Skip to main content
SpringerLink
Log in

Enzymatic, Non-enzymatatic Antioxidant Levels and Heat Shock Protein Expression as Indicators of Metal Induced Toxicity and Reproductive Modulation in Female Indian Major Carp Cirrhinus cirrhosus

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Effects of zinc (Zn) and lead (Pb) exposure on oxidative biomarkers and heat shock protein (HSP) expression, and their possible relation to ovarian steroidogenesis in fish were investigated. Female Cirrhinus cirrhosus were exposed to 1/10th of LC50 of metals for 30 days, and kept for another 30 days without metal exposure. Metal concentrations, antioxidants, HSPs, 17β-estradiol and steroidogenic enzymes were analysed in brain and ovary after 15 and 30 days of exposure and a 15 and 30 day recovery period. Activities of enzymatic and non-enzymatic antioxidants showed duration dependent variation in both exposure and recovery period. HSP70 and HSP90 expressions increased following metal exposure, with the expression being higher in brain than ovary. 17β-Estradiol, steroidogenic enzymes decreased significantly (p < 0.05) after metal exposure. The present study suggests that metals have differential and tissue specific influence on oxidative status and manipulate ovarian steroidogenesis probably through the modulation of HSPs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdel-Tawwab M, El-Sayed GO, Shady SH (2016) Growth, biochemical variables, and zinc bioaccumulation in Nile tilapia, Oreochromis niloticus (L.) as affected by water-born zinc toxicity and exposure period. Int Aquat Res 8:197–206

    Google Scholar 

  • Ahmad AK, Shuhaimi-Othman M (2010) Heavy metal concentrations in sediments and fishes from Lake Chini, Pahang, Malaysia. J Biol Sci 10:93–100

    CAS  Google Scholar 

  • APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. APHA-AWWA-WEF, Washington DC

    Google Scholar 

  • 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 6:1–13

    Google Scholar 

  • Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014:360438. https://doi.org/10.1155/2014/360438

    Article  CAS  Google Scholar 

  • Becker J, Craig EA (1994) Heat-shock proteins as molecular chaperones. Eur J Biochem 219:11–23

    CAS  Google Scholar 

  • Belyaeva EA, Sokolova TV, Emelyanova LV, Zakharova IO (2012) Mitochondrial electron transport chain in heavy metal-induced neurotoxicity: effects of cadmium, mercury and copper. Sci World J 2012:136063. https://doi.org/10.1100/2012/136063

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Google Scholar 

  • Canbek M, Demir TA, Uyanoglu M, Bayramoglu G, Emiroglu O, Arslan N, Koyuncu O (2007) Preliminary assessment of heavy metals in water and some cyprinidae species from the Porsuk River, Turkey. J Appl Biol Sci 1:91–95

    CAS  Google Scholar 

  • Charrier JG, McFall AS, Richards-Henderson NK, Anastasio C (2014) Hydrogen peroxide formation in a surrogate lung fluid by transition metals and quinones present in particulate matter. Environ Sci Technol 48:7010–7017

    CAS  Google Scholar 

  • Chaudhary S, Parvez S (2012) An in vitro approach to assess the neurotoxicity of valproic acid-induced oxidative stress in cerebellum and cerebral cortex of young rats. Neuroscience 225:258–268

    CAS  Google Scholar 

  • Cheung APL, Lam THJ, Chan KM (2004) Regulation of Tilapia metallothionein gene expression by heavy metal ions. Marine Environmental research, twelfth international symposium on pollutant responses in marine organisms 58:389–394

    CAS  Google Scholar 

  • Dhurmeea Z, Pethybridge H, Appadoo C, Bodin N (2018) Lipid and fatty acid dynamics in mature female albacore tuna (Thunnus alalunga) in the western Indian Ocean. PLoS ONE 13:e0194558

    Google Scholar 

  • Dix TA, Aikens J (1993) Mechanisms and biological relevance of lipid peroxidation initiation. Chem Res Toxicol 6:2–18

    CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    CAS  Google Scholar 

  • Eroglu A, DoganKanak EG, Atli G, Canli M (2015) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Pollut Res Int 22:3229–3237

    CAS  Google Scholar 

  • Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, Lamas S (2015) Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol 6:183–197

    CAS  Google Scholar 

  • Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, London

    Google Scholar 

  • He L, He T, Farrar S, Ji L, Liu T, Ma X (2017) Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem 44:532–553

    Google Scholar 

  • Jarabak J (1969) Soluble 17β-hydroxysteroid dehydrogenase of human placenta. Methods Enzymol 15:746–752

    CAS  Google Scholar 

  • Juliani CC, Silva-Zacarin ECM, Santos DC, Boer PA (2008) Effects of atrazine on female Wistar rats: morphological alterations in ovarian follicles and immunocytochemical labeling of 90 kDa heat shock protein. Micron 39:607–616

    CAS  Google Scholar 

  • Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61:310–318

    CAS  Google Scholar 

  • Khalid M, Saima J, Qaisar M, Muhammad I, Jamshid H (2014) Synergistic effects of toxic elements on heat shock proteins. Bio Med Res Int 2014:564136

    Google Scholar 

  • Ksenia JG, Victor JN, Helmut S, Rik ILE, Marc J-FS (2011) Global proteomics analysis of testis and ovary in adult zebrafish (Danio rerio). Fish Physiol Biochem 37:619–647

    Google Scholar 

  • Lehninger AL, Nelson DL, Cox MM, Harris DA (1993). Principles of Biochemistry (2nd edn). Trends in Biochemical Sciences-Library Compendium, 18: 354-354

    Google Scholar 

  • Li L, Wang S, Lin YT, Liu WT, Chi T (2015) A covering model application on Chinese industrial hazardous waste management based on integer program method. Ecol Indic 51:237–243

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • McGeer JC, Brix KV, Skeaff JM, DeForest DK, Brigham SI, Adams WJ, Green A (2003) Inverse relationship between bioconcentration factor and exposure concentration for metals: implications for hazard assessment of metals in the aquatic environment. Environ Toxicol Chem 22:1017–1037

    CAS  Google Scholar 

  • Menon AV, Chang J, Kim J (2016) Mechanisms of divalent metal toxicity in affective disorders. Toxicology 339:58–72

    CAS  Google Scholar 

  • Moniruzzaman M, Hasan NK, Maitra SK (2016) Melatonin actions on ovaprim (synthetic GnRH and domperidone)-induced oocyte maturation in carp. Reproduction 151:285–296

    CAS  Google Scholar 

  • Moniruzzaman M, Midday P, Dhara A, Das D, Ghosal I, Mukherjee D, Chakraborty SB (2017) Change in redox state and heat shock protein expression in an Indian major carp Cirrhinus cirrhosus exposed to zinc and lead. J Toxicol Sci 42:731–740

    CAS  Google Scholar 

  • Murugan SS, Karuppasami R, Poongodi K, Puvaneswari S (2008) Bioaccumulation pattern of zinc in freshwater fish Channa punctatus (Bloch.) after chronic exposure. Turk J Fish Aquat Sc. 8:55–59

    Google Scholar 

  • Nampoothiri LP, Gupta S (2006) Simultaneous effect of lead and cadmium on granulosa cells: a cellular model for ovarian toxicity. Reprod Toxicol 21:179–185

    CAS  Google Scholar 

  • Radons J (2016) The human HSP70 family of chaperones: where do we stand? Cell Stress Chaperones 21:379–404

    CAS  Google Scholar 

  • Rao MV, Chawla SL, Sharma SR (2009) Protective role of vitamin E on nickel and/or chromium induced oxidative stress in the mouse ovary. Food Chem Toxicol 47:1368–1371

    CAS  Google Scholar 

  • Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–113

    CAS  Google Scholar 

  • Sanches Filho PJ, Caldas JS, da Rosa NN, Pereira FOP (2017) Toxicity test and Cd, Cr, Pb and Zn bioccumulation in Phalloceros caudimaculatus. Egypt J Basic Appl Sci 4:206–211

    Google Scholar 

  • Stetler RA, Gan Y, Zhang W, Liou AK, Gao Y, Cao G, Chen J (2010) Heat shock proteins: cellular and molecular mechanisms in the central nervous system. Prog Neurobiol 92:184–211

    CAS  Google Scholar 

  • Szczerbik P, Mikołajczyk T, Sokołowska-Mikołajczyk M, Socha M, Chyb J, Epler P (2006) Influence of long-term exposure to dietary cadmium on growth, maturation and reproduction of goldfish (subspecies: Prussian carp Carassius auratus gibelio B.). Aquat Toxicol 77:126–135

    CAS  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    CAS  Google Scholar 

  • Wang H, Liang Y, Li S, Chang J (2013) Acute toxicity, respiratory reaction, and sensitivity of three cyprinid fish species caused by exposure to four heavy metals. PLoS ONE 8(6):e65282

    CAS  Google Scholar 

  • Wang S, He G, Chen M, Zuo T, Xu W, Liu X (2017) The role of antioxidant enzymes in the ovaries. Oxid Med Cell Longev 2017

  • Wang Y, Li Y, Chen Q, Liu Z (2018) Diethylstilbestrol impaired oogenesis of yellow catfish juveniles through disrupting hypothalamic–pituitary–gonadal axis and germ cell development. J Appl Toxicol 38:308–317

    Google Scholar 

  • Wiebe JP (1976) Steroidogensis in rat Leydig cells: changes in activity of 5-ane and 3-ene-3β hydroxysteroid dehydrogenase during sexual maturation. Endocrinology 98:505–513

    CAS  Google Scholar 

  • Xavier C, Liu X, Liu Y, Wu H (2018) The important functions of GSH-dependent enzyme glutaredoxin 2 (Grx2). In: Glutathione in health and disease, vol 27. Intech Open, London

    Google Scholar 

  • Zudaire I, Murua H, Grande M, Pernet F, Bodin N (2014) Accumulation and mobilization of lipids in relation to reproduction of yellowfin tuna (Thunnus albacares) in the Western Indian Ocean. Fish Res 160:50–59

    Google Scholar 

Download references

Acknowledgements

MM thankfully acknowledge DST-NPDF Programme (PDF/2017/001308), DST, Govt. of India for financial support.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Calcutta, 35 Ballygunge Circular Road, Kolkata, West Bengal, 700019, India

    Mahammed Moniruzzaman, Debjit Das, Anindita Dhara & Suman Bhusan Chakraborty

Authors
  1. Mahammed Moniruzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Debjit Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anindita Dhara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Suman Bhusan Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suman Bhusan Chakraborty.

Additional information

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

Moniruzzaman, M., Das, D., Dhara, A. et al. Enzymatic, Non-enzymatatic Antioxidant Levels and Heat Shock Protein Expression as Indicators of Metal Induced Toxicity and Reproductive Modulation in Female Indian Major Carp Cirrhinus cirrhosus. Bull Environ Contam Toxicol 104, 235–244 (2020). https://doi.org/10.1007/s00128-019-02766-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-019-02766-z

Keywords

Search

Navigation