Impact of Metal Toxicity on Oxidative Balance and Mitochondrial Enzyme Function in Muscle of Tilapia

  • Debjit Das
  • Mahammed Moniruzzaman
  • Soumalya Mukhopadhyay
  • Samya Karan
  • Adity Sarbajna
  • Suman Bhusan Chakraborty
Article

Abstract

Present study investigates the effect of metal accumulation on antioxidant level and mitochondrial enzymes function in muscle of Oreochromis mossambicus. Metal accumulation in muscle upregulated stress marker malondialdehyde and the activity of different antioxidant enzymes with no significant alteration in glutathione system. Metal exposure to fish muscle decreased the activity of mitochondrial enzymes. AMP deaminase, aldolase, cytochrome C oxidase and lipoamide reductase showed positive correlation with acetylcholinesterase, glutathione reductase, reduced glutathione and glutathione peroxidase, but negative correlation with superoxide dismutase, catalase, glutathione S-transferase and thiobarbituric acid reactive substance. Analysis of these biomarkers clearly indicates the change in oxidative load in muscle tissues and provides insight to muscle response to the metal exposure. Therefore, the study outlines the potential use of biomarkers in context of muscle mitochondrial enzymes relating to oxidative processes that take place in the fish muscle following metal exposure and toxicity.

Keywords

Oreochromis mossambicus Metals Antioxidants Muscle Mitochondrial enzymes 

Notes

Acknowledgements

Financial assistance from the Department of Environment (Sanction No. 1884/EN/P/T-VIII-2/029/2013), Government of West Bengal, West Bengal, India, is thankfully acknowledged. MM thankfully acknowledging DBT Research Associateship Programme, Govt. of India, IISC, Bangalore, for financial support.

References

  1. Akinyemi AJ, Okonkwo PK, Faboya OA, Onikanni SA, Fadaka A, Olayide I, Akinyemi EO, Oboh G (2017) Curcumin improves episodic memory in cadmium induced memory impairment through inhibition of acetylcholinesterase and adenosine deaminase activities in a rat model. Metab Brain Dis 32:87–95CrossRefGoogle Scholar
  2. Ambedkar G, Muniyan M (2011) Bioaccumulation of some heavy metals in the selected five freshwater fish from Kollidam River, Tamilnadu, India. Adv Appl Sci Res 2:221–225Google Scholar
  3. Anand SS (2005) Protective effect of vitamin B6 in chromium-induced oxidative stress in liver. J Appl Toxicol 25:440–443CrossRefGoogle Scholar
  4. APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. APHA, Washington, DCGoogle Scholar
  5. Athikesavan S, Vincent S, Ambrose T, Velmurugan B (2006) Nickel induced histopathological changes in the different tissues of freshwater fish, Hypophthalmichthys molitrix (Valenciennes). J EnvBiol 37:391–395Google Scholar
  6. Authman MM, Zaki MS, Khallaf EA, Abbas HH (2015) Use of fish as bio-indicator of the effects of heavy metals pollution. J Aquac Res Dev 6:328CrossRefGoogle Scholar
  7. Barbagli C, Crescenzi GS (1981) Influence of freezing and thawing on the release of cytochrome oxidase from chicken’s liver and from beef and trout muscle. J Food Sci 46:491–493CrossRefGoogle Scholar
  8. Brewer SK, Little EE, DeLonay AJ, Beauvais SL, Jones SB, Ellersieck MR (2001) Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch Environ Contam Toxicol 40:70–76CrossRefGoogle Scholar
  9. Carvalho C, Fernandes MN (2008) Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilodus lineatus. Comp Biochem Physiol A 151:437–442CrossRefGoogle Scholar
  10. Das D, Moniruzzaman M, Sarbajna A, Chakraborty SB (2017) Effect of heavy metals on tissue-specific antioxidant response in Indian major carps. Environ Sci Pollut Res 24:18010–18024CrossRefGoogle Scholar
  11. Dube PN, Alavandi S, Hosetti BB (2013) Effect of exposure to sublethal concentrations of sodium cyanide on the carbohydrate metabolism of the Indian Major Carp Labeo rohita (Hamilton, 1822). Pesq Vet Bras 33:914–919CrossRefGoogle Scholar
  12. El Khalil H, El Hamiani O, Bitton G, Ouazzani N, Boularbah A (2008) Heavy metal contamination from mining sites in South Morocco: monitoring metal content and toxicity of soil runoff and groundwater. Environ Monit Assess 136:147–160CrossRefGoogle Scholar
  13. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–90CrossRefGoogle Scholar
  14. El-Moselhy KM, Othman AI, El-Azem HA,.El-Metwally MEA (2014) Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. EJBAS 1:97–105Google Scholar
  15. Fernandes DRT (2007) Chemical and biochemical tools to assess pollution exposure in aquatic ecosystems. Dissertation, University of AlgarveGoogle Scholar
  16. Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400Google Scholar
  17. Greco L, Serrano R, Blanes MA, Serrano E, Capri E (2010) Bioaccumulation markers and biochemical responses in European sea bass (Dicentrarchus labrax) raised under different environmental conditions. Ecotoxicol Environ Saf 73:38–45CrossRefGoogle Scholar
  18. Imar MR, Carlos JRS (2011) Metal levels in fish captured in puertorico and estimation of risk from fish consumption. Arch Environ Contam Toxicol 60:132–144CrossRefGoogle Scholar
  19. King J (1959) A routine method for the estimation of lactic dehydrogenase activity. J Med Lab Technol 16:265Google Scholar
  20. Kun E, Abood LG (1949) Colorimetric estimation of succinic dehydrogenase by triphenyltetrazolium chloride. Science 109:144–146CrossRefGoogle Scholar
  21. Lionetto MG, Caricato R, Calisi A, Giordano ME, Schettino T (2013) Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. Biomed Res Int 2013:321213CrossRefGoogle Scholar
  22. Liu XD, Thiele DJ (1997) Yeast metallothionein gene expression in response to metals and oxidative stress. Methods 11:289–299CrossRefGoogle Scholar
  23. Macomber L, Elsey SP, Hausinger RP (2011) Fructose-1,6-bisphosphate aldolase (class II) is the primary site of nickel toxicity in Escherichia coli. Mol Microbial 82:1291–1300CrossRefGoogle Scholar
  24. Moniruzzaman M, Hasan KN, Maitra SK (2016) Melatonin actions on ovaprim (synthetic GnRH and domperidone)-induced oocyte maturation in carp. Reproduction 151(4):285–296CrossRefGoogle Scholar
  25. Perumalsamy N, Arumugam K (2013) Enzymes activity in fish exposed to heavy metals and the electro-plating effluent at sub-lethal concentrations. Water Qual Expo Health 5:93–101CrossRefGoogle Scholar
  26. Rajeshkumar V, Lee TH, Chuang SC (2013) Palladium-catalyzed oxidative insertion of carbon monoxide to n-sulfonyl-2-aminobiaryls through c–h bond activation: access to bioactive phenanthridinone derivatives in one pot. Org Let 15:1468–1471CrossRefGoogle Scholar
  27. Richards OC, Rutter WJ (1961) Preparation and properties of yeast aldolase. J BiolChem 236:3177–3184Google Scholar
  28. Rodríguez-Fuentes G, Sandoval-Gío JJ, Arroyo-Silva A, Noreña-Barroso E, Escalante-Herrera KS, Olvera-Espinosa F (2015) Evaluation of the estrogenic and oxidative stress effects of the UV filter 3-benzophenone in zebrafish (Danio rerio) eleuthero-embryos. Ecotoxicol Environ Saf 115:14–18CrossRefGoogle Scholar
  29. Sanches Filho PJ, Caldas JS, da Rosa NN, Pereira FOP (2017) Toxicity test and Cd, Cr, Pb and Zn bioccumulation in Phalloceros caudimaculatus. EJBAS 4(3):206–211Google Scholar
  30. SAS (1996) Institute Inc. SAS/IML Software: Usage and Reference, Version, 6Google Scholar
  31. Scheffe H (1999) The analysis of variance, vol 72. Wiley, New YorkGoogle Scholar
  32. Smiley KL, Suelter CH (1967) Univalent cations as allosteric activators of muscle adenosine 5′-phosphate deaminase. J Biol Chem 242:1980–1981Google Scholar
  33. Sullivan KM, Somero GN (1983) Size-and diet-related variations in enzymic activity and tissue composition in the sablefish, Anoplopoma fimbria. Biol Bull 164(2):315–326CrossRefGoogle Scholar
  34. Swain PS, Rao SB, Rajendran D, Dominic G, Selvaraju S (2016) Nano zinc, an alternative to conventional zinc as animal feed supplement: a review. Anim Nutr 2:134–141CrossRefGoogle Scholar
  35. Szarkowska L, Klingenberg M (1963) On the role of ubiquinone in mitochondria. Spectrophotometric chemical measurements of its redox reactions. Biochem Z 338:674–697Google Scholar
  36. Tao S, Liang T, Cao J, Dawson RW, Liu C (1999) Synergistic effect of Cu and Pb uptake by Fish. Ecotoxicol Environ Saf 44:190–195CrossRefGoogle Scholar
  37. Tavazzi B, Di Pierro D, Amorini AM, Fazzina G, Galvano M, Lupi A, Giardina B, Lazzarino G (2000) Direct NAD (P) H hydrolysis into ADP-ribose (P) and nicotinamide induced by reactive oxygen species: a new mechanism of oxygen radical toxicity. Free radic Res 33:1–2CrossRefGoogle Scholar
  38. Thijssen HH, Janssen YP, Vervoort LT (1994) Microsomal lipoamide reductase provides vitamin K epoxide reductase with reducing equivalents. Biochem J 297:277–280CrossRefGoogle Scholar
  39. Villescas R, Ostwald R, Morimoto H, Bennett EL (1981) Effects of neonatal undernutrition and cold stress on behavior and biochemical brain parameters in rats. J Nutr 111:1103–1110CrossRefGoogle Scholar
  40. Wang R, Wang WX (2012) Contrasting mercury accumulation patterns in tilapia (Oreochromis niloticus) and implications on somatic growth dilution. Aquat Toxicol 114/115:23–30CrossRefGoogle Scholar
  41. Yücebilgiç G, Bilgin R, Tamer L, Tükel S (2003) Effects of lead on Na+-K+ ATPase and Ca+ 2 ATPase activities and lipid peroxidation in blood of workers. Int J Toxicol 22:95–97CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of CalcuttaKolkataIndia
  2. 2.Department of StatisticsVisva-Bharati UniversitySantiniketanIndia
  3. 3.Department of ZoologySurendranath CollegeKolkataIndia

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