Protective effect of curcumin against perfluorooctane sulfonate induced oxidative stress

Abstract

Background and Aims: The potential effects of perfluorooctane sulfonate (PFOS) on the environment and human health have aroused great concerns in recent years. To our knowledge, there are limited studies related with the effect of curcumin on PFOS induced damage in the literature. The existing studies are focused on DNA damage. No study has been found examining the effect on the antioxidant system. We planned this study to investigate the impact of curcumin on the antioxidant defense system response in rats exposed to PFOS. Methods: The animals were divided into six groups, with the first group used as control. Groups II to VI were orally treated with curcumin (80 mg/kg), PFOS (1.25 mg/kg), PFOS (1.25 mg/kg) + curcumin, PFOS (2.5 mg/kg), and PFOS (2.5 mg/kg) + curcumin daily for 30 days, respectively. For oxidative stress, liver, kidney, and brain samples were homogenized. The activities of antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT) activities, and malondialdehyde (MDA) content were determined. Data from the experiments were statistically analyzed by SPSS 11.0 program. Results: Our data showed that PFOS increased MDA level, while the activities of SOD and CAT decreased. It was observed that the application of curcumin together with PFOS decreased the MDA level and increased the antioxidant enzyme activities. Conclusion: As an antioxidant, curcumin plays an important protective role against oxidative damage and inhibits PFOS-induced lipid peroxidation.

Keywords

• Curcumin
• perfluorooctane sulfonate
• antioxidant
• oxidative stress
• lipid peroxidati

References

1. Aebi, H. (1984). Catalase in vitro. Methods in enzymology. 105, 121 126. https://doi.org/10.1016/s0076-6879(84)05016-3 google scholar
2. Abudayyak, M., Öztaş, E., & Özhan, G. (2021). Determination of Per-flourooctanoic Acid Toxicity in a Human Hepatocarcinoma. Cell Line. Health Pollut. 11(31), 210909. https://doi.org/10.5696/2156-9614-11.31.210909. google scholar
3. Agarwal, B.A., Jain, S., Agarwal, N.K., Mediratta, P.K., & Sharma, K.K. (2011). Modulation of pentylenetetrazole-induced kindling and oxidative stress by curcumin in mice. Phytomedicine, 18(8-9), 756759. https://doi.org/10.1016/j.phymed.2010.11.007 google scholar
4. AL-Harbi, M.S., Hamza, R.Z., & Dwary, A.A. (2014). Ameliorative effect of selenium and curcumin on sodium fluoride induced hepatotoxicity and oxidative stress in male mice. Journal of Chemical and Pharmaceutical Research, 6(4), 984-998. https://doi. org/10.1016/S2222-1808(14)60771-4 google scholar
5. Adonaylo, V.N., & Oteiza, P.I. (1999). Lead intoxication: antioxidant defenses and oxidative damage in rat brain. Toxicology, 135(2-3), 77-85. https://doi.org/10.1016/S0300-483X(99)00051-7 google scholar
6. Beesoon, S., & Martin, J.W. (2015). Isomer-specific binding affin-ity of perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) to serum proteins. Environmental Science & Technology, 49 (9), 5722-5731. https://doi.org/10.1021/es505399w google scholar
7. Bright, J.J. (2007). Curcumin and autoimmune disease. Advances in Experimental Medicine and Biology, 595, 425-51. https://doi. org/10.1007/978-0-387-46401-5_19 google scholar
8. Ceccatelli, S., Cottrill, B., Dinovi, M., Edler, L., Grasl-Kraupp, B., Hog-strand, C,... Schwerdtle, T. (2018). Risk to human health related to the presence of perfluorooctane sulfonic acid and perfluoroocta-noic acid in food. European Food Safety Authority Journal, 16 (12), e05194. https://doi.org/10.2903/j.efsa.2018.5194 google scholar

9. Comporti, M. (1989). Three models of free radical-induced cell injury. Chemico- Biological Interactions, 72(1-2), 1-56. https://doi. org/10.1016/0009-2797(89)90016-1 google scholar
10. Dai, C., Tang, S., Li, D., Zhao, K., & Xiao, X. (2015). Curcumin attenu-ates quinocetone- induced oxidative stress and genotoxicity in human hepatocyte L02 cells. Toxicology Mechanisms and Meth-ods, 25(4), 340-346. https://doi.org/10.3109/15376516.2015.1045 659 google scholar
11. Damiano, S., Longobardi, C., Andretta, E., Prisco, F., Piegari, G., Squillacioti, C.,...Ciarcia, R. (2021). Antioxidative effects of cur-cumin on the hepatotoxicity ınduced by ochratoxin a in rats. Antioxidants, 10(1), 125. https://doi.org/10.3390/antiox10010125 google scholar
12. Dikmen, M., Kaya-Tilki, E., Engur, S., & Ozturk, Y. (2017). Neuritogen-ic activity of epigallocatechin gallate and curcumin combination on rat adrenal pheochromocytoma cells. Fresenius Environmental Bulletin, 26(7), 4726-4733. google scholar
13. Dhore, R., & Murthy, G.S. (2021). Per/polyfluoroalkyl substances production, applications and environmental impacts. Bio-resource Technology, 341, 125808. https://doi.org/10.1016/j. biortech.2021.125808 google scholar
14. Dorts, J., Kestemont, P,, Marchand, PA, D’Hollander, W., Thezenas, M. L., Raes, M., & Silvesre, F. (2011). Ecotoxicoproteomics in gills of the sentinel fish species, Cottus gobio, exposed to perfluorooc-tane sulfonate (PFOS). Aquatic Toxicology, 103(1-2), 1-8. https:// doi.org/10.1016/j.aquatox.2011.01.015 google scholar
15. Edrees, N.E., Galal, A.A.A., Monaem, A.R.A., Beheiry, R.R., & Met-wally, M.M.M. (2008). Curcumin alleviates colistin-induced neph-rotoxicity and neurotoxicity in rats via attenuation of oxidative stress, inflammation and apoptosis. Chemico-Biological Interac-tions, 294, 56-64. https://doi.org/10.1016/j.cbi.2018.08.012 google scholar
16. Eke, D., & Çelik, A. (2016). Curcumin prevents perfluorooctane sulfonate induced genotoxicity and oxidative DNA damage in rat peripheral blood. Drug and Chemical Toxicology, 39(1), 97-103. https://doi.org/10.3109/01480545.2015.1041601 google scholar
17. El-Hack, M.E.A., El-Saadony, M.T, Swelum, A.A., Arif, M., Ghanima, M.M.A., Shukry, M., Noreldin, A., Taha, AE., & El-Tarabilyi, K.A. (2021). Curcumin, the active substance of turmeric: its effects on health and ways to improve its bioavailability. Journal of the Science of Food and Agriculture, 101, 5747-762. https://doi. org/10.1002/jsfa.11372 google scholar
18. Endirlik, B., & Gürbay, A. (2018). Perflorooktanoik asit: Maruziyet yolları, toksikokinetik özellikleri ve insan sağlığı üzerindeki etkileri. Journal of Pharmacetical Sciences, 43(2), 135-156. google scholar
19. Eybl, V., Kotyzova, D., & Bludovska, M. (2004). The effect of curcum-in on cadmium-induced oxidative damage and trace elements level in the liver of rats and mice. Toxicology Letters, 151(1),79-85. https://doi.org/10.1016/j.toxlet.2004.02.019 google scholar
20. Farzaei, M.H., Zobeiri, M., Parvizi, F., El-Senduny, F. F., Marmouzi, I., Coy-Barrera, E.,...Abdollahi, M . (2018). Curcumin in Liver Diseas-es: A systematic review of the cellular mechanisms of oxidative stress and clinical perspective. Nutrients, 10(7), 855. https://doi. org/10.3390/nu10070855 google scholar
21. Fu, Y., Zheng, S., Lin, J., Ryerse, J., & Chen, A. (2008). Curcumin protects the rat liver from CCl4-caused injury and fibrogenesis by attenuating oxidative stress and suppressing inflammation. Molecular Pharmacology,73(2), 399-409. https://doi.org/10.1124/ mol.107.039818 google scholar
22. Garda-Nino, W.R., & Pedraza-Chavem, J. (2014). Protective effect of cur-cumin against heavy metals-induced liver damage. Food and Chemical Toxicology, 69, 182-201. https://doi.org/10.1016/j.fct.2014.04.016 google scholar
23. Grasl-Kraupp, B., Hogstrand, C., Hoogenboom, L., Leblanc, J.C., Nebbia, C.S., Nielsen, E.,.Schwerdtle T. (2020) Risk to human 164 health related to the presence of perfluoroalkyl substances in food. European Food Safety Authority Journal, 18(9), 6223. https:// doi.org/10.2903/j.efsa.2020.6223 google scholar
24. Hosseini, A., & Hosseinzadeh, H. (2018), Antidotal or protective effects of Curcuma longa (turmeric) and its active ingredient, cur-cumin, against natural and chemical toxicities: A review. Biomedi-cine & Pharmacotherapy, 99, 411-421. https://doi.org/10.1016/j. biopha.2018.01.072 google scholar
25. Kanwal, Z., Raza, M. A., Manzoor, F., Riaz, S., Jabeen, G., Fatima, S., & Naseem, S. (2019). A Comparative Assessment of Nanotoxicity Induced by Metal (Silver, Nickel) and Metal Oxide (Cobalt, Chro-mium) Nanoparticles in Labeo rohita. Nanomaterials (Basel), 9(2), 309. https://doi.org/10.3390/nano9020309 google scholar
26. Lee, YC.G., Chou, HC., Chen, YT., Tung, SY., Ko, TL., Buyandelger B., Wen, LL., & Juan, SH. (2022). L-Carnitine reduces reactive oxy-gen species/endoplasmic reticulum stress and maintains mito-chondrial function during autophagy-mediated cell apoptosis in perfluorooctanesulfonate-treated renal tubular cells. Scientifc Reports, 12, 4673 https://doi.org/10.1038/s41598-022-08771-3 google scholar
27. Long, Y., Wang, Y., Ji, G., Yan, L., Hu, F., & Gu, A. (2013). Neurotoxicity of perfluorooctane sulfonate to hippocampal cells in adult mice. PLoS One, 8(1): e54176. https://doi.org/10.1371/journal.pone.0054176 google scholar
28. Lopez-Doval, S., Salgado, R., Pereiro, N., Moyano, R., & Lafuente, A. (2014). Perfluorooctane sulfonate effects on the reproductive axis in adult male rats. Environmental Research, 134, 158-168. https:// doi.org/ 10.1016/j.envres.2014.07.006. google scholar
29. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265-275. https://doi.org/10.1016/ S0021-9258(19)52451-6 google scholar
30. Maheshwari, R. K., Singh, A. K., Gaddipati, J., & Srimal, R. C. (2006). Multiple biological activities of curcumin: A short review. Life Sci-ences, 78(18), 2081-2087. https://doi.org/10.1016/j.lfs.2005.12.007 google scholar
31. Mandour, D. A., Maher, I., Abd El, M. A., & Moawad, R. S. (2022). Quercetin ameliorated Perfluorooctane Sulphonate-Induced he-patic toxicity in adult male albino rats (biochemical, histological and immunohistochemical study). Egyptian Journal of Histology. (in press). https://doi.org/10.21608/ejh.2022.1391.1685 google scholar
32. Moghaddam, A. H., Nabavi, S. F., Nabavi, S. M., Loizzo, M. R., Rooh-bakhsh, A., & Setzer, W.N. (2015). Ameliorative effects of curcumin against sodium fluoride induced hepatotoxicity. Progress in Nutri-tion, 17(4), 324-330. google scholar
33. Pachkowski, B., Post, G. B., & Stern, A. H. (2019). The derivation of a Reference Dose (RfD) for perfluorooctane sulfonate (PFOS) based on immune suppression. Environmental Research, 171, 452-469. doi: 10.1016/j.envres.2018.08.004. google scholar
34. Park, E. J., Jeon, C. H., Ko, G., Kim, J., & Sohn, D. H. (2000). Protective effect of curcumin in rat liver injury induced by carbon tetrachlo-ride. The Journal of Pharmacy and Pharmacology, 52(4), 437-440. https://doi.org/10.1211/0022357001774048 google scholar
35. Rathore, S., Mukim, M., Sharma, P., Devi, S., Nagar, J. C., & Khalid, M. (2020). Curcumin: A Review for Health Benefits Kingdom of Saudi Arabia. International Journal of Research and Review, 7 (1), 273-290. google scholar
36. Reyes-Gordillo, K., Segovia, J., Shibayama, M., Vergara, P., Moreno, M. G., & Muriel, P. (2007). Curcumin protects against acute liver damage in the rat by inhibiting NF-kB, proinflammatory cytokines production and oxidative stress. Biochimica et Biophysica Acta, 1770 (6), 989-996. https://doi.org/10.1016/j.bbagen.2007.02.004 google scholar
37. Qin, W.,Ren, X., Zhao, L., Guo L. (2022). Exposure to perfluorooc-tanesulfonate reduced cell viability and insulin release capacity of p cells. Journal of Environmental Sciences, 1 15, 162-172. https:// doi.org/10.1016/j.jes.2021.07.004 google scholar
38. Qin X. D., Qian Z., Dharmage S. C., Perret J., Geiger S. E., Rigdon S.,.Dong G. H. (2017). Association of perfluoroalkyl substances exposure with impaired lung function in children.Environmental Research, 155, 15-21. https://doi.org/10.1016/j.envres.2017.01.025 google scholar
39. Saikat, S., Kreis, I., Davies, B., Bridgman, S., & Kamanyire, R. (2013). The impact of PFOS on health in the general population: a re-view. Environmental Science: Processes & Impacts 5(2), 329-35. doi: 10.1039/c2em30698k. google scholar
40. Sankar, P., Telang, A.G., & Manimaran, A. (2018). Protective effect of curcumin on cypermethrin-induced oxidative stress in Wistar rats. Nutrients, 64(5), 487-493. https://doi.org/10.3390/nu10070855 google scholar
41. Singh, R., & Sharma, P. (2011). Hepatoprotective effect of curcumin on lindane-induced oxidative stress in male Wistar Rats. Toxicol-ogy International, 18(2), 124-129. https://doi.org/10.4103/0971-6580.84264 google scholar
42. Sun, Y., Oberley, L. W., & Li, Y. (1988). A simple method for clinical assay of superoxide dismutase. Clinical Chemistry, 34, 497-500. google scholar
43. Tang, L., Yu, J., Zhuge, S., Chen, H., Zhang, L., & Jiang, G. (2022). Oxidative stress and Cx43-mediated apoptosis are involved in PFOS-induced nephrotoxicity, Toxicology, 478, 153283. https:// doi.org/10.1016/j.tox.2022.153283 google scholar
44. Tapia, E., Sanchez-Lozada, L. G., Garcia-Nino, W. R., Garcia, E., Ce-recedo, A., Garcia-Arroyo, F. E,...Pedraza-Chaverr(, J. (2014). Cur-cumin prevents maleate-induced nephrotoxicity: Relation to hemodynamic alterations, oxidative stress, mitochondrial oxygen consumption, and activity of respiratory complex I. Free Radical Research, 48(11), 1342-1354. https://doi.org/10.3109/10715762.2 014.954109 google scholar
45. Tsuda, S. (2016). Differential toxicity between perfluorooc-tane sulfonate (PFOS) and perfluorooctanoic acid (PFOA). The Journal of Toxicological Sciences, 41(Special), 27-36. https://doi. org/10.2131/jts.41.SP27 google scholar
46. Torres, L., Redko, A., Limper, C., Imbiakha, B., Chang, S., & August, A. (2021). Effect of Perfluorooctanesulfonic acid (PFOS) on immune cell development and function in mice. Immunology Letters, 233, 31-41. https://doi.org/10.1016/j.imlet.2021.03.006 google scholar
47. Wang, G., Sun, S., Wu, X., Yang, S., Wu, Y., Zhao, J., Zhang, H., Chen W. (2020). Intestinal environmental disorders associate with the tissue damages induced by perfluorooctane sulfonate exposure. Ecotoxicology and Environmental Safety, 197 110590. https://doi. org/10.1016/j.ecoenv.2020.110590 google scholar
48. Wang, P., Liu, D., Yan, S., Cui, J., Liang, Y., & Ren, S. (2022). Adverse effects of perfluorooctane sulfonate on the liver and relevant mechanisms. Toxics, 10(5), 265. doi: 10.3390/toxics10050265. google scholar
49. Wen, L., Chen, YT., Lee, YC. G., Ko, TL, Chou, H-C., & Juan, SH. (2021). Perfluorooctane sulfonate induces autophagy-associated apop-tosis through oxidative stress and the activation of extracellular signal-regulated kinases in renal tubular cells. PLoS ONE 16 (1): e0245442. https://doi.org/10.1371/journal.pone.0245442 google scholar
50. Wiels0e, M., Long, M. H., Ghisari, M., & Bonefeld-Jorgensen, E. C. (2015). Perfluoroalkylated substances (PFAS) affect oxidative stress biomarkers in vitro. Chemosphere, 129, 239-245, 10.1016/j. chemosphere.2014.10.014 google scholar
51. Xing, J., Wang, G., Zhao, J., Wang, E., Yin, B., Fang, D.,...Chen, W. (2016). Toxicity assessment of perfluorooctane sulfonate using acute and subchronic male C57BL/6J mouse models. Environ-mental Pollution, 210, 388-396. https://doi.org/10.1016/j.en-vpol.2015.12.008 google scholar
52. Xu, C., Jiang, Z. Y., Liu, Q., Liu, H., & Gu, A. (2017). Estrogen recep-tor beta mediates hepatotoxicity induced by perfluorooctane sulfonate in Mouse. Environmental Science and Pollution Research, 24, 13414-13423. https://doi.org/10.1007/s11356-017-8943-3. google scholar
53. Xu, D., Li, C., Wen, Y., & Liu, W. (2013). Antioxidant defense system responses and DNA damage of earthworms exposed to Perfluo-rooctane sulfonate (PFOS). Environmental Pollution, 174, 121-127. https://doi.org/10.1016/j.envpol.2012.10.030 google scholar
54. Xu, X.Y., Meng, X., Li, S., Gan, R.Y., Li, Y., & Li, H.B. (2018). Bioactivity, health benefits, and related molecular mechanisms of curcumin: Current progress, challenges, and perspectives. Nutrients, 10(10), 1553. https://doi.org/10.3390/nu10101553 google scholar
55. Yagi, K., Nishigaki, I., & Ohama, H. (1968). Measurement of serum TBA value. Vitamin, 37, 105-112. google scholar
56. Zheng, L, Dong, G. H., Jin, Y. H., & He, Q. C. (2009). Immunotoxic changes associated with a 7-day oral exposure to perfluorooc-tanesulfonate (PFOS) in adult male C57BL/6 mice. Archives of Toxi-cology, 83(7):679-89. https://doi.org/10.1007/s00204-008-0361-3. google scholar
57. Zhang, L., Lei, C., Chen, J., Yang, K., Zhu, L., & Lin, D. (2015). Effect of natural and synthetic surface coatings on the toxicity of mul-tiwalled carbon nanotubes toward green algae. Carbon, 83, 198207, 10.1016/j.carbon.2014.11.050 google scholar