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23.05.2022

Hesperidin Attenuates Oxidative Stress, Inflammation, Apoptosis, and Cardiac Dysfunction in Sodium Fluoride‐Induced Cardiotoxicity in Rats

verfasst von: Behçet Varışlı, Ekrem Darendelioğlu, Cuneyt Caglayan, Fatih Mehmet Kandemir, Adnan Ayna, Aydın Genç, Özge Kandemir

Erschienen in: Cardiovascular Toxicology | Ausgabe 8/2022

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Abstract

Excessive fluoride intake has been reported to cause toxicities to brain, thyroid, kidney, liver and testis tissues. Hesperidin (HSP) is an antioxidant that possesses anti-allergenic, anti-carcinogenic, anti-oxidant and anti-inflammatory activities. Presently, the studies focusing on the toxic effects of sodium fluoride (NaF) on heart tissue at biochemical and molecular level are limited. This study was designed to evaluate the ameliorative effects of HSP on toxicity of NaF on the heart of rats in vivo by observing the alterations in oxidative injury markers (MDA, SOD, CAT, GPX and GSH), pro-inflammatory markers (NF-κB, IL-1β, TNF-α), expressions of apoptotic genes (caspase-3, -6, -9, Bax, Bcl-2, p53, cytochrome c), levels of autophagic markers (Beclin 1, LC3A, LC3B), expression levels of PI3K/Akt/mTOR and cardiac markers. HSP treatment attenuated the NaF-induced heart tissue injury by increasing activities of SOD, CAT and GPx and levels of GSH, and suppressing lipid peroxidation. In addition, HSP reversed the changes in expression of apoptotic (caspase-3, -6, -9, Bax, Bcl-2, p53, cytochrome c), levels of autophagic and inflammatory parameters (Beclin 1, LC3A, LC3B, NF-κB, IL-1β, TNF-α), in the NaF-induced cardiotoxicity. HSP also modulated the gene expression levels of PI3K/Akt/mTOR signaling pathway and levels of cardiac markers (LDH, CK-MB). Overall, these findings reveal that HSP treatment can be used for the treatment of NaF-induced cardiotoxicity.

Caron, S. (2020). Where does the fluorine come from? A review on the challenges associated with the synthesis of organofluorine compounds. Organic Process Research & Development, 24, 470–480. https://doi.org/10.1021/acs.oprd.0c00030CrossRef

James, P., Harding, M., Beecher, T., Browne, D., Cronin, M., Guiney, H., O’Mullane, D., & Whelton, H. (2020). Impact of reducing water fluoride on dental caries and fluorosis. Journal of Dental Research, 100, 507–514. https://doi.org/10.1177/0022034520978777CrossRefPubMed

Solanki, Y. S., Agarwal, M., Maheshwari, K., Gupta, S., Shukla, P., & Gupta, A. B. (2021). Removal of fluoride from water by using a coagulant (inorganic polymeric coagulant). Environmental Science and Pollution Research, 28, 3897–3905. https://doi.org/10.1007/s11356-020-09579-2CrossRefPubMed

Caglayan, C., Kandemir, F. M., Darendelioğlu, E., Küçükler, S., & Ayna, A. (2021). Hesperidin protects liver and kidney against sodium fluoride-induced toxicity through anti-apoptotic and anti-autophagic mechanisms. Life Sciences, 281, 119730. https://doi.org/10.1016/j.lfs.2021.119730CrossRefPubMed

Pal, P., & Mukhopadhyay, P. K. (2021). Fluoride induced testicular toxicities in adult Wistar rats. Toxicology Mechanisms and Methods, 31, 383–392. https://doi.org/10.1080/15376516.2021.1891489CrossRefPubMed

Oyagbemi, A. A., Omobowale, T. O., Ola-Davies, O. E., Asenuga, E. R., Ajibade, T. O., Adejumobi, O. A., Afolabi, J. M., Ogunpolu, B. S., Falayi, O. O., Saba, A. B., Adedapo, A. A., & Yakubu, M. A. (2018). Luteolin-mediated Kim-1/NF-kB/Nrf2 signaling pathways protects sodium fluoride-induced hypertension and cardiovascular complications. BioFactors, 44, 518–531. https://doi.org/10.1002/biof.1449CrossRefPubMed

Atmaca, N., Atmaca, H. T., Kanici, A., & Anteplioglu, T. (2014). Protective effect of resveratrol on sodium fluoride-induced oxidative stress, hepatotoxicity and neurotoxicity in rats. Food and Chemical Toxicology, 70, 191–197. https://doi.org/10.1016/j.fct.2014.05.011CrossRefPubMed

Akinrinde, A. S., Tijani, M., Awodele, O. A., & Oyagbemi, A. A. (2021). Fluoride-induced hepatotoxicity is prevented by L-Arginine supplementation via suppression of oxidative stress and stimulation of nitric oxide production in rats. Toxicology and Environmental Health Sciences, 13, 57–64. https://doi.org/10.1007/s13530-020-00070-6CrossRef

Özbolat, S. N., & Ayna, A. (2021). Chrysin suppresses HT-29 cell death induced by diclofenac through apoptosis and oxidative damage. Nutrition and Cancer, 73, 1419–1428. https://doi.org/10.1080/01635581.2020.1801775CrossRefPubMed

10.

Gulcin, İ. (2020). Antioxidants and antioxidant methods: An updated overview. Archives of toxicology, 94, 651–715. https://doi.org/10.1007/s00204-020-02689-3CrossRefPubMed

11.

Jucá, M. M., Cysne Filho, F. M. S., de Almeida, J. C., Mesquita, D. D. S., Barriga, J. R. D. M., Dias, K. C. F., Barbosa, T. M., Vasconcelos, L. C., Leal, L. K. A. M., Ribeiro, J. E., & Vasconcelos, S. M. M. (2020). Flavonoids: biological activities and therapeutic potential. Natural Product Research, 34, 692–705. https://doi.org/10.1080/14786419.2018.1493588CrossRefPubMed

12.

Kuzu, M., Kandemir, F. M., Yıldırım, S., Çağlayan, C., & Küçükler, S. (2021). Attenuation of sodium arsenite-induced cardiotoxicity and neurotoxicity with the antioxidant, anti-inflammatory, and antiapoptotic effects of hesperidin. Environmental Science and Pollution Research, 28, 10818–10831. https://doi.org/10.1007/s11356-020-11327-5CrossRefPubMed

13.

Caglayan, C., Demir, Y., Kucukler, S., Taslimi, P., Kandemir, F. M., & Gulçin, İ. (2019). The effects of hesperidin on sodium arsenite-induced different organ toxicity in rats on metabolic enzymes as antidiabetic and anticholinergics potentials: a biochemical approach. Journal of Food Biochemistry, 43, e12720. https://doi.org/10.1111/jfbc.12720CrossRefPubMed

14.

Shi, X., Niu, L., Zhao, L., Wang, B., Jin, Y., & Li, X. (2018). The antiallergic activity of flavonoids extracted from Citri Reticulatae Pericarpium. Journal of Food Processing and Preservation, 42, e13588. https://doi.org/10.1111/jfpp.13588CrossRef

15.

Pandey, P., & Khan, F. (2021). A mechanistic review of the anticancer potential of hesperidin, a natural flavonoid from citrus fruits. Nutrition Research, 92, 21–31. https://doi.org/10.1016/j.nutres.2021.05.011CrossRefPubMed

16.

Küçükler, S., Çomaklı, S., Özdemir, S., Çağlayan, C., & Kandemir, F. M. (2021). Hesperidin protects against the chlorpyrifos-induced chronic hepato-renal toxicity in rats associated with oxidative stress, inflammation, apoptosis, autophagy, and up-regulation of PARP-1/VEGF. Environmental Toxicology, 36, 1600–1617. https://doi.org/10.1002/tox.23156CrossRefPubMed

17.

Turk, E., Kandemir, F. M., Yildirim, S., Caglayan, C., Kucukler, S., & Kuzu, M. (2019). Protective effect of hesperidin on sodium arsenite-induced nephrotoxicity and hepatotoxicity in rats. Biological Trace Element Research, 189, 95–108. https://doi.org/10.1007/s12011-018-1443-6CrossRefPubMed

18.

Umarani, V., Muvvala, S., Ramesh, A., Lakshmi, B. V., & Sravanthi, N. (2015). Rutin potentially attenuates fluoride-induced oxidative stress-mediated cardiotoxicity, blood toxicity and dyslipidemia in rats. Toxicology Mechanism and Methods, 25, 143–149. https://doi.org/10.3109/15376516.2014.1003359CrossRef

19.

Nabavi, S. F., Nabavi, S. M., Mirzaei, M., & Moghaddam, A. H. (2012). Protective effect of quercetin against sodium fluoride induced oxidative stress in rat’s heart. Food & Function, 3, 437–441. https://doi.org/10.1039/C2FO10264ACrossRef

20.

Sun, Y., Oberley, L. W., & Li, Y. (1988). A simple method for clinical assay of superoxide dismutase. Clinical Chemisty, 34, 497–500. https://doi.org/10.1093/clinchem/34.3.497CrossRef

21.

Aebi, H. (1984). [13] Catalase in vitro. Methods in Enzymology, 105, 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3CrossRefPubMed

22.

Lawrence, R. A., & Burk, R. F. (1976). Glutathione peroxidase activity in selenium-deficient rat liver. Biochemical and Biophysical Research Communications, 71, 952–958. https://doi.org/10.1016/0006-291X(76)90747-6CrossRefPubMed

23.

Sedlak, J., & Lindsay, R. H. (1968). Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analitical Biochemistry, 25, 192–205. https://doi.org/10.1016/0003-2697(68)90092-4CrossRef

24.

Placer, Z. A., Cushman, L. L., & Johnson, B. C. (1966). Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Analitical Biochemistry, 16, 359–364. https://doi.org/10.1016/0003-2697(66)90167-9CrossRef

25.

Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193, 265–275. https://doi.org/10.1016/S0021-9258(19)52451-6CrossRefPubMed

26.

Kucukler, S., Caglayan, C., Darendelioğlu, E., & Kandemir, F. M. (2020). Morin attenuates acrylamide-induced testicular toxicity in rats by regulating the NF-κB, Bax/Bcl-2 and PI3K/Akt/mTOR signaling pathways. Life Sciences, 261, 118301. https://doi.org/10.1016/j.lfs.2020.118301CrossRefPubMed

27.

Tartik, M., Darendelioglu, E., Aykutoglu, G., & Baydas, G. (2016). Turkish propolis supresses MCF-7 cell death induced by homocysteine. Biomedicine and Pharmacotherapy, 82, 704–712. https://doi.org/10.1016/j.biopha.2016.06.013CrossRefPubMed

28.

Song, C., Shi, D., Chang, K., Li, X., Dong, Q., Ma, X., Wang, X., Guo, Z., Liu, Y., & Wang, J. (2021). Sodium fluoride activates the extrinsic apoptosis via regulating NOX4/ROS-mediated p53/DR5 signaling pathway in lung cells both in vitro and in vivo. Free Radical Biology and Medicine, 169, 137–148. https://doi.org/10.1016/j.freeradbiomed.2021.04.007CrossRefPubMed

29.

Brillo, V., Chieregato, L., Leanza, L., Muccioli, S., & Costa, R. (2021). Mitochondrial dynamics, ROS, and cell signaling: a blended overview. Life. https://doi.org/10.3390/life11040332CrossRefPubMedPubMedCentral

30.

Herb, M., & Schramm, M. (2021). Functions of ROS in macrophages and antimicrobial immunity. Antioxidants. https://doi.org/10.3390/antiox10020313CrossRefPubMedPubMedCentral

31.

Schieber, M., & Chandel, N. S. (2014). ROS function in redox signaling and oxidative stress. Current Biology, 24, R453–R462. https://doi.org/10.1016/j.cub.2014.03.034CrossRefPubMed

32.

Kucukler, S., Darendelioğlu, E., Caglayan, C., Ayna, A., Yıldırım, S., & Kandemir, F. M. (2020). Zingerone attenuates vancomycin-induced hepatotoxicity in rats through regulation of oxidative stress, inflammation and apoptosis. Life Sciences, 259, 118382. https://doi.org/10.1016/j.lfs.2020.118382CrossRefPubMed

33.

Caglayan, C., Kandemir, F. M., Yildirim, S., Kucukler, S., & Eser, G. (2019). Rutin protects mercuric chloride-induced nephrotoxicity via targeting of aquaporin 1 level, oxidative stress, apoptosis and inflammation in rats. Journal of Trace Element Medicine Biology, 54, 69–78. https://doi.org/10.1016/j.jtemb.2019.04.007CrossRef

34.

Nkpaa, K. W., & Onyeso, G. I. (2018). Rutin attenuates neurobehavioral deficits, oxidative stress, neuro-inflammation and apoptosis in fluoride treated rats. Neuroscience Letters, 682, 92–99. https://doi.org/10.1016/j.neulet.2018.06.023CrossRefPubMed

35.

Bouasla, A., Barour, C., Bouasla, I., & Messarah, M. (2021). Beneficial effects of Punica granatum l. juice and gallic acid against kidney oxidative damage caused by sodium fluoride. Pharmaceutical Chemistry Journal, 55, 920–928. https://doi.org/10.1007/s11094-021-02516-8CrossRef

36.

Yamaguti, P. M., Simões, A., Ganzerla, E., Souza, D. N., Nogueira, F. N., & Nicolau, J. (2013). Effects of single exposure of sodium fluoride on lipid peroxidation and antioxidant enzymes in salivary glands of rats. Oxidative Medicine and Cellular Longevity, 2013, 674593. https://doi.org/10.1155/2013/674593CrossRefPubMedPubMedCentral

37.

Semis, H. S., Kandemir, F. M., Kaynar, O., Dogan, T., & Arikan, S. M. (2021). The protective effects of hesperidin against paclitaxel-induced peripheral neuropathy in rats. Life Sciences, 287, 120104. https://doi.org/10.1016/j.lfs.2021.120104CrossRefPubMed

38.

Volpe, C. M. O., Villar-Delfino, P. H., dos Anjos, P. M. F., & Nogueira-Machado, J. A. (2018). Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death & Disease, 9, 119. https://doi.org/10.1038/s41419-017-0135-zCrossRef

39.

Yu, H., Lin, L., Zhang, Z., Zhang, H., & Hu, H. (2020). Targeting NF-κB pathway for the therapy of diseases: Mechanism and clinical study. Signal Transduction and Targeted Therapy, 5, 209. https://doi.org/10.1038/s41392-020-00312-6CrossRefPubMedPubMedCentral

40.

Chen, L., Kuang, P., Liu, H., Wei, Q., Cui, H., Fang, J., Zuo, Z., Deng, J., Li, Y., Wang, X., & Zhao, L. (2019). Sodium fluoride (NaF) induces inflammatory responses via activating MAPKs/NF-κB signaling pathway and reducing anti-inflammatory cytokine expression in the mouse liver. Biological Trace Element Research, 189, 157–171. https://doi.org/10.1007/s12011-018-1458-zCrossRefPubMed

41.

Holze, C., Michaudel, C., Mackowiak, C., Haas, D. A., Benda, C., Hubel, P., Pennemann, F. L., Schnepf, D., Wettmarshausen, J., Braun, M., Leung, D. W., Amarasinghe, G. K., Perocchi, F., Staeheli, P., Ryffel, B., & Pichlmair, A. (2018). Oxeiptosis, a ROS-induced caspase-independent apoptosis-like cell-death pathway. Nature Immunology, 19, 130–140. https://doi.org/10.1038/s41590-017-0013-yCrossRefPubMed

42.

Gao, J., Tian, X., Yan, X., Wang, Y., Wei, J., Wang, X., Yan, X., & Song, G. (2021). Selenium exerts protective effects against fluoride-induced apoptosis and oxidative stress and altered the expression of Bcl-2/Caspase family. Biological Trace Element Research, 199, 682–692. https://doi.org/10.1007/s12011-020-02185-wCrossRefPubMed

43.

Wei, Q., Luo, Q., Liu, H., Chen, L., Cui, H., Fang, J., Zuo, Z., Deng, J., Li, Y., Wang, X., & Zhao, L. (2018). The mitochondrial pathway is involved in sodium fluoride (NaF)-induced renal apoptosis in mice. Toxicology Research, 7, 792–808. https://doi.org/10.1039/c8tx00130hCrossRefPubMedPubMedCentral

44.

Rodius, S., de Klein, N., Jeanty, C., Sánchez-Iranzo, H., Crespo, I., Ibberson, M., Xenarios, I., Dittmar, G., Mercader, N., Niclou, S. P., & Azuaje, F. (2020). Fisetin protects against cardiac cell death through reduction of ROS production and caspases activity. Scientific Reports, 10, 2896. https://doi.org/10.1038/s41598-020-59894-4CrossRefPubMedPubMedCentral

45.

Benzer, F., Kandemir, F. M., Ozkaraca, M., Kucukler, S., & Caglayan, C. (2018). Curcumin ameliorates doxorubicin-induced cardiotoxicity by abrogation of inflammation, apoptosis, oxidative DNA damage, and protein oxidation in rats. Journal of Biochemical and Molecular Toxicology, 32, e22030. https://doi.org/10.1002/jbt.22030CrossRef

46.

Yang, H., Xing, R., Liu, S., Yu, H., & Li, P. (2019). Analysis of the protective effects of γ-aminobutyric acid during fluoride-induced hypothyroidism in male Kunming mice. Pharmaceutical Biology, 57, 28–36. https://doi.org/10.1080/13880209.2018.1563621CrossRef

47.

Hoxhaj, G., & Manning, B. D. (2020). The PI3K–AKT network at the interface of oncogenic signalling and cancer metabolism. Nature Reviews Cancer, 20, 74–88. https://doi.org/10.1038/s41568-019-0216-7CrossRefPubMed

48.

Korkmaz, R., Yüksek, V., & Dede, S. (2021). The effects of sodium fluoride (NaF) treatment on the PI3K/Akt signal pathway in NRK-52E cells. Biological Trace Element Research. https://doi.org/10.1007/s12011-021-02927-4CrossRefPubMed

49.

Ma, L., Zhang, R., Li, D., Qiao, T., & Guo, X. (2021). Fluoride regulates chondrocyte proliferation and autophagy via PI3K/AKT/mTOR signaling pathway. Chemico-Biological Interactions, 349, 109659. https://doi.org/10.1016/j.cbi.2021.109659CrossRefPubMed

50.

Li, X., Hu, X., Wang, J., Xu, W., Yi, C., Ma, R., & Jiang, H. (2018). Inhibition of autophagy via activation of PI3K/Akt/mTOR pathway contributes to the protection of hesperidin against myocardial ischemia/reperfusion injury. International Journal of Molecular Medicine, 42, 1917–1924. https://doi.org/10.3892/ijmm.2018.3794CrossRefPubMedPubMedCentral

51.

Kandemir, F. M., Yıldırım, S., Kucukler, S., Caglayan, C., Darendelioğlu, E., & Dortbudak, M. B. (2020). Protective effects of morin against acrylamide-induced hepatotoxicity and nephrotoxicity: A multi-biomarker approach. Food and Chemical Toxicology, 138, 111190. https://doi.org/10.1016/j.fct.2020.111190CrossRefPubMed

52.

He, C., & Levine, B. (2010). The beclin 1 interactome. Current Opinion in Cell Biology, 22, 140–149. https://doi.org/10.1016/j.ceb.2010.01.001CrossRefPubMedPubMedCentral

53.

Kang, R., Zeh, H. J., Lotze, M. T., & Tang, D. (2011). The Beclin 1 network regulates autophagy and apoptosis. Cell Death & Differentiation, 18, 571–580. https://doi.org/10.1038/cdd.2010.191CrossRef

54.

Koukourakis, M. I., Kalamida, D., Giatromanolaki, A., Zois, C. E., Sivridis, E., Pouliliou, S., Mitrakas, A., Gatter, K. C., & Harris, A. L. (2015). Autophagosome proteins LC3A, LC3B and LC3C have distinct subcellular distribution kinetics and expression in cancer cell lines. PLoS ONE, 10, e0137675. https://doi.org/10.1371/journal.pone.0137675CrossRefPubMedPubMedCentral

55.

Gur, C., Kandemir, O., & Kandemir, F. M. (2022). Investigation of the effects of hesperidin administration on abamectin-induced testicular toxicity in rats through oxidative stress, endoplasmic reticulum stress, inflammation, apoptosis, autophagy, and JAK2/STAT3 pathways. Environmental Toxicology, 37, 401–412. https://doi.org/10.1002/tox.23406CrossRefPubMed

Titel: Hesperidin Attenuates Oxidative Stress, Inflammation, Apoptosis, and Cardiac Dysfunction in Sodium Fluoride‐Induced Cardiotoxicity in Rats
verfasst von: Behçet Varışlı
Ekrem Darendelioğlu
Cuneyt Caglayan
Fatih Mehmet Kandemir
Adnan Ayna
Aydın Genç
Özge Kandemir
Publikationsdatum: 23.05.2022
Verlag: Springer US
Erschienen in: Cardiovascular Toxicology / Ausgabe 8/2022
Print ISSN: 1530-7905
Elektronische ISSN: 1559-0259
DOI: https://doi.org/10.1007/s12012-022-09751-9

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Hesperidin Attenuates Oxidative Stress, Inflammation, Apoptosis, and Cardiac Dysfunction in Sodium Fluoride‐Induced Cardiotoxicity in Rats

Abstract

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Abstract

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