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Cytotoxicity, redox and immune status in African catfish, Clarias gariepinus (Burchell, 1822) exposed to bisphenol A (BPA) and its analogues

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Abstract

The objective of the study was to determine the comparative toxicities and immune dysfunction in the African catfish, Clarias gariepinus, exposed to bisphenol A (BPA) and its two analogues: bisphenol AP (BPAP) and bisphenol P (BPP). Juveniles of C. gariepinus were exposed to sublethal concentrations (70 and 140 μg/L) of BPA, BPAP and BPP for 7, 14 or 21 days after which various endpoints which are indicative of cytotoxicity, oxidative stress and haematological and innate immune parameters were determined in the liver homogenates or blood plasma. The exposure of C. gariepinus to BPA and its analogues caused significant increased activities of lactate dehydrogenase, catalase and superoxide dismutase. The exposed fish had increased levels of DNA fragmentation, lipid peroxidation, white blood cells, nitric oxide and respiratory burst, while the red blood cell counts and the percentage packed cell volume decreased significantly in the exposed fish compared to control. The toxic effects elicited by the bisphenols were both concentration- and duration-dependent. Generally, BPA exerted the most toxic effects on the fish, followed by BPAP, while BPP exerted the least toxic effects to C. gariepinus. Summarily, the findings indicated that BPA and its two analogues studied in the research are capable of causing cytotoxicity, oxidative stress and immune dysfunction in C. gariepinus.

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All data sets, on which the conclusions of the manuscript rely on, are present in the “Results” section in the manuscript.

References

  • Abdel-Tawwab M, Hamed HS (2018) Effect of bisphenol A toxicity on growth performance, biochemical variables, and oxidative stress biomarkers of Nile tilapia, Oreochromis niloticus (L.). J Appl Ichthyol 00:1–9

    Google Scholar 

  • Abou KN, Abd-Elkareem M, Sayed A (2017) Nigella sativa seed protects against 4 nonylphenol-induced hematotoxicity in Clarias gariepinus (Burchell, 1822) oxidant/antioxidant rebalance. Aqua Nut 23:1467-1474

  • Adeyemi JA (2014) Oxidative stress and antioxidant enzymes activities in the African catfish, Clarias gariepinus experimentally challenged with Escherichia coli and Vibrio fischeri. Fish Physiol Biochem 40:347–354

    Article  CAS  Google Scholar 

  • Adeyemi JA, Arowolo OK, Olawuyi ST, Alegbeleye D, Ogunleye A, Bamidele OS, Adedire CO (2018) Effect of co-administration of green tea (Camellia sinensis) on clove- (Syzygium aromaticum) induced hepatotoxicity and oxidative stress in Wistar rats. Indian J Physiol Pharmacol 62:195–201

    CAS  Google Scholar 

  • Adeyemi JA, Gallimberti M, Olise CC, Rocha BA, Adedire CO, Barbosa F Jr (2020) Evaluation of bisphenol A levels in Nigerian thermal receipts and estimation of daily dermal exposure. Environ Sci Pollut Res 27:37645–37649

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Aiswarya R, James K (2016) Effect of bisphenol A on certain hematological parameters of Heteropneustes fossilis, Bloch. Int J Emerg Trends Sci Technol 3:4493–4497

    Google Scholar 

  • Akram R, Iqbal R, Hussain R, Jabeen F, Ali M (2021) Evaluation of oxidative stress, antioxidant enzymes and genotoxic potential of bisphenol A in fresh water bighead carp (Aristichthys nobils) fish at low concentrations. Environ Pollut 268:115896

    Article  CAS  Google Scholar 

  • Albuquerque DMN, Lopes JB, Ferraz MS, Ribeiro MN, Silva SRG, Costa EMS, Lima DCP, Ferreira JDM, Gomes PEB, Lopes JCO (2017) Vitamin E and organic selenium for broilers from 22 to 42 days old: performance and carcass traits. An Acad Bras Cienc 89:1259–1268

    Article  CAS  Google Scholar 

  • Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programs. In Shariff M, Arthur JR, Subasinghe RP (eds.) Diseases in Asian aquaculture ii. Fish health section. Manila: Asian Fish Soc P 85-202

  • Arnold SM, Clark KE, Staples CA, Klecka GM, Dimond SS, Caspers N, Hentges SG (2013) Relevance of drinking water as a source of human exposure to Bisphenol A. J Expo Sci Environ Epidemiol 23:137–144

    Article  CAS  Google Scholar 

  • Azevedo LF, Carneiro MFH, Dechandt CRP, Cassoli JS, Alberici LC, Barbosa F Jr (2020) Global liver proteomic analysis of Wistar rats chronically exposed to low-levels of bisphenol A and S. Environ Res 182:109080

    Article  CAS  Google Scholar 

  • Azevedo LF, Dechandt CRP, Rocha CCS, Carneiro MFH, Alberici LC, Barbosa F Jr (2019) Long-term exposure to bisphenol A or S promotes glucose intolerance and changes in hepatic mitochondrial metabolism in male Wistar rats. Food Chem Toxicol 132:110694

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Bradford M (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  Google Scholar 

  • Chakrabarti S, Poidevin M, Lemaitre B (2014) The Drosophila MAPK p38c 354 regulates oxidative stress and lipid homeostasis in the intestine. PLoS Genet 10:355–1004659

    Article  Google Scholar 

  • Chen D, Kannan K, Tan H, Zheng Z, Feng YL, Wu Y (2016) Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity-a review. Environ Sci Technol 50:5438–5453

    Article  CAS  Google Scholar 

  • Crain DA, Eriksen M, Iguchi T, Jobling S, Laufer H, LeBlanc GA, Guillette LJ Jr (2007) An ecological assessment of bisphenol-A: evidence from comparative biology. Reprod Toxicol 24:225–239

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Faheem M, Lone KP (2018) Oxidative stress and histopathologic biomarkers of exposure to Bisphenol-A in the freshwater fish Ctenopharyngodon idella. Braz J Pharm Sci 53:1–9

    Article  Google Scholar 

  • Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34

    Article  CAS  Google Scholar 

  • Gercel-Taylor C (1982) Diphenylamine assay of DNA fragmentation for chemosensitivity testing. https://doi.org/10.1385/1-59259-889-7:079

  • Global Industry Analysts Inc (2015) Bisphenol a market trends. Retrieved from https://www.strategyr.com/MarketResearch/Bisphenol_A_Market_ Trends.asp. Accessed July 2021

  • Guevara-Guzman R, Emson PC, Kendrick KM (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J Neurochem 62:807–810

    Article  CAS  Google Scholar 

  • Han L, Cai S, Gao M, Hasegawa J, Wang P, Zhang J, Zhang D (2019) Selective catalytic reduction of NOx with NH3 by using novel catalysts. State of the art and future prospects. Chem Rev 119:10916–10976

    Article  CAS  Google Scholar 

  • Howell BF, Mccune S, Schaffer R (1979) Lactate-to-pyruvate or pyruvate-to-lactate assay for lactate dehydrogenase: a re-examination. Clin Chem 25:269–272

    Article  CAS  Google Scholar 

  • Huang YQ, Wong CKC, Zheng JS, Bouwman H, Barra R, Wahlstrom B, Neretin L, Wong MH (2012) Bisphenol A (BPA) in China: a review of sources, environmental levels, and potential human health impacts. Environ Int 42:91–99

    Article  CAS  Google Scholar 

  • Kaya Ö, Kaptaner B (2016) Antioxidant defense system parameters in isolated fish hepatocytes exposed to Bisphenol A Effect of vitamin C. Acta Biol Hung 67:225–235

    Article  CAS  Google Scholar 

  • Kaptaner B, Yilmaz C, Aykut H, Dogan E, Fidan C, Bostanci M, Yildiz F (2021) Bisphenol S leads to cytotoxicity-induced antioxidant responses and oxidative stress in isolated rainbow trout (Oncorhyncus mykiss) hepatocytes. Mol Biol Rep 48:7657–7666

    Article  CAS  Google Scholar 

  • Krishnapriya K, Shobana G, Narmadha S, Ramesh M, Maruthappan V (2017) Sublethal concentration of bisphenol A induces hematological and biochemical responses in an Indian major carp Labeo rohita. Ecohydrol Hydrobiol 17:306–313

    Article  Google Scholar 

  • Kumar N, Sharma JG, Singh SP, Singh A, Krishna VH, Chakrabarti R (2019) Validation of growth enhancing, immunostimulatory and disease resistance properties of Achyranthes aspera in Labeo rohita fry in pond conditions. Heliyon 5:01246

    Article  Google Scholar 

  • Kumar V, Sankaranarayanan M, Durgapal M, Zhou S, Ashok S, Park S (2013) Simultaneous production of 3-hydroxypropionic acid and 1,3-propanediol from glycerol using resting cells of the lactate dehydrogenase-deficient recombinant Klebsiella pneumonia overexpressing an aldehyde dehydrogenase. Bioresour Technol 135:555–563

    Article  CAS  Google Scholar 

  • Kwak HI, Bae MO, Lee MH, Lee YS, Lee BJ, Kang KS, Chae CH, Sung HJ, Shin JS, Kim JH, Mar WC, Sheen YY, Cho MH (2001) Effects of nonylphenol bisphenol A and their mixture on the viviparous swordtail fish (Xiphophorus helleri). Environ Toxicol Chem 20:787–795

    Article  CAS  Google Scholar 

  • Lakshmaiah G (2016) Acute lethal and chronic sublethal toxic stress induced alterations in lactate dehydrogenase activity of phorate intoxicated freshwater fish Cyprinus carpio. Int J Fish Aquat Stud 4:685–689

    Google Scholar 

  • Madhu S, Pooja C (2015) Acute toxicity of 4-nonylphenol on haemotological profile of fresh water fish Channa punctatus. Res J Recent. Sci 4:25–31

    Google Scholar 

  • Maharajan K, Muthulakshmi S, Nataraj B, Mathan R (2018) Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos (Danio rerio): a multi biomarker study. Aquat Toxicol 196:132–145

    Article  CAS  Google Scholar 

  • Martínez JG, García VA, Carrasco SP (2012) DNA fragmentation and membrane damage of Bocachico Prochilodus magdalenae (Ostariophysi: Prochilodontidae) sperm following cryopreservation with dimethylsulfoxide and glucose. Neotrop Ichthyol 10:577–586

    Article  Google Scholar 

  • Mekkawy AI, Mahmoud UM, Sayed AE (2011) Effects of 4-nonylphenol on blood cells of the African catfish Clarias gariepinus (Burchell, 1822). Tissue Cell 43:223–229

    Article  CAS  Google Scholar 

  • Michałowicz J (2014) Bisphenol A: sources, toxicity and biotransformation. Environ Toxicol Pharmacol 37:738–758

    Article  Google Scholar 

  • Owolabi O, Babarinsa M (2020) Assessment of growth performance, nutrient utilization and haematological profile of Clarias gariepinus fed with nanoselenium formulated diets. IOP Conference Series: Materials Science and Engineering 805:012014

    Article  CAS  Google Scholar 

  • Parhamifar L, Andersen H, Moghimi SM (2019) Lactate dehydrogenase assay for assessment of polycation cytotoxicity. Methods Mol Biol 1943:291–299

    Article  CAS  Google Scholar 

  • Penttilä IM, Mahlamäki E, Mononen I, Kärkkäinen P (1985) Adaptation of the May-Grünwald-Giemsa staining method for automated differential counting of blood leukocytes by a Hematrak analyzer. Scand J Haematol 34:274–280

    Article  Google Scholar 

  • Qiu W, Chen J, Li Y, Chen Z, Jiang L, Yang M, Wu M (2016) Oxidative stress and immune disturbance after long-term exposure to bisphenol A in juvenile common carp (Cyprinus carpio). Ecotoxicol Environ Saf 130:93–102

    Article  CAS  Google Scholar 

  • Revathi RP, Iyapparajb RA, Vasanthic P, Srinivasanc N, Munuswamyd, Palavesama A (2019) Protective responses of antioxidant enzymes against bisphenol-A induced oxidative stress in Asian Seabass Lates calcarifer. Indian J Geo-Mar Sci 49:1458–1463

    Google Scholar 

  • Roberts RJ, Ellis AE (2001) The anatomy and physiology of teleost. In: Roberts RJ (Ed) Fish Pathology. WB Saunders, Philadelphia, USA

  • Rochester JR (2013) Bisphenol A and human health: a review of the literature. Reprod Toxicol 42:132–155

    Article  CAS  Google Scholar 

  • Rombout JH, Huttenhuis HBT, Picchietti S, Scapigliati S (2005) Phylogeny and ontogeny of fish leucocytes. Fish Shellfish Immunol 19:441–455

    Article  CAS  Google Scholar 

  • Rusia V, Sood SK (1992) Routine haematological tests. In: Mukerjee KL(Ed) Medical Laboratory Technology. McGraw Hill Publishing Co. Ltd, 252-258

  • Sakai AK, Allendorf FW, Holt JS, Lod DM, Molofsky JKA, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol System 32:305–332

    Article  Google Scholar 

  • Sharma M, Chadha P (2015) Acute toxicity of 4-nonylphenol on haemotological profile of fresh water fish Channa punctatus. Res J of Rec Sci 4:25–31

    Google Scholar 

  • Shioda T, Wakabayashi M (2000) Effect of certain chemicals on the reproduction of Medaka (Oryzias latipes). Chemosphere 40:239–243

    Article  CAS  Google Scholar 

  • Snieszko SF (1960) Microhematocrit as a tool in fishery research and management. U.S. Fish & wildlife service, Spec Sci Report Fisheries no. 341

  • Sohoni P, Tyler CR, Hurd K, Caunter J, Hetheridge M, Williams T, Woods C, Evans M, Toy R, Gargas M, Sumpter JP (2001) Reproductive effects of long-term exposure to Bisphenol A in the fathead minnow Pimephales promelas. Environ Sci Technol 35:2917–2925

    Article  CAS  Google Scholar 

  • Talukdar B, Kalita HK, Basumatary S, Saikia DJ, Sarma D (2017) Cytotoxic and genotoxic effects of acid mine drainage on fish Channa punctata (Bloch). Ecotoxicol Environ Saf 144:72–78

    Article  CAS  Google Scholar 

  • Varshney R, Kale RK (1990) Effects of calmodulin antagonist. Int J Radiat Biol 58:733–743

    Article  CAS  Google Scholar 

  • Wink DA, Hines HB, Cheng RYS, Switzer CH, Flores-Santana W, Vitek MP, Colton CA (2011) Nitric oxide and redox mechanisms in the immune response. J Leukoc Biol 89:873–891

    Article  CAS  Google Scholar 

  • Wu M, Xu H, Yang M, Xu G (2011) Effects of chronic bisphenol A exposure on hepatic antioxidant parameters in medaka (Oryzias latipes). Toxicol Environ Chem 93:270–278

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Mr Ojuola Micheal Olayemi for his assistance with collection of blood samples from the fish.

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Authors and Affiliations

  1. Department of Biology, School of Life Sciences, Federal University of Technology Akure, P.M.B. 704, Akure, Nigeria

    Oluwakemi D. Samuel, Joseph A. Adeyemi & Chris O. Adedire

  2. Department of Biochemistry, School of Life Sciences, Federal University of Technology, Akure, Nigeria

    Olufemi S. Bamidele

  3. Department of Clinical Analyses, Toxicology and Food Sciences, School of Pharmaceutical Sciences of Ribeirao Preto, University of Sao Paulo, Sao Paulo, Brazil

    Joseph A. Adeyemi & Fernando Barbosa Jr

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  1. Oluwakemi D. Samuel
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  2. Joseph A. Adeyemi
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  3. Olufemi S. Bamidele
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  5. Chris O. Adedire
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Contributions

JAA, FB and COA were involved in the design of the experiment. ODS, JAA and OSB were involved in data acquisition and analyses. ODS, JAA and OSB were involved in writing the draft of the manuscript. JAA, FB and COA were involved in writing the final draft of the manuscript.

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Correspondence to Joseph A. Adeyemi.

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The experimental procedures were in conformity with national and international standards on the use of laboratory animals. Also, the study was approved by institutional committee on the care and use of animal for experiments.

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Samuel, O.D., Adeyemi, J.A., Bamidele, O.S. et al. Cytotoxicity, redox and immune status in African catfish, Clarias gariepinus (Burchell, 1822) exposed to bisphenol A (BPA) and its analogues. Environ Sci Pollut Res 29, 74185–74196 (2022). https://doi.org/10.1007/s11356-022-21068-2

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