safra de 1996/1997. Inf Econ 28:41–60

    Google Scholar 

  • Serfor-Armah Y, Nyarko BJB, Adotey DK, Adomako D, Akah EHK (2005) The impact of small-scale mining activities on the levels of mercury in the environment: the case of Prestea and its environs. J Radioanal Nucl Chem 262:685–690. doi:10.1007/s10967-004-0493-8

    Google Scholar 

  • Shastri Y, Diwekar U (2008) Optimal control of lake pH for mercury bioaccumulation control. Ecol Modell 216:1–17. doi:10.1016/j.ecolmodel.2008.03.019

    CAS  Google Scholar 

  • Shaw BP, Sahu A, Panigrahi AK (1989) Mercury in bed sediment of the Rushikulya river estuary. J Environ Biol 10:59–64

    CAS  Google Scholar 

  • Sinha TKP, Kumar K (1992) Acute toxicity of mercuric chloride to Anabas testudineus (Bloch). Environ Ecol 10:720–722

    CAS  Google Scholar 

  • Soares SS, Martins H, Aureliano M (2006) Vanadium distribution following decavanadate administration. Arch Environ Contam Toxicol 50:60–64. doi:10.1007/s00244-004-0246-2

    CAS  Google Scholar 

  • Soares SS, Martins H, Duarte RO, Moura JJG, Coucelo J, Gutiérrez-Merino C, Aureliano M (2007) Vanadium distribution, lipid peroxidation and oxidative stress markers upon decavanadate in vivo administration. J Inorg Biochem 101:80–88. doi:10.1016/j.jinorgbio.2006.08.002

    CAS  Google Scholar 

  • 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 C 147:168–178. doi:10.1016/j.cbpc.2007.09.003

    CAS  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptation in nature. Braz J Med Res 29:1715–1733

    CAS  Google Scholar 

  • Sun Y, Hongxia Y, Zhangc J, Yin Y, Shen H, Liu H, Wang X (2006) Bioaccumulation and antioxidant responses in goldfish Carassius auratus under HC orange no. 1 exposure. Ecotoxicol Environ Saf 63:430–437. doi:10.1016/j.ecoenv.2005.02.001

    CAS  Google Scholar 

  • USEPA (US Environmental Protection Agency) (2002) Mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry EPA 821-R-02–019, Method 163, revision E. US Environmental Protection Agency, Office of Water, Washington, DC 38p

    Google Scholar 

  • USP (United States Pharmacopeia) (2000) Analytical methods flame atomic absorption spectrometry varian, Publication no 85

  • 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. doi:10.1016/S1382-6689(02)00126-6

    Google Scholar 

  • Verlecar XN, Jena KB, Chainy GBN (2007) Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. Chem Biol Interact 167:219–226. doi:10.1016/j.cbi.2007.01.018

    CAS  Google Scholar 

  • Verlecar XN, Jena KB, Chainy GBN (2008) Modulation of antioxidant defenses in digestive gland of Perna viridis (L.), on mercury exposure. Chemosphere 71:1977–1985. doi:10.1016/j.chemosphere.2007.12.014

    CAS  Google Scholar 

  • Verma SR, Jain M, Tonk IP (1983) In vivo effects of mercuric chloride on tissue ATPases of Notopterus notopterus. Toxicol Lett 16:305–309. doi:10.1016/0378-4274(83)90191-1

    CAS  Google Scholar 

  • Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antartic molluscs. Mar Environ Res 44:69–84. doi:10.1016/S0141-1136(96)00103-1

    CAS  Google Scholar 

  • Viarengo A, Burlando B, Dondero F, Marrò A, Fabbri R (1999) Metallothionein as a tool in biomonitoring programmes. Biomarkers 4:455–466. doi:10.1080/135475099230615

    CAS  Google Scholar 

  • Viarengo A, Burlando B, Giordana A, Bolognesi C, Gabrielides GP (2000) Networking and expert-system analysis: next frontier in biomonitoring. Mar Environ Res 49:483–486. doi:10.1016/S0141-1136(00)00027-1

    CAS  Google Scholar 

  • Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C 146:281–300. doi:10.1016/j.cbpc.2007.04.011

    CAS  Google Scholar 

  • Vieira LM, Alho CJR (2000) Biomagnification of mercury in the Pantanal, Brazil. Available via DIALOG. http://www.cpap.embrapa.br/agencia/congresso/Bioticos/VIEIRA-081.pdf. Accessed 12 Jan 2006

  • Wedekind C, Siebenthala BV, Gingold RG (2007) The weaker points of fish acute toxicity tests and how tests on embryos can solve some issues. Environ Pollut 148:385–389. doi:10.1016/j.envpol.2006.11.022

    CAS  Google Scholar 

  • WHO (World Health Organization) (2003) Concise International Chemical Assessment Document 50. Elemental mercury and inorganic mercury compounds: human health aspects, Geneva

  • Wilce MC, Parker MW (1994) Structure and function of glutathione S-transferases. Biochim Biophys Acta 1205:1–18. doi:10.1016/0167-4838(94)90086-8

    CAS  Google Scholar 

  • Wilhelm Filho D, Torres MA, Zaniboni-Filho E, Pedrosa RC (2005) Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes, 1847). Aquaculture 244:349–357. doi:10.1016/j.aquaculture.2004.11.024

    Google Scholar 

  • Zhang J, Shen H, Wang X, Wu J, Xue Y (2004) Effects of chronic exposure of 2, 4-dichlorophenol on the antioxidant system in liver of freshwater fish Carassius auratus. Chemosphere 55:167–174. doi:10.1016/j.chemosphere.2003.10.048

    CAS  Google Scholar 

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Acknowledgments

This study was supported by São Paulo State Research Foundation (FAPESP—Proc. 06/50772-6) and the National Council for the Development of Research and Technology (CNPq). The authors are thankful to Águas Claras fish farm, which provided the fish.

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Correspondence to Ana Lúcia Kalinin.

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Monteiro, D.A., Rantin, F.T. & Kalinin, A.L. Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz, 1829). Ecotoxicology 19, 105–123 (2010). https://doi.org/10.1007/s10646-009-0395-1

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