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Borax Alleviates Copper-Induced Renal Injury via Inhibiting the DNA Damage and Apoptosis in Rainbow Trout

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Abstract

The aim of this study was to determine the therapeutic potential of borax against copper in the kidney tissue of the rainbow trout fed with added borax (BX) (1.25, 2.5, and 5 mg/kg) and/or copper (Cu) (500,1000 mg/kg) contents. For this purpose, two treatment groups had designed, and glutathione peroxidase (GPx), superoxide dismutase (SOD), and catalase (CAT) enzyme activities were determined. Besides, oxidative DNA damage (8-hydroxy-2′-deoxyguanosine, 8-OHdG), caspase-3, and malondialdehyde (MDA) levels were assessed in kidneys of all treatment groups. In molecular pathway, hsp70, CYP1A, and antioxidant gene expression levels were determined. In the results of the analysis, antioxidant enzyme activity and gene expression were increased; 8-OHdG, caspase-3, and MDA levels were decreased in groups fed with borax supplemented feeds compared to the copper-treated group. The alterations among the groups were found as significant (p < 0.05). CYP1A and hsp70 gene expressions were upregulated in copper and copper combined groups (p < 0.05). The findings of present research showed that borax had alleviative effect on copper-induced toxicity and could be used as an antidote in fish nutrition.

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References

  1. Halliwell B, Gutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease. Methods Enzymol 186:1–85

    Article  CAS  PubMed  Google Scholar 

  2. Alak G, Atamanalp M, Topal A, Arslan H, Kocaman EM, Oruç E (2013) Effect of sub-lethal lead toxicity on the histopathological and antioxidant enzyme activity of rainbow trout (Onchorynchus mykiss). Fresenius Environ Bull 22(5):733–738

    CAS  Google Scholar 

  3. Alak G, Atamanalp M, Topal A, Arslan H, Oruç E, Altun S (2013) Histopathological and biochemical effect of humic acid against cadmium toxicity in brown trout gills and muscle. Turk J Fısh Aquat Sci 13:315–320

    Google Scholar 

  4. Kırıcı M, Turk C, Caglayan C, Kırıcı M (2017) Toxic effects of copper sulphate pentahydrate on antioxidant enzyme activities and lipid peroxidation of freshwater fish Capoeta umbla (Heckel, 1843) tissues. Appl Ecol Environ Res 15(3):1685–1696

    Article  Google Scholar 

  5. Alak G, Ucar A, Yeltekin AÇ, Çomaklı S, Parlak V, Tas IH, Özkaraca M, Kirmanoğlu EM, Bolat İ, Atamanalp M, Türkez H (2018) Neuroprotective effects of dietary borax in the brain tissue of rainbow trout (Oncorhynchus mykiss) exposed to copper-induced toxicity. Fish Physiol Biochem 44(5):1409–1420

    Article  CAS  PubMed  Google Scholar 

  6. Alak G, Parlak V, Aslan ME, Ucar A, Atamanalp M, Türkez H (2018) Borax supplementation alleviates hematotoxicity and DNA damage in rainbow trout (Oncorhynchus mykiss) exposed to copper. Biol Trace Elem Res. https://doi.org/10.1007/s12011-018-1399-6

  7. Miller DD (1996) Minerals. In: Fennema OR (ed) Food chemistry. Marcel Dekker, New York, pp 617–649

    Google Scholar 

  8. Comba B, Oto G, Mis L, Özdemir H, Comba A (2016) Effects of borax on inflammation, haematological parameters and total oxidant-antioxidant status in rats applied 3–methylcholanthrene. Kafkas Univ Vet Fak Derg 22(4):539–544

    Google Scholar 

  9. Pawa S, Shakir A (2006) Boron ameliorates fulminant hepatic failure by counteracting the changes associated with the oxidative stress. Chem Biol Interact 160:89–98

    Article  CAS  PubMed  Google Scholar 

  10. Çoban FK, Ince S, Kucukkurt I, Demirel HH, Hazman O (2015) Boron attenuates malathion-induced oxidative stress and acetylcholinesterase inhibition in rats. Drug Chem Toxicol 38(4):391–399

    Article  CAS  PubMed  Google Scholar 

  11. Weydert CJ, Cullen JJ (2010) Measurement of superoxide dismutase, catalase, and glutathione peroxidase in cultured cells and tissue. Nat Protoc 5(1):51–66

    Article  CAS  PubMed  Google Scholar 

  12. Alak G, Ucar A, Parlak V, Yeltekin AÇ, Tas IH, Ölmez D, Kocaman EM, Yılgın M, Atamanalp M, Yanık T (2017a) Assessment of 8-hydroxy-2-deoxyguanosine activity, gene expression and antioxidant enzyme activity on rainbow trout (Oncorhynchus mykiss) tissue exposed to biopesticide. Comp Biochem Physiol C: Toxicol Pharmacol 203:51–58

    CAS  Google Scholar 

  13. Alak G, Yeltekin AÇ, Tas IH, Ucar A, Parlak V, Topal A, Kocaman EM, Atamanalp M (2017b) Investigation of 8-OHdG, CYP1A, HSP70 and transcriptional analyses of antioxidant defence system in liver tissues of rainbow trout exposed to eprinomectin. Fish Shellfish Immunol 65:136–144

    Article  CAS  PubMed  Google Scholar 

  14. Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34(3):497–500

    CAS  PubMed  Google Scholar 

  15. Aebi H (1974) Catalase. In: Methods of enzymatic analysis. Academic Press, New York, Bergmeyer, HU, USA, pp 673–678

  16. Beutler E (1984) Red Cell Metab: A Manual of Biochemical Methods, 2nd edn. Grune and Starton, NewYork

    Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. Luo Y, Su Y, Lin RZ, Shi HH, Wang XR (2006) 2-chlorophenol induced ROS generation in fish Carassius auratus based on the EPR method. Chemosphere 65(6):1064–1073

    Article  CAS  PubMed  Google Scholar 

  19. Geyikoğlu F, Türkez H (2008) Boron compounds reduce vanadium tetraoxide genotoxicity in human lymphocytes. Environ Toxicol Pharmacol 26:342–347

    Article  CAS  PubMed  Google Scholar 

  20. Nielsen FH (1994) Biochemical and physiologic consequences of boron deprivation in humans. Environ Health Perspect 102:59–63

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Hunt DC (1998) Regulation of enzymatic activity, one possible role of dietary boron in higher animals and humans. Biol Trace Elem Res 66:205–225

    Article  CAS  PubMed  Google Scholar 

  22. Mohora M, Boghianu L, Muscurel C, Dute C, Dumitrache C (2002) Effect of boric acid redox status in the rat livers. Rom J Biophys 12(3–4):77–82

    CAS  Google Scholar 

  23. Yıldız G, Köksal BH, Sızmaz Ö (2011) Rasyonlara ilave edilen maya ve borik asidin broylerde performans, karkas ve bazı kan parametreleri üzerine etkisi. Kafkas Üniv Vet Fak Derg 17(3):429–434

    Google Scholar 

  24. Ince S, Kucukkurt I, Cigerci IH, Fidan AF, Eryavuz A (2010) The effects of dietary boric acid and borax supplementation on lipid peroxidation, antioxidant activity, and DNA damage in rats. J Trace Elem Med Biol 24:161–164

    Article  CAS  PubMed  Google Scholar 

  25. Yazıcı S, Aksit H, Korkut O, Sunay B, Çelik T (2014) Effects of boric acid and 2-aminoethoxydiphenyl borate on necrotizing enterocolitis. Gastroenterology 58(1):61–67

    Google Scholar 

  26. Khaliq H, Jing W, Ke X, Ke-Li Y, Peng-peng S, Cui L, Wei-wei Q, Zhixin L, Hua-Zhen L, Hui S, Ju-Ming Z, Ke-Mei P (2018) Boron affects the development of the kidney through modulation of apoptosis, antioxidant capacity, and nrf2 pathway in the African ostrich chicks. Biol Trace Elem Res 186:226–237

    Article  CAS  PubMed  Google Scholar 

  27. Kramer HF, Goodyear LJ, Exercise MAPK (2007) NF-kappaB signaling in skeletal muscle. J Appl Physiol 103:388–395

    Article  CAS  PubMed  Google Scholar 

  28. Bimei J, Liang P, Deng G, Tu Z, Liu M, Xiao X (2011) Increased stability of Bcl-2 in HSP70-mediated protection against apoptosis induced by oxidative stress. Cell Stress Chaperones 16:143–152

    Article  CAS  Google Scholar 

  29. Kısım A, Uzunoglu S (2012) Hormesis: antecedent phenomena for adaptation to low doses of toxic agents. J For Med 26(3):180–190

    Google Scholar 

  30. Evans CG, Chang L, Gestwicki JE (2010) Heat Shock Protein 70 (Hsp70) as an emerging drug target. J Med Chem 53(12):4585–4602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lu C, Gallegos R, Li P, Xia CQ, Pusalkar S, Uttamsingh V, Nix D, Miwa GT, Gan LS (2006) Investigation of drug-drug interaction potential of bortezomib in vivo in female Sprague-Dawley rats and in vıtro in human liver microsomes. Drug Metab Dispos 34(4):702–708

    Article  CAS  PubMed  Google Scholar 

  32. Valdehita A, Fernandez-Cruz ML, Torrent F, Sericano JL, Navas JM (2012) Differences in the induction of CYP1A and related genes in cultured rainbow trout Oncorhynchus mykiss. Additional considerations for the use of EROD activity as a biomarker. J Fish Biol 81:270–287

    Article  CAS  PubMed  Google Scholar 

  33. Cárcamo JG, Aguilar MN, Carreño CF, Vera T, Arias-Darraz L, Figueroa JE, Romerob AP, Alvarez M, Yañez AJ (2017) Consecutive emamectin benzoate and deltamethrin treatments affect the expressions and activities of detoxification enzymes in the rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C 191:129–137

    Google Scholar 

  34. Sun Y, Zhang G, He Z, Wang Y, Cui J, Li Y (2016) Effects of copper oxide nanoparticles on developing zebrafish embryos and larvae. Int J Nanomedicine 11:905–918

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors thank Mr. Ismail Hakkı TAŞ from Qiagen for the support in molecular analyses.

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Authors and Affiliations

  1. Department of Aquaculture, Faculty of Fisheries, Atatürk University, TR-25240, Erzurum, Turkey

    Gonca Alak, Arzu Uçar, Veysel Parlak & Muhammed Atamanalp

  2. Department of Chemistry, Faculty of Science, University of Yüzüncü Yıl, TR-65080, Van, Turkey

    Aslı Çilingir Yeltekin

  3. Department of Molecular Biology and Genetic, Faculty of Science, University of Erzurum Technical, TR-25240, Erzurum, Turkey

    Hasan Türkez

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  1. Gonca Alak
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  2. Aslı Çilingir Yeltekin
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  3. Arzu Uçar
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  4. Veysel Parlak
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  5. Hasan Türkez
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  6. Muhammed Atamanalp
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Correspondence to Gonca Alak or Muhammed Atamanalp.

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Alak, G., Yeltekin, A.Ç., Uçar, A. et al. Borax Alleviates Copper-Induced Renal Injury via Inhibiting the DNA Damage and Apoptosis in Rainbow Trout. Biol Trace Elem Res 191, 495–501 (2019). https://doi.org/10.1007/s12011-018-1622-5

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  • DOI: https://doi.org/10.1007/s12011-018-1622-5

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