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Neuro-amelioration of Ficus lyrata (fiddle-leaf fig) extract conjugated with selenium nanoparticles against aluminium toxicity in rat brain: relevance to neurotransmitters, oxidative, inflammatory, and apoptotic events

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Abstract

Aluminium is a non-essential metal, and its accumulation in the brain is linked with potent neurotoxic action and the development of many neurological diseases. This investigation, therefore, intended to examine the antagonistic efficacy of Ficus lyrata (fiddle-leaf fig) extract (FLE) conjugated with selenium nanoparticles (FLE-SeNPs) against aluminium chloride (AlCl3)-induced hippocampal injury in rats. Rats were allocated to five groups: control, FLE, AlCl3 (100 mg/kg), AlCl3 + FLE (100 mg/kg), and AlCl3 + FLE-SeNPs (0.5 mg/kg). All agents were administered orally every day for 42 days. The result revealed that pre-treated rats with FLE-SeNPs showed markedly lower acetylcholinesterase and Na+/K+-ATPase activities in the hippocampus than those in AlCl3 group. Additionally, FLE-SeNPs counteracted the oxidant stress-mediated by AlCl3 by increasing superoxide dismutase, catalase, glutathione peroxidase, glutathione reductase, and glutathione contents in rat hippocampus. Besides, the formulated nanoparticles decreased the hippocampal malondialdehyde, carbonyl protein, and nitric oxide levels of AlCl3-exposed animals. Furthermore, FLE-SeNPs attenuated neural tissue inflammation, as demonstrated by decreased interleukin-1 beta, interleukin-6, nuclear factor kappa B, and glial fibrillary acidic protein. Remarkable anti-apoptotic action was exerted by FLE-SeNPs by increasing B cell lymphoma 2 and decreasing caspase-3 and Bcl-2-associated-X protein in AlCl3-exposed rats. The abovementioned results correlated well with the hippocampal histopathological findings. Given these results, SeNPs synthesized with FLE imparted a remarkable neuroprotective action against AlCl3-induced neurotoxicity by reversing oxidative damage, neuronal inflammation, and apoptosis in exposed rats.

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References

  • Abbas F, Eladl MA, El-Sherbiny M, Abozied N, Nabil A, Mahmoud SM et al (2022) Celastrol and thymoquinone alleviate aluminum chloride-induced neurotoxicity: behavioral psychomotor performance, neurotransmitter level, oxidative-inflammatory markers, and BDNF expression in rat brain. Biomed Pharmacother 151:113072

    Article  CAS  Google Scholar 

  • Abozaid OAR, Sallam MW, El-Sonbaty S, Aziza S, Emad B, Ahmed ESA (2022) Resveratrol-selenium nanoparticles alleviate neuroinflammation and neurotoxicity in a rat model of Alzheimer’s disease by regulating Sirt1/miRNA-134/GSK3β expression. Biol Trace Elem Res 200(12):5104–5114. https://doi.org/10.1007/s12011-021-03073-7

    Article  CAS  Google Scholar 

  • Adetuyi BO, Adebisi OA, Adetuyi OA, Ogunlana OO, Toloyai PE, Egbuna C et al (2022) Ficus exasperata attenuates acetaminophen-induced hepatic damage via NF-κB signaling mechanism in experimental rat model. Biomed Res Int 2022:6032511. https://doi.org/10.1155/2022/6032511

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Al-Brakati A, Albarakati AJA, Daabo H, Baty RS, Salem FEH, Habotta OA et al (2020) Neuromodulatory effects of green coffee bean extract against brain damage in male albino rats with experimentally induced diabetes. Metab Brain Dis 35(7):1175–1187

    Article  CAS  Google Scholar 

  • Al-Brakati A, Alsharif KF, Alzahrani KJ, Kabrah S, Al-Amer O, Oyouni AA et al (2021) Using green biosynthesized lycopene-coated selenium nanoparticles to rescue renal damage in glycerol-induced acute kidney injury in rats. Int J Nanomed 16:4335–4349. https://doi.org/10.2147/ijn.s306186

    Article  Google Scholar 

  • Albrakati A, Alsharif KF, Al Omairi NE, Alsanie WF, Almalki ASA, Abd Elmageed ZY et al (2021) Neuroprotective efficiency of prodigiosins conjugated with selenium nanoparticles in rats exposed to chronic unpredictable mild stress is mediated through antioxidative, anti-inflammatory, anti-apoptotic, and neuromodulatory activities. Int J Nanomed 16:8447–8464. https://doi.org/10.2147/ijn.s323436

    Article  CAS  Google Scholar 

  • Ali HFH, El-Sayed NM, Khodeer DM, Ahmed AAM, Hanna PA, Moustafa YMA (2020) Nano selenium ameliorates oxidative stress and inflammatory response associated with cypermethrin-induced neurotoxicity in rats. Ecotoxicol Environ Saf 195:110479. https://doi.org/10.1016/j.ecoenv.2020.110479

    Article  CAS  Google Scholar 

  • Alqasoumi SI, Basudan OA, Al-Rehaily AJ, Abdel-Kader MS (2014) Phytochemical and pharmacological study of Ficus palmata growing in Saudi Arabia. Saudi Pharm J 22(5):460–71 S1319–0164(13)00121–7

    Article  Google Scholar 

  • Bashir DW, Rashad MM, Ahmed YH, Drweesh EA, Elzahany EAM, Abou-El-Sherbini KS et al (2021) The ameliorative effect of nanoselenium on histopathological and biochemical alterations induced by melamine toxicity on the brain of adult male albino rats. Neurotoxicology 86:37–51. https://doi.org/10.1016/j.neuro.2021.06.006

    Article  CAS  Google Scholar 

  • Becker A, Helmuth M, Trzeczak D, Chindo BA (2021) Methanol extract of Ficus platyphylla decreases cerebral ischemia induced injury in mice. J Ethnopharmacol 278:114219

    Article  CAS  Google Scholar 

  • Bhangale JO, & Acharya SR (2016). Anti-Parkinson activity of petroleum ether extract of Ficus religiosa (L.) leaves. Adv Pharmacol Sci 2016:9436106. https://doi.org/10.1155/2016/9436106

  • Campisi A, Raciti G, Sposito G, Grasso R, Chiacchio MA, Spatuzza M et al (2021) Amyloid-beta induces different expression pattern of tissue transglutaminase and its isoforms on olfactory ensheathing cells: modulatory effect of indicaxanthin. Int J Mol Sci 22(7):3388

    Article  CAS  Google Scholar 

  • Campos HM, da Costa M, da Silva Moreira LK, da Silva Neri HF, da Silva CRB, Pruccoli L et al (2022) Protective effects of chrysin against the neurotoxicity induced by aluminium: in vitro and in vivo studies. Toxicology 465:153033

    Article  CAS  Google Scholar 

  • Cao Z, Wang P, Gao X, Shao B, Zhao S, Li Y (2019) Lycopene attenuates aluminum-induced hippocampal lesions by inhibiting oxidative stress-mediated inflammation and apoptosis in the rat. J Inorg Biochem 193:143–151

    Article  CAS  Google Scholar 

  • Dai W, Chen C, Feng H, Li G, Peng W, Liu X et al (2021) Protection of Ficus pandurata Hance against acute alcohol-induced liver damage in mice via suppressing oxidative stress, inflammation, and apoptosis. J Ethnopharmacol 275:114140

    Article  CAS  Google Scholar 

  • Ebokaiwe AP, Okori S, Nwankwo JO, Ejike C, Osawe SO (2021) Selenium nanoparticles and metformin ameliorate streptozotocin-instigated brain oxidative-inflammatory stress and neurobehavioral alterations in rats. Naunyn Schmiedebergs Arch Pharmacol 394(4):591–602. https://doi.org/10.1007/s00210-020-02000-2

    Article  CAS  Google Scholar 

  • Elfouly A, Awny M, Ibrahim MK, Aboelsaad M, Tian J, Sayed M (2021) Effects of long-acting testosterone undecanoate on behavioral parameters and Na +, K(+)-ATPase mRNA expression in mice with Alzheimer’s disease. Neurochem Res 46(9):2238–2248. https://doi.org/10.1007/s11064-021-03357-3

    Article  CAS  Google Scholar 

  • El-Hawary SS, Ali ZY, Younis IY (2019) Hepatoprotective potential of standardized Ficus species in intrahepatic cholestasis rat model: Involvement of nuclear factor-κB, and Farnesoid X receptor signaling pathways. J Ethnopharmacol 231:262–274. https://doi.org/10.1016/j.jep.2018.11.026

    Article  CAS  Google Scholar 

  • El-Hawary SS, Sobeh M, Badr WK, Abdelfattah MAO, Ali ZY, El-Tantawy ME et al (2020) HPLC-PDA-MS/MS profiling of secondary metabolites from Opuntia ficus-indica cladode, peel and fruit pulp extracts and their antioxidant, neuroprotective effect in rats with aluminum chloride induced neurotoxicity. Saudi J Biol Sci 27(10):2829–2838. https://doi.org/10.1016/j.sjbs.2020.07.003

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  Google Scholar 

  • Factor VM, Kiss A, Woitach JT, Wirth PJ, Thorgeirsson SS (1998) Disruption of redox homeostasis in the transforming growth factor-α/c-myc transgenic mouse model of accelerated hepatocarcinogenesis. J Biol Chem 273(25):15846–15853

    Article  CAS  Google Scholar 

  • Farag MA, Abdelfattah MS, Badr SE, Wessjohann LA (2014) Profiling the chemical content of Ficus lyrata extracts via UPLC-PDA-qTOF-MS and chemometrics. Nat Prod Res 28(19):1549–1556. https://doi.org/10.1080/14786419.2014.926353

    Article  CAS  Google Scholar 

  • Firdaus Z, Kumar D, Singh SK, Singh TD (2022) Centella asiatica alleviates AlCl(3)-induced cognitive impairment, oxidative stress, and neurodegeneration by modulating cholinergic activity and oxidative burden in rat brain. Biol Trace Elem Res 200(12):5115–5126. https://doi.org/10.1007/s12011-021-03083-5

    Article  CAS  Google Scholar 

  • Fouad D, Alhatem H, Abdel-Gaber R, Ataya F (2019) Hepatotoxicity and renal toxicity induced by gamma-radiation and the modulatory protective effect of Ficus carica in male albino rats. Res Vet Sci 125:24–35

    Article  CAS  Google Scholar 

  • Foyet HS, Tchinda Deffo S, Koagne Yewo P, Antioch I, Zingue S, Asongalem EA et al (2017) Ficus sycomorus extract reversed behavioral impairment and brain oxidative stress induced by unpredictable chronic mild stress in rats. BMC Complement Altern Med 17(1):1–15

    Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids (Research Support, U.S. Gov't, P.H.S.). Anal Biochem 126(1):131–8

    Article  CAS  Google Scholar 

  • Hosny EN, Sawie HG, Elhadidy ME, Khadrawy YA (2019) Evaluation of antioxidant and anti-inflammatory efficacy of caffeine in rat model of neurotoxicity. Nutr Neurosci 22(11):789–796. https://doi.org/10.1080/1028415x.2018.1446812

    Article  CAS  Google Scholar 

  • Jangra A, Kasbe P, Pandey SN, Dwivedi S, Gurjar SS, Kwatra M et al (2015) Hesperidin and silibinin ameliorate aluminum-induced neurotoxicity: modulation of antioxidants and inflammatory cytokines level in mice hippocampus. Biol Trace Elem Res 168(2):462–471

    Article  CAS  Google Scholar 

  • Ji D, Wu X, Li D, Liu P, Zhang S, Gao D et al (2020) Protective effects of chondroitin sulphate nano-selenium on a mouse model of Alzheimer’s disease. Int J Biol Macromol 154:233–245. https://doi.org/10.1016/j.ijbiomac.2020.03.079

    Article  CAS  Google Scholar 

  • Justin Thenmozhi A, Dhivyabharathi M, Manivasagam T, Essa MM (2016) Tannoid principles of Emblica officinalis attenuated aluminum chloride induced apoptosis by suppressing oxidative stress and tau pathology via Akt/GSK-3βsignaling pathway. J Ethnopharmacol 194:20–29. https://doi.org/10.1016/j.jep.2016.08.047

    Article  CAS  Google Scholar 

  • Karunanidhi P, Verma N, Kumar DN, Agrawal AK, Singh S (2021) Triphenylphosphonium functionalized Ficus religiosa L. extract loaded nanoparticles improve the mitochondrial function in oxidative stress induced diabetes. AAPS Pharm Sci Tech 22(5):158. https://doi.org/10.1208/s12249-021-02016-8

    Article  CAS  Google Scholar 

  • Kasbe P, Jangra A, Lahkar M (2015) Mangiferin ameliorates aluminium chloride-induced cognitive dysfunction via alleviation of hippocampal oxido-nitrosative stress, proinflammatory cytokines and acetylcholinesterase level. J Trace Elem Med Biol 31:107–112

    Article  CAS  Google Scholar 

  • Kassab RB, Theyab A, Al-Ghamdy AO, Algahtani M, Mufti AH, Alsharif KF et al (2022) Protocatechuic acid abrogates oxidative insults, inflammation, and apoptosis in liver and kidney associated with monosodium glutamate intoxication in rats. Environ Sci Pollut Res Int 29(8):12208–12221. https://doi.org/10.1007/s11356-021-16578-4

    Article  CAS  Google Scholar 

  • Khalil HMA, Azouz RA, Hozyen HF, Aljuaydi SH, AbuBakr HO, Emam SR et al (2022) Selenium nanoparticles impart robust neuroprotection against deltamethrin-induced neurotoxicity in male rats by reversing behavioral alterations, oxidative damage, apoptosis, and neuronal loss. Neurotoxicology 91:329–339. https://doi.org/10.1016/j.neuro.2022.06.006

    Article  CAS  Google Scholar 

  • Lakshmi B, Sudhakar M, Prakash KS (2015) Protective effect of selenium against aluminum chloride-induced Alzheimer’s disease: behavioral and biochemical alterations in rats. Biol Trace Elem Res 165(1):67–74

    Article  CAS  Google Scholar 

  • Levine, R. L., Garland, D., Oliver, C. N., Amici, A., Climent, I., Lenz, A.-G., et al. (1990). [49] Determination of carbonyl content in oxidatively modified proteins. Methods in enzymology, Elsevier, pp. 464–478

  • Li Z, Li S, Hu L, Li F, Cheung AC, Shao W et al (2017) Mechanisms underlying action of Xinmailong injection, a traditional Chinese medicine in cardiac function improvement. Afr J Tradit Complement Altern Med 14(2):241–252

    Article  Google Scholar 

  • Li Z, Liu Y, Wang F, Gao Z, Elhefny MA, Habotta OA et al (2021) Neuroprotective effects of protocatechuic acid on sodium arsenate induced toxicity in mice: Role of oxidative stress, inflammation, and apoptosis. Chem Biol Interact 337:109392

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175

    Article  CAS  Google Scholar 

  • Mohamed KM, Abdelfattah MS, El-khadragy M, Al-Megrin WA, Fehaid A, Kassab RB et al. (2023). Rutin-loaded selenium nanoparticles modulated the redox status, inflammatory, and apoptotic pathways associated with pentylenetetrazole-induced epilepsy in mice. Green Process Synth 12(1):. https://doi.org/10.1515/gps-2023-0010.

  • Mohd Ariff A, Abu Bakar NA, Omar E, Ismail NH, Ali AM, Mohd Kasim NA et al (2020) Ficus deltoidea suppresses endothelial activation, inflammation, monocytes adhesion and oxidative stress via NF-κB and eNOS pathways in stimulated human coronary artery endothelial cells. BMC Complement Med Ther 20(1):1–13

    Article  Google Scholar 

  • Nakaji M, Hayashi Y, Ninomiya T, Yano Y, Yoon S, Seo Y et al (2002) Histological grading and staging in chronic hepatitis: its practical correlation. Pathol Int 52(11):683–690

    Article  Google Scholar 

  • Nurdiana S, Goh Y, Hafandi A, Dom S, Syimaláain AN, Syaffinaz NN et al (2018) Improvement of spatial learning and memory, cortical gyrification patterns and brain oxidative stress markers in diabetic rats treated with Ficus deltoidea leaf extract and vitexin. J Tradit Complement Med 8(1):190–202

    Article  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  Google Scholar 

  • Othman MS, Al-Bagawi AH, Obeidat ST, Fareid MA, Habotta OA, Moneim AEA (2022) Antitumor activity of zinc nanoparticles synthesized with berberine on human epithelial colorectal adenocarcinoma (Caco-2) cells through acting on Cox-2/NF-kB and p53 pathways. Anticancer Agents Med Chem 22(10):2002–2010. https://doi.org/10.2174/1871520621666211004115839

    Article  CAS  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169

    CAS  Google Scholar 

  • Pinz MP, Vogt AG, da Costa Rodrigues K, Dos Reis AS, Duarte LFB, Fronza MG et al (2021) 2021 Effect of a purine derivative containing selenium to improve memory decline and anxiety through modulation of the cholinergic system and Na(+)/K(+)-ATPase in an Alzheimer’s disease model. Metab Brain Dis 36(5):871–888. https://doi.org/10.1007/s11011-021-00703-w

    Article  CAS  Google Scholar 

  • Rodrigues KC, Bortolatto CF, da Motta KP, de Oliveira RL, Paltian JJ, Krüger R et al (2021) The neurotherapeutic role of a selenium-functionalized quinoline in hypothalamic obese rats. Psychopharmacology 238(7):1937–1951. https://doi.org/10.1007/s00213-021-05821-y

    Article  CAS  Google Scholar 

  • Sadek KM, Lebda MA, Abouzed TK, Nasr SM, Shoukry M (2017) Neuro- and nephrotoxicity of subchronic cadmium chloride exposure and the potential chemoprotective effects of selenium nanoparticles. Metab Brain Dis 32(5):1659–1673. https://doi.org/10.1007/s11011-017-0053-x

    Article  CAS  Google Scholar 

  • Shunan D, Yu M, Guan H, Zhou Y (2021) Neuroprotective effect of Betalain against AlCl3-induced Alzheimer’s disease in Sprague Dawley rats via putative modulation of oxidative stress and nuclear factor kappa B (NF-κB) signaling pathway. Biomed Pharmacother 137:111369. https://doi.org/10.1016/j.biopha.2021.111369

    Article  CAS  Google Scholar 

  • Sohn E, Kim YJ, Kim JH, Jeong SJ (2021) Ficus erecta Thunb leaves ameliorate cognitive deficit and neuronal damage in a mouse model of amyloid-β-induced Alzheimer’s disease. Front Pharmacol 12:607403. https://doi.org/10.3389/fphar.2021.607403

    Article  CAS  Google Scholar 

  • Subash, S., Essa, M. M., Al-Asmi, A., Al-Adawi, S., & Vaishnav, R. (2014). Chronic dietary supplementation of 4% figs on the modification of oxidative stress in Alzheimer’s disease transgenic mouse model. Biomed Res Int, 2014:546357. https://doi.org/10.1155/2014/546357.

  • Yin T, Yang L, Liu Y, Zhou X, Sun J, Liu J (2015) Sialic acid (SA)-modified selenium nanoparticles coated with a high blood-brain barrier permeability peptide-B6 peptide for potential use in Alzheimer’s disease. Acta Biomater 25:172–183. https://doi.org/10.1016/j.actbio.2015.06.035

    Article  CAS  Google Scholar 

  • Yuan X, Fu Z, Ji P, Guo L, Al-Ghamdy AO, Alkandiri A et al (2020) Selenium nanoparticles pre-treatment reverse behavioral, oxidative damage, neuronal loss and neurochemical alterations in pentylenetetrazole-induced epileptic seizures in mice. Int J Nanomed 15:6339

    Article  CAS  Google Scholar 

  • Yue D, Zeng C, Okyere SK, Chen Z, Hu Y (2021) Glycine nano-selenium prevents brain oxidative stress and neurobehavioral abnormalities caused by MPTP in rats. J Trace Elem Med Biol 64:126680. https://doi.org/10.1016/j.jtemb.2020.126680

    Article  CAS  Google Scholar 

  • Zhang Y, Li Y, Ma P, Chen J, Xie W (2020) Ficus carica leaves extract inhibited pancreatic β-cell apoptosis by inhibiting AMPK/JNK/caspase-3 signaling pathway and antioxidation. Biomed Pharmacother 122:109689

    Article  CAS  Google Scholar 

  • Zolkiffly SZI, Stanslas J, Abdul Hamid H, Mehat MZ (2021) Ficus deltoidea: potential inhibitor of pro-inflammatory mediators in lipopolysaccharide-induced activation of microglial cells. J Ethnopharmacol 279:114309. https://doi.org/10.1016/j.jep.2021.114309

    Article  CAS  Google Scholar 

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Funding

This research has been funded by the Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2023R23), Princess Nourah bint Abdulrahman Uinvsrsity Riyadh, Saudi Arabia.

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Mohga S. Abdalla, Ahmed E. Abdel Moneim, and Mohamed S. Abdelfattah: conceptualization and methodology. Sara S. Elganzoury and Ola A. Habotta: data curation and analysis. Manal F. El-Khadragy and Ola A. Habotta: resources, validation, writing — original draft preparation, and writing — reviewing and editing.

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Correspondence to Ahmed E. Abdel Moneim.

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The experimental protocol was reviewed and approved by the Committee of Research Ethics for Laboratory Animal Care, Department of Zoology and Entomology, Faculty of Science, Helwan University (Cairo, Egypt; approval no, HU2021/Z/AES0321-01).

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Elganzoury, S.S., Abdelfattah, M.S., Habotta, O.A. et al. Neuro-amelioration of Ficus lyrata (fiddle-leaf fig) extract conjugated with selenium nanoparticles against aluminium toxicity in rat brain: relevance to neurotransmitters, oxidative, inflammatory, and apoptotic events. Environ Sci Pollut Res 30, 65822–65834 (2023). https://doi.org/10.1007/s11356-023-26935-0

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