Heavy Metal- induced Toxicity in Fish: Insights into Molecular Responses

PDF

Published: 2023-10-13

DOI: 10.56557/upjoz/2023/v44i213703

Page: 321-333


Reema Rose Mani *

Department of Zoology, Alphonsa College, Pala, Kottayam District, -686574, Kerala, India.

Simimole Sebastian

Department of Zoology, Alphonsa College, Pala, Kottayam District, -686574, Kerala, India.

Aaggi Philip

Department of Zoology, Alphonsa College, Pala, Kottayam District, -686574, Kerala, India.

*Author to whom correspondence should be addressed.


Abstract

Environmental pollution by heavy metals has evolved to be a huge concern due to its fatal impact on ecosystem health. Extensive application of heavy metals in a wide range of fields including that of agriculture, industry, technology and medicine has led to an increased exposure to the metals. Trace metals are considered to be systemic toxicants known to induce cellular, molecular, biochemical alterations, even at lower levels of exposure. Due to the high sensitivity to dissolved toxicants and the topmost position in aquatic food web, fish is prone to heavy metal toxicity significantly. These metals have been reported to affect DNA and proteins involved in metabolism, detoxification, and damage repair, paving way to carcinogenesis and mortality. Significance of early determination of metal exposure necessitates the need for effective biomarkers that reflects metal induced damage in fish. This review gives an overview on the genetic alterations and molecular changes in fish in response to toxicity induced by heavy metals.

Keywords: Heavy metals, bioaccumulation, toxicity, DNA damage, oxidative stress, biomarkers


How to Cite

Mani , R. R., Sebastian , S., & Philip , A. (2023). Heavy Metal- induced Toxicity in Fish: Insights into Molecular Responses. UTTAR PRADESH JOURNAL OF ZOOLOGY, 44(21), 321–333. https://doi.org/10.56557/upjoz/2023/v44i213703

Downloads

Download data is not yet available.

References

Fergusson JE. The heavy element: Chemistry, environmental impact and health effects. Pergamon Press; 1990.

Linnik PM, Zubenko IB. Role of bottom sediments in the secondary pollution of aquatic environments by heavy-metal compounds. Lakes and Reservoirs: Research and Management. 2000;5(1): 11–21.

Available:https://doi.org/10.1046/j.1440-1770.2000.00094.x

Malik RN, Husain SZ, Nazir I. Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad, Pakistan. Pakistan Journal of Botany. 2010;42(1).

Agah H, Leermakers M, Elskens M, Fatemi SMR, Baeyens W. Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf. Environmental Monitoring and Assessment. 2009;157(1–4):499–514.

Available:https://doi.org/10.1007/s10661-008-0551-8

Indrajith H, Pathiratne K, Pathiratne A. Heavy metal levels in two food fish species from Negombo estuary, Sri Lanka: Relationships with the body size. Sri Lanka Journal of Aquatic Sciences. 2010;13(0):63.

Available:https://doi.org/10.4038/sljas.v13i0.2207

Wright DA, Welbourn P. Environmental toxicology. Cambridge University Press; 2002.

Available:https://doi.org/10.1017/CBO9780511805998

Mansour SA, Sidky MM. Ecotoxicological Studies. 3. Heavy metals contaminating water and fish from Fayoum Governorate, Egypt. Food Chemistry. 2002;78(1):15–22. Available:https://doi.org/10.1016/S0308-8146(01)00197-2

Jezierska B, Witeska M. The metal uptake and accumulation in fish living in polluted waters. In Soil and Water Pollution Monitoring, Protection and Remediation. Springer Netherlands. 2007;107–114.

Available:https://doi.org/10.1007/978-1-4020-4728-2_6

Authman MM. Use of fish as bio-indicator of the effects of heavy metals pollution. Journal of Aquaculture Research & Development. 2015;06(04). Available:https://doi.org/10.4172/2155-9546.1000328

Huseen HM, Mohammed AJ. Heavy metals causing toxicity in fishes. Journal of Physics: Conference Series. 2019;1294(6):062028. Available:https://doi.org/10.1088/1742-6596/1294/6/062028

Afshan S, Ali S, Ameen U, Farid M, Bharwana S, Hannan F, Ahmad R. Effect of different heavy metal pollution on fish. Research Journal of Chemical and Environmental Sciences; 2014.

Abadi DRV, Dobaradaran S, Nabipour I, Lamani X, Ravanipour M, Tahmasebi R, Nazmara S. Comparative investigation of heavy metal, trace, and macro element contents in commercially valuable fish species harvested off from the Persian Gulf. Environmental Science and Pollution Research. 2015;22(9):6670–6678.

Available:https://doi.org/10.1007/s11356-014-3852-1

Javed M, Usmani N. An overview of the adverse effects of heavy metal contamination on fish health. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences. 2019;89(2):389–403.

Available:https://doi.org/10.1007/s40011-017-0875-7

Sfakianakis DG, Renieri E, Kentouri M, Tsatsakis AM. Effect of heavy metals on fish larvae deformities: A review. Environmental Research. 2015;137:246–255. Available:https://doi.org/10.1016/j.envres.2014.12.014

van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology. 2003;13(2):57–149.

Available:https://doi.org/10.1016/S1382-6689(02)00126-6

Monserrat JM, Martínez PE, Geracitano LA, Lund Amado L, Martinez Gaspar Martins C, Lopes Leães Pinho G, Soares Chaves I, Ferreira-Cravo M, Ventura-Lima J, Bianchini A. Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2007;146(1–2):221–234. Available:https://doi.org/10.1016/j.cbpc.2006.08.012

Wood RD, Mitchell M, Sgouros J, Lindahl T. Human DNA repair genes. Science. 2001;291(5507): 1284–1289.

Available:https://doi.org/10.1126/science.1056154

Ahmad I, Ahmad A, Ahmad M. Binding properties of pendimethalin herbicide to DNA: multispectroscopic and molecular docking approaches. Physical Chemistry Chemical Physics. 2016;18(9): 6476–6485.

Available:https://doi.org/10.1039/C5CP07351K

Ahmad I, Ahmad M. Fresh water fish, Channa punctatus, as a model for pendimethalin genotoxicity testing: A new approach toward aquatic environmental contaminants. Environmental Toxicology. 2016;31(11):1520–1529.

Available:https://doi.org/10.1002/tox.22156

Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metal toxicity and the environment. 2012;133–164.

Available:https://doi.org/10.1007/978-3-7643-8340-4_6

Silbergeld EK. Facilitative mechanisms of lead as a carcinogen. In Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis. 2003;533: 1–2. Available:https://doi.org/10.1016/j.mrfmmm.2003.07.010

Waalkes M. Cadmium carcinogenesis. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 2003;533(1–2):107–120. Available:https://doi.org/10.1016/j.mrfmmm.2003.07.011

Arkhipchuk VV, Garanko NN. Using the nucleolar biomarker and the micronucleus test on in vivo fish fin cells. Ecotoxicology and Environmental Safety. 2005;62(1):42–52. Available:https://doi.org/10.1016/j.ecoenv.2005.01.001

Bopp SK, Abicht HK, Knauer K. Copper-induced oxidative stress in rainbow trout gill cells. Aquatic Toxicology. 2008;86(2): 197–204. Available:https://doi.org/10.1016/j.aquatox.2007.10.014

Buschini A, Pinelli S, Pellacani C, Giordani F, Ferrari MB, Bisceglie F, Giannetto M, Pelosi G, Tarasconi P. Synthesis, characterization and deepening in the comprehension of the biological action mechanisms of a new nickel complex with antiproliferative activity. Journal of Inorganic Biochemistry. 2009;103(5):666–677.

Available:https://doi.org/10.1016/j.jinorgbio.2008.12.016

Gómez SE, del Razo LM, Muñoz Sanchez JL. Induction of DNA damage by free radicals generated either by organic or inorganic arsenic (in Cultures of B and T Lymphocytes. Biological Trace Element Research. 2005;108(1–3):115–126. Available:https://doi.org/10.1385/BTER:108:1-3:115

Zhou X, Li Q, Arita A, Sun H, Costa M. Effects of nickel, chromate, and arsenite on histone 3 lysine methylation. Toxicology and Applied Pharmacology. 2009;236(1): 78–84.

Available:https://doi.org/10.1016/j.taap.2009.01.009

Gonzalez P, Dominique Y, Massabuau JC, Boudou A, Bourdineaud JP. Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the zebrafish (Danio rerio). Environmental Science and Technology. 2005;39(11). Available:https://doi.org/10.1021/es0483490

Sandrini JZ, Bianchini A, Trindade GS, Nery LEM, Marins LFF. Reactive oxygen species generation and expression of DNA repair-related genes after copper exposure in zebrafish (Danio rerio) ZFL cells. Aquatic Toxicology. 2009;95(4). Available:https://doi.org/10.1016/j.aquatox.2009.02.016

Pereira S, Camilleri V, Floriani M, Cavalié I, Garnier-Laplace J, Adam-Guillermin C. Genotoxicity of uranium contamination in embryonic zebrafish cells. Aquatic Toxicology. 2012;109.

Available:https://doi.org/10.1016/j.aquatox.2011.11.011

Soulivongsa L, Tengjaroenkul B, Neeratanaphan L. Effects of contamination by heavy metals and metalloids on chromosomes, serum biochemistry and histopathology of the bonylip barb fish near sepon gold-copper mine, Lao PDR. International Journal of Environmental Research and Public Health. 2020;17(24):9492.

Available:https://doi.org/10.3390/ijerph17249492

Panda BB, Achary VMM. Mitogen-activated protein kinase signal transduction and DNA repair network are involved in aluminum-induced DNA damage and adaptive response in root cells of Allium cepa L. Frontiers in Plant Science; 2014. Available:https://doi.org/10.3389/fpls.2014.00256

Tabrez S, Ahmad M. Oxidative stress-mediated genotoxicity of wastewaters collected from two different stations in northern India. Mutation Research - Genetic Toxicology and Environmental Mutagenesis. 2011;726(1).

Available:https://doi.org/10.1016/j.mrgentox.2011.07.012

Segura-Muñoz SI, Beltramini Trevilato TM, Takayanagui AMM, Hering SE, Cupo P. Heavy metals in water from pressure drinkers. Latin American Nutrition Archives. 2003;53(1).

da Rocha CAM, de Lima PDL, Santos RA dos, Burbano RMR. Evaluation of genotoxic effects of xenobiotics in fishes using comet assay—A review. Reviews in Fisheries Science. 2009;17(2):170–173.

Available:https://doi.org/10.1080/10641260802541791

Bolognesi C, Hayashi M. Micronucleus assay in aquatic animals. Mutagenesis. 2011;26(1):205–213.

Available:https://doi.org/10.1093/mutage/geq073

Gopal V, Parvathy S, Balasubramanian PR. Effect of heavy metals on the blood protein biochemistry of the fish Cyprinus carpio and its use as a bioindicator of pollution stress. Environmental Monitoring and Assessment. 1997;48(2). Available:https://doi.org/10.1023/A:1005767517819

Khan Mohd. S, Javed M, Rehman Md. T, Urooj M, Ahmad Md. I. Heavy metal pollution and risk assessment by the battery of toxicity tests. Scientific Reports. 2020;10(1):16593.

Available:https://doi.org/10.1038/s41598-020-73468-4

Mutlu E, Aydin S, Kutlu B. Turkish Journal of Fisheries and Aquatic Sciences. 2015;15(2).

Available:https://doi.org/10.4194/1303-2712-v15_2_35

Tabrez S, Zughaibi TA, Javed M. Bioaccumulation of heavy metals and their toxicity assessment in Mystus species. Saudi Journal of Biological Sciences. 2021;28(2):1459–1464.

Available:https://doi.org/10.1016/j.sjbs.2020.11.085

Mazeaud MM, Mazeaud F, Donaldson EM. Primary and secondary effects of stress in fish: Some new data with a general review. Transactions of the American Fisheries Society. 1977;106(3):201–212.

Available:https://doi.org/10.1577/1548-8659(1977)106<201:PASEOS>2.0.CO;2

Abdel-Tawwab M, Mousaad MN, Sharafeldin KM, Ismaiel NE. Changes in growth and biochemical status of common carp, Cyprinus carpio L. exposed to water-born zinc toxicity for different periods. International Aquatic Research. 2013; 5(1):11. Available:https://doi.org/10.1186/2008-6970-5-11

Javed M, Ahmad MI, Usmani N, Ahmad M. Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water /704/172/4081 /631/601 article. Scientific Reports. 2017;7(1). Available:https://doi.org/10.1038/s41598-017-01749-6

Abdel Rahman AN, ElHady M, Hassanin ME, Mohamed AAR. Alleviative effects of dietary Indian lotus leaves on heavy metals-induced hepato-renal toxicity, oxidative stress, and histopathological alterations in Nile tilapia, Oreochromis niloticus (L.). Aquaculture. 2019;509. Available:https://doi.org/10.1016/j.aquaculture.2019.05.030

Javed M, Ahmad I, Ahmad A, Usmani N, Ahmad M. Studies on the alterations in haematological indices, micronuclei induction and pathological marker enzyme activities in Channa punctatus (spotted snakehead) perciformes, channidae exposed to thermal power plant effluent. SpringerPlus. 2016;5(1).

Available:https://doi.org/10.1186/s40064-016-2478-9

Y, H, Ahi M. The Effect of lead and zeolite on hematological and some biochemical parameters in nile fish (Oreochromis niloticus). In Current Progress in Biological Research. 2013). Available:https://doi.org/10.5772/53076

Zorriehzahra MJ, Hassan MD, Gholizadeh M, Saidi AA. Study of some hematological and biochemical parameters of Rainbow trout (Oncorhynchus mykiss) fry in western part of Mazandaran province, Iran. Iranian Journal of Fisheries Sciences. 2010; 9(1).

Rojas V, Morales-Lange B, Avendaño-Herrera R, Poblete-Morales M, Tapia-Cammas D, Guzmán F, Marshall SH, Mercado L. Detection of muscle-specific creatine kinase expression as physiological indicator for Atlantic salmon (Salmo salar L) skeletal muscle damage. Aquaculture. 2018;496.

Available:https://doi.org/10.1016/j.aquaculture.2018.07.006

Hamer DH. Metallothionein. Annual Review of Biochemistry. 1986;55(1):913–951.

Available:https://doi.org/10.1146/annurev.bi.55.070186.004405

Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS. Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. In Aquatic Toxicology. 2006;76(2):160–202.

Available:https://doi.org/10.1016/j.aquatox.2005.08.015

Bae H, Nam SS, Park HS, Park K. Metallothionein mRNA Sequencing and induction by cadmium in gills of the crucian carp, Carassius auratus. Journal of Health Science. 2005;51(3):284–290.

Available:https://doi.org/10.1248/jhs.51.284

Lange A, Ausseil O, Segner H. Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2002;131(3): 231–243. Available:https://doi.org/10.1016/S1532-0456(02)00010-8

Woo S, Yum S, Jung JH, Shim WJ, Lee CH, Lee TK. Heavy metal-induced differential gene expression of metallothionein in Javanese Medaka, Oryzias javanicus. Marine Biotechnology. 2006;8(6):654–662.

Available:https://doi.org/10.1007/s10126-006-6046-0

Min EY, Ahn TY, Kang JC. Bioaccumulation, alterations of metallothionein, and antioxidant enzymes in the mullet Mugil cephalus exposed to hexavalent chromium. Fisheries and Aquatic Sciences. 2016;19(1):19.

Available:https://doi.org/10.1186/s41240-016-0020-1

Chatterjee S, Datta S, Das TK, Veer V, Mishra D, Chakraborty A, Chattopadhyay B, Datta S, Mukhopadhyay SK, Gupta DK. Metal accumulation and metallothionein induction in Oreochromis niloticus grown in wastewater fed fishponds. Ecological Engineering. 2016;90. Available:https://doi.org/10.1016/j.ecoleng.2016.01.049

Sevcikova M. Modra H, Kruzikova K, Zitka O, Hynek D, Adam V, Celechovska O, Kizek R, Svobodova Z. Effect of metals on metallothionein content in fish from Skalka and Želivka reservoirs. International Journal of Electrochemical Science. 2013; 8(2).

Sinaie M, Bastami KD, Ghorbanpour M, Najafzadeh H, Shekari M, Haghparast S. Metallothionein biosynthesis as a detoxification mechanism in mercury exposure in fish, spotted scat (Scatophagus argus). Fish Physiology and Biochemistry. 2010;36(4): 1235–1242. Available:https://doi.org/10.1007/s10695-010-9403-x

Swaleh SB, Banday UZ, Usmani N. Comparative study of biochemical, histological and molecular biomarkers of heavy metal contamination in Cyprinus carpio collected from warm-monomictic lake and government culture pond. Chemosphere. 2019;236:124182. Available:https://doi.org/10.1016/j.chemosphere.2019.06.152

English TE, Storey KB. Freezing and anoxia stresses induce expression of metallothionein in the foot muscle and hepatopancreas of the marine gastropod Littorina littorea. Journal of Experimental Biology. 2003;206(14):2517–2524.

Available:https://doi.org/10.1242/jeb.00465

Mosleh YY, Paris-Palacios S, Arnoult F, Couderchet M, Biagianti-Risbourg S, Vernet G. Metallothionein induction in aquatic oligochaetetubifex tubifex exposed to herbicide isoproturon. Environmental Toxicology. 2004;19(1):88–93.

Available:https://doi.org/10.1002/tox.10153

Belcastro M, Marino T, Russo N, Toscano M. The role of glutathione in cadmium ion detoxification: Coordination modes and binding properties – A density functional study. Journal of Inorganic Biochemistry. 2009;103(1):50–57.

Available:https://doi.org/10.1016/j.jinorgbio.2008.09.002

Singhal RK, Anderson ME, Meister A. Glutathione, a first line of defense against cadmium toxicity. The FASEB Journal. 1987;1(3):220–223. Available:https://doi.org/10.1096/fasebj.1.3.2887478

Thomas P, Wofford HW, Neff JM. Effect of cadmium on glutathione content of mullet (Mugil cephalus) tissues. In Physiological Mechanisms of Marine Pollutant Toxicity. 1982;109–125). Elsevier.

Available:https://doi.org/10.1016/B978-0-12-718460-9.50009-2

Stephensen E, Sturve J, Förlin L. Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2002; 133(3):435–442. Available:https://doi.org/10.1016/S1532-0456(02)00129-1

Kuroshima R. Hepatic metallothionein and glutathione levels in Red Sea bream. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology. 1995;110(1):95–100.

Available:https://doi.org/10.1016/0742-8413(94)00066-J

Thomas P, Wayne Wofford H. Effects of cadmium and Aroclor 1254 on lipid peroxidation, glutathione peroxidase activity, and selected antioxidants in Atlantic croaker tissues. Aquatic Toxicology. 1993;27(1–2):159–177.

Available:https://doi.org/10.1016/0166-445X(93)90052-3

Gurer-Orhan H, Sabır HU, Özgüneş H. Correlation between clinical indicators of lead poisoning and oxidative stress parameters in controls and lead-exposed workers. Toxicology. 2004;195(2–3):147–154.

Available:https://doi.org/10.1016/j.tox.2003.09.009

Kretzschmar M. Regulation of hepatic glutathione metabolism and its role in hepatotoxicity. Experimental and Toxicologic Pathology. 1996;48(5):439–446. Available:https://doi.org/10.1016/S0940-2993(96)80054-6

Fent K. Ecotoxicological problems associated with contaminated sites. Toxicology Letters. 2003;140–141: 353–365. Available:https://doi.org/10.1016/S0378-4274(03)00032-8

Moore MJ, Mitrofanov IV, Valentini SS, Volkov VV, Kurbskiy AV, Zhimbey EN, Eglinton LB, Stegeman JJ. Cytochrome P4501A expression, chemical contaminants and histopathology in roach, goby and sturgeon and chemical contaminants in sediments from the Caspian Sea, Lake Balkhash and the Ily River Delta, Kazakhstan. Marine Pollution Bulletin. 2003;46(1):107–119. Available:https://doi.org/10.1016/S0025-326X(02)00325-9

Williams DE, Lech JJ, Buhler DR. Xenobiotics and xenoestrogens in fish: modulation of cytochrome P450 and carcinogenesis. Mutation Research/ Fundamental and Molecular Mechanisms of Mutagenesis. 1998;399(2): 179–192. Available:https://doi.org/10.1016/S0027-5107(97)00255-8

Orrego R, Jiménez B, Bordajandi LR, Gavilán JF, Inzunza B, Abad E, González MJ, Rivera J, Barra R. EROD induction and PCDD/F levels in fish liver from the Biobio River in Chile. Chemosphere. 2005;60(7):829–835.

Available:https://doi.org/10.1016/j.chemosphere.2005.02.008

Parente TEM, De-Oliveira ACAX, Paumgartten FJR. Induced cytochrome P450 1A activity in cichlid fishes from Guandu River and Jacarepaguá Lake, Rio de Janeiro, Brazil. Environmental Pollution. 2008;152(1):233–238.

Available:https://doi.org/10.1016/j.envpol.2007.04.025

Schlezinger JJ, Stegeman JJ. Induction and suppression of cytochrome P450 1A by 3,3′,4,4′,5-pentachlorobiphenyl and its relationship to oxidative stress in the marine fish scup (Stenotomus chrysops). Aquatic Toxicology. 2001;52(2):101–115. Available:https://doi.org/10.1016/S0166-445X(00)00141-7

Faverney CR, Lafaurie M, Girard JP, Rahmani R. Effects of heavy metals and 3-methylcholanthrene on expression and induction of CYP1A1 and metallothionein levels in trout (Oncorhynchus mykiss) hepatocyte cultures. Environmental Toxicology and Chemistry. 2000;19(9): 2239–2248. Available:https://doi.org/10.1002/etc.5620190914

Huang GY, Ying GG, Liang YQ, Liu SS, Liu YS. Expression patterns of metallothionein, cytochrome P450 1A and vitellogenin genes in western mosquitofish (Gambusia affinis) in response to heavy metals. Ecotoxicology and Environmental Safety. 2014;105(1):97–102. Available:https://doi.org/10.1016/j.ecoenv.2014.04.012

Espín S, Martínez-López E, Jiménez P, María-Mojica P, García-Fernández AJ. Delta-aminolevulinic acid dehydratase (δALAD) activity in four free-living bird species exposed to different levels of lead under natural conditions. Environmental Research. 2015;137:185–198.

Available:https://doi.org/10.1016/j.envres.2014.12.017

Moore M. A commentary on the impacts of metals and metalloids in the environment upon the metabolism of drugs and chemicals. Toxicology Letters. 2004; 148(3):153–158. Available:https://doi.org/10.1016/j.toxlet.2003.10.027

Anwar-Mohamed A, El-Sherbeni A, Kim SH, Elshenawy OH, Althurwi HN, Zordoky BNM, El-Kadi AOS. Acute arsenic treatment alters cytochrome P450 expression and arachidonic acid metabolism in lung, liver and kidney of C57Bl/6 mice. Xenobiotica. 2013; 43(8):719–729. Available:https://doi.org/10.3109/00498254.2012.754113

Zhao H, Wang Y, Guo M, Fei D, Mu M, Yu H, Xing M. Hepatoprotective effects of zinc (II) via cytochrome P-450/reactive oxygen species and canonical apoptosis pathways after arsenite waterborne exposure in common carp. Chemosphere. 2019; 236:124869. Available:https://doi.org/10.1016/j.chemosphere.2019.124869

Brüschweiler BJ, Würgler FE, Fent K. Inhibitory effects of heavy metals on cytochrome P4501A induction in permanent fish hepatoma cells. Archives of Environmental Contamination and Toxicology. 1996;31(4):475–482. Available:https://doi.org/10.1007/BF00212430

Maier A, Dalton TP, Puga A. Disruption of dioxin-inducible phase I and phase II gene expression patterns by cadmium, chromium, and arsenic. Molecular Carcinogenesis. 2000;28(4):225–235.

Available:https://doi.org/10.1002/1098-2744(200008)28:4<225: AID-MC5>3.0.CO;2-O

Lemaire-Gony S, Lemaire P, Pulsford AL. Effects of cadmium and benzo(a)pyrene on the immune system, gill ATPase and EROD activity of European sea bass Dicentrarchus labrax. Aquatic Toxicology. 1995;31(4):297–313.

Available:https://doi.org/10.1016/0166-445X(94)00073-Y

Gupta RS, Singh B. Phylogenetic analysis of 70 kD heat shock protein sequences suggest a chimeric origin for the eukaryotic cell nucleus. Current Biology. 1994; 4(12):1104–1114.

Available:https://doi.org/10.1016/S0960-9822(00)00249-9

Eder KJ, Leutenegger CM, Köhler HR, Werner I. Effects of neurotoxic insecticides on heat-shock proteins and cytokine transcription in Chinook salmon (Oncorhynchus tshawytscha). Ecotoxicology and Environmental Safety. 2009;72(1):182–190. Available:https://doi.org/10.1016/j.ecoenv.2008.04.020

Farcy E, Voiseux C, Lebel JM, Fievet B. Seasonal changes in mRNA encoding for cell stress markers in the oyster Crassostrea gigas exposed to radioactive discharges in their natural environment. Science of The Total Environment. 2007;374(2–3):328–341. Available:https://doi.org/10.1016/j.scitotenv.2006.11.014

Jiang X, Guan X, Yao L, Zhang H, Jin X, Han Y. Effects of single and joint subacute exposure of copper and cadmium on heat shock proteins in common carp (Cyprinus carpio). Biological Trace Element Research. 2016;169(2):374–381. Available:https://doi.org/10.1007/s12011-015-0402-8

Madách K, Molvarec A, Rigó J, Nagy B, Pénzes I, Karádi I, Prohászka Z. Elevated serum 70kDa heat shock protein level reflects tissue damage and disease severity in the syndrome of hemolysis, elevated liver enzymes, and low platelet count. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2008;139(2):133–138.

Available:https://doi.org/10.1016/j.ejogrb.2007.12.012

Rajeshkumar S, Mini J, Munuswamy N. Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. In Ecotoxicology and Environmental Safety. 2013;98. Available:https://doi.org/10.1016/j.ecoenv.2013.07.029

Rhee JS, Kim RO, Choi HG, Lee J, Lee YM, Lee JS. Molecular and biochemical modulation of heat shock protein 20 (Hsp20) gene by temperature stress and hydrogen peroxide (H2O2) in the monogonont rotifer, Brachionus sp. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2011;154(1):19–27.

Available:https://doi.org/10.1016/j.cbpc.2011.02.009

Xing H, Li S, Wang X, Gao X, Xu S, Wang X. Effects of atrazine and chlorpyrifos on the mRNA levels of HSP70 and HSC70 in the liver, brain, kidney and gill of common carp (Cyprinus carpio L.). Chemosphere. 2013;90(3):910–916.

Available:https://doi.org/10.1016/j.chemosphere.2012.06.028

Qian Z, Liu X, Wang L, Wang X, Li Y, Xiang J, Wang P. Gene expression profiles of four heat shock proteins in response to different acute stresses in shrimp, Litopenaeus vannamei. Comparative Biochemistry and Physiology, Part C. 2012;156(3- 4):211-220.

Feng Q, Boone AN, Vijayan MM. Copper impact on heat shock protein 70 expression and apoptosis in rainbow trout hepatocytes. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2003;135(3):345-355.

Ng GHB, Xu H, Pi N, Kelly BC, Gong Z. Differential GFP expression patterns induced by different heavy metals in Tg(hsp70:gfp) transgenic medaka (Oryzias latipes). Marine Biotechnology. 2015; 17(3):317–327.

Available:https://doi.org/10.1007/s10126-015-9620-5

Jing J, Liu H, Chen H, Hu S, Xiao K, Ma X. Acute effect of copper and cadmium exposure on the expression of heat shock protein 70 in the Cyprinidae fish Tanichthys albonubes. Chemosphere. 2013;91(8):1113–1122.

Available:https://doi.org/10.1016/j.chemosphere.2013.01.014

Sørensen JG, Loeschcke V. Studying stress responses in the post-genomic era: Its ecological and evolutionary role. Journal of Biosciences. 2007;32(3): 447–456.

Available:https://doi.org/10.1007/s12038-007-0044-x

Lewis FA, Patterson CN, Knight M, Richards CS. The relationship between Schistosoma mansoni and Biomphalaria glabrata: Genetic and molecular approaches. Parasitology. 2001;123(7):169–179. Available:https://doi.org/10.1017/S0031182001007831

Sanchez W, Palluel O, Meunier L, Coquery M, Porcher JM, Aït-Aïssa S. Copper-induced oxidative stress in three-spined stickleback: Relationship with hepatic metal levels. Environmental Toxicology and Pharmacology. 2005;19(1):177–183. Available:https://doi.org/10.1016/j.etap.2004.07.003

Arojojoye OA, Oyagbemi AA, Afolabi JM. Toxicological assessment of heavy metal bioaccumulation and oxidative stress biomarkers in Clarias gariepinus from Igbokoda River of South Western Nigeria. Bulletin of Environmental Contamination and Toxicology. 2018; 100(6):765–771. Available:https://doi.org/10.1007/s00128-018-2341-5

Farombi EO, Adelowo OA, Ajimoko YR. Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. International Journal of Environmental Research and Public Health. 2007; 4(2):158–165. Available:https://doi.org/10.3390/ijerph2007040011

Cao L, Huang W, Shan X, Ye Z, Dou S. Tissue-specific accumulation of cadmium and its effects on antioxidative responses in Japanese flounder juveniles. Environmental Toxicology and Pharmacology. 2012;33(1):16–25.

Available:https://doi.org/10.1016/j.etap.2011.10.003

Liu XJ, Luo Z, Li CH, Xiong BX, Zhao YH, Li XD. Antioxidant responses, hepatic intermediary metabolism, histology and ultrastructure in Synechogobius hasta exposed to waterborne cadmium. Ecotoxicology and Environmental Safety. 2011;74(5):1156–1163. Available:https://doi.org/10.1016/j.ecoenv.2011.02.015

Ransberry VE, Morash AJ, Blewett TA, Wood CM, McClelland GB. Oxidative stress and metabolic responses to copper in freshwater- and seawater-acclimated killifish, Fundulus heteroclitus. Aquatic Toxicology. 2015;161.

Available:https://doi.org/10.1016/j.aquatox.2015.02.013

Souza IC, Duarte ID, Pimentel NQ, Rocha LD, Morozesk M, Bonomo MM, Azevedo VC, Pereira CDS, Monferrán MV, Milanez CRD, Matsumoto ST, Wunderlin DA, Fernandes MN. Matching metal pollution with bioavailability, bioaccumulation and biomarkers response in fish (Centropomus parallelus) resident in neotropical estuaries. Environmental Pollution. 2013; 180:136–144. Available:https://doi.org/10.1016/j.envpol.2013.05.017

Radi AAR, Matkovics B. Effects of metal ions on the antioxidant enzyme activities, protein contents and lipid peroxidation of carp tissues. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology. 1988;90(1):69–72. Available:https://doi.org/10.1016/0742-8413(88)90099-0

Olsson PE, Kling P, Hogstrand C. Mechanisms of heavy metal accumulation and toxicity in fish. In Metal Metabolism in Aquatic Environments. Springer US. 1998;321–350. Available:https://doi.org/10.1007/978-1-4757-2761-6_10

Nuran Ercal BSP, Hande Gurer-Orhan BSP, Nukhet Aykin-Burns BSP. Toxic metals and oxidative stress part I: Mechanisms involved in me-tal induced oxidative damage. Current Topics in Medicinal Chemistry. 2001;1(6): 529–539. Available:https://doi.org/10.2174/1568026013394831

Neeratanaphan L, Kamollerd C, Suwannathada P, Suwannathada P, Tengjaroenkul B. Genotoxicity and oxidative stress in experimental hybrid catfish exposed to heavy metals in a municipal landfill reservoir. International Journal of Environmental Research and Public Health. 2020;17(6):1980. Available:https://doi.org/10.3390/ijerph17061980