Skip to main content

Advertisement

SpringerLink
Log in

Effect of diphenyl diselenide diet supplementation on oxidative stress biomarkers in two species of freshwater fish exposed to the insecticide fipronil

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The ability of diphenyl diselenide [(PhSe)2] to attenuate oxidative damage was evaluated in the liver, gills, brain, and muscle of carp (Cyprinus carpio) and silver catfish (Rhamdia quelen) experimentally exposed to fipronil (FPN). Initially, the fish were fed a diet without (PhSe)2 or a diet containing 3.0 mg/kg of (PhSe)2 for 60 days. After the 60-day period, the fish were exposed to 0.65 µg/L of FPN for 192 h. The results showed that carp exposed to FPN and not fed with (PhSe)2 exhibited acetylcholinesterase (AChE) inhibition in brain and muscle, and increased thiobarbituric acid-reactive substance (TBARS) in liver, gills, and brain. Furthermore, FPN decreased nonprotein thiols (NPSH) and δ-aminolevulinate dehydratase (δ-ALA-D) in carp liver and gills, and increased plasma glucose and protein levels. In silver catfish, FPN inhibited AChE and increased TBARS levels in muscle. In addition, glutathione S-transferase (GST) decreased in liver and muscle, and plasma glucose was increased. (PhSe)2 reversed some of these effects. It prevented the increase in TBARS levels in liver, gills, and brain in carp and in silver catfish muscle, and reversed the increase in plasma glucose levels in both species. Additionally, (PhSe)2 increased the NPSH levels in carp and silver catfish that had decreased in response to FPN exposure. However, (PhSe)2 was not effective in reversing the AChE inhibition in brain and muscle or the δ-ALA-D decrease in carp liver. Thus, (PhSe)2 protects tissues of both species of fish, mainly by preventing or counteracting the effects of FPN, on TBARS levels, antioxidants, and present anti-hyperglycemic property.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baldisserotto B (2009) Piscicultura continental no Rio Grande do Sul: situação atual, problemas e perspectivas para o futuro. Ciênc Rural 39:291–299

    Article  Google Scholar 

  • Barbosa NBV, Rocha JBT, Zeni G, Emanuelli T, Beque MC, Braga AL (1998) Effect of organic forms of selenium on δ-aminolevulinate dehydratase from liver, kidney, and brain of adult rats. Toxicol Appl Pharmacol 149:243–253

    Article  CAS  PubMed  Google Scholar 

  • Barbosa NBV, Rocha JBT, Soares JCM, Wondracek DC, Goncalves JF, Schetinger MRC, Nogueira CW (2008) Dietary diphenyl diselenide reduces the STZ induced toxicity. Food Chem Toxicol 46:186–194

    Article  CAS  PubMed  Google Scholar 

  • Beggel S, Werner I, Connon RE, Geist JP (2012) Impacts of the phenylpyrazole insecticide fipronil on larval fish: time-series gene transcription responses in fathead minnow (Pimephales promelas) following short-term exposure. Sci Total Environ 426(1):160–165

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–309

    Article  CAS  PubMed  Google Scholar 

  • Clasen B, Loro VL, Cattaneo R, Moraes B, Lópes T, Avila LA, Zanella R, Reimche GB, Baldisserotto B (2012) Effects of the commercial formulation containing fipronil on the non-target organism Cyprinus carpio: implications for rice-fish cultivation. Ecotoxicol Environ Saf 77:45–51

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  PubMed  Google Scholar 

  • Fiuza TL, Oliveira CS, Costa M, Oliveira VA, Zeni G, Pereira ME (2015) Effectiveness of (PhSe)2 in protect against the HgCl2 toxicity. J Trace Elem Med Biol 29:255–262

    Article  CAS  Google Scholar 

  • Gan J, Bondarenko S, Oki L, Haver D, Li JX (2012) Occurrence of fipronil and its biologically active derivatives in urban residential runoff. Environ Sci Technol 46(3):1489–1495

    Article  CAS  PubMed  Google Scholar 

  • Glusczak L, Loro VL, Pretto A, Moraes BS, Raabe A, Duarte MF, Fonseca MB, Menezes CC, Valladão DMS (2011) Acute exposure to glyphosate herbicide affects oxidative parameters in piava (Leporinus obtusidens). Arch Environ Contam Toxicol 61:624–630

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jacoby WB (1974) Glutathione S-transferase, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326:1–21

    Article  CAS  PubMed  Google Scholar 

  • Mabuchi K, Miya M, Senou H, Suzuki T, Nishida M (2006) Complete mitochondrial DNA sequence of the Lake Biwa wild strain of common carp (Cyprinus carpio L.): further evidence for an ancient origin. Aquaculture 257:68–77

    Article  CAS  Google Scholar 

  • Marchesan E, Sartori GMS, Avila LA, Machado SLO, Zanella R, Primel EG, Macedo VRM, Marchezan MG (2010) Resíduos de agrotóxicos na água de rios da Depressão Central do Estado do Rio Grande do Sul, Brasil. Ciênc Rural 40:1053–1059

    Article  Google Scholar 

  • Menezes CC, Leitemperger J, Santi A, Lópes T, Veiverberg CA, Peixoto S, Adaime MB, Zanella R, Barbosa NBV, Loro VL (2012) The effects of diphenyl diselenide on oxidative stress biomarkers in Cyprinus carpio exposed to herbicide quinclorac (Facet). Ecotoxicol Environ Saf 81:91–97

    Article  Google Scholar 

  • Menezes C, Leitemperger J, Toni C, Santi A, Lópes T, Barbosa NBV, Neto JR, Loro VL (2013) Comparative study on effects of dietary with diphenyl diselenide on oxidative stress in carp (Cyprinus carpio) and silver catfish (Rhamdia sp.) exposed to herbicide clomazone. Environ Toxicol Pharmacol 36:706–714

    Article  CAS  PubMed  Google Scholar 

  • Menezes C, Ruiz-Jarabo I, Martos-Sitcha JA, Leitemperger J, Baldisserotto B, Mancera JM, Rosemberg DB, Loro VL (2014a) Diet with diphenyl diselenide mitigates quinclorac toxicity in silver catfish (Rhamdia quelen). PLoS ONE 9(12):e114233

    Article  PubMed  PubMed Central  Google Scholar 

  • Menezes C, Leitemperger J, Santi A, Dias G, Pedron FA, Neto JR, Salman SM, Barbosa NBV, Loro VL (2014b) Evaluation of the effects induced by dietary diphenyl diselenide on common carp Cyprinus capio. Fish Physiol Biochem 40:141–149

    Article  CAS  PubMed  Google Scholar 

  • Menezes C, Leitemperger J, Murussi C, Toni C, Araújo MCS, Farias IL, Perazzo GX, Barbosa NV, Loro VL (2014c) Herbicide clomazone effects on δ-aminolevulinic acid activity and metabolic parameters in Cyprinus carpio. Bull Environ Contam Toxicol 92:393–398

    Article  CAS  PubMed  Google Scholar 

  • Menezes C, Marins A, Murussi C, Pretto A, Leitemperger J, Loro VL (2016) Effects of diphenyl diselenide on growth, oxidative damage, and antioxidant response in silver catfish. Sci Total Environ 542:231–237

    Article  CAS  PubMed  Google Scholar 

  • Monteiro DA, Rantin FT, Kalinin AL (2009) The effects of selenium on oxidative stress biomarkers in the freshwater characid fish matrinxã, Brycon cephalus (Gunther, 1869) exposed to organophosphate insecticide Folisuper 600 BR® (methyl parathion). Comp Biochem Physiol C 149:40–49

    Google Scholar 

  • Moraes BS, Loro VL, Pretto A, Fonseca MB, Menezes C, Marchezan E, Reimche GB, Avila LA (2009) Toxicological and metabolic parameters of the teleost fish (Leporinus obtusidens) in response to commercial herbicides containing clomazone and propanil. Pestic Biochem Physiol 95:57–62

    Article  CAS  Google Scholar 

  • Murussi CR, Costa M, Menezes C, Leitemperger J, Guerra L, Lópes T, Severo E, Zanella R, Loro VL (2015) Integrated assessment of biomarker response in carp (Cyprinus carpio) and silver catfish (Rhamdia quelen) exposed to clomazone. Arch Environ Contam Toxicol 68:646–654

    Article  CAS  PubMed  Google Scholar 

  • Nogueira CW, Rocha JBT (2010) Diphenyl diselenide a Janus-Faced molecule. J Braz Chem Soc 21:2055–2071

    Article  CAS  Google Scholar 

  • Paulmier C (1986) Selenium reagents and intermediates in organic synthesis. Pergamon Books, Oxford, pp 25–51

    Google Scholar 

  • Ribeiro MCP, Ávila DS, Schiar VPP, dos Santos DB, Meinerz DF, Duarte MMF, Monteiro R, Puntel R, de Bem AF, Hassan W, Barbosa NBV, Rocha JBT (2013) Diphenyl diselenide supplementation reduces biochemical alterations associated with oxidative stress in rats fed with fructose and hydrochlorothiazide. Chem Biol Interact 204:191–199

    Article  CAS  PubMed  Google Scholar 

  • Roe JH (1954) Chemical determination of ascorbic, dehydroascorbic and diketogulonic acids. In: Glick D (ed) Methods of biochemical analysis. Interscience Publishers, New York, pp 115–139

    Chapter  Google Scholar 

  • Roex EWM, Keijzers R, van Gestel CAM (2003) Acetylcholinesterase inhibition and increased food consumption rate in the zebrafish, Danio rerio, after chronic exposure to parathion. Aquat Toxicol 64:451–460

    Article  CAS  PubMed  Google Scholar 

  • Sassa S (1982) δ-Aminolevulic acid dehydratase assay. Enzyme 28:133–145

    CAS  PubMed  Google Scholar 

  • Schlenk D, Huggett DB, Allgood J, Bennett E, Rimoldi J, Beeler AB, Block D, Holder AW, Hovinga R, Bedient P (2001) Toxicity of fipronil and its degradation products to Procambarus sp.: field and laboratory studies. Arch Environ Contam Toxicol 41(3):325–332

    Article  CAS  PubMed  Google Scholar 

  • Stara A, Kristan J, Zuskova E, Velisek J (2013) Effect of chronic exposure to prometryne on oxidative stress and antioxidant response in common carp (Cyprinus carpio L.). Pestic Biochem Physiol 105:18–23

    Article  CAS  PubMed  Google Scholar 

  • Stehr CM, Linbo TL, Incardona JP, Scholz NL (2006) The developmental neurotoxicity of fipronil: notochord degeneration and locomotor defects in zebrafish embryos and larvae. Toxicol Sci 92(1):270–278

    Article  CAS  PubMed  Google Scholar 

  • Vandeputte M (2003) Selective breeding of quantitative traits in the common carp (Cyprinus carpio): a review. Aquat Living Resour 16:399–407

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Programa de Pós - Graduação em Biodiversidade Animal, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil

    Charlene Menezes & Vania Lucia Loro

  2. Programa de Pós - Graduação em Bioquímica Toxicológica, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil

    Jossiele Leitemperger, Camila Murussi & Vania Lucia Loro

  3. LARP – Laboratório de Análises de Resíduos de Pesticidas, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil

    Mariela de Souza Viera, Martha B. Adaime & Renato Zanella

  4. Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Santa Maria, Santa Maria, RS, 97105-900, Brazil

    Charlene Menezes

Authors
  1. Charlene Menezes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jossiele Leitemperger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camila Murussi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariela de Souza Viera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martha B. Adaime
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renato Zanella
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vania Lucia Loro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charlene Menezes.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Menezes, C., Leitemperger, J., Murussi, C. et al. Effect of diphenyl diselenide diet supplementation on oxidative stress biomarkers in two species of freshwater fish exposed to the insecticide fipronil. Fish Physiol Biochem 42, 1357–1368 (2016). https://doi.org/10.1007/s10695-016-0223-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0223-5

Keywords

Search

Navigation