449
Views
1
CrossRef citations to date
0
Altmetric
Original Research

Nose to brain delivery of naringin-loaded chitosan nanoparticles for potential use in oxaliplatin-induced chemobrain in rats: impact on oxidative stress, cGAS/STING and HMGB1/RAGE/TLR2/MYD88 inflammatory axes

, ORCID Icon, &
Pages 1859-1873 | Received 17 Jan 2023, Accepted 26 May 2023, Published online: 27 Jun 2023

References

  • Ahles TA, Root JC, Ryan EL. Cancer- and cancer treatment–associated cognitive change: an update on the state of the science. J Clin Oncol. 2012 Oct 20;30(30):3675–3686.
  • John J, Kinra M, Mudgal J, et al. Animal models of chemotherapy-induced cognitive decline in preclinical drug development. Psychopharmacol (Berl). 2021 Nov 1;238(11):3025–3053.
  • Hwa Yun B, Guo J, Bellamri M, et al. DNA adducts: formation, biological effects, and new biospecimens for mass spectrometric measurements in humans. Mass Spectrom Rev. 2020 Mar 1;39(1–2):55–82.
  • Cui L, Zhang ZH, Sun E, et al. Effect of β-Cyclodextrin complexation on solubility and enzymatic conversion of naringin. Int J Mol Sci. 2012;13(11):14251–14261. doi: 10.3390/ijms131114251
  • Bai Y, Peng W, Yang C, et al. Pharmacokinetics and Metabolism of Naringin and Active Metabolite Naringenin in Rats, Dogs, Humans, and the Differences Between Species. Front Pharmacol. 2020;11:11. InternetAvailable from. https://www.frontiersin.org/articles/10.3389/fphar.2020.00364
  • Zbarsky V, Datla KP, Parkar S, et al. Neuroprotective properties of the natural phenolic antioxidants curcumin and naringenin but not quercetin and fisetin in a 6-OHDA model of Parkinson’s disease. Free Radic Res. 2005 Jan 1;39(10):1119–1125.
  • Ahmed S, Khan H, Aschner M, et al. Therapeutic potential of naringin in neurological disorders. Food Chem Toxicol. 2019 Oct 1;132:110646.
  • Chen R, Qi QL, Wang MT, et al. Therapeutic potential of naringin: an overview. Pharm Biol. 2016 Dec 1;54(12):3203–3210.
  • Formica ML, Real DA, Picchio ML, et al. On a highway to the brain: a review on nose-to-brain drug delivery using nanoparticles. Appl Mater Today. 2022 Dec 1;29:101631.
  • Agrawal M, Dethe MR, Ahmed H, et al. Nose-to-brain drug delivery for the treatment of Alzheimer’s disease: current advancements and challenges. Expert Opin Drug Deliv. 2022 Jan 2;19(1):87–102.
  • Montegiove N, Calzoni E, Emiliani C, et al. Biopolymer nanoparticles for nose-to-brain drug delivery: a new promising approach for the treatment of neurological diseases. J Funct Biomater. 2022;13(3):125. doi: 10.3390/jfb13030125
  • Alberto M, Paiva-Santos AC, Veiga F, et al. Lipid and polymeric nanoparticles: successful strategies for nose-to-brain drug delivery in the treatment of depression and anxiety disorders. Pharmaceutics. 2022;14(12):2742. doi: 10.3390/pharmaceutics14122742
  • Casettari L, Illum L. Chitosan in nasal delivery systems for therapeutic drugs. J Control Release. 2014 Sep 28;190:189–200. doi:10.1016/j.jconrel.2014.05.003.
  • El-Safy S, Tammam SN, Abdel-Halim M, et al. Collagenase loaded chitosan nanoparticles for digestion of the collagenous scar in liver fibrosis: the effect of chitosan intrinsic collagen binding on the success of targeting. Eur J Pharm Biopharm. 2020 Mar 1;148:54–66.
  • Jhaveri J, Raichura Z, Khan T, et al. Chitosan nanoparticles-insight into properties, functionalization and applications in drug delivery and theranostics. Molecules. 2021;26(2):272. doi: 10.3390/molecules26020272
  • Hassan RH, Gad HA, El-Din SB, et al. Chitosan nanoparticles for intranasal delivery of olmesartan medoxomil: pharmacokinetic and pharmacodynamic perspectives. Int J Pharm. 2022 Nov 25;628:122278.
  • Bhattamisra SK, Shak AT, Xi LW, et al. Nose to brain delivery of rotigotine loaded chitosan nanoparticles in human SH-SY5Y neuroblastoma cells and animal model of Parkinson’s disease. Int J Pharm. 2020 Apr 15;579:119148.
  • Wilson B, Mohamed Alobaid BN, Geetha KM, et al. Chitosan nanoparticles to enhance nasal absorption and brain targeting of sitagliptin to treat Alzheimer’s disease. J Drug Deliv Sci Technol. 2021 Feb 1;61:102176.
  • Sunena SS, Mishra DN. Nose to brain delivery of galantamine loaded nanoparticles: in-vivo pharmacodynamic and biochemical study in mice. Curr Drug Deliv. 2019;16(1):51–58. doi: 10.2174/1567201815666181004094707
  • Calvo P, Remuñán-López C, Vila-Jato JL, et al. Novel hydrophilic chitosan-polyethylene oxide nanoparticles as protein carriers. J Appl Polym Sci. 1997 Jan 3;63(1):125–132.
  • Abd-Allah H, Abdel-Aziz RTA, Nasr M. Chitosan nanoparticles making their way to clinical practice: a feasibility study on their topical use for acne treatment. Int j biol macromol. 2020 Aug 1;156:262–270. doi:10.1016/j.ijbiomac.2020.04.040.
  • Percie du Sert N, Hurst V, Ahluwalia A, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol. 2020 Jul 14;18(7):e3000410.
  • Kaur G, Prakash A. Involvement of the nitric oxide signaling in modulation of naringin against intranasal manganese and intracerbroventricular β-amyloid induced neurotoxicity in rats. J Nutr Biochem. 2020 Feb 1;76:108255. doi:10.1016/j.jnutbio.2019.108255.
  • Zhang X, Guan Z, Wang X, et al. Curcumin alleviates oxaliplatin-induced peripheral neuropathic pain through inhibiting oxidative stress-mediated activation of NF-κB and mitigating inflammation. Biol Pharm Bull. 2020;43(2):348–355. doi: 10.1248/bpb.b19-00862
  • Hanna DMF, Tadros MG, Khalifa AE. ADIOL protects against 3-NP-induced neurotoxicity in rats: possible impact of its anti-oxidant, anti-inflammatory and anti-apoptotic actions. Prog Neuropsychopharmacol Biol Psychiatry. 2015 Jul 3;60:36–51. doi:10.1016/j.pnpbp.2015.02.005.
  • Ayoub IM, George MY, Menze ET, et al. Insights into the neuroprotective effects of salvia officinalis L. and salvia microphylla kunth in the memory impairment rat model. Food Funct. 2022;13(4):2253–2268. doi: 10.1039/D1FO02988F
  • Ibrahim SS, Abo Elseoud OG, Mohamedy MH, et al. Nose-to-brain delivery of chrysin transfersomal and composite vesicles in doxorubicin-induced cognitive impairment in rats: insights on formulation, oxidative stress and TLR4/NF-Kb/NLRP3/NLRP3 pathways. Neuropharmacology. 2021 Oct 1;197:108738. doi:10.1016/j.neuropharm.2021.108738.
  • George MY, El-Derany MO, Ahmed Y, et al. Design and evaluation of chrysin-loaded nanoemulsion against lithium/pilocarpine-induced status epilepticus in rats; emphasis on formulation, neuronal excitotoxicity, oxidative stress, microglia polarization, and AMPK/SIRT-1/PGC-1α pathway. Expert Opin Drug Deliv. 2023 Jan 2;20(1):159–174.
  • Bancroft JD, Gamble M. Theory and practice of histological techniques. In: Bancroft J Gamble M, editors. Theory and practice of histological techniques. Sixth Edition) [Internet ed. Edinburgh: Churchill Livingstone; 2008. p. ix. Available from: https://www.sciencedirect.com/science/article/pii/B978044310279050004X
  • Ellman GL, Courtney KD, Andres V, et al. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961 Jul 1;7(2):88–95.
  • Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963 May;61:882–888.
  • Satoh K. Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta. 1978 Nov 15;90(1):37–43.
  • Skehan P, Storeng R, Scudiero D, et al. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst. 1990 Jul 4;82(13):1107–1112.
  • Was H, Borkowska A, Bagues A, et al., Mechanisms of chemotherapy-induced neurotoxicity. Front Pharmacol. 13: InternetAvailable from. 2022; 10.3389/fphar.2022.750507.
  • Liu H, Gao C. Preparation and properties of ionically cross-linked chitosan nanoparticles. Polym Adv Technol. 2009 Jul 1;20(7):613–619.
  • Fereig SA, El-Zaafarany GM, Arafa MG, et al. Tacrolimus-loaded chitosan nanoparticles for enhanced skin deposition and management of plaque psoriasis. Carbohydr Polym. 2021 Sep 15;268:118238.
  • Gan Q, Wang T, Cochrane C, et al. Modulation of surface charge, particle size and morphological properties of chitosan–TPP nanoparticles intended for gene delivery. Colloids Surf B Biointerfaces. 2005 Aug 1;44(2):65–73.
  • Elmowafy E, Osman R, El-Shamy AH, et al. Nanocomplexes of an insulinotropic drug: optimization, microparticle formation, and antidiabetic activity in rats. Int J Nanomedicine. 2014;9:4449–4465. doi: 10.2147/IJN.S66876
  • Deng QY, Zhou CR, Luo BH. Preparation and characterization of chitosan nanoparticles containing lysozyme. Pharmaceutical Biology. 2006 Jan 1;44(5):336–342.
  • Hashad RA, Ishak RAH, Fahmy S, et al. Chitosan-tripolyphosphate nanoparticles: optimization of formulation parameters for improving process yield at a novel pH using artificial neural networks. Int j biol macromol. 2016 May 1;86:50–58.
  • Bianchi E, Di Cesare Mannelli L, Micheli L, et al. Apoptotic process induced by oxaliplatin in rat hippocampus causes memory impairment. Basic Clin Pharmacol Toxicol. 2017 Jan 1;120(1):14–21.
  • Fardell JE, Vardy J, Monds LA, et al. The long-term impact of oxaliplatin chemotherapy on rodent cognition and peripheral neuropathy. Behav Brain Res. 2015 Sep 15;291:80–88.
  • Fardell JE, Vardy J, Shah JD, et al. Cognitive impairments caused by oxaliplatin and 5-fluorouracil chemotherapy are ameliorated by physical activity. Psychopharmacol (Berl). 2012 Mar 1;220(1):183–193.
  • Johnston IN, Tan M, Cao J, et al. Ibudilast reduces oxaliplatin-induced tactile allodynia and cognitive impairments in rats. Behav Brain Res. 2017 Sep 15;334:109–118.
  • Zhou X, Huang Z, Zhang J, et al. Chronic oral administration of magnesium-l-threonate prevents oxaliplatin-induced memory and emotional deficits by normalization of TNF-α/NF-κB signaling in rats. Neurosci Bull. 2021 Jan 1;37(1):55–69.
  • Prakash A, Shur B, Kumar A. Naringin protects memory impairment and mitochondrial oxidative damage against aluminum-induced neurotoxicity in rats. Int J Neurosci. 2013 Sep 1;123(9):636–645.
  • Chtourou Y, Gargouri B, Kebieche M, et al. Naringin abrogates cisplatin-induced cognitive deficits and cholinergic dysfunction through the down-regulation of AChE expression and iNOS signaling pathways in hippocampus of aged rats. J Mol Neurosci. 2015 Jun 1;56(2):349–362.
  • Kwatra M, Jangra A, Mishra M, et al. Naringin and sertraline ameliorate doxorubicin-induced behavioral deficits through modulation of serotonin level and mitochondrial complexes protection pathway in rat hippocampus. Neurochem Res. 2016 Sep 1;41(9):2352–2366.
  • George MY, Menze ET, Esmat A, et al. Potential therapeutic antipsychotic effects of Naringin against ketamine-induced deficits in rats: involvement of Akt/GSK-3β and Wnt/β-catenin signaling pathways. Life Sci. 2020 May 15;249:117535.
  • Meng X, Fu M, Wang S, et al. Naringin ameliorates memory deficits and exerts neuroprotective effects in a mouse model of Alzheimer’s disease by regulating multiple metabolic pathways. Mol Med Rep. 2021 May 1;23(5):332.
  • Hassan HM, Elnagar MR, Abdelrazik E, et al., Neuroprotective effect of naringin against cerebellar changes in Alzheimer’s disease through modulation of autophagy, oxidative stress and tau expression: an experimental study. Front Neuroanat. 16: InternetAvailable from. 2022; 10.3389/fnana.2022.1012422.
  • Semis HS, Kandemir FM, Caglayan C, et al. Protective effect of naringin against oxaliplatin-induced peripheral neuropathy in rats: a behavioral and molecular study. J Biochem Mol Toxicol. 2022 Sep 1;36(9):e23121.
  • Ren X, Clair D, Butterfield DA. Dysregulation of cytokine mediated chemotherapy induced cognitive impairment. Pharmacological Research. 2017 Mar 1;117:267–273. doi:10.1016/j.phrs.2017.01.001.
  • Jacobs S, McCully CL, Murphy RF, et al. Extracellular fluid concentrations of cisplatin, carboplatin, and oxaliplatin in brain, muscle, and blood measured using microdialysis in nonhuman primates. Cancer Chemother Pharmacol. 2010 Apr 1;65(5):817–824.
  • Valerio Branca JJ, Maresca M, Morucci G, et al. Oxaliplatin-induced blood brain barrier loosening: a new point of view on chemotherapy-induced neurotoxicity. Oncotarget [Internet]. 2018 [cited 2018 Jan 1]; Available from: https://www.oncotarget.com/article/25193/text/
  • Jugait S, Areti A, Nellaiappan K, et al. Neuroprotective Effect of baicalein against oxaliplatin-induced peripheral neuropathy: impact on oxidative stress, neuro-inflammation and WNT/β-catenin signaling. Mol Neurobiol. 2022 Jul 1;59(7):4334–4350.
  • Podratz JL, Staff NP, Froemel D, et al. Drosophila melanogaster: a new model to study cisplatin-induced neurotoxicity. Neurobiol Dis. 2011 Aug 1;43(2):330–337.
  • Fong CW. Platinum anti-cancer drugs: free radical mechanism of Pt-DNA adduct formation and anti-neoplastic effect. Free Radic Biol Med. 2016 Jun 1;95:216–229. doi:10.1016/j.freeradbiomed.2016.03.006.
  • Viswanatha GL, Shylaja H, Moolemath Y. The beneficial role of Naringin- a citrus bioflavonoid, against oxidative stress-induced neurobehavioral disorders and cognitive dysfunction in rodents: a systematic review and meta-analysis. Biomed Pharmacother. 2017 Oct 1;94:909–929. doi:10.1016/j.biopha.2017.07.072.
  • Kwon J, Bakhoum SF. The Cytosolic DNA-Sensing Cgas–STING pathway in cancer. Cancer Discov. 2020 Jan 9;10(1):26–39.
  • Yum S, Li M, Chen ZJ. Old dogs, new trick: classic cancer therapies activate cGAS. Cell Res. 2020 Aug 1;30(8):639–648.
  • Decout A, Katz JD, Venkatraman S, et al. The Cgas–STING pathway as a therapeutic target in inflammatory diseases. Nat Rev Immunol. 2021 Sep 1;21(9):548–569.
  • Li K, Gong Y, Qiu D, et al. Hyperbaric oxygen facilitates teniposide-induced Cgas-STING activation to enhance the antitumor efficacy of PD-1 antibody in HCC. J Immunother Cancer. 2022 Aug 1;10(8):e004006.
  • Tsubota M, Fukuda R, Hayashi Y, et al. Role of non-macrophage cell-derived HMGB1 in oxaliplatin-induced peripheral neuropathy and its prevention by the thrombin/thrombomodulin system in rodents: negative impact of anticoagulants. J Neuroinflammation. 2019 Oct 30;16(1):199.
  • Sims GP, Rowe DC, Rietdijk ST, et al. HMGB1 and RAGE in Inflammation and Cancer. Annu Rev Immunol. 2010 Mar 1;28(1):367–388.
  • Andersson U, Yang H, Harris H. Extracellular HMGB1 as a therapeutic target in inflammatory diseases. Expert Opin Ther Targets. 2018 Mar 4;22(3):263–277.
  • Gil M, Kim YK, Hong SB, et al. Naringin decreases TNF-α and HMGB1 release from LPS-Stimulated macrophages and improves survival in a CLP-Induced sepsis mice. PLoS One. 2016 Oct 7;11(10):e0164186.
  • Wang H, Xu YS, Wang ML, et al. Protective effect of naringin against the LPS-induced apoptosis of PC12 cells: implications for the treatment of neurodegenerative disorders. Int J Mol Med. 2017 Apr 1;39(4):819–830.
  • Syed AA, Reza MI, Shafiq M, et al. Naringin ameliorates type 2 diabetes mellitus-induced steatohepatitis by inhibiting RAGE/NF-κB mediated mitochondrial apoptosis. Life Sci. 2020 Sep 15;257:118118.
  • Cheng H, Jiang X, Zhang Q, et al. Naringin inhibits colorectal cancer cell growth by repressing the PI3K/AKT/mTOR signaling pathway. Exp Ther Med. 2020 Jun 1;19(6):3798–3804.
  • Feng J, Chen X, Lu S, et al. Naringin attenuates cerebral ischemia-reperfusion injury through inhibiting peroxynitrite-mediated mitophagy activation. Mol Neurobiol. 2018 Dec 1;55(12):9029–9042.
  • Vllasaliu D, Exposito-Harris R, Heras A, et al. Tight junction modulation by chitosan nanoparticles: comparison with chitosan solution. Int J Pharm. 2010 Nov 15;400(1):183–193.

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.