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Protective efficacy of naringenin against cadmium-induced redox imbalance in Labeo rohita: an integrated biomarker approach

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Abstract

The protective efficacy of dietary naringenin (NG) has been investigated against the toxicity caused by cadmium chloride (CdCl2) using biomarkers of oxidative stress in the liver, gills and kidney of Labeo rohita. The fish were exposed to environmentally relevant concentrations of CdCl2 (0.37 and 0.62 mg/L) and simultaneously orally administered with NG (50 mg/kg bw/day) for 60 days. Tissue (gills, liver and kidney) samples were collected on days 15, 30 and 60 of the experiment and analysed for endogenous antioxidants and oxidative stress biomarkers. CdCl2 exposure for 15 and 30 days induced the development of adaptive mechanism as demonstrated by the enhanced activities of superoxide dismutase, catalase, glutathione peroxidase and glutathione-S-transferase in all three tissues. However, on the 60th day, CdCl2-induced oxidative damage was stipulated by a decline in the enzyme activities and reduced glutathione (GSH) content significantly (p < 0.05) below control levels along with enhanced levels of lipid peroxidation. Oral administration of NG in toxicant exposed fish significantly restored the altered levels of antioxidants, oxidative enzymes and lipid peroxidation. Besides, integrated biomarker response (IBR) analysis was applied by combining all the biomarkers to indicate the overall stress response index. IBR analysis confirmed the altered levels of biomarkers, the oxidative stress induced by CdCl2 exposure and the ameliorative potential of NG. The present study suggested that NG might have protective role against Cd-induced oxidative insult which might be ascribed to the ability of NG to chelate metals and scavenge free radicals.

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References

  • Abdel-Rahim EA, Abdel-Mobdy YE, Ali RF, Mahmoud HA (2014) Hepatoprotective effects of Solanum nigrum Linn fruits against cadmium chloride toxicity in albino rats. Biol Trace Elem Res 160(3):400–408

    Article  CAS  Google Scholar 

  • Abougabal K, Moselhy WA, Korni FM (2020) The effect of cadmium toxicity on Oreochromis niloticus and human health. Afr J Aquat Sci 45(3):303–309

    Article  CAS  Google Scholar 

  • Amaro MI, Rocha J, Vila-Real H, Eduardo-Figueira M, Mota-Filipe H, Sepodes B, Ribeiro MH (2009) Anti-inflammatory activity of naringin and the biosynthesised naringenin by naringinase immobilized in microstructured materials in a model of DSS-induced colitis in mice. Food Res Int 42(8):1010–1017

    Article  Google Scholar 

  • Arroyo VS, Flores KM, Ortiz LB, Gómez-Quiroz LE, Gutiérrez-Ruiz MC (2012) Liver and cadmium toxicity. J Drug Metab Toxicol S5:1–7

    Google Scholar 

  • Asagba SO, Eriyamremu GE, Igberaese ME (2008) Bioaccumulation of cadmium and its biochemical effect on selected tissues of the catfish (Clarias gariepinus). Fish Physiol Biochem 34(1):61–69

    Article  CAS  Google Scholar 

  • Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Saf 73:1884–1889

    Article  CAS  Google Scholar 

  • Aulakh MS, Khurana MP, Singh D (2009) Water pollution related to agricultural, industrial, and urban activities, and its effects on the food chain: case studies from Punjab. J New Seeds 10(2):112–137

    Article  Google Scholar 

  • Banerjee BD, Seth V, Bhattacharya A, Pasha ST, Chakraborty AK (1999) Biochemical effects of some pesticides on lipid peroxidation and free-radical scavengers. Toxicol Lett 107(1–3):33–47

    Article  CAS  Google Scholar 

  • Basha PS, Rani AU (2003) Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environ Saf 56(2):218–221

    Article  CAS  Google Scholar 

  • Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322

    Article  CAS  Google Scholar 

  • Bhardwaj JK, Panchal H (2021) Quercetin mediated attenuation of cadmium-induced oxidative toxicity and apoptosis of spermatogenic cells in caprine testes in vitro. Environ Mol Mutagen 62(6):374–384

    Article  CAS  Google Scholar 

  • Bhardwaj JK, Panchal H, Saraf P (2021) Cadmium as a testicular toxicant: a review. J Appl Toxicol 41(1):105–117

    Article  CAS  Google Scholar 

  • Bhardwaj R, Gupta A, Garg JK (2017) Evaluation of heavy metal contamination using environmetrics and indexing approach for River Yamuna, Delhi stretch. India Water Sci 31(1):52–66

    Article  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. In: Fleischer S, Packer L (eds) Methods in enzymology. Academic Press, pp 302–310

    Google Scholar 

  • Capaldo A, Gay F, Scudiero R, Trinchella F, Caputo I, Lepretti M, Marabotti A, Esposito C, Laforgia V (2016) Histological changes, apoptosis and metallothionein levels in Triturus carnifex (Amphibia, Urodela) exposed to environmental cadmium concentrations. Aquat Toxicol 173:63–73

    Article  CAS  Google Scholar 

  • Casalino E, Calzaretti G, Sblano C, Landriscina C (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179(1–2):37–50

    Article  CAS  Google Scholar 

  • Casalino E, Cesare S, Clemente L (1997) Enzyme activity alteration by cadmium administration to rats: the possibility of iron involvement in lipid peroxidation. Arch Biochem Biophys 346(2):171–179

    Article  CAS  Google Scholar 

  • Çavaş T, Ergene-Gözükara S (2005) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74(3):264–271

    Article  Google Scholar 

  • Cheng IF, Breen K (2000) On the ability of four flavonoids, baicilein, luteolin, naringenin, and quercetin, to suppress the Fenton reaction of the iron-ATP complex. Biometals 13(1):77–83

    Article  CAS  Google Scholar 

  • Choi JS, Park KY, Moon SH, Rhee SH, Young HS (1994) Antimutagenic effect of plant flavonoids in the Salmonella assay system. Arch Pharm Res 17(2):71–75

    Article  CAS  Google Scholar 

  • Cobbina SJ, Chen Y, Zhou Z, Wu X, Zhao T, Zhang Z, Feng W, Wang W, Li Q, Wu X, Yang L (2015) Toxicity assessment due to sub-chronic exposure to individual and mixtures of four toxic heavy metals. J Hazard Mater 294:109–120

    Article  CAS  Google Scholar 

  • Dabas A, Nagpure NS, Kumar R, Kushwaha B, Kumar P, Lakra WS (2012) Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel Channa Punctatus. Fish Physiol Biochem 38(2):469–482

    Article  CAS  Google Scholar 

  • Danabas D, Yildirim NC, Yildirim N, Onal AO, Uslu G, Unlu E, Danabas S, Ergin C, Tayhan N (2015) Changes in antioxidant defense system in gills of Capoeta umbla caught from Uzuncayir Dam Lake Turkey. Biochem Syst Ecol 63:72–79

    Article  CAS  Google Scholar 

  • Dorta DJ, Leite S, DeMarco KC, Prado IM, Rodrigues T, Mingatto FE, Uyemura SA, Santos AC, Curti C (2003) A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97(3):251–257

    Article  CAS  Google Scholar 

  • Dringen R (2000) Glutathione metabolism and oxidative stress in neurodegeneration. Eur J Biochem 267(16):4903–4903

    Article  CAS  Google Scholar 

  • El-Boshy ME, Risha EF, Abdelhamid FM, Mubarak MS, Hadda TB (2015) Protective effects of selenium against cadmium induced hematological disturbances, immunosuppressive, oxidative stress and hepatorenal damage in rats. J Trace Elem Med Biol 29:104–110

    Article  CAS  Google Scholar 

  • El-Ghasham A, Mehana EE, Abdel-Reheem M (2008) Evaluation of lead and cadmium levels in freshwater fish farms at Qassim region KSA. J Agric Vet Sci 1(2):59–69

    Google Scholar 

  • Fernández-Luqueño F, López-Valdez F, Gamero-Melo P, Luna-Suárez S, Aguilera-González EN, Martínez AI, García-Guillermo MD, Hernández-Martínez G, Herrera-Mendoza R, Álvarez-Garza MA, Pérez-Velázquez IR (2013) Heavy metal pollution in drinking water-a global risk for human health: a review. Afr J Environ Sci Technol 7(7):567–584

    Google Scholar 

  • Gad SC (2014) Cadmium. In: Wexler P (ed) Encyclopedia of toxicology. Academic Press, Oxford, pp 613–616

    Chapter  Google Scholar 

  • GHS (2013) Globally harmonized system of classification and labelling of chemicals (GHS), Fifth Revised Edition, UN New York and Geneva. http://www.unece.org/trans/danger/publi/ghs/ghs_rev05/05files_e.html. Accessed 10 Feb 2020

  • Gibson BW (2005) The human mitochondrial proteome: oxidative stress protein modifications and oxidative phosphorylation. J Biochem Cellbiol 37:927–934

    CAS  Google Scholar 

  • Gnanasoundari M, Pari L (2006) Impact of naringenin on oxytetracycline-mediated oxidative damage in kidney of rats. Ren Fail 28:599–605

    Article  CAS  Google Scholar 

  • Goodarzi Z, Karami E, Yousefi S, Dehdashti A, Bandegi AR, Ghanbari A (2020) Hepatoprotective effect of atorvastatin on cadmium chloride induced hepatotoxicity in rats. Life Sci 254:117770

    Article  CAS  Google Scholar 

  • Guerlet E, Vasseur P, Giambérini L (2010) Spatial and temporal variations of biological responses to environmental pollution in the freshwater zebra mussel. Ecotoxicol Environ Saf 73(6):1170–1181

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    Article  CAS  Google Scholar 

  • Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179(3):687–699

    Article  CAS  Google Scholar 

  • Honohan T, Hale RL, Brown JP, Wingard RE (1976) Synthesis and metabolic fate of hesperetin-3-14C. J Agric Food Chem 24(5):906–911

    Article  CAS  Google Scholar 

  • Huang B, Hu P, Hu A, Li Y, Shi W, Huang J, Jiang Q, Xu S, Li L, Wu Q (2019) Naringenin attenuates carotid restenosis in rats after balloon injury through its anti-inflammation and anti-oxidative effects via the RIP1-RIP3-MLKL signaling pathway. Eur J Pharmacol 855:167–174

    Article  CAS  Google Scholar 

  • Huang YH, Shih CM, Huang CJ, Lin CM, Chou CM, Tsai ML, Liu TP, Chiu JF, Chen CT (2006) Effects of cadmium on structure and enzymatic activity of Cu, Zn-SOD and oxidative status in neural cells. J Cell Biochem 98(3):577–589

    Article  CAS  Google Scholar 

  • Idrees N, Tabassum B, Abd Allah EF, Hashem A, Sarah R, Hashim M (2018) Groundwater contamination with cadmium concentrations in some West UP Regions India. Saudi J Biol Sci 25(7):1365–1368

    Article  CAS  Google Scholar 

  • Jain A, Yadav A, Bozhkov AI, Padalko VI, Flora SJS (2011) Therapeutic efficacy of silymarin and naringenin in reducing arsenic–induced hepatic damage in young rats. Ecotoxicol Environ Saf 74(4):607–614

    Article  CAS  Google Scholar 

  • Jamakala O, Rani UA (2015) Amelioration effect of zinc and iron supplementation on selected oxidative stress enzymes in liver and kidney of cadmium-treated male albino rat. Toxicol Int 22(1):1–9

    Article  CAS  Google Scholar 

  • Jindal R, Verma S (2015) In vivo genotoxicity and cytotoxicity assessment of cadmium chloride in peripheral erythrocytes of Labeo rohita (Hamilton). Ecotoxicol Environ Saf 118:1–10

    Article  CAS  Google Scholar 

  • Kapoor R, Kakkar P (2014) Naringenin accords hepatoprotection from streptozotocin induced diabetes in vivo by modulating mitochondrial dysfunction and apoptotic signaling cascade. Toxicol Rep 1:569–581

    Article  CAS  Google Scholar 

  • Karaytug S, Sevgiler Y, Karayakar F (2014) Comparison of the protective effects of antioxidant compounds in the liver and kidney of Cd-and Cr-exposed common carp. Environ Toxicol 29(2):129–137

    Article  CAS  Google Scholar 

  • Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186(1):189–195

    Article  CAS  Google Scholar 

  • Kumar P, Singh A (2010) Cadmium toxicity in fish: an overview. GERF Bull Biosci 1(1):41–47

    Google Scholar 

  • Lee CH, Jeong TS, Choi YK, Hyun BH, Oh GT, Kim EH, Kim JR, Han JI, Bok SH (2001) Anti-atherogenic effect of citrus flavonoids, naringin and naringenin, associated with hepatic ACAT and aortic VCAM-1 and MCP-1 in high cholesterol-fed rabbits. Biochem Biophys Res Commun 284(3):681–688

    Article  CAS  Google Scholar 

  • Lee MH, Yoon S, Moon JO (2004) The flavonoid naringenin inhibits dimethylnitrosamine-induced liver damage in rats. Biol Pharm Bull 27(1):72–76

    Article  CAS  Google Scholar 

  • Liu H, Lai W, Liu X, Yang H, Fang Y, Tian L, Li K, Nie H, Zhang W, Shi Y, Bian L (2020) Exposure to copper oxide nanoparticles triggers oxidative stress and endoplasmic reticulum (ER)-stress induced toxicology and apoptosis in male rat liver and BRL-3A cell. J Hazard Mater 401(123349):1–12

    Google Scholar 

  • Liu J, Qu W, Kadiiska MB (2009) Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol Appl Pharmacol 238(3):209–214

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Luck H (1965) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 885–894

    Chapter  Google Scholar 

  • McRae NK, Gaw S, Brooks BW, Glover CN (2019) Oxidative stress in the galaxiid fish, Galaxias maculatus, exposed to binary waterborne mixtures of the pro-oxidant cadmium and the anti-oxidant diclofenac. Environ Pollut 247:638–646

    Article  CAS  Google Scholar 

  • McRae NK, Gaw S, Glover CN (2018) Effects of waterborne cadmium on metabolic rate, oxidative stress, and ion regulation in the freshwater fish, inanga (Galaxias maculatus). Aquat Toxicol 194:1–9

    Article  CAS  Google Scholar 

  • Mershiba SD, Dassprakash MV, Saraswathy SD (2013) Protective effect of naringenin on hepatic and renal dysfunction and oxidative stress in arsenic intoxicated rats. Mol Biol Rep 40(5):3681–3691

    Article  CAS  Google Scholar 

  • Messaoudi I, El Heni J, Hammouda F, Saïd K, Kerkeni A (2009) Protective effects of selenium, zinc, or their combination on cadmium-induced oxidative stress in rat kidney. Biol Trace Elem Res 130(2):152–161

    Article  CAS  Google Scholar 

  • Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ (1984) Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder cancer. Cancer Res 44(11):5086–5091

    CAS  Google Scholar 

  • Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582(1):67–78

    Article  CAS  Google Scholar 

  • Naik AP, Shyama SK, D’Costa AH (2020) Evaluation of genotoxicity, enzymatic alterations and cadmium accumulation in Mozambique tilapia Oreochromis mossambicus exposed to sub lethal concentrations of cadmium chloride. Environ Chem Ecotoxicol 2:126–131

    Article  Google Scholar 

  • Newairy AA, El-Sharaky AS, Badreldeen MM, Eweda SM, Sheweita SA (2007) The hepatoprotective effects of selenium against cadmium toxicity in rats. Toxicology 242:23–30

    Article  CAS  Google Scholar 

  • Ognjanovic BI, Markovic SD, Pavlovic SZ, Zikic RV, Stajn AS, Saicic ZS (2008) Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: protective effect of selenium. Physiol Res 57(3):403–411

    Article  CAS  Google Scholar 

  • Organization for Economic Cooperation and Development (2001) OECD guidelines for testing of chemicals. Guideline 423: Acute Oral Toxicity-Acute Toxic Class Method. Adopted 17 December 2001, OECD, Paris. https://ntp.niehs.nih.gov/iccvam/suppdocs/feddocs/oecd/oecd_gl423.pdf (accessed 25 October 2019)

  • Ozkaya A, Sahin Z, Dag U, Ozkaraca M (2016) Effects of naringenin on oxidative stress and histopathological changes in the liver of lead acetate administered rats. J Biochem Mol Toxicol 30:243–248

    Article  CAS  Google Scholar 

  • Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish Channa Punctata Bloch. Chem Biol Interact 174(3):183–192

    Article  CAS  Google Scholar 

  • Pari L, Murugavel P (2005) Role of diallyl tetrasulfide in ameliorating the cadmium induced biochemical changes in rats. Environ Toxicol Pharmacol 20(3):493–500

    Article  CAS  Google Scholar 

  • Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74

    Article  CAS  Google Scholar 

  • Poletta GL, Simoniello MF, Mudry MD (2016) Biomarkers of oxidative damage and antioxidant defense capacity in Caiman latirostris blood. Comp Biochem Physiol C Toxicol Pharmacol 179:29–36

    Article  CAS  Google Scholar 

  • Prabu SM, Shagirtha K, Renugadevi J (2011a) Quercetin in combination with vitamins (C and E) improve oxidative stress and hepatic injury in cadmium intoxicated rats. Biomed Prev Nutr 1(1):1–7

    Article  Google Scholar 

  • Prabu SM, Shagirtha K, Renugadevi J (2011b) Naringenin in combination with vitamins C and E potentially protects oxidative stress-mediated hepatic injury in cadmium-intoxicated rats. J Nutr Sci Vitaminol 57(2):177–185

    Article  CAS  Google Scholar 

  • Priscilla DH, Jayakumar M, Thirumurugan K (2015) Flavanone naringenin: An effective antihyperglycemic and antihyperlipidemic nutraceutical agent on high fat diet fed streptozotocin induced type 2 diabetic rats. J Funct Foods 14:363–373

    Article  CAS  Google Scholar 

  • Prusty AK, Kohli MPS, Sahu NP, Pal AK, Saharan N, Mohapatra S, Gupta SK (2011) Effect of short term exposure of fenvalerate on biochemical and haematological responses in Labeo rohita (Hamilton) fingerlings. Pest Biochem Phys 100(2):124–129

    Article  CAS  Google Scholar 

  • Qu R, Wang X, Wang Z, Wei Z, Wang L (2014) Metal accumulation and antioxidant defenses in the freshwater fish Carassius auratus in response to single and combined exposure to cadmium and hydroxylated multi-walled carbon nanotubes. J Hazard Mater 275:89–98

    Article  CAS  Google Scholar 

  • Rajendran P, Nandakumar N, Rengarajan T, Palaniswami R, Gnanadhas EN, Lakshminarasaiah U, Gopas J, Nishigaki I (2014) Antioxidants and human diseases. Clin Chim Acta 436:332–347

    Article  CAS  Google Scholar 

  • Renugadevi J, Prabu SM (2010) Cadmium-induced hepatotoxicity in rats and the protective effect of naringenin. Exp Toxicol Pathol 62(2):171–181

    Article  CAS  Google Scholar 

  • Serafim A, Company R, Lopes B, Fonseca VF, França S, Vasconcelos RP, Bebianno MJ, Cabral HN (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Indic 19:215–225

    Article  CAS  Google Scholar 

  • Shimada H, Takamure Y, Shimada A, Yasutake A, Waalkes MP, Imamura Y (2004) Strain differences of cadmium-induced hepatotoxicity in Wistar-Imamichi and Fischer 344 rats: involvement of cadmium accumulation. Toxicology 203(1–3):189–197

    Article  CAS  Google Scholar 

  • Stohs SJ, Bagachi D (1995) Oxidative mechanism in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Tamele IJ, Vázquez Loureiro P (2020) Lead, mercury and cadmium in fish and shellfish from the Indian Ocean and Red Sea (African Countries): Public health challenges. J Mar Sci Eng 8(5):1–33

    Article  Google Scholar 

  • Ural MŞ (2013) Chlorpyrifos-induced changes in oxidant/antioxidant status and haematological parameters of Cyprinus carpio carpio: ameliorative effect of lycopene. Chemosphere 90(7):2059–2064

    Article  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(2):178–189

    Article  CAS  Google Scholar 

  • Valko MMHCM, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208

    Article  CAS  Google Scholar 

  • van Acker FA, Schouten O, Haenen GR, van der Vijgh WJ, Bast A (2000) Flavonoids can replace α-tocopherol as an antioxidant. FEBS Lett 473(2):145–148

    Article  Google Scholar 

  • Verma Y, Rani V, Rana SVS (2020) Assessment of cadmium sulphide nanoparticles toxicity in the gills of a fresh water fish. Environ Nanotechnol Monit Manag 13:1–7

    Google Scholar 

  • Vieira LR, Gravato C, Soares AMVM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76(10):1416–1427

    Article  CAS  Google Scholar 

  • Vinodhini R, Narayanan M (2009) Biochemical changes of antioxidant enzymes in common carp (Cyprinus carpio L.) after heavy metal exposure. Turk J Vet Anim Sci 33(4):273–278

    CAS  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192(2–3):95–117

    Article  CAS  Google Scholar 

  • Wang J, Yang Z, Lin L, Zhao Z, Liu Z, Liu X (2012) Protective effect of naringenin against lead-induced oxidative stress in rats. Biol Trace Elem Res 146(3):354–359

    Article  CAS  Google Scholar 

  • Wen B, Jin SR, Chen ZZ, Gao JZ, Liu YN, Liu JH, Feng XS (2018) Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defence and innate immunity of the discus fish (Symphysodon aequifasciatus). Environ Pollut 243:462–471

    Article  CAS  Google Scholar 

  • Zeng H, Shao B, Zhuang J, Peng Y, Chen H, Yu Q, Xu C, Fu X, Zhou H, Cao Y, Yu X (2020) Naringenin reduces early brain injury in subarachnoid hemorrhage (SAH) mice: The role of the AMPK/SIRT3 signaling pathway. J Funct Foods 72(104043):1–13

    Google Scholar 

  • Zhang B, Wei YZ, Wang GQ, Li DD, Shi JS, Zhang F (2019) Targeting MAPK pathways by naringenin modulates microglia M1/M2 polarization in lipopolysaccharide-stimulated cultures. Front Cell Neurosci 12(531):1–11

    Google Scholar 

  • Ziech D, Franco R, Georgakilas AG, Georgakila S, Malamou-Mitsi V, Schoneveld O, Pappa A, Panayiotidis MI (2010) The role of reactive oxygen species and oxidative stress in environmental carcinogenesis and biomarker development. Chem Biol Interact 188(2):334–339

    Article  CAS  Google Scholar 

  • Zirong X, Shijun B (2007) Effects of waterborne Cd exposure on glutathione metabolism in Nile tilapia (Oreochromis niloticus) liver. Ecotoxicol Environ Saf 67(1):89–94

    Article  Google Scholar 

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Acknowledgements

The authors are thankful to the Chairperson, Department of Zoology, Panjab University, Chandigarh, for providing the necessary research facility, and DST INSPIRE, New Delhi, India, for providing financial assistance to carry out this work.

Funding

The research was funded by DST INSPIRE, New Delhi, India, as SRF to Sakshi Verma (IF120406).

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  1. Aquatic Biology Laboratory, Department of Zoology, Panjab University, Chandigarh, 160014, India

    Sakshi Verma & Rajinder Jindal

  2. Department of Zoology, Hans Raj Mahila Maha Vidyalaya, Jalandhar, 144008, Punjab, India

    Sakshi Verma

  3. Department of Zoology, Maharaja Agrasen University, Baddi, 174103, Himachal Pradesh, India

    Smriti Batoye

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Verma, S., Batoye, S. & Jindal, R. Protective efficacy of naringenin against cadmium-induced redox imbalance in Labeo rohita: an integrated biomarker approach. Environ Sci Pollut Res 29, 25591–25604 (2022). https://doi.org/10.1007/s11356-021-17703-z

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