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Arsenic-induced responses in freshwater teleosts

Abstract

The environment is currently polluted by thousands of chemicals or xenobiotics introduced into the environment by man to meet the demands of the modern era. Every day we encounter this negative side of human civilization, but have done little to lessen the rate of pollution. Although the entire biosphere is polluted it is water resources that are the most polluted because water is the ultimate sink for many contaminants. Thus, fish are the most vulnerable of all animal species. They are helpless because they cannot avoid the polluted habitat and face this contamination by default. Nevertheless, fish are found to survive under extreme conditions when their natural habitat has been compromised to a great extent. However, fish are highly sensitive to small environmental changes and their populations gradually dwindle if pollution continues unabated. However, we know that there are instances when water is cleaned and the rate of repopulation by different fish species has gained momentum, restoring the ecological balance. Thus, fish are considered reliable bioindicators of water pollution and fish ecotoxicology has received much attention in recent years, and fish toxicology has been able to defend a significant position in the arena of xenobiotics research over the years. This review deals with some of the major intoxication and detoxication signals manifested by fish exposed to arsenic (As), which is presently one of the most worrying metalloids in water pollution.

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Abbreviations

ACh:

Acetylcholine

AChE:

Acetylcholinesterase

ACOX:

Acyl co-A oxidase

CD:

Conjugated dienes

GPx:

Glutathione peroxidase

GR:

Glutathione reductase

GSH:

Glutathione reduced

GSSG:

Glutathione oxidized

GST:

Glutathione-S-transferase

HSP -70:

Heat shock protein 70

LPO:

Lipid peroxidation

MDA:

Malondialdehyde

MT:

Metallothionein

NAC:

N-acetyl-cysteine

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

–SH:

Thiol groups

TBARS:

Thiobarbituric acid reactive substances

References

  • Acharyya SK, Chakraborty P, Lahiri S, Raymahashay BC, Guha S, Bhowmik A (1999) Arsenic poisoning in the Ganges delta. Nature 401(6753): 545- 546

    Article  PubMed  CAS  Google Scholar 

  • Agarwal A, Bhattacharya S (1990) Purification of a metallothionein-like protein (MLP) from the serum of Hg treated rats using phosphorylcholine-sepharose affinity column. Indian J Exp Biol 28:648–652

    Google Scholar 

  • Albores A, Koropatnick J, Cherian MG, Zelazowski AJ (1992) Arsenic induces and enhances rat hepatic metallothionein production in vivo. Chem Biol Interact 85:127–140

    Article  PubMed  CAS  Google Scholar 

  • Albro PW, Corbett JT, Schroeder JL (1986) Generation of hydrogen peroxide by incidental metal ion-catalyzed autooxidation of glutathione. J Inorg Biochem 27:191–203

    Article  PubMed  CAS  Google Scholar 

  • Anderson LCD, Bruland KW (1991) Biogeochemistry of arsenic in natural waters: the importance of methylated species. Environ Sci Technol 25:420–427

    Article  CAS  Google Scholar 

  • Atkinson BG, Walden DB (1985) Changes in eukaryotic gene expression in response to environmental stress. Academic, Orlando, Florida

    Google Scholar 

  • Barrett WC, DeGnore JP, Keng YF, Zhang ZY, Yim MB, Chock PB (1999) Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J Biol Chem 274:34543–34546

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharya A (2004) Intoxication signals, detoxication signals and peroxisomal response of Clarias batrachus to arsenic. PhD Dissertation, Visva Bharati University, Santiniketan, India

  • Bhattacharya A, Bhattacharya S (2005) Induction of oxidative stress by arsenic in Clarias batrachus: involvement of peroxisomes. Ecotoxicol Environ Saf (Elsevier, USA, published on line; available at www.science direct.com; DOI: 10.1016/j.ecoenv. 2005.11.002)

  • Birge WJ, Hudson JE, Black JA, Westerman AG (1978) Embryo-larval bioassays on inorganic coal elements and in situ biomonitoring of coal-waste effluents. In: Samuel DE, Stauffer JR, Hocutt CH, Mason WT (eds) Surface mining and fish/wildlife needs in the Eastern United States (PB 298353). Springfield, VA, NTIS, pp 97–104

  • Bose SN (1993) Toxic response to cadmium, mercury and zinc in rat and mouse. Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Bucher E, Hofer R, Krumschnabel G, Doblander C (1993) Disturbances in the pro-oxidant-antioxidant balance in the liver of bullhead (Cottus gobio L.) exposed to treated paper mill effluents. Chemosphere 27:1329–1338

    Article  CAS  Google Scholar 

  • Carpene E, Cortesi P, Tacconi S, Cattami O, Isane G, Serrazanetti GP (1987) Cd-matallothionein and metal enzymes interaction in the goldfish Carassius auratus. Comp Biochem Physiol 86C: 267–272

    CAS  Google Scholar 

  • Chakraborti D, Mukherjee SC, Pati S, Sengupta MK, Rahman MM, Chowdhury UK, Lodh D, Chanda CR, Chakraborti AK, Basu GK (2003) Arsenic groundwater contamination in middle ganga plain, Bihar, India: a future danger? Environ Health Perspect 111:1194–1197

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S (1983) Adaptive and detoxifying mechanisms in a fresh water perch Anabas testudineus (Bloch) exposed to certain industrial pollutants. Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Chatterjee S, Bhattacharya S (1984) Detoxication of industrial pollutants by the glutathione-S-transferase system in the liver of Anabas testudineus (Bloch). Toxicol Lett 22:187–198

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Bhattacharya S (1986) Inductive changes in hepatic metallothionein profile in climbing perch, Anabas testudineus (Bloch) by industrial pollutants. Indian J Exp Biol 24:455–457

    PubMed  CAS  Google Scholar 

  • Cherian MG (1995) Metallothionein and its interaction with metals. Handb Exp Pharmacol 115:121–138

    CAS  Google Scholar 

  • Dalal R (1989) Involvement of hepatic metallothionein and aniline hydroxylase in the detoxication of industrial pollutants in an air breathing freshwater teleosts, Channa punctatus (Bloch): evaluation of toxic response syndrome. Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Dalal R, Bhattacharya S (1991) Effect of chronic nonlethal doses of nonmetals and metals on hepatic MT in Channa punctatus (Bloch). Indian J Exp Biol 29:693–694

    PubMed  CAS  Google Scholar 

  • Das D, Sarkar D, Bhattacharya S (1998) Lipid peroxidative damage by arsenic intoxication is countered by glutathione-glutathione-S-transferase system and metallothionein in the liver of climbing perch, Anabas testudineus. Biomed Environ Sci 11:187–195

    Google Scholar 

  • De Pomerai D (1996) Heat-shock proteins as biomarkers of pollution. Hum Exp Toxicol 15:279–285

    Article  PubMed  Google Scholar 

  • Denu JM, Tanner KG (1998) Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37:5633–5642

    Article  PubMed  CAS  Google Scholar 

  • DiGiulio RT, Washburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxicol Chem 8:1103–1123

    Article  CAS  Google Scholar 

  • DiGiulio RT, Habig C, Gallagher EP (1993) Effects of Black Rock Harbour sediments on indices of biotransformation, oxidative stress, and DNA integrity in channel catfish. Aquat Toxicol 26:1–22

    Article  CAS  Google Scholar 

  • Eckwert H, Köhler HR (1997) The indicative value of the hsp70 stress response as a marker for metal effects in Oniscus asellus (Isopoda) field populations: variability between populations from metal-polluted and uncontaminated sites. Appl Soil Toxicol 6:275–282

    Article  Google Scholar 

  • Emerit J, Chaudiere J (1989) Free radicals and lipid peroxidation in cell pathology. In: Miquel J, Quintanilha AT, Weber H (eds) CRC handbook of free radicals and antioxidants in biomedicine. CRC Press, Boca Raton, Florida, pp 177–185

    Google Scholar 

  • Filho DW (1996) Fish antioxidant defences – a comparative approach. Braz J Med BioI Res 29:1735–1742

    Google Scholar 

  • Guhathakurta S, Bhattacharya S (1984) Regional activity of acetylcholine concentration in the brain of the goat, Capra capra. Com Physiol Ecol 9:405–408

    Google Scholar 

  • Hammond PB, Beliles RP (1984) Metals. In: Doull J, Klaassen CD, Amdur MO (eds) Toxicology: the basic science of poisons. Macmillan Publishing Co., NY, pp 409–467

    Google Scholar 

  • Hartwell SI, Jin JH, Cherry DS, Cairns J (1989) Toxicity versus avoidance response of golden shiner, Notemigonus crysoleucas, to five metals. J Fish Biol 35:447–456

    Article  CAS  Google Scholar 

  • Hasspieler BM, Behar IV, DiGiulio RT (1994) Glutathione-dependent defense in channel catfish (Ictalurus punctatus) and brown bullhead (Ameriurus nebulosus). Ecotoxicol Environ Saf 28:82–90

    Article  PubMed  CAS  Google Scholar 

  • Irwin RJ, VanMouwerik M, Stevens L, Seese MD, Basham W (1997) Environmental contaminants encyclopedia. National Park Service, Water Resources Division, Fort Collins, Colorado, pp 1–114

  • James MO (1987) Conjugation of organic pollutants in aquatic species. Environ Health Persp 71:97–104

    Article  CAS  Google Scholar 

  • Jana S, Sahana SS, Choudhuri MA, Choudhuri DK (1986) Heavy metal pollutant induced changes in some biochemical parameters in the freshwater fish Clarias batrachus L. Acta Physiol Hung 68:39–43

    PubMed  CAS  Google Scholar 

  • Jash NB, Bhattacharya S (1983) Delayed toxicity of carbofuran in freshwater teleosts, Channa punctatus (Bloch) and Anabas testudineus (Bloch). Water Air Soil Pollut 19:209–213

    Article  CAS  Google Scholar 

  • Jash NB, Chatterjee S, Bhattacharya S (1982) Role of acetylcholine in the recovery of brain acetylcholinesterase in Channa punctatus (Bloch) exposed to Furadan. Comp Physiol Ecol 7:56–58

    CAS  Google Scholar 

  • Kägi JHR (1993) Evolution, structure and chemical activity of class I metallothioneins: an overview. In: Suzuki KT, Imura N, Kimura M (eds) Metallothionein III: biological roles and medical implications. Birkhauser Verlag, Berlin, pp 29–56

    Google Scholar 

  • Kägi JH, Kojima Y (1987) Chemistry and biochemistry of metallothionein. Exper Suppl 52:25–61

    Google Scholar 

  • Kägi JHR, Schaffer A (1988) Biochemistry of metallothionein. Biochemistry 27:8509–8515

    Article  PubMed  Google Scholar 

  • Kappus H (1987) Oxidative stress in chemical toxicity. Arch Toxicol 60:144–149

    Article  PubMed  CAS  Google Scholar 

  • Klaassen CD (1995) Heavy metals and heavy-metal antagonists. In: Hardman JG, Limbird LE, Molinoff PM, Ruddon RW, Gilman AG (eds) Goodman and Gilman’s pharmacological basis of therapeutics, 9th edn. McGraw-Hill, New York, pp 1649–1672

    Google Scholar 

  • Kreppel H, Bauman JW, Liu J, McKim JM Jr, Klaassen CD (1993a) Induction of metallothionein by arsenicals in mice. Fundam Appl Toxicol 20:184–189

    Article  PubMed  CAS  Google Scholar 

  • Kreppel H, Paepcke U, Thiermann H, Szinnicz L, Reichl FX, Singh PK, Jones MM (1993b) Therapeutic efficacy of new dimercaptosuccinic acid (DMSA) analogues in acute arsenic trioxide poisoning in mice. Arch Toxicol 67:580–585

    Article  PubMed  CAS  Google Scholar 

  • Kuroshima R (1995) Hepatic metallothionein and glutathione levels in red sea bream. Comp Biochem Physiol 110C:95–100

    CAS  Google Scholar 

  • Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH (1999) Stress proteins (hsp’s): methods of detection and their use as an environmental biomarker. Ecotoxicology 8:351–368

    Article  CAS  Google Scholar 

  • Lima AR, Curtis C, Hammermeister DE, Markee TP, Northcott CE, Brooke LT (1984) Acute and chronic toxicities of arsenic (III) to fathead minnows, flagfish, daphnids, and an amphipod. Arch Environ Contam Toxicol 13:595–601

    Article  CAS  Google Scholar 

  • Lopez-Torres M, Perez-Campo R, Cadenas S, Rojas C, Barja G (1993) A comparative study of free radicals in vertebrates – II. Non-enzymatic antioxidants and oxidative stress. Comp Biochem Physiol 105B:757–763

    CAS  Google Scholar 

  • Luc HEH, Snoeckx RN, Cornelussen FA, Van N, Robert SR, Ger JV (2001) Heat shock proteins and cardiovascular pathophysiology. Physiol Rev 81:1461–1497

    Google Scholar 

  • Mather-Mihaich E, DiGiulio RT (1991) Oxidant, mixed-function oxidase and peroxisomal responses in channel catfish exposed to a bleached kraft mill effluent. Arch Environ Contam Toxicol 20:391–397

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay B, Bose S, Bhattacharya S (1994) Induction of metallothionein in rat liver by cadmium chloride: probable mechanism of action. Biomed Environ Sci 1:232–240

    Google Scholar 

  • National Academy of Sciences (NAS) (1977) Arsenic Drinking Water And Health, Safe Drinking Water Committee, Washington D.C. 332

  • National Research Council of Canada (NRCC) 1978. Effects of arsenic in the Canadian environment. Natl Res Counc Can Publ NRCC 15391:1–249

    Google Scholar 

  • Nriagu JO, Pacyna JM (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:134–139

    Article  PubMed  CAS  Google Scholar 

  • Otto DM, Moon TW (1995) 3,3′,4,4′-Tetrachlorobiphenyl effects on antioxidant enzymes and glutathione status in different tissues of rainbow trout. Pharmacol Toxicol 77:281–287

    PubMed  CAS  Google Scholar 

  • Page JD, Wilson IB (1985) Acetylcholinesterase: inhibition by tetranitromethane and arsenite: binding of arsenite by tyrosine residues. J Biol Chem 260:1475–1478

    PubMed  CAS  Google Scholar 

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496

    Article  PubMed  CAS  Google Scholar 

  • Qian Y, Castranova V, Shi X (2003) New perspectives in arsenic induced cell signal transduction. J Inorg Biochem 96:271–278

    Article  PubMed  CAS  Google Scholar 

  • Quig D (1998) Cysteine metabolism and metal toxicity. Altern Meds Rev 3:262–270

    CAS  Google Scholar 

  • Radi AAR, Hai DQ, Matkovics B, Gabrielak T (1985) Comparative antioxidantenzyme study in freshwater fish with different types of feeding behaviour. Comp Biochem Physiol 81C: 395–399

    CAS  Google Scholar 

  • Rodriguez-Ariza A, Peinado I, Pueyo C, Lopez-Barea I (1993) Biochemical indicators of oxidative stress in fish from polluted littoral areas. Can J Fish Aquat Sci 50:2568–2573

    CAS  Google Scholar 

  • Roesijadi G (1992) Metallothionein in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114

    Article  CAS  Google Scholar 

  • Roy S (2003) Interactive mechanism of intoxication and detoxication in Clarias batrachus hepatocytes exposed to cadmium and lead. Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Roy S (2004) Arsenic toxicity to Channa punctatus (Bloch): mechanism of intoxication, detoxication and stimulation of stress protein synthesis. Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Roy S, Bhattacharya S (2005) Arsenic induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotox Environ Saf (Elsevier, USA published on line; available at www.science direct.com, DOI: 10.1016/j.ecoenv. 2005.07.005)

  • Roy S, Bhattacharya A, Roy S, Bhattacharya S (2004) Arsenic induced lipid peroxidation at non-lethal doses. In: Bhattacharya S, Maitra SK (eds) Current issues in environmental and fish biology. Daya Publishing House, Delhi, pp 52–63

    Google Scholar 

  • Roy S, Chattoraj A, Bhattacharya S (2006) Arsenic-induced changes in optic tectal histoarchitecture acetylcholinesterase–acetylcholine profile in Channa punctatus: amelioration by selenium. Comp Biochem Physiol C 144(1):16–24

    Google Scholar 

  • Santra A, Maiti A, Das S, Lahiri S, Chakraborty SK, Mazumder DN (2000) Hepatic damage caused by chronic arsenic toxicity in experimental animals. J Toxicol Clin Toxicol 38:395–405

    Article  PubMed  CAS  Google Scholar 

  • Sarkar D (1997) Role of reduced glutathione, glutathione-S-transferase, metallothonein and lipid peroxidation in the detoxication mechanism in Anabas testudineus (Bloch). Ph. D. Dissertation, Visva Bharati University, Santiniketan, India

  • Shukla JP, Pandey K (1984) Impaired ovarian functions in arsenic-treated freshwater fish, Colisa fasciatus (Bl. and Sch.). Toxicol Lett 20:1–3

    Article  PubMed  CAS  Google Scholar 

  • Shukla JP, Shukla KN, Dwivedi UN (1987) Survivality and impaired growth in arsenic treated fingerlings of Channa punctatus, a fresh water murrel. Acta Hydrochim Hydrobiol 15:307–311

    Article  CAS  Google Scholar 

  • Sorensen EM, Ramirez-Mitchell R, Pradzynski A, Bayer TL, Wenz LL (1985) Sterological analysis of hepatocytes changes parallel arsenic accumulation in the livers of green sunfish. J Environ Pathol Toxicol Oncol 6:195–210

    PubMed  CAS  Google Scholar 

  • Spehar RL, Fiandt JT (1986) Acute and chronic effects of water quality criteria-based metal mixtures on three aquatic species. Environ Toxicol Chem 5:917–931

    Article  CAS  Google Scholar 

  • Stoytchevaa M, Sharkovab V, Panayotova M (1998) Electrochemical approach in studying the inhibition of acetylcholinesterase by arsenate (III): analytical characterization and application for arsenic determination. Anal Chim Acta 364:195–201

    Article  Google Scholar 

  • Styblo M, Yamauchi H, Thomas DJ (1995) Comparative in vitro methylation of trivalent and pentavalent arsenicals. Toxicol Appl Pharmacol 135:172–178

    Article  PubMed  CAS  Google Scholar 

  • Styblo M, Serves SV, Cullen WR, Thomas DJ (1997) Comparative inhibition of yeast glutathione reductase by arsenicals and arsenothiols. Chem Res Toxicol 10:27–33

    Article  PubMed  CAS  Google Scholar 

  • Suzuki KT, Sunaga H, Kotayashi E, Hatekeyama S (1987) Environmental and injected cadmium are sequestered by two major isoforms of basal copper, zinc-metallothionein in gibel (Carassius auratus langsdorfi) liver. Comp Biochem Physiol 87C: 87–94

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tripathi N, Kannan GM, Pant BP, Jaiswal DK, Malhotra PR, Flora SJS (1997) Arsenic-induced changes in certain neurotransmitter levels and their recoveries following chelation in rat whole brain. Toxicol Lett 92:201–208

    Article  PubMed  CAS  Google Scholar 

  • Ullrich V, Bachschmid M (2000) Superoxide as a messenger of endothelial function. Biochem Biophys Res Commun 278:1–8

    Article  PubMed  CAS  Google Scholar 

  • Wakao N, Koyatsu H, Komai Y (1988) Microbial oxidation of arsenite and occurrence of arsenite-oxidizing bacteria in acid mine water from a sulfur-pyrite mine. Geomicrobiol J 6:11–24

    CAS  Google Scholar 

  • Weiss CM (1961) Physiological effect of organic phosphorus insecticides on several species of fish. Trans Am Fish Soc 90:143–152

    Article  CAS  Google Scholar 

  • Welch AH, Lico MS, Hughes JL (1988) Arsenic in groundwater of the Western United States. Ground Water 26:333–347

    Article  CAS  Google Scholar 

  • Yeh JY, Cheng LC, Ou BR, Whanger DP, Chang LW (2002) Differential influences of various arsenic compounds on glutathione redox status and antioxidative enzymes in porcine endothelial cells. Cell Mol Life Sci 59:1972–1982

    Google Scholar 

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Acknowledgements

The authors are grateful to the Indian Council of Agricultural Research, New Delhi, where AB and SR were Senior Research Fellows, for financial support [F-4(16)/98-ASR-I]. The authors would also like to thank the UGC for the DSA support to the Department, which enabled the study.

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Bhattacharya, S., Bhattacharya, A. & Roy, S. Arsenic-induced responses in freshwater teleosts. Fish Physiol Biochem 33, 463–473 (2007). https://doi.org/10.1007/s10695-007-9173-2

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  • DOI: https://doi.org/10.1007/s10695-007-9173-2

Keywords

  • Arsenic
  • AChE–ACh system
  • Detoxication
  • GSH–GST system
  • HSP
  • Intoxication
  • Lipid peroxidation
  • Metallothionein
  • ROS