Skip to main content
Log in

Distinctive fingerprints of genotoxicity induced by As, Cr, Cd, and Ni in a freshwater fish

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Genotoxicity of three toxic elements (chromium, cadmium, nickel) and a metalloid (arsenic) has been studied in a freshwater fish, Channa punctatus using micronuclei (MN) test, comet assay, and erythrocyte nuclear alterations (ENAs) as fingerprints of genotoxicity. These tests yielded different results suggesting involvement of different mechanisms for their genotoxicity. While highest frequency of blebbed nuclei was observed in chromium-treated fish (6.5 ± 0.76), lowest was observed in cadmium-treated fish (4.0 ± 1.0). Maximum number of notched nuclei was recorded in arsenic-treated fish (5.5 ± 1.15) whereas highest numbers of lobed nuclei were found in cadmium-treated fish (4.5 ± 0.13). These differences might be attributed to selective bioaccumulation and chemodynamics of each element. Other parameters used to determine genotoxicity viz.: lipid peroxidation and DNA damage also suggested different mechanisms of their genotoxicity. It is suggested that an integrative approach, using a battery of tests for determining genotoxicity, should be made while making environmental health risk assessment and ecotoxicological studies of these toxic elements.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahmad L, 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 b-naphthoflavone. Mutat Res 608:16–28

    Article  CAS  Google Scholar 

  • Ali D, Nagpure NS, Kumar S, Kumar R, Kushwaha B (2008) Genotoxicity assessment of acute exposure of chlorpyrifos to freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Chemosphere 71:1823–1831

    Article  CAS  Google Scholar 

  • Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343:121–135

    Article  CAS  Google Scholar 

  • Aramphongohan A, Laovitthayanggoon S, Himakoun L (2009) Snakehead-fish cell line, SSN-1 (Ophicephalus striatus) as a model for cadmium genotoxicity testing. Toxicol in Vitro 23:963–968

    Article  CAS  Google Scholar 

  • Arunachalam KD, Annamalai SK, Kuruva JK (2013) In-vivo evaluation of hexavalent chromium induced DNA damage by alkaline comet assay and oxidative stress in Catla catla. Am J Environ Sci 9:470–482

    Article  CAS  Google Scholar 

  • Berces J, Otos M, Szirmai S, Crane-Uruena C, Koteles GJ (1993) Using the micronucleus assay to detect genotoxic effects of metal ions. Environ. Hlth. Perespec. Suppl 101:11–13

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brendler-Schwaab S, Hartman A, Pfuhler S, Speit G (2005) The in vivo comet assay: use and status in genotoxicity testing. Mutagenesis 20:245–254

    Article  CAS  Google Scholar 

  • Carrasco KR, Tilbury KL, Meyers MS (1990) Assessment of the piscine micronucleus test as in situ biological indicator of chemical contaminant effects. CanJ Fish Aquat. Sci 47:2123–2136

    Article  CAS  Google Scholar 

  • Cavas T, Garanko NN, Arkhipchuk VV (2005) Induction of micronuclei and binuclei in blood, gill and liver cells of fishes sub chronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol 43:569–574

    Article  CAS  Google Scholar 

  • Cavas T, Konen S (2008) In vivo genotoxicity testing of the amnesic shellfish poison (domoic acid) in piscine erythrocytes using the micronucleus test and the comet assay. Aquat Toxicol 90:154–159

    Article  CAS  Google Scholar 

  • Das S, Unni B, Bhattacharjee M, Wann SB, Rao PG (2012) Toxicological effects of arsenic exposure in a freshwater teleost fish, Channa punctatus. African J Biotech 11:4447–4454

    CAS  Google Scholar 

  • De Flora S, Vigano L, D’Agostini F, Camoirano A, M B, Bennicelli C, Melodia F, A A (1993) Multiple genotoxicity biomarkers in fish exposed in situ to polluted river water. Mutat Res 319:167–177

    Article  Google Scholar 

  • Fatima M, Usmani N, Firdaus F, Zafeer MF, Ahmad S, Akhtar K, Dawar Husain SM, Ahmad MH, Anis E, Mobarak Hossain M (2015) In vivo induction of antioxidant response and oxidative stress associated with genotoxicity and histopathological alteration in two commercial fish species due to heavy metals exposure in northern India (Kali) river. Comp. Biochem Physiol (C) 176-177:17–30

    CAS  Google Scholar 

  • Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455:81–95

    Article  CAS  Google Scholar 

  • Finney DJ (1985) Probit analysis. Cambridge University Press, Cambridge

    Google Scholar 

  • Fontanetti CS, Christofoletti CA, Pinheiro TG, Souza TS, Pedro-Escher J (2010) Microscopy as a tool in toxicological evaluations. Uni Esta Paul:1001–1007

  • Gasulla J, Picco SJ, Carriquiriborde P, Dulout FN, Ronoco AE, de Luca JC (2016) Genotoxicity effects induced by Cd (+2), Cr (+6), Cu (+2) in the gill and liver of Odontesthes bonariensis (Piscies, Atherinopsidae). Bull Environ Cont Toxicol 96:591–595

    Article  CAS  Google Scholar 

  • Gomes JMM, Ribeiro HJ, Procopio MS, Alvarenga BM, Castro ACS, Dutra WO, da Silva JBB, Correa Junior JD (2015) What the erythrocytic nuclear alteration frequencies could tell us about genotoxicity and macrophage iron storage? PlosOne. https://doi.org/10.1371/joumal.pone.0143029

  • Grant KR (2015) Fish hematology and associated disorders. Clin Lab Med 35:681–701

    Article  Google Scholar 

  • Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG (2009) Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol 32:138–143

    Article  CAS  Google Scholar 

  • Guilherme S, Gaivao I, Santos MA, Pacheco M (2010) European eel (Anguilla anguilla) genotoxic and pro-oxidant responses following a short-term exposure to a glyphosate-based herbicide. Mutagenesis 25:523–530

    Article  CAS  Google Scholar 

  • Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, Tucker JD (1991) Micronuclei as an indox of cytogenetic damage: past, present and future. Environ Mol Mutagen 18:277–291

    Article  CAS  Google Scholar 

  • Heddle JA, Hite M, Kirkhart B, Mavoumin K, Mac Gregor JT, Newell GT, Salamone MF (1983) The induction of micronuclei as a measure of genotoxicity. A report of the U.S. environmental protection agency gene-tox program. Mutat Res 123:61–118

    Article  CAS  Google Scholar 

  • Hovhannisyan GG (2010) Fluorescence in situ hybridization in combination with the comet assay and micronucleus test in genetic toxicology. Mol Cytogenet 3:17–28

    Article  CAS  Google Scholar 

  • Huang X, Frenkel K, Klein CB, Costa M (1993) Nickel induces increased oxidants in intact cultured mammalian cells as detected by dichlorofluorescein fluorescence. ToxicolApplPharmacol 120:29–36

    CAS  Google Scholar 

  • Huang XI, Klein CB, Costa M (1994) Crystalline Ni3S2 specifically enhances the formation of oxidants in the nuclei of CHO cells as detected by dichlorofluorescein. Carcinogenesis 15:545–548

    Article  CAS  Google Scholar 

  • Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdisci Toxicol 7:60–72

    Article  CAS  Google Scholar 

  • Jindal R, Verma S (2015) In vivo genotoxicity and cytotoxicity assessment of cadmium chloride in peripheral erythrocytes of Labeo rohita (Hamilton). Ecotoxicol Environ Saf 118:1–10

    Article  CAS  Google Scholar 

  • Joshi S, Husain MM, Chandra R, Hasan SK, Srivastava RC (2005) Hydroxyl radical formation resulting from the interaction of nickel complexes of L. histidine, glutathione or L. cysteine and hydrogen peroxide. Hum Exp Toxicol 24:13–17

    Article  CAS  Google Scholar 

  • Kumar A, Kesari VP, Khan PK (2013) Fish micronucleus assay to assess genotoxic potential of arsenic at its guideline exposure in aquatic environment. Biometals 26(2):337

    Article  CAS  Google Scholar 

  • Lushchak OV, Kubrak OI, Torous IM, Nazarchuk TY, Storey KB, Lushchak VI (2009) Trivalent chromium induces oxidative stress in gold fish brain. Chemo 75:56–62

    Article  CAS  Google Scholar 

  • Lushchuk OV, Kubrak OI, Lozinsky OV, Storey JM, Storey KB, Lushchuk VI (2009) Chromium (III) induces oxidative stress in goldfish liver and kidney. Aquat Toxicol 93:45–52

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mai W, Yan J, Wang L, Zheng Y, Xin Y, Wang W (2010) Acute acidic exposure induces p53-mediated oxidative stress and DNA damage in tilapia (Oreochromis niloticus) blood cells. Aquat Toxicol 100:271–281

    Article  CAS  Google Scholar 

  • Mishra AK, Mohanty B (2009) Chronic exposure to sublethal hexavalent chromium affects organ histopathology and serum cortisol profile of a teleost, Channapunctatus (Bloch). Sci Total Environ 407:5031–5038

    Article  CAS  Google Scholar 

  • Nordberg GF, Nogawa K, Nordberg M, Friedmann JM (2007) Cadmium. In: Nordberg GF, Fowler BA, Norberg M, Friberg L (eds) Handbook on the toxicology of metals. Elsevier, Amsterdam, pp 445–486

    Chapter  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • Oliveira-Filho EC, Muniz DH, Ferreira MF, Grisolia CK (2010) Evaluation of acute toxicity, cytotoxicity and genotoxicity of a nickel mining waste to Oreochromis niloticus. Bull Environ ContToxicol 85:467–471

    Article  CAS  Google Scholar 

  • Ozkan F, Gunduz SG, Berkoz M, Hunt AO (2011) Induction of micronuclei and other nuclear abnormalities in peripheral erythrocytes of Nile tilapia, Oreochromis niloticus, following exposure to sublethal cadmium doses. Turkish J Zool 35:585–592

    Google Scholar 

  • Pantaleao SM, Alcantara AV, Alves JPH, Spano MA (2006) The piscine micronucleus test to assess the impact of pollution on the Japaratuba river in Brazil. Environ Mol Mut 47:219–224

    Article  CAS  Google Scholar 

  • Pavlaki MD, Araujo MJ, Cardoso DN, Silva ARR, Cruz A, Mendo S, Soares AMVM, Calado R, Loureiro S (2016) Ecotoxicity and genotoxicity of cadmium in different marine trophic levels. Environ Pollut 215:203–212

    Article  CAS  Google Scholar 

  • Privezentsev KV, Sirota NP, Gaznev AL (1996) Effects of combined action of Cd and gamma radiation on DNA damage and repair in lymphoid tissues of mice. Radiats Biol Radioecol 36:234–240

    CAS  Google Scholar 

  • Ribeiro HJ, Procopio MS, Gomes JMM, Vieira FD, Russo RC, Balzuweit K (2011) Functional dissimilarity of melanomacrophage centres in the liver and spleen from females of the teleost fish Prochilodus argenteus. Cell Tissue Res 346:417–425

    Article  CAS  Google Scholar 

  • Roling JA, Brain LJ, Gardea-Torresdey J, Bader J, Baldwin WS (2006) Hexavalent chromium reduces larval growth and alters gene expression in mummichog (Fundulus heteroclitus). Environ Toxicol Chem 25:2725–2733

    Article  CAS  Google Scholar 

  • Russo C, Rocco L, Morescalchi M, StinsoV (2004) Assessment of environmental stress by the micronucleus test and the comet assay on the genome of teleosts populations from two natural environments. Ecotox Environ Saf 57: 168-174

  • Saotome K, Hayashi M (2003) Application of sea urchin micronucleus assay to monitoring aquatic pollution: influence of sample osmolality. Mutagen 18:73–76

    Article  CAS  Google Scholar 

  • Satizabal LD, Magor BG (2015) Isolation and cytochemical characterization of melanomacrophages and melanomacrophage clusters from goldfish (Carassius auratus L.). Develop Comp Immunol 48:221–228

    Article  CAS  Google Scholar 

  • Scalon MC, Rechenmacher C, Siebel AM, Kayser ML, Rodrigues MT, Maluf SW, Rodrigues MA, Silva LB (2010) Evaluation of Sinos river water genotoxicity using the comet assay in fish. Braz J Biol 70:1217–1222

    Article  CAS  Google Scholar 

  • Schmid W (1995) The micronucleus test. MutatRes 31:9–15

    Google Scholar 

  • Singh NP, McCay MT, Tice RR, Schneider EL (1988) A simple technique for quantification of low levels of DNA damage in individual cell. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  • Siraj M, Khisroon M, Khan A, Zaidi F, Ullah A, Rahman G (2018) Biomonitoring of tissue accumulation and genotoxic effect of heavy metals in Cyprinus carpio from river Kabul Khyber Pakhtunkhwa Pakistan. Bull Environ Contam Toxicol 100:344–349

    Article  CAS  Google Scholar 

  • Tang S, Cai Q, Chibli H, Allagadda V, Nadeau JL, Mayer GD (2013) Cadmium sulfate and CdTe- quantum dots alter DNA repair in Zebra fish (Daniorerio) liver cells. Toxicol Appl Pharm 272:443–452

    Article  CAS  Google Scholar 

  • Taju G, Abdul MS, Nambi KSN, Sahul Hameed AS (2017) Application of fish cell lines for evaluating the chromium induced cytotoxicity, genotoxicity and oxidative stress. Chemosphere 184(1-12)

  • Utani K, Kohno Y, Okamoto A, Shimizu N (2010) Emergence of micronuclei and effects on the fate of cells under replication stress. PLoS ONE 5:1–12

    Article  CAS  Google Scholar 

  • Vazzana M, Celi M, Tramati C, Ferrantelli V, Arizza V, Parrinello N (2014) In vitro effect of cadmium and copper on separated blood leukocytes of Dicentrarchus labrax. Ecotox Environ Saf 102:113–120

    Article  CAS  Google Scholar 

Download references

Funding

One of the authors (MS) is thankful to University Grant Commission, New Delhi, for financial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suresh Vir Singh Rana.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, M., Khan, H., Verma, Y. et al. Distinctive fingerprints of genotoxicity induced by As, Cr, Cd, and Ni in a freshwater fish. Environ Sci Pollut Res 26, 19445–19452 (2019). https://doi.org/10.1007/s11356-019-05274-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05274-z

Keywords

Navigation