Assessment of the protective and ameliorative impact of quercetin nanoparticles against neuronal damage induced in the hippocampus by acrolein
Tóm tắt
The most frequent kind of dementia in the senior population is Alzheimer's disease (AD). Antioxidant quercetin has a low bioavailability. The bioavailability of quercetin nanoparticles was demonstrated to be higher. Acrolein is thought to be the strongest unsaturated aldehyde. Acrolein contributes to the propagation of oxidative damage and thus the aetiology of AD. This study aimed to investigate histopathological and ultrastructural changes that may arise in the hippocampus following acrolein treatment. Quercetin nanoparticles' ameliorative and protective effects on acrolein-induced neurotoxicity and oxidative stress were assessed.
We successfully synthesised quercetin nanoparticles with uniform size distributions and particle diameters in the range of 3.63–4.57 nm using transmission electron microscopy (TEM) and 3.7 nm using dynamic light scattering (DLS). Administration of acrolein was associated with histopathological alterations in the hippocampal structure, such as increased apoptotic neurones, dystrophic changes, neuronophagia, and atrophic ischaemia in cells, as well as marked damage to the ultrastructure of the hippocampus, which was obvious in shrunken pyramidal neurones with pyknotic nuclei and completely degenerated chromatin material, as well as in damaged astrocytes and microglial cells. Treatment with quercetin nanoparticles has been found to protect against and ameliorate the toxic effects and oxidative stress induced by acrolein in the hippocampus.
This could pave the way for additional research in nanomedicine and a new line of therapeutic intervention in AD using nanoparticles such as quercetin nanoparticles.
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Tài liệu tham khảo
Abd El-Rahmanand SN, Suhailah S (2014) Quercetin nanoparticles: preparation and characterization. Indian J Drugs 2:96–103
Abraham K, Andres S, Palavinskas R, Berg K, Appel KE, Lampen A (2011) Toxicology and risk assessment of acrolein in food. Mol Nutr Food Res 55:1277–1290
Afifi OK, Embaby AS (2016) Histological study on the protective role of ascorbic acid on cadmium-induced cerebral cortical neurotoxicity in adult male albino rats. J Microsc Ultrastruct 4:36–45
Alizadeh A, Dyck SM, Karimi-Abdolrezaee S (2015) Myelin damage and repair in pathologic CNS: challenges and prospects. Front Mol Neurosci 8:35
Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14
Aytac Z, Kusku SI, Durgun E, Uyar T (2016) Quercetin/β-cyclodextrin inclusion complex embedded nanofibres: slow release and high solubility. Food Chem 197:864–871
Batiha GE-S, Beshbishy AM, Ikram M, Mulla ZS, El-Hack MEA, Taha AE et al (2020) The pharmacological activity, biochemical properties, and pharmacokinetics of the major natural polyphenolic flavonoid: Quercetin. Foods 9:374
Birinci Y, Niazi JH, Aktay-Çetin O, Basaga H (2020) Quercetin in the form of a nano-antioxidant (QTiO2) provides stabilization of quercetin and maximizes its antioxidant capacity in the mouse fibroblast model. Enzyme Microb Technol 138:109559
Bisht K, Sharma KP, Lecours C, Gabriela Sánchez M, El Hajj H, Milior G et al (2016) Dark microglia: a new phenotype predominantly associated with pathological states. Glia 64:826–839
Caruthers SD, Wickline SA, Lanza GM (2007) Nanotechnological applications in medicine. Curr Opin Biotechnol 18:26–30
Chen B-Q, Zhao Y, Zhang Y, Pan Y-J, Xia H-Y, Kankala RK et al (2023) Immune-regulating camouflaged nanoplatforms: a promising strategy to improve cancer nano-immunotherapy. Bioactive Mater 21:1–19
Chen C, Lu J, Peng W, Mak MS, Yang Y, Zhu Z et al (2022) Acrolein, an endogenous aldehyde induces Alzheimer’s disease-like pathologies in mice: a new sporadic AD animal model. Pharmacol Res 175:106003
da Silva BL, Schnorr CE, Santos DC, Rostirolla DC, Moresco KS, Ozório P et al (2020) Chronic acrolein exposure in Wistar rats: the effects of guarana extracts. J Funct Foods 65:103733
Dhawan S, Kapil R, Singh B (2011) Formulation development and systematic optimization of solid lipid nanoparticles of quercetin for improved brain delivery. J Pharm Pharmacol 63:342–351
Ebokaiwe AP, Ushang OR, Ogunwa TH, Kikiowo B, Olusanya O (2022) Quercetin attenuates cyclophosphamide induced-immunosuppressive indoleamine 2, 3-dioxygenase in the hippocampus and cerebral cortex of male Wister rats. J Biochem Mol Toxicol 36:e23179
El-Maghrabey MH, El-Shaheny R, El Hamd MA, Al-Khateeb LA, Kishikawa N, Kuroda N (2022) Aldehydes’ sources, toxicity, environmental analysis, and control in food. In: Organic pollutants: toxicity and solutions, pp 117–151
Erhan E, Salcan I, Bayram R, Suleyman B, Dilber M, Yazici GN et al (2021) Protective effect of lutein against acrolein-induced ototoxicity in rats. Biomed Pharmacother 137:111281
Fujikawa DG, Zhao S, Ke X, Shinmei SS, Allen SG (2010) Mild as well as severe insults produce necrotic, not apoptotic, cells: evidence from 60-min seizures. Neurosci Lett 469:333–337
Ghaffari F, Moghaddam AH, Zare M (2018) Neuroprotective effect of quercetin nanocrystal in a 6-hydroxydopamine model of Parkinson disease: biochemical and behavioural evidence. Basic Clin Neurosci 9:317
Ghoneim FM, Khalaf HA, Elsamanoudy AZ, El-Khair SMA, Helaly AM, Mahmoud E-HM et al (2015) Protective effect of chronic caffeine intake on gene expression of brain-derived neurotrophic factor signalling and the immunoreactivity of glial fibrillary acidic protein and Ki-67 in Alzheimer’s disease. Int J Clin Exp Pathol 8:7710
Ghosh A, Mandal AK, Sarkar S, Panda S, Das N (2009) Nanoencapsulation of quercetin enhances its dietary efficacy in combating arsenic-induced oxidative damage in the liver and brain of rats. Life Sci 84:75–80
Ghosh A, Sarkar S, Mandal AK, Das N (2013) Neuroprotective role of nano encapsulated quercetin in combating ischemia-reperfusion induced neuronal damage in young and aged rats. PLoS ONE 8:e57735
Gianaris A, Liu N-K, Wang X-F, Oakes E, Brenia J, Gianaris T et al (2016) Unilateral microinjection of acrolein into thoracic spinal cord produces acute and chronic injury and functional deficits. Neuroscience 326:84–94
Gigault J, El Hadri H, Nguyen B, Grassl B, Rowenczyk L, Tufenkji N et al (2021) Nanoplastics are neither microplastics nor engineered nanoparticles. Nat Nanotechnol 16:501–507
Goma AA, El Okle OS, Tohamy HG (2021) Protective effect of methylene blue against copper oxide nanoparticle-induced neurobehavioral toxicity. Behav Brain Res 398:112942
Grewal AK, Singh TG, Sharma D, Sharma V, Singh M, Rahman MH et al (2021) Mechanistic insights and perspectives involved in neuroprotective action of quercetin. Biomed Pharmacother 140:111729
Hayden MR, Grant DG, Aroor AR, DeMarco VG (2018) Ultrastructural remodelling of the neurovascular unit in the female diabetic db/db model–part II: microglia and mitochondria. Neuroglia 1:311–326
Hellwig K, Kvartsberg H, Portelius E, Andreasson U, Oberstein TJ, Lewczuk P et al (2015) Neurogranin and YKL-40: independent markers of synaptic degeneration and neuroinflammation in Alzheimer’s disease. Alzheimer’s Res Therapy 7:1–8
Henning RJ, Johnson GT, Coyle JP, Harbison RD (2017) Acrolein can cause cardiovascular disease: a review. Cardiovasc Toxicol 17:227–236
Hernández-Cruz EY, Amador-Martínez I, Aranda-Rivera AK, Cruz-Gregorio A, Chaverri JP (2022) Renal damage induced by cadmium and its possible therapy by mitochondrial transplantation. Chem Biol Interact 361:109961
Huang Y-J, Jin M-H, Pi R-B, Zhang J-J, Ouyang Y, Chao X-J et al (2013) Acrolein induces Alzheimer’s disease-like pathologies in vitro and in vivo. Toxicol Lett 217:184–191
Huang Y, Qin J, Chen M, Chao X, Chen Z, Ramaswamy C et al (2014) Lithium prevents acrolein-induced neurotoxicity in HT22 mouse hippocampal cells. Neurochem Res 39:677–684
Iyer AM, Dadlani V, Pawar HA (2022) Review on acrylamide: a hidden hazard in fried carbohydrate-rich food. Curr Nutr Food Sci 18:274–286
Jiménez-Morales JM, Hernández-Cuenca YE, Reyes-Abrahantes A, Ruiz-García H, Barajas-Olmos F, García-Ortiz H et al (2022) MicroRNA delivery systems in glioma therapy and perspectives: a systematic review. J Control Release 349:712–730
Jing M, Jiang Q, Zhu Y, Fan D, Wang M, Zhao Y (2022) Effect of acrolein, a lipid oxidation product, on the formation of the heterocyclic aromatic amine 2-amino-1-methyl-6-phenylimidazo [4, 5-b] pyridine (PhIP) in model systems and roasted tilapia fish patties. Food Chem X 14:100315
Kakran M, Sahoo NG, Li L, Judeh Z (2012) Fabrication of quercetin nanoparticles by anti-solvent precipitation method for enhanced dissolution. Powder Technol 223:59–64
Kalafatakis I, Savvaki M, Velona T, Karagogeos D (2021) Implication of contactins in demyelinating pathologies. Life 11:51
Kaur D, Sharma V, Deshmukh R (2019) Activation of microglia and astrocytes: a roadway to neuroinflammation and Alzheimer’s disease. Inflammopharmacology 27:663–677
Khammash D, Rajagopal SK, Polk TA (2023) The neurobiology of ageing. In: Neurobiology of brain disorders, 977–993
Khoramjouy M, Naderi N, Kobarfard F, Heidarli E, Faizi M (2021) An intensified acrolein exposure can affect memory and cognition in rats. Neurotox Res 39:277–291
Kobori M, Takahashi Y, Sakurai M, Akimoto Y, Tsushida T, Oike H et al (2016) Quercetin suppresses immune cell accumulation and improves mitochondrial gene expression in adipose tissue of diet-induced obese mice. Mol Nutr Food Res 60:300–312
Krstic D, Knuesel I (2013) Deciphering the mechanism underlying late-onset Alzheimer’s disease. Nat Rev Neurol 9:25–34
Krukowski K, Nolan A, Becker M, Picard K, Vernoux N, Frias ES et al (2021) Novel microglia-mediated mechanisms underlying synaptic loss and cognitive impairment after traumatic brain injury. Brain Behav Immunity 98:122–135
Kumar M, Bansal N (2022) A revisit to etiopathogenesis and therapeutic strategies in Alzheimer’s disease. Curr Drug Targets 23:486–512
Kuo Y-C, Chou P-R (2014) Neuroprotection against degeneration of SK-N-MC cells using neuron growth factor-encapsulated liposomes with the surface report and transferrin. J Pharm Sci 103:2484–2497
Lai F, Franceschini I, Corrias F, Sala MC, Cilurzo F, Sinico C et al (2015) Maltodextrin fast dissolving films for quercetin nanocrystal delivery. A feasibility study. Carbohydr Polym 121:217–223
Leung G, Sun W, Zheng L, Brookes S, Tully M, Shi R (2011) Anti-acrolein treatment improves behavioural outcome and alleviates myelin damage in experimental autoimmune encephalomyelitis mouse. Neuroscience 173:150–155
Li H, Zhao X, Ma Y, Zhai G, Li L, Lou H (2009) Enhancement of gastrointestinal absorption of quercetin by solid lipid nanoparticles. J Control Release 133:238–244
Li Z, Deng H, Guo X, Yan S, Lu C, Zhao Z et al (2022) Effective dose/duration of natural flavonoid quercetin for treatment of diabetic nephropathy: a systematic review and meta-analysis of rodent data. Phytomedicine 154348.
Luo C-l, Liu Y-q, Wang P, Song C-h, Wang K-j, Dai L-p et al (2016) The effect of quercetin nanoparticle on cervical cancer progression by inducing apoptosis, autophagy and anti-proliferation via JAK2 suppression. Biomed Pharmacother 82:595–605
Maczurek A, Hager K, Kenklies M, Sharman M, Martins R, Engel J et al (2008) Lipoic acid as an anti-inflammatory and neuroprotective treatment for Alzheimer’s disease. Adv Drug Deliv Rev 60:1463–1470
Masters CL, Bateman R, Blennow K, Rowe CC, Sperling RA, Cummings JL (2015) Alzheimer’s disease. Nat Rev Dis Primers 1:1–18
Meng Q, Meng H, Pan Y, Liu J, Li J, Qi Y et al (2022) Influence of nanoparticle size on blood–brain barrier penetration and the accumulation of anti-seizure medicines in the brain. J Mater Chem B 10:271–281
Michala A-S, Pritsa A (2022) Quercetin: a molecule of great biochemical and clinical value and its beneficial effect on diabetes and cancer. Diseases 10:37
Millar PR, Luckett PH, Gordon BA, Benzinger TL, Schindler SE, Fagan AM et al (2022) Predicting brain age from functional connectivity in symptomatic and preclinical Alzheimer disease. Neuroimage 256:119228
Minaei A, Sabzichi M, Ramezani F, Hamishehkar H, Samadi N (2016) Co-delivery with nano-quercetin enhances doxorubicin-mediated cytotoxicity against MCF-7 cells. Mol Biol Rep 43:99–105
Mishra R, Kulkarni S (2022) A review of various pharmacological effects of quercetin with its barriers and approaches for solubility and permeability enhancement. Nat Prod J 12:9–21
Mohamed HK, Mohamed HZ-E-A (2018) A histological and immunohistochemical study on the possible protective role of silymarin on cerebellar cortex neurotoxicity of lactating albino rats and their pups induced by gibberellic acid during late pregnancy and early postnatal period. Egyptian Journal of Histology 41:345–371
Mori F, Tanji K, Yoshida Y, Wakabayashi K (2002) Thalamic retrograde degeneration in the congenitally hydrocephalic rat is attributable to apoptotic cell death. Neuropathology 22:186–193
Nahum V, Domb AJ (2022) Solid lipid microspheres decorated nanoparticles as drug carriers. Int J Pharm 621:121797
Nasrabady SE, Rizvi B, Goldman JE, Brickman AM (2018) White matter changes in Alzheimer’s disease: a focus on myelin and oligodendrocytes. Acta Neuropathol Commun 6:1–10
Palle S, Neerati P (2017) Quercetin nanoparticles attenuate scopolamine-induced spatial memory deficits and pathological damages in rats. Bull Facul Pharm Cairo Univ 55:101–106
Pinheiro R, Granja A, Loureiro JA, Pereira M, Pinheiro M, Neves AR et al (2020) Quercetin lipid nanoparticles functionalized with transferrin for Alzheimer’s disease. Eur J Pharm Sci 148:105314
Pocernich CB, Butterfield DA (2012) Elevation of glutathione as a therapeutic strategy in Alzheimer’s disease. BBA-Mol Basis Dis 1822:625–630
Qin L-H, Wang C, Qin L-W, Liang Y-F, Wang G-H (2019) Spore powder of Ganoderma lucidum for Alzheimer's disease: a protocol for systematic review. Medicine 98
Rahman MM, Islam MR, Akash S, Harun-Or-Rashid M, Ray TK, Rahaman MS et al (2022) Recent advancements of nanoparticles application in cancer and neurodegenerative disorders: at a glance. Biomed Pharmacother 153:113305
Ries M, Sastre M (2016) Mechanisms of Aβ clearance and degradation by glial cells. Front Ageing Neurosci 8:160
Rifaai RA, Mokhemer SA, Saber EA, Abd El-Aleem SA, El-Tahawy NFG (2020) Neuroprotective effect of quercetin nanoparticles: a possible prophylactic and therapeutic role in Alzheimer’s disease. J Chem Neuroanat 107:101795
Riphagen JM, Suresh MB, Salat DH, AsDN I (2022) The canonical pattern of Alzheimer’s disease atrophy is linked to white matter hyperintensities in normal controls, differently in normal controls compared to in AD. Neurobiol Aging 114:105–112
Rummel NG, Butterfield DA (2022) Altered metabolism in Alzheimer disease brain: role of oxidative stress. Antioxid Redox Signal 36:1289–1305
Salahuddin P, Fatima MT, Uversky VN, Khan RH, Islam Z, Furkan M (2021) The role of amyloids in Alzheimer’s and Parkinson’s diseases. Int J Biol Macromol 190:44–55
Salter MW, Stevens B (2017) Microglia emerge as central players in brain disease. Nat Med 23:1018–1027
Savonenko AV, Wong PC, Li T (2023) Alzheimer diseases. Neurobiology of brain disorders. Elsevier, pp 313–336
Selmanoğlu G, Özgün GM, Karacaoğlu E (2018) Acrolein-mediated neurotoxicity in growing Wistar male rats. Pestic Biochem Physiol 149:37–43
Selvakumar K, Bavithra S, Krishnamoorthy G, Arunakaran J (2018) Impact of quercetin on tight junctional proteins and BDNF signalling molecules in the hippocampus of PCBs-exposed rats. Interdiscip Toxicol 11:294
Suvarna KS, Layton C, Bancroft JD (2018) Bancroft's theory and practice of histological techniques. Elsevier health sciences