17
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Borax attenuates oxidative stress, inflammation, and apoptosis by modulating Nrf2/ROS balance in acrylamide-induced neurotoxicity in rainbow trout

, , , , , , & show all
Received 17 Jan 2024, Accepted 16 Jun 2024, Published online: 28 Jun 2024

References

  • Aboubakr, M., Ibrahim, S. S., Said, A. M., Elgendey, F., & Anis, A. (2019). Neuroprotective effects of clove oil in acrylamide induced neurotoxicity in rats. Pakistan Veterinary Journal, 39(01), 111–115. https://doi.org/10.29261/pakvetj/2018.117
  • Aboubakr, M., Elmahdy, A. M., Taima, S., Emam, M. A., Farag, A., Alkafafy, M., Said, A. M., & Soliman, A. (2023). Protective effects of N acetylcysteine and vitamin E against acrylamide-induced neurotoxicity in rats. The Pakistan Veterinary Journal, 43(2), 262–268. https://doi.org/10.29261/pakvetj/2023.027
  • Alak, G., Ucar, A., Parlak, V., Yeltekin, A. Ç., Özgeriş, F. B., Atamanalp, M., & Türkez, H. (2020). Antioxidant potential of Ulexite in Zebrafish brain: Assessment of oxidative DNA damage, apoptosis, and response of antioxidant defense system. Biological Trace Element Research, 199(3), 1092–1099. https://doi.org/10.1007/s12011-020-02231-7
  • Alak, G., Özgeriş, F. B., Yeltekin, A. Ç., Parlak, V., Ucar, A., Caglar, O., Türkez, H., & Atamanalp, M. (2020). Hematological and hepatic effects of Ulexite in Zebrafish. Environmental Toxicology and Pharmacology, 80, 103496https://doi.org/10.1016/j.etap.2020.103496
  • Alak, G., Parlak, V., Ucar, A., Cilingir Yeltekin, A., Ozgeris, F. B., Cağlar, O., Atamanalp, M., & Türkez, H. (2020). Oxidative and DNA damage potential of colemanite on zebrafish: Brain, liver and blood. Turkish Journal of Fisheries and Aquatic Sciences, 20(8), 593–602. https://doi.org/10.4194/1303-2712-v20_8_02
  • Alak, G., Parlak, V., Aslan, M. E., Ucar, A., Atamanalp, M., & Türkez, H. (2019). Borax supplementation alleviates hematotoxicity and DNA damage in rainbow trout (Oncorhynchus mykiss) exposed to copper. Biological Trace Element Research, 187(2), 536–542. https://doi.org/10.1007/s12011-018-1399-6
  • Alak, G., Parlak, V., Yeltekin, A. Ç., Ucar, A., Çomaklı, S., Topal, A., Atamanalp, M., Özkaraca, M., & Türkez, H. (2019). The protective effect exerted by dietary borax on toxicity metabolism in rainbow trout (Oncorhynchus mykiss) tissues. Comparative Biochemistry and Physiology Part C, 216, 82–92. https://doi.org/10.1016/j.cbpc.2018.10.005
  • Alak, G., Ucar, A., Çilingir Yeltekin, A., Parlak, V., Nardemir, G., Kızılkaya, M., Hakkı Taş, İ., Yılgın, M., Atamanalp, M., Topal, A., Mahmut Kocaman, E., & Yanık, T. (2019). Neurophysiological responses in the brain tissues of rainbow trout (Oncorhynchus mykiss) treated with bio-pesticide. Drug and Chemical Toxicology, 42(2), 203–209. https://doi.org/10.1080/01480545.2018.1526180
  • Alak, G., Yeltekin, A. Ç., Özgeriş, F. B., Parlak, V., Uçar, A., Keleş, M. S., & Atamanalp, M. (2019). Therapeutic effect of N-acetyl cysteine as an antioxidant on rainbow trout’s brain in cypermethrin toxicity. Chemosphere, 221, 30–36. https://doi.org/10.1016/j.chemosphere.2018.12.196
  • Alak, G., Ucar, A., Yeltekin, A. Ç., Çomaklı, S., Parlak, V., Taş, I. H., Özkaraca, M., Topal, A., Kirman, E. M., Bolat, İ., Atamanalp, M., & Türkez, H. (2018). Neuroprotective effects of dietary borax in the brain tissue of rainbow trout (Oncorhynchus mykiss) exposed to copper-induced toxicity. Fish Physiology and Biochemistry, 44(5), 1409–1420. https://doi.org/10.1007/s10695-018-0530-0
  • Alak, G., Yeltekin, A. Ç., Tas, I. H., Ucar, A., Parlak, V., Topal, A., Kocaman, E. M., & Atamanalp, M. (2017). Investigation of 8-OHdG, CYP1A, HSP70 and transcriptional analyses of antioxidant defence system in liver tissues of rainbow trout exposed to eprinomectin. Fish & Shellfish Immunology, 65, 136–144. https://doi.org/10.1016/j.fsi.2017.04.004
  • Atamanalp, M., Parlak, V., Özgeriş, F. B., Çilingir Yeltekin, A., Ucar, A., Keleş, M. S., & Alak, G. (2021). Treatment of oxidative stress, apoptosis, and DNA injury with N-acetylcysteine at simulative pesticide toxicity in fish. Toxicology Mechanisms and Methods, 31(3), 224–234. https://doi.org/10.1080/15376516.2021.1871794
  • Atamanalp, M., Türkez, H., Yeltekin, A. Ç., Özgeriş, F. B., Ucar, A., Çağlar, Ö., Parlak, V., Oner, S., & Alak, G. (2022). Borax relieved the acrylamide-induced hematotoxic, hepatotoxic, immunotoxic and genotoxic damages in rainbow trout by regulating apoptosis and Nrf2 signaling pathway. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 259, 109396. https://doi.org/10.1016/j.cbpc.2022.109396
  • Behairy, A., Elkomy, A., Elsayed, F., Gaballa, M. M., Soliman, A., & Aboubakr, M. (2024). Antioxidant and anti-inflammatory potential of spirulina and thymoquinone mitigate the methotrexate-induced neurotoxicity. Naunyn-Schmiedeberg’s Archives of Pharmacology, 397(3), 1875–1888. https://doi.org/10.1007/s00210-023-02739-4
  • Boas, S. M., Joyce, K. L., & Cowell, R. M. (2021). The NRF2-dependent transcriptional regulation of antioxidant defense pathways: Relevance for cell type-specific vulnerability to neurodegeneration and therapeutic intervention. Antioxidants, 11(1), 8. https://doi.org/10.3390/antiox11010008
  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
  • Cacciatore, I., Türkez, H., Di Rienzo, A., Ciulla, M., Mardinoglu, A., & Di Stefano, A. (2021). Boron-based hybrids as novel scaffolds for the development of drugs with neuroprotective properties. RSC Medicinal Chemistry, 12(11), 1944–1949. https://doi.org/10.1039/D1MD00177A
  • Chen, X., Xiao, J.-W., Cao, P., Zhang, Y., Cai, W.-J., Song, J.-Y., Gao, W.-M., & Li, B. (2021). Brain-derived neurotrophic factor protects against acrylamide-induced neuronal and synaptic injury via the TrkB-MAPK-Erk1/2 pathway. Neural Regeneration Research, 16(1), 150https://doi.org/10.4103/1673-5374.286976
  • Çolak, S., Geyikoğlu, F., Keles, O. N., Türkez, H., Topal, A., & Unal, B. (2011). The neuroprotective role of boric acid on aluminum chloride-induced neurotoxicity. Toxicology and Industrial Health, 27(8), 700–710. https://doi.org/10.1177/0748233710395349
  • Comba, B., Oto, G., Mis, L., Özdemir, H., & Comba, A. (2016). Effects of borax on inflammation, haematological parameters and total oxidant-antioxidant status in rats applied 3–methylcholanthrene. Kafkas Universitesi Veteriner Fakultesi Dergisi, 22(4), 539–544. https://doi.org/10.9775/kvfd.2016.15001
  • Giustina, A. D., de Souza Goldim, M. P., Danielski, L. G., Garbossa, L., Junior, A. N. O., Cidreira, T., Denicol, T., Bonfante, S., da Rosa, N., Fortunato, J. J., Palandi, J., de Oliveira, B. H., Martins, D. F., Bobinski, F., Garcez, M., Bellettini-Santos, T., Budni, J., Colpo, G., Scaini, G., … Petronilho, F. (2020). Lipoic acid and fish oil combination potentiates neuroinflammation and oxidative stress regulation and prevents cognitive decline of rats after sepsis. Molecular Neurobiology, 57(11), 4451–4466. https://doi.org/10.1007/s12035-020-02032-y
  • Edobor, H. D., Musa, S. A., Umana, U. E., Oderinde, G. P., & Agbon, A. N. (2021). Neuroprotective effect of phoenix dactylifera (date palm) on paraquat triggered cortico-nigral neurotoxicity. The Journal of Neurobehavioral Sciences, 8(3), 199https://doi.org/10.4103/jnbs.jnbs_28_21
  • Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82(1), 70–77. https://doi.org/10.1016/0003-9861(59)90090-6
  • Elsayed, A., Elkomy, A., Alkafafy, M., Elkammar, R., Fadl, S. E., Abdelhiee, E. Y., Abdeen, A., Youssef, G., Shaheen, H., Soliman, A., & Aboubakr, M. (2022). Ameliorating effect of lycopene and N-acetylcysteine against cisplatin-induced cardiac injury in rats. Pakistan Veterinary Journal, 42(1), 107–111.
  • Erdemli, M. E., Aladag, M. A., Altinoz, E., Demirtas, S., Turkoz, Y., Yigitcan, B., & Bag, H. G. (2018). Acrylamide applied during pregnancy causes the neurotoxic effect by lowering BDNF levels in the fetal brain. Neurotoxicology and Teratology, 67, 37–43. https://doi.org/10.1016/j.ntt.2018.03.005
  • Esmaeelpanah, E., Razavi, B. M., Vahdati Hasani, F., & Hosseinzadeh, H. (2018). Evaluation of epigallocatechin gallate and epicatechin gallate effects on acrylamide-induced neurotoxicity in rats and cytotoxicity in PC 12 cells. Drug and Chemical Toxicology, 41(4), 441–448. https://doi.org/10.1080/01480545.2017.1381108
  • Farag, O. M., Abd-Elsalam, R. M., Ogaly, H. A., Ali, S. E., El Badawy, S. A., Alsherbiny, M. A., Li, C. G., & Ahmed, K. A. (2021). Metabolomic profiling and neuroprotective effects of purslane seeds extract against acrylamide toxicity in rat’s brain. Neurochemical Research, 46(4), 819–842. https://doi.org/10.1007/s11064-020-03209-6
  • Goggi, J., Pullar, I. A., Carney, S. L., & Bradford, H. F. (2003). Signalling pathways involved in the short-term potentiation of dopamine release by BDNF. Brain Research, 968(1), 156–161. https://doi.org/10.1016/S0006-8993(03)02234-0
  • Huang, X., Fei, G-q., Liu, W-j., Ding, J., Wang, Y., Wang, H., Ji, J-l., & Wang, X. (2020). Adipose-derived mesenchymal stem cells protect against CMS-induced depression-like behaviors in mice via regulating the Nrf2/HO-1 and TLR4/NF-κB signaling pathways. Acta Pharmacologica Sinica, 41(5), 612–619. https://doi.org/10.1038/s41401-019-0317-6
  • Jang, D. I., Lee, A. H., Shin, H. Y., Song, H. R., Park, J. H., Kang, T. B., Lee, S. R., & Yang, S. H. (2021). The role of Tumor Necrosis Factor Alpha (TNF-α) in Autoimmune disease and current TNF-α inhibitors in therapeutics. International Journal of Molecular Sciences, 22(5), 2719. https://doi.org/10.3390/ijms22052719
  • Jing, Z., Xu, A., Liang, Y. Q., Zhang, Z., Yu, C., Hong, P., & Li, Y. (2019). Biodegradable poly (acrylic acid-co-acrylamide)/poly (vinyl alcohol) double network hydrogels with tunable mechanics and high self-healing performance. Polymers, 11(6), 952https://doi.org/10.3390/polym11060952
  • Kacar, S., & Sahinturk, V. (2021). The protective agents used against acrylamide toxicity: An in vitro cell culture study-based review. Cell Journal, 23(4), 367
  • Kerschensteiner, M., Gallmeier, E., Behrens, L., Leal, V. V., Misgeld, T., Klinkert, W. E. F., Kolbeck, R., Hoppe, E., Oropeza-Wekerle, R.-L., Bartke, I., Stadelmann, C., Lassmann, H., Wekerle, H., & Hohlfeld, R. (1999). Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: A neuroprotective role of inflammation? The Journal of Experimental Medicine, 189(5), 865–870. https://doi.org/10.1084/jem.189.5.865
  • Kachot, R. L., Patel, U. D., Patel, H. B., Modi, C. M., Chauhan, R., Kariya, M. H., & Bhadaniya, A. R. (2023). Neurotoxicity of acrylamide in adult zebrafish following short-term and long-term exposure: Evaluation of behavior alterations, oxidative stress markers, expression of antioxidant genes, and histological examination of the brain and eyes. Environmental Science and Pollution Research, 30(14), 40116–40131. https://doi.org/10.1007/s11356-022-25112-z
  • Lebda, M. A., Gad, S. B., & Rashed, R. R. (2015). The effect of lipoic acid on acrylamide-induced neuropathy in rats with reference to biochemical, hematological, and behavioral alterations. Pharma­ceutical Biology, 53(8), 1207–1213. https://doi.org/10.3109/13880209.2014.970288
  • Liu, Y., Meng, X., Sun, L., Pei, K., Chen, L., Zhang, S., & Hu, M. (2022). Protective effects of hydroxy-α-sanshool from the pericarp of Zanthoxylum bungeanum Maxim. On D-galactose/AlCl3-induced Alzheimer’s disease-like mice via Nrf2/HO-1 signaling pathways. European Journal of Pharmacology, 914, 174691. https://doi.org/10.1016/j.ejphar.2021.174691
  • Liu, L., Liu, Y., Cheng, X., & Qiao, X. (2021). The alleviative effects of quercetin on cadmium-induced necroptosis via inhibition ROS/iNOS/NF-κB pathway in the chicken brain. Biological Trace Element Research, 199(4), 1584–1594. https://doi.org/10.1007/s12011-020-02563-4
  • Loewengart, G. (2001). Toxicity of boron to rainbow trout: A weight-of-the-evidence assessment. Environmental Toxicology and Chemistry, 20(4), 796–803. https://doi.org/10.1897/1551-5028(2001)020<0796:TOBTRT>2.0.CO;2
  • Matthews, V. B., Åström, M.-B., Chan, M. H. S., Bruce, C. R., Krabbe, K. S., Prelovsek, O., Åkerström, T., Yfanti, C., Broholm, C., Mortensen, O. H., Penkowa, M., Hojman, P., Zankari, A., Watt, M. J., Bruunsgaard, H., Pedersen, B. K., & Febbraio, M. A. (2009). Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase. Diabetologia, 52(7), 1409–1418. https://doi.org/10.1007/s00125-009-1364-1
  • Murer, M. G., Yan, Q., & Raisman-Vozari, R. (2001). Brain-derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Progress in Neurobiology, 63(1), 71–124. https://doi.org/10.1016/S0301-0082(00)00014-9
  • Nan, B., Yang, C., Li, L., Ye, H., Yan, H., Wang, M., & Yuan, Y. (2021). Allicin alleviated acrylamide-induced NLRP3 inflammasome activation via oxidative stress and endoplasmic reticulum stress in Kupffer cells and SD rats liver. Food and Chemical Toxicology, 2021(148), 111937. https://doi.org/10.1016/j.fct.2020.111937
  • OECD. (2013). Test No. 210: Fish, Early-life Stage Toxicity Test. OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing. https://doi.org/10.1787/9789264203785-en
  • Pan, X., Wu, X., Yan, D., Peng, C., Rao, C., & Yan, H. (2018). Acrylamide-induced oxidative stress and inflammatory response are alleviated by N-acetylcysteine in PC12 cells: Involvement of the crosstalk between Nrf2 and NF-κB pathways regulated by MAPKs. Toxicology Letters, 288, 55–64. https://doi.org/10.1016/j.toxlet.2018.02.002
  • Petersen, D. W., & Lech, J. J. (1987). Hepatic effects of acrylamide in rainbow trout. Toxicology and Applied Pharmacology, 89(2), 249–255. https://doi.org/10.1016/0041-008X(87)90045-7
  • Rose-John, S., Winthrop, K., & Calabrese, L. (2017). The role of IL-6 in host defence against infections: Immunobiology and clinical implications. Nature Reviews Rheumatology, 13(7), 399–409. https://doi.org/10.1038/nrrheum.2017.83
  • Sayre, L. M., Perry, G., & Smith, M. A. (2008). Oxidative stress and neurotoxicity. Chemical Research in Toxicology, 21(1), 172–188. https://doi.org/10.1021/tx700210j
  • Sheikholeslami, M. A., Ghafghazi, S., Pouriran, R., Mortazavi, S. E., & Parvardeh, S. (2021). Attenuating effect of paroxetine on memory impairment following cerebral ischemia-reperfusion injury in rat: The involvement of BDNF and antioxidant capacity. European Journal of Pharmacology, 893, 173821https://doi.org/10.1016/j.ejphar.2020.173821
  • Thabet, N. M., & Moustafa, E. M. (2018). Protective effect of rutin against brain injury induced by acrylamide or gamma radiation: Role of PI3K/AKT/GSK-3β/NRF2 signalling pathway. Archives of Physiology and Biochemistry, 124(2), 185–193. https://doi.org/10.1080/13813455.2017.1374978
  • Tilg, H., & Diehl, A. M. (2000). Cytokines in alcoholic and nonalcoholic steatohepatitis. New England Journal of Medicine, 343(20), 1467–1476. https://doi.org/10.1056/NEJM200011163432007
  • Türkez, H., Arslan, M. E., Tatar, A., & Mardinoglu, A. (2021). Promising potential of boron compounds against Glioblastoma: In vitro antioxidant, anti-inflammatory and anticancer studies. Neurochemistry International, 149, 105137https://doi.org/10.1016/j.neuint.2021.105137
  • Türkez, H., Arslan, M. E., Di Stefano, A., Cacciatore, I., & Mardinoğlu, A. (2020). Nonpharmacological treatment options for Alzheimer’s disease: From animal testing to clinical studies. Turkish Journal of Zoology, 44(2), 81–89. https://doi.org/10.3906/zoo-1911-32
  • Türkez, H., Geyikoğlu, F., & Çolak, S. U. A. T. (2011). The protective effect of boric acid on aluminum-induced hepatotoxicity and genotoxicity in rats. Turkish Journal of Biology, 35(3), 293–301. https://doi.org/10.3906/biy-0902-11
  • Ucar, A., Ozgeris, F. B., Parlak, V., Yeltekin, A. C., Türkez, H., Alak, G., & Atamanalp, M. (2022). Ulexite modulates the neurotoxicological outcomes of acetylferrocene-exposed rainbow trout. Environmental and Molecular Mutagenesis, 63(6), 286–295. https://doi.org/10.1002/em.22498
  • Ucar, A., Parlak, V., Ozgeris, F. B., Yeltekin, A. C., Arslan, M. E., Alak, G., Türkez, H., Kocaman, E. M., & Atamanalp, M. (2022). Magnetic nanoparticles-induced neurotoxicity and oxidative stress in brain of rainbow trout: Mitigation by ulexite through modulation of antioxidant, anti-inflammatory, and antiapoptotic activities. Science of The Total Environment, 838, 155718https://doi.org/10.1016/j.scitotenv.2022.155718
  • Volpe, R. (1994). Evidence that the immunosuppressive effects of antithyroid drugs are mediated through actions on the thyroid cell, modulating thyrocyte-immunocyte signaling: a review. Thyroid, 4(2), 217–223.
  • Wang, N., & Wang, N. (2021). Brain-derived neurotrophic factor in autoimmune inflammatory diseases (Review). Experimental and Therapeutic Medicine, 22(5), 1292 https://doi.org/10.3892/etm.2021.10727
  • Wang, Y., Wang, D., Yin, K., Liu, Y., Lu, H., Zhao, H., & Xing, M. (2022). Lycopene attenuates oxidative stress, inflammation, and apoptosis by modulating Nrf2/NF-κB balance in sulfamethoxazole-induced neurotoxicity in grass carp (Ctenopharyngodon Idella). Fish & Shellfish Immunology, 121, 322–331. https://doi.org/10.1016/j.fsi.2022.01.012
  • Xie, L., Huang, W., Li, J., Chen, G., Xiao, Q., Zhang, Y., He, H., Wang, Q., & He, J. (2022). The protective effects and mechanisms of modified Lvdou Gancao decoction on acute alcohol intoxication in mice. Journal of Ethnopharmacology, 282, 114593https://doi.org/10.1016/j.jep.2021.114593
  • Xing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X. F., & Achong, M. K. (1998). IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. Journal of Clinical Investigation, 101(2), 311–320. https://doi.org/10.1172/JCI1368
  • Yeltekin, A. Ç., Ucar, A., Parlak, V., Özgeriş, F. B., Türkez, H., Esenbuğa, N., Atamanalp, M., & Alak, G. (2022). Borax exerts protective effect against ferrocene-induced neurotoxicity in Oncorhynchus mykiss. Journal of Trace Elements in Medicine and Biology, 72, 126996. https://doi.org/10.1016/j.jtemb.2022.126996
  • Yousef, M. I., & El-Demerdash, F. M. (2006). Acrylamide-induced oxidative stress and biochemical perturbations in rats. Toxicology, 219(1–3), 133–141. https://doi.org/10.1016/j.tox.2005.11.008
  • Zhao, H., Huang, J., Li, Y., Lv, X., Zhou, H., Wang, H., Xu, Y., Wang, C., Wang, J., & Liu, Z. (2020). ROS-scavenging hydrogel to promote healing of bacteria infected diabetic wounds. Biomaterials, 258, 120286.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.