Influence of Selected Natural Antioxidants on Iron-Induced Enzymatic Alterations Related to Oxidative Stress

Yıl 2024, Cilt: 45 Sayı: 2, 256 – 262, 30.06.2024

Melike Karaman , Emine Toraman

https://doi.org/10.17776/csj.1425012

Öz

Iron is required in various biological processes of the cell, but excess iron causes oxidative stress. Oxidative stress can be prevented by antioxidants with free radical scavenging properties. Tannic acid and gallic acid are phenolic compounds with antioxidant properties found naturally in plants. In this study, the effects of gallic acid and tannic acid on iron-induced oxidative stress parameters were investigated in a fruit fly model. Effect of the compounds against iron-induced oxidative stress were evaluated by determining spectrophotometrically superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) and acetylcholinesterase (AChE) enzyme activities, and levels of reduced glutathione (GSH) and malondialdehyde (MDA) in larvae (n: 10) and adults (n: 20) of wild type Oregon R strain of Drosophila melanogaster. Iron treatment decreased enzyme activities and GSH levels, but increased MDA levels. Co-treatment of these compounds with iron ameliorated iron-induced changes, especially in larvae. On the other hand, iron-induced decrease in AChE activity was increased in adults by treatment of these compounds with iron. The results showed that natural phenolic compounds have the potential to ameliorate iron-induced changes in oxidative stress parameters.

Anahtar Kelimeler

Antioxidant, Drosophila, Phenolic compound

Kaynakça

• [1] Gammella E., Recalcati S., Rybinska I., Buratti P., Cairo G., Iron-Induced Damage in Cardiomyopathy: Oxidative-Dependent and Independent Mechanisms, Oxid Med Cell Longev, 2015 (2015) 1–10.
• [2] Emerit J., Beaumont C., Trivin, F. Iron metabolism, free radicals, and oxidative injury, Biomedicine & Pharmacotherapy, 55 (2001) 333–339.
• [3] Fraga C., Iron toxicity and antioxidant nutrients, Toxicology, 180 (2002) 23–32.
• [4] Jomova K., Valko M., Importance of Iron Chelation in Free Radical-Induced Oxidative Stress and Human Disease, Curr. Pharm. Des., 17 (2011) 3460–3473.
• [5] Abbas M., Saeed F., Anjum F.M., Afzaal M., Tufail T., Bashir M.S., et al., Natural polyphenols: An overview, Int. J. Food Prop., 20 (2017) 1689–1699.
• [6] Andrade R.G., Dalvi L.T., Silva J.M.C., Lopes G.K.B., Alonso A., Hermes-Lima M., The antioxidant effect of tannic acid on the in vitro copper-mediated formation of free radicals, Arch. Biochem. Biophys, 437 (2005) 1–9.
• [7] Dong G., Liu H., Yu X., Zhang X., Lu H., Zhou T., et al., Antimicrobial and anti-biofilm activity of tannic acid against Staphylococcus aureus, Nat. Prod. Res., 32 (2018) 2225–2228.
• [8] Baldwin A., Booth B.W., Biomedical applications of tannic acid, J Biomater Appl, 36 (2022) 1503–1523.
• [9] Kaczmarek B., Tannic Acid with Antiviral and Antibacterial Activity as A Promising Component of Biomaterials—A Minireview, Materials, 13 (2020) 3224.
• [10] Badhani B., Sharma N., Kakkar R., Gallic acid: a versatile antioxidant with promising therapeutic and industrial applications, RSC Adv., 5 (2015) 27540–27557.
• [11] Al Zahrani N.A., El-Shishtawy R.M., Asiri A.M., Recent developments of gallic acid derivatives and their hybrids in medicinal chemistry: A review, Eur. J. Med. Chem., 204 (2020) 112609.
• [12] Bai J., Zhang Y., Tang C., Hou Y., Ai X., Chen X., et al., Gallic acid: Pharmacological activities and molecular mechanisms involved in inflammation-related diseases, Biomedicine & Pharmacotherapy, 133 (2021) 110985.
• [13] Vijaya Padma V., Sowmya P., Arun Felix T., Baskaran R., Poornima P., Protective effect of gallic acid against lindane induced toxicity in experimental rats, Food and Chemical Toxicology, 49 (2011) 991–998.
• [14] Akomolafe S.F., Akinyemi A.J., Anadozie S.O., Phenolic Acids (Gallic and Tannic Acids) Modulate Antioxidant Status and Cisplatin Induced Nephrotoxicity in Rats, Int. Sch. Res. Notices, 2014 (2014) 1–8.
• [15] Yesilkent E.N., Ceylan H., Investigation of the multi-targeted protection potential of tannic acid against doxorubicin-induced kidney damage in rats, Chem. Biol. Interact, 365 (2022) 110111.
• [16] Kizir D., Karaman M., Ceylan H., Tannic acid may ameliorate doxorubicin-induced changes in oxidative stress parameters in rat spleen, Naunyn Schmiedebergs Arch. Pharmacol., 396 (2023) 3605–3613.
• [17] Silva R.L. dos S., Lins T.L.B.G., Monte A.P.O. do, de Andrade K.O., de Sousa Barberino R., da Silva G.A.L., et al., Protective effect of gallic acid on doxorubicin-induced ovarian toxicity in mouse, Reproductive Toxicology, 115 (2023) 147–156.
• [18] Ong C., Yung L.Y.L., Cai Y., Bay B.H., Baeg G.H. Drosophila melanogaster as a model organism to study nanotoxicity. Nanotoxicology, 9 (2015) 396–403.
• [19] Read R.D. Drosophila melanogaster as a model system for human brain cancers, Glia, 59 (2011) 1364–1376.
• [20] Jafari M. Drosophila melanogaster as a model system for the evaluation of anti-aging compounds, Fly, 4 (2010) 253–257.
• [21] Gonzalez C. Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics, Nature Reviews Cancer, 13 (2013) 172–183.
• [22] Kaun K.R., Devineni A. V., Heberlein U. Drosophila melanogaster as a model to study drug addiction, Human Genetics, 131 (2012) 959–975.
• [23] Mirzoyan Z., Sollazzo M., Allocca M., Valenza A.M., Grifoni D. Bellosta, P. Drosophila melanogaster: A Model Organism to Study Cancer, Frontiers in Genetics, 10 (2019).
• [24] Bradford M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal Biochem., 72 (1976) 248–254.
• [25] Sun Y., Oberley L.W., Li Y., A simple method for clinical assay of superoxide dismutase., Clin. Chem., 34 (1988) 497–500.
• [26] Aebi H., [13] Catalase in vitro, In: Methods in Enzymology, (1984) 121–126.
• [27] Wendel A., [44] Glutathione peroxidase, In: Methods Enzymol, (1981) 325–333.
• [28] Ellman G.L., Courtney K.D., Andres V., Featherstone R.M., A new and rapid colorimetric determination of acetylcholinesterase activity, Biochem Pharmacol, 7 (1961) 88–95.
• [29] Sedlak J., Lindsay R.H., Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent, Anal Biochem, 25 (1968) 192–205.
• [30] Ohkawa H., Ohishi N., Yagi K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Anal Biochem, 95 (1979) 351–358.
• [31] Onuoha T., Akpafun A.S. Akpofure I.H. Effects of Heavy Metals on Soil and Water in Amai Delta State, Nigeria, Journal of Soil Science and Plant Physiology, 5 (2023) 1–5.
• [32] Valko M., Morris H., Cronin M., Metals, Toxicity and Oxidative Stress, Curr Med Chem, 12 (2005) 1161–1208.
• [33] Packer L., Weber S.U., Rimbach G., Molecular Aspects of α-Tocotrienol Antioxidant Action and Cell Signalling, J. Nutr., 131 (2001) 369S-373S.
• [34] Galleano M., Puntarulo S., Dietary α-tocopherol supplementation on antioxidant defenses after in vivo iron overload in rats, Toxicology, 124 (1997) 73–81.
• [35] Lucesoli F., Fraga C.G., Oxidative stress in testes of rats subjected to chronic iron intoxication and α-tocopherol supplementation, Toxicology, 132 (1999) 179–186.
• [36] Milchak L.M., Douglas Bricker J., The effects of glutathione and vitamin E on iron toxicity in isolated rat hepatocytes, Toxicol Lett., 126 (2002) 169–177.
• [37] Koyu A., Ozguner F., Caliskan S., Karaca H., Preventive effect of vitamin E on iron-induced oxidative damage in rabbit, Toxicol Ind. Health, 21 (2005) 239–242.
• [38] Siqueira E.M. de A., Marin A.M.F., da Cunha M. de S.B., Fustinoni A.M., de Sant’Ana L.P., Arruda S.F., Consumption of baru seeds [Dipteryx alata Vog.], a Brazilian savanna nut, prevents iron- induced oxidative stress in rats, Food Research International, 45 (2012) 427–433.
• [39] Sarkar R., Hazra B., Mandal N., Reducing power and iron chelating property of Terminalia chebula (Retz.) alleviates iron induced liver toxicity in mice, BMC Complement Altern Med., 12 (2012) 144.
• [40] Ghate N.B., Chaudhuri D., Das A., Panja S., Mandal N., An Antioxidant Extract of the Insectivorous Plant Drosera burmannii Vahl. Alleviates Iron-Induced Oxidative Stress and Hepatic Injury in Mice, PLoS One, 10 (2015) e0128221.
• [41] Aziza S.A.H., Azab M.E., El-Shall S.K., Ameliorating Role of Rutin on Oxidative Stress Induced by Iron Overload in Hepatic Tissue of Rats, Pakistan Journal of Biological Sciences, 17 (2014) 964–977.
• [42] Basu T., Panja S., Shendge A.K., Das A., Mandal N. A natural antioxidant, tannic acid mitigates iron‐overload induced hepatotoxicity in Swiss albino mice through ROS regulation, Environmental Toxicology, 33 (2018) 603–618.
• [43] Kerdsomboon K., Chumsawat W., Auesukaree C. Effects of Moringa oleifera leaf extracts and its bioactive compound gallic acid on reducing toxicities of heavy metals and metalloid in Saccharomyces cerevisiae, Chemosphere, 270 (2021) 128659.
• [44] Bermejo-Bescós P., Piñero-Estrada E., Villar del Fresno Á.M., Neuroprotection by Spirulina platensis protean extract and phycocyanin against iron-induced toxicity in SH-SY5Y neuroblastoma cells, Toxicology in Vitro, 22 (2008) 1496–1502.
• [45] Pohanka M., Copper, aluminum, iron and calcium inhibit human acetylcholinesterase in vitro, Environ Toxicol Pharmacol, 37 (2014) 455–459.
• [46] Perez V., Martins de Lima M., da Silva R., Dornelles A., Vedana G., Bogo M., et al., Iron Leads to Memory Impairment that is Associated with a Decrease in Acetylcholinesterase Pathways, Curr Neurovasc Res, 7 (2010) 15–22.
• [47] Halmenschelager P.T., da Rocha J.B.T., Biochemical CuSO4 Toxicity in Drosophila melanogaster Depends on Sex and Developmental Stage of Exposure, Biol Trace Elem. Res., 189 (2019) 574–585.
• [48] Ogienko A.A., Omelina E.S., Bylino O.V., Batin M.A., Georgiev P.G., Pindyurin A.V. Drosophila as a Model Organism to Study Basic Mechanisms of Longevity, International Journal of Molecular Sciences, 23 (2022) 11244.
• [49] Wangler M.F., Yamamoto S., Bellen H.J. Fruit Flies in Biomedical Research, Genetics, 199 (2015) 639–653.
• [50] Nainu F., Nakanishi Y., Shiratsuchi A. Fruit fly as a model organism in the study of human diseases and drug discovery, Journal of Center for Medical Education Sapporo Medical University, 10 (2019) 21–32.
• [51] Jafari M., Rose M.R. Rules for the use of model organisms in antiaging pharmacology, Aging Cell, 5 (2006) 17–22.

Yıl 2024, Cilt: 45 Sayı: 2, 256 – 262, 30.06.2024

Melike Karaman , Emine Toraman

https://doi.org/10.17776/csj.1425012

Öz

Kaynakça

• [1] Gammella E., Recalcati S., Rybinska I., Buratti P., Cairo G., Iron-Induced Damage in Cardiomyopathy: Oxidative-Dependent and Independent Mechanisms, Oxid Med Cell Longev, 2015 (2015) 1–10.
• [2] Emerit J., Beaumont C., Trivin, F. Iron metabolism, free radicals, and oxidative injury, Biomedicine & Pharmacotherapy, 55 (2001) 333–339.
• [3] Fraga C., Iron toxicity and antioxidant nutrients, Toxicology, 180 (2002) 23–32.
• [4] Jomova K., Valko M., Importance of Iron Chelation in Free Radical-Induced Oxidative Stress and Human Disease, Curr. Pharm. Des., 17 (2011) 3460–3473.
• [5] Abbas M., Saeed F., Anjum F.M., Afzaal M., Tufail T., Bashir M.S., et al., Natural polyphenols: An overview, Int. J. Food Prop., 20 (2017) 1689–1699.
• [6] Andrade R.G., Dalvi L.T., Silva J.M.C., Lopes G.K.B., Alonso A., Hermes-Lima M., The antioxidant effect of tannic acid on the in vitro copper-mediated formation of free radicals, Arch. Biochem. Biophys, 437 (2005) 1–9.
• [7] Dong G., Liu H., Yu X., Zhang X., Lu H., Zhou T., et al., Antimicrobial and anti-biofilm activity of tannic acid against Staphylococcus aureus, Nat. Prod. Res., 32 (2018) 2225–2228.
• [8] Baldwin A., Booth B.W., Biomedical applications of tannic acid, J Biomater Appl, 36 (2022) 1503–1523.
• [9] Kaczmarek B., Tannic Acid with Antiviral and Antibacterial Activity as A Promising Component of Biomaterials—A Minireview, Materials, 13 (2020) 3224.
• [10] Badhani B., Sharma N., Kakkar R., Gallic acid: a versatile antioxidant with promising therapeutic and industrial applications, RSC Adv., 5 (2015) 27540–27557.
• [11] Al Zahrani N.A., El-Shishtawy R.M., Asiri A.M., Recent developments of gallic acid derivatives and their hybrids in medicinal chemistry: A review, Eur. J. Med. Chem., 204 (2020) 112609.
• [12] Bai J., Zhang Y., Tang C., Hou Y., Ai X., Chen X., et al., Gallic acid: Pharmacological activities and molecular mechanisms involved in inflammation-related diseases, Biomedicine & Pharmacotherapy, 133 (2021) 110985.
• [13] Vijaya Padma V., Sowmya P., Arun Felix T., Baskaran R., Poornima P., Protective effect of gallic acid against lindane induced toxicity in experimental rats, Food and Chemical Toxicology, 49 (2011) 991–998.
• [14] Akomolafe S.F., Akinyemi A.J., Anadozie S.O., Phenolic Acids (Gallic and Tannic Acids) Modulate Antioxidant Status and Cisplatin Induced Nephrotoxicity in Rats, Int. Sch. Res. Notices, 2014 (2014) 1–8.
• [15] Yesilkent E.N., Ceylan H., Investigation of the multi-targeted protection potential of tannic acid against doxorubicin-induced kidney damage in rats, Chem. Biol. Interact, 365 (2022) 110111.
• [16] Kizir D., Karaman M., Ceylan H., Tannic acid may ameliorate doxorubicin-induced changes in oxidative stress parameters in rat spleen, Naunyn Schmiedebergs Arch. Pharmacol., 396 (2023) 3605–3613.
• [17] Silva R.L. dos S., Lins T.L.B.G., Monte A.P.O. do, de Andrade K.O., de Sousa Barberino R., da Silva G.A.L., et al., Protective effect of gallic acid on doxorubicin-induced ovarian toxicity in mouse, Reproductive Toxicology, 115 (2023) 147–156.
• [18] Ong C., Yung L.Y.L., Cai Y., Bay B.H., Baeg G.H. Drosophila melanogaster as a model organism to study nanotoxicity. Nanotoxicology, 9 (2015) 396–403.
• [19] Read R.D. Drosophila melanogaster as a model system for human brain cancers, Glia, 59 (2011) 1364–1376.
• [20] Jafari M. Drosophila melanogaster as a model system for the evaluation of anti-aging compounds, Fly, 4 (2010) 253–257.
• [21] Gonzalez C. Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics, Nature Reviews Cancer, 13 (2013) 172–183.
• [22] Kaun K.R., Devineni A. V., Heberlein U. Drosophila melanogaster as a model to study drug addiction, Human Genetics, 131 (2012) 959–975.
• [23] Mirzoyan Z., Sollazzo M., Allocca M., Valenza A.M., Grifoni D. Bellosta, P. Drosophila melanogaster: A Model Organism to Study Cancer, Frontiers in Genetics, 10 (2019).
• [24] Bradford M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal Biochem., 72 (1976) 248–254.
• [25] Sun Y., Oberley L.W., Li Y., A simple method for clinical assay of superoxide dismutase., Clin. Chem., 34 (1988) 497–500.
• [26] Aebi H., [13] Catalase in vitro, In: Methods in Enzymology, (1984) 121–126.
• [27] Wendel A., [44] Glutathione peroxidase, In: Methods Enzymol, (1981) 325–333.
• [28] Ellman G.L., Courtney K.D., Andres V., Featherstone R.M., A new and rapid colorimetric determination of acetylcholinesterase activity, Biochem Pharmacol, 7 (1961) 88–95.
• [29] Sedlak J., Lindsay R.H., Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent, Anal Biochem, 25 (1968) 192–205.
• [30] Ohkawa H., Ohishi N., Yagi K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Anal Biochem, 95 (1979) 351–358.
• [31] Onuoha T., Akpafun A.S. Akpofure I.H. Effects of Heavy Metals on Soil and Water in Amai Delta State, Nigeria, Journal of Soil Science and Plant Physiology, 5 (2023) 1–5.
• [32] Valko M., Morris H., Cronin M., Metals, Toxicity and Oxidative Stress, Curr Med Chem, 12 (2005) 1161–1208.
• [33] Packer L., Weber S.U., Rimbach G., Molecular Aspects of α-Tocotrienol Antioxidant Action and Cell Signalling, J. Nutr., 131 (2001) 369S-373S.
• [34] Galleano M., Puntarulo S., Dietary α-tocopherol supplementation on antioxidant defenses after in vivo iron overload in rats, Toxicology, 124 (1997) 73–81.
• [35] Lucesoli F., Fraga C.G., Oxidative stress in testes of rats subjected to chronic iron intoxication and α-tocopherol supplementation, Toxicology, 132 (1999) 179–186.
• [36] Milchak L.M., Douglas Bricker J., The effects of glutathione and vitamin E on iron toxicity in isolated rat hepatocytes, Toxicol Lett., 126 (2002) 169–177.
• [37] Koyu A., Ozguner F., Caliskan S., Karaca H., Preventive effect of vitamin E on iron-induced oxidative damage in rabbit, Toxicol Ind. Health, 21 (2005) 239–242.
• [38] Siqueira E.M. de A., Marin A.M.F., da Cunha M. de S.B., Fustinoni A.M., de Sant’Ana L.P., Arruda S.F., Consumption of baru seeds [Dipteryx alata Vog.], a Brazilian savanna nut, prevents iron- induced oxidative stress in rats, Food Research International, 45 (2012) 427–433.
• [39] Sarkar R., Hazra B., Mandal N., Reducing power and iron chelating property of Terminalia chebula (Retz.) alleviates iron induced liver toxicity in mice, BMC Complement Altern Med., 12 (2012) 144.
• [40] Ghate N.B., Chaudhuri D., Das A., Panja S., Mandal N., An Antioxidant Extract of the Insectivorous Plant Drosera burmannii Vahl. Alleviates Iron-Induced Oxidative Stress and Hepatic Injury in Mice, PLoS One, 10 (2015) e0128221.
• [41] Aziza S.A.H., Azab M.E., El-Shall S.K., Ameliorating Role of Rutin on Oxidative Stress Induced by Iron Overload in Hepatic Tissue of Rats, Pakistan Journal of Biological Sciences, 17 (2014) 964–977.
• [42] Basu T., Panja S., Shendge A.K., Das A., Mandal N. A natural antioxidant, tannic acid mitigates iron‐overload induced hepatotoxicity in Swiss albino mice through ROS regulation, Environmental Toxicology, 33 (2018) 603–618.
• [43] Kerdsomboon K., Chumsawat W., Auesukaree C. Effects of Moringa oleifera leaf extracts and its bioactive compound gallic acid on reducing toxicities of heavy metals and metalloid in Saccharomyces cerevisiae, Chemosphere, 270 (2021) 128659.
• [44] Bermejo-Bescós P., Piñero-Estrada E., Villar del Fresno Á.M., Neuroprotection by Spirulina platensis protean extract and phycocyanin against iron-induced toxicity in SH-SY5Y neuroblastoma cells, Toxicology in Vitro, 22 (2008) 1496–1502.
• [45] Pohanka M., Copper, aluminum, iron and calcium inhibit human acetylcholinesterase in vitro, Environ Toxicol Pharmacol, 37 (2014) 455–459.
• [46] Perez V., Martins de Lima M., da Silva R., Dornelles A., Vedana G., Bogo M., et al., Iron Leads to Memory Impairment that is Associated with a Decrease in Acetylcholinesterase Pathways, Curr Neurovasc Res, 7 (2010) 15–22.
• [47] Halmenschelager P.T., da Rocha J.B.T., Biochemical CuSO4 Toxicity in Drosophila melanogaster Depends on Sex and Developmental Stage of Exposure, Biol Trace Elem. Res., 189 (2019) 574–585.
• [48] Ogienko A.A., Omelina E.S., Bylino O.V., Batin M.A., Georgiev P.G., Pindyurin A.V. Drosophila as a Model Organism to Study Basic Mechanisms of Longevity, International Journal of Molecular Sciences, 23 (2022) 11244.
• [49] Wangler M.F., Yamamoto S., Bellen H.J. Fruit Flies in Biomedical Research, Genetics, 199 (2015) 639–653.
• [50] Nainu F., Nakanishi Y., Shiratsuchi A. Fruit fly as a model organism in the study of human diseases and drug discovery, Journal of Center for Medical Education Sapporo Medical University, 10 (2019) 21–32.
• [51] Jafari M., Rose M.R. Rules for the use of model organisms in antiaging pharmacology, Aging Cell, 5 (2006) 17–22.

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