Nasal Administration of bFGF-Loaded Nanoliposomes Attenuates Neuronal Injury and Cognitive Deficits in Mice with Vascular Dementia Induced by Repeated Cerebral Ischemia‒Reperfusion

References

• Sharma B, Singh N. Pitavastatin and 4’-hydroxy-3’-methoxyacetophenone (HMAP) reduce cognitive dysfunction in vascular dementia during experimental diabetes. Curr Neurovasc Res. 2010;7(3):180–191. doi:10.2174/156720210792231831
   PubMed Web of Science ®Google Scholar
• Sharma B, Singh N. Attenuation of vascular dementia by sodium butyrate in streptozotocin diabetic rats. Psychopharmacology. 2011;215(4):677–687. doi:10.1007/s00213-011-2164-0
   PubMed Web of Science ®Google Scholar
• Gorelick PB, Scuteri A, Black SE, et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American heart association/American stroke association. Stroke. 2011;42(9):2672–2713. doi:10.1161/STR.0b013e3182299496
   PubMed Web of Science ®Google Scholar
• O’Brien JT, Thomas A. Vascular dementia. Lancet. 2015;386(10004):1698–1706. doi:10.1016/S0140-6736(15)00463-8
   PubMed Web of Science ®Google Scholar
• Toyama K, Koibuchi N, Uekawa K, et al. Apoptosis signal-regulating kinase 1 is a novel target molecule for cognitive impairment induced by chronic cerebral hypoperfusion. Arteriosclerosis Thrombosis Vasc Biol. 2014;34(3):616–625. doi:10.1161/ATVBAHA.113.302440
   PubMed Web of Science ®Google Scholar
• Wang J, Jin H, Hua Y, Keep RF, Xi G. Role of protease-activated receptor-1 in brain injury after experimental global cerebral ischemia. Stroke. 2012;43(9):2476–2482. doi:10.1161/STROKEAHA.112.661819
   PubMed Web of Science ®Google Scholar
• Khan S, Yuldasheva NY, Batten TFC, Pickles AR, Kellett KAB, Saha S. Tau pathology and neurochemical changes associated with memory dysfunction in an optimised murine model of global cerebral ischaemia - a potential model for vascular dementia? Neurochem Int. 2018;118:134–144. doi:10.1016/j.neuint.2018.04.004
   PubMed Web of Science ®Google Scholar
• Siracusa R, Impellizzeri D, Cordaro M, et al. anti-inflammatory and neuroprotective effects of co-UltraPEALut in a mouse model of vascular dementia. Front Neurol. 2017;8:233. doi:10.3389/fneur.2017.00233
   PubMed Web of Science ®Google Scholar
• Lénárt N, Brough D, Dénes Á. Inflammasomes link vascular disease with neuroinflammation and brain disorders. J Cereb Blood Flow Metab. 2016;36(10):1668–1685. doi:10.1177/0271678X16662043
   PubMed Web of Science ®Google Scholar
• Zhu T, Zhu M, Qiu Y, et al. Puerarin alleviates vascular cognitive impairment in vascular dementia rats. Front Behav Neurosci. 2021;15:717008. doi:10.3389/fnbeh.2021.717008
   PubMed Web of Science ®Google Scholar
• Du SQ, Wang XR, Xiao LY, et al. Molecular mechanisms of vascular dementia: what can be learned from animal models of chronic cerebral hypoperfusion? Mol Neurobiol. 2017;54(5):3670–3682. doi:10.1007/s12035-016-9915-1
   PubMed Web of Science ®Google Scholar
• Cervellati C, Romani A, Seripa D, et al. Oxidative balance, homocysteine, and uric acid levels in older patients with Late Onset Alzheimer’s Disease or Vascular Dementia. J Neurol Sci. 2014;337(1–2):156–161. doi:10.1016/j.jns.2013.11.041
   PubMed Web of Science ®Google Scholar
• Werner S, Unsicker K, von Bohlen Und Halbach O. Fibroblast growth factor-2 deficiency causes defects in adult hippocampal neurogenesis, which are not rescued by exogenous fibroblast growth factor-2. J Neurosci Res. 2011;89(10):1605–1617. doi:10.1002/jnr.22680
   PubMed Web of Science ®Google Scholar
• Woodbury ME, Ikezu T. Fibroblast growth factor-2 signaling in neurogenesis and neurodegeneration. J Neuroimmune Pharmacol. 2014;9(2):92–101. doi:10.1007/s11481-013-9501-5
   PubMed Web of Science ®Google Scholar
• Tang MM, Lin WJ, Zhang JT, Zhao YW, Li YC. Exogenous FGF2 reverses depressive-like behaviors and restores the suppressed FGF2-ERK1/2 signaling and the impaired hippocampal neurogenesis induced by neuroinflammation. Brain Behav Immun. 2017;66:322–331. doi:10.1016/j.bbi.2017.05.013
   PubMed Web of Science ®Google Scholar
• Guo ZH, Mattson MP. Neurotrophic factors protect cortical synaptic terminals against amyloid and oxidative stress-induced impairment of glucose transport, glutamate transport and mitochondrial function. Cereb Cortex. 2000;10(1):50–57. doi:10.1093/cercor/10.1.50
   PubMed Web of Science ®Google Scholar
• Zhao YZ, Lin M, Lin Q, et al. Intranasal delivery of bFGF with nanoliposomes enhances in vivo neuroprotection and neural injury recovery in a rodent stroke model. J Control Release. 2016;224:165–175. doi:10.1016/j.jconrel.2016.01.017
   PubMed Web of Science ®Google Scholar
• Lochhead JJ, Thorne RG. Intranasal delivery of biologics to the central nervous system. Adv Drug Delivery Rev. 2012;64(7):614–628. doi:10.1016/j.addr.2011.11.002
   PubMed Web of Science ®Google Scholar
• Mainardes RM, Urban MC, Cinto PO, Chaud MV, Evangelista RC, Gremião MP. Liposomes and micro/nanoparticles as colloidal carriers for nasal drug delivery. Curr Drug Delivery. 2006;3(3):275–285. doi:10.2174/156720106777731019
   PubMedGoogle Scholar
• Hong SS, Oh KT, Choi HG, Lim SJ. Liposomal formulations for nose-to-brain delivery: recent advances and future perspectives. Pharmaceutics. 2019;11(10):540. doi:10.3390/pharmaceutics11100540
   PubMed Web of Science ®Google Scholar
• Fan Y, Chen M, Zhang J, Maincent P, Xia X, Wu W. Updated progress of nanocarrier-based intranasal drug delivery systems for treatment of brain diseases. Crit Rev Ther Drug Carrier Syst. 2018;35(5):433–467. doi:10.1615/CritRevTherDrugCarrierSyst.2018024697
   PubMed Web of Science ®Google Scholar
• Zhang C, Chen J, Feng C, et al. Intranasal nanoparticles of basic fibroblast growth factor for brain delivery to treat Alzheimer’s disease. Int J Pharm. 2014;461(1–2):192–202. doi:10.1016/j.ijpharm.2013.11.049
   PubMed Web of Science ®Google Scholar
• Khan AR, Liu M, Khan MW, Zhai G. Progress in brain targeting drug delivery system by nasal route. J Control Release. 2017;268:364–389. doi:10.1016/j.jconrel.2017.09.001
   PubMed Web of Science ®Google Scholar
• Upadhyay P, Trivedi J, Pundarikakshudu K, Sheth N. Direct and enhanced delivery of nanoliposomes of anti schizophrenic agent to the brain through nasal route. Saudi Pharm J. 2017;25(3):346–358. doi:10.1016/j.jsps.2016.07.003
   PubMed Web of Science ®Google Scholar
• Tafaghodi M, Abolghasem Sajadi Tabassi S, Jaafari MR, Zakavi SR, Momen-Nejad M. Evaluation of the clearance characteristics of various microspheres in the human nose by gamma-scintigraphy. Int J Pharm. 2004;280(1–2):125–135. doi:10.1016/j.ijpharm.2004.05.009
   PubMed Web of Science ®Google Scholar
• Yuba E, Harada A, Sakanishi Y, Watarai S, Kono K. A liposome-based antigen delivery system using pH-sensitive fusogenic polymers for cancer immunotherapy. Biomaterials. 2013;34(12):3042–3052. doi:10.1016/j.biomaterials.2012.12.031
   PubMed Web of Science ®Google Scholar
• Aisha AF, Majid AM, Ismail Z. Preparation and characterization of nano liposomes of Orthosiphon stamineus ethanolic extract in soybean phospholipids. BMC Biotech. 2014;14:23. doi:10.1186/1472-6750-14-23
   PubMed Web of Science ®Google Scholar
• Dinda SC, Pattnaik G. Nanobiotechnology-based drug delivery in brain targeting. Current Pharm Biotechnol. 2013;14(15):1264–1274. doi:10.2174/1389201015666140608143719
   PubMed Web of Science ®Google Scholar
• Sheng WS, Xu HL, Zheng L, et al. Intrarenal delivery of bFGF-loaded liposome under guiding of ultrasound-targeted microbubble destruction prevent diabetic nephropathy through inhibition of inflammation. Artif Cells Nanomed Biotechnol. 2018;46(sup2):373–385. doi:10.1080/21691401.2018.1457538
   PubMed Web of Science ®Google Scholar
• Zhao YZ, Zhang M, Tian XQ, Zheng L, Lu CT. Using basic fibroblast growth factor nanoliposome combined with ultrasound-introduced technology to early intervene the diabetic cardiomyopathy. Int j Nanomed. 2016;11:675–686. doi:10.2147/IJN.S99376
   PubMed Web of Science ®Google Scholar
• Xiang Q, Xiao J, Zhang H, et al. Preparation and characterisation of bFGF-encapsulated liposomes and evaluation of wound-healing activities in the rat. Burns. 2011;37(5):886–895. doi:10.1016/j.burns.2011.01.018
   PubMed Web of Science ®Google Scholar
• Zhang M, Yu WZ, Shen XT, et al. Advanced interfere treatment of diabetic cardiomyopathy rats by aFGF-loaded heparin-modified microbubbles and UTMD technique. Cardiovasc Drugs Ther. 2016;30(3):247–261. doi:10.1007/s10557-016-6639-4
   PubMed Web of Science ®Google Scholar
• He JT, Li H, Yang L, Cheng KL. Involvement of endothelin-1, H(2)S and Nrf2 in beneficial effects of remote ischemic preconditioning in global cerebral ischemia-induced vascular dementia in mice. Cell Mol Neurobiol. 2019;39(5):671–686. doi:10.1007/s10571-019-00670-y
   PubMed Web of Science ®Google Scholar
• Liu B, Kou J, Li F, et al. Lemon essential oil ameliorates age-associated cognitive dysfunction via modulating hippocampal synaptic density and inhibiting acetylcholinesterase. Aging. 2020;12(9):8622–8639. doi:10.18632/aging.103179
   PubMedGoogle Scholar
• Lueptow LM. Novel object recognition test for the investigation of learning and memory in mice. J Visualized Exp. 2017;126:55718. doi:10.3791/55718
   Google Scholar
• Fang YC, Chan L, Liou JP, et al. HDAC inhibitor protects chronic cerebral hypoperfusion and oxygen-glucose deprivation injuries via H3K14 and H4K5 acetylation-mediated BDNF expression. J Cell Mol Med. 2020;24(12):6966–6977. doi:10.1111/jcmm.15358
   PubMed Web of Science ®Google Scholar
• Zhuge XZ, Hu WX, Liu YM, et al. PD98059 protects SH-SY5Y cells against oxidative stress in oxygen-glucose deprivation/reperfusion. Transl Neurosci. 2023;14(1):20220300.
   PubMed Web of Science ®Google Scholar
• Yuan ZL, Mo YZ, Li DL, Xie L, Chen MH. Inhibition of ERK downregulates autophagy via mitigating mitochondrial fragmentation to protect SH-SY5Y cells from OGD/R injury. Cell Commun Signaling. 2023;21(1):204. doi:10.1186/s12964-023-01211-3
   PubMed Web of Science ®Google Scholar
• Xu J, Liu J, Li Q, et al. Pterostilbene alleviates Aβ(1-42) -induced cognitive dysfunction via inhibition of oxidative stress by activating Nrf2 signaling pathway. Mol Nutr Food Res. 2021;65(2):e2000711. doi:10.1002/mnfr.202000711
   PubMed Web of Science ®Google Scholar
• Yadav A, Sunkaria A, Singhal N, Sandhir R. Resveratrol loaded solid lipid nanoparticles attenuate mitochondrial oxidative stress in vascular dementia by activating Nrf2/HO-1 pathway. Neurochem Int. 2018;112:239–254. doi:10.1016/j.neuint.2017.08.001
   PubMed Web of Science ®Google Scholar
• Liu Y, Lu JB, Ye ZR. Permeability of injured blood brain barrier for exogenous bFGF and protection mechanism of bFGF in rat brain ischemia. Neuropathology. 2006;26(3):257–266. doi:10.1111/j.1440-1789.2006.00693.x
   PubMed Web of Science ®Google Scholar
• Wakayama K, Shimamura M, Yoshida S, et al. Prevention of vascular dementia via immunotherapeutic blockade of renin-angiotensin system in a rat model. Brain Res. 2021;1772:147667. doi:10.1016/j.brainres.2021.147667
   PubMed Web of Science ®Google Scholar
• Chen C, Chen W, Nong Z, et al. Hyperbaric oxygen alleviated cognitive impairments in mice induced by repeated cerebral ischemia-reperfusion injury via inhibition of autophagy. Life Sci. 2020;241:117170. doi:10.1016/j.lfs.2019.117170
   PubMed Web of Science ®Google Scholar
• Higaki A, Mogi M, Iwanami J, et al. Predicting outcome of Morris water maze test in vascular dementia mouse model with deep learning. PLoS One. 2018;13(2):e0191708. doi:10.1371/journal.pone.0191708
   PubMed Web of Science ®Google Scholar
• Sun M, Wu L, Chen G, Mo X, Shi C. Hemodynamic changes and neuronal damage detected by 9.4 T MRI in rats with chronic cerebral ischemia and cognitive impairment. Brain Behav. 2022;12(7):e2642. doi:10.1002/brb3.2642
   PubMed Web of Science ®Google Scholar
• Xue Y, Qu Z, Fu J, et al. The protective effect of astaxanthin on learning and memory deficits and oxidative stress in a mouse model of repeated cerebral ischemia/reperfusion. Brain Res Bull. 2017;131:221–228. doi:10.1016/j.brainresbull.2017.04.019
   PubMed Web of Science ®Google Scholar
• Xu J, Huai Y, Meng N, et al. L-3-n-butylphthalide activates Akt/mTOR signaling, inhibits neuronal apoptosis and autophagy and improves cognitive impairment in mice with repeated cerebral ischemia-reperfusion injury. Neurochem Res. 2017;42(10):2968–2981. doi:10.1007/s11064-017-2328-3
   PubMed Web of Science ®Google Scholar
• Moscovitch M, Cabeza R, Winocur G, Nadel L. Episodic memory and beyond: the hippocampus and neocortex in transformation. Ann Rev Psychol. 2016;67:105–134. doi:10.1146/annurev-psych-113011-143733
   PubMed Web of Science ®Google Scholar
• Bartsch T, Döhring J, Rohr A, Jansen O, Deuschl G. CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness. Proc Natl Acad Sci USA. 2011;108(42):17562–17567. doi:10.1073/pnas.1110266108
   PubMed Web of Science ®Google Scholar
• Gao L, Guo X, Liu S, et al. DL-3-n-butylphthalide imparts neuroprotection via Nrf2/SIRT3 pathway in a mouse model of vascular dementia. Brain Res. 2022;1779:147785. doi:10.1016/j.brainres.2022.147785
   PubMed Web of Science ®Google Scholar
• Li XJ, Hou JC, Sun P, et al. Neuroprotective effects of tongluojiunao in neurons exposed to oxygen and glucose deprivation. J Ethnopharmacol. 2012;141(3):927–933. doi:10.1016/j.jep.2012.03.042
   PubMed Web of Science ®Google Scholar
• Zhao T, Fu Y, Sun H, Liu X. Ligustrazine suppresses neuron apoptosis via the Bax/Bcl-2 and caspase-3 pathway in PC12 cells and in rats with vascular dementia. IUBMB Life. 2018;70(1):60–70. doi:10.1002/iub.1704
   PubMed Web of Science ®Google Scholar
• Annunziato L, Amoroso S, Pannaccione A, et al. Apoptosis induced in neuronal cells by oxidative stress: role played by caspases and intracellular calcium ions. Toxicol Lett. 2003;139(2–3):125–133. doi:10.1016/s0378-4274(02)00427-7
   PubMed Web of Science ®Google Scholar
• Choi DH, Lee KH, Kim JH, et al. NADPH oxidase 1, a novel molecular source of ROS in hippocampal neuronal death in vascular dementia. Antioxid Redox Signaling. 2014;21(4):533–550. doi:10.1089/ars.2012.5129
   PubMed Web of Science ®Google Scholar
• Guo S, Xu JJ, Wei N, et al. Honokiol attenuates the memory impairments, oxidative stress, neuroinflammation, and GSK-3β activation in vascular dementia rats. J Alzheimers Dis. 2019;71(1):97–108. doi:10.3233/JAD-190324
   PubMed Web of Science ®Google Scholar
• Manzanero S, Santro T, Arumugam TV. Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury. Neurochem Int. 2013;62(5):712–718. doi:10.1016/j.neuint.2012.11.009
   PubMed Web of Science ®Google Scholar
• Zarezadeh M, Baluchnejadmojarad T, Kiasalari Z, Afshin-Majd S, Roghani M. Garlic active constituent s-allyl cysteine protects against lipopolysaccharide-induced cognitive deficits in the rat: possible involved mechanisms. Eur J Pharmacol. 2017;795:13–21. doi:10.1016/j.ejphar.2016.11.051
   PubMed Web of Science ®Google Scholar
• Chen H, Yoshioka H, Kim GS, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid Redox Signaling. 2011;14(8):1505–1517. doi:10.1089/ars.2010.3576
   PubMed Web of Science ®Google Scholar
• Malinska D, Kulawiak B, Kudin AP, et al. Complex III-dependent superoxide production of brain mitochondria contributes to seizure-related ROS formation. BBA. 2010;1797(6–7):1163–1170. doi:10.1016/j.bbabio.2010.03.001
   PubMed Web of Science ®Google Scholar
• Wang D, Wang Y, Shan M, et al. Apelin receptor homodimer inhibits apoptosis in vascular dementia. Exp Cell Res. 2021;407(1):112739. doi:10.1016/j.yexcr.2021.112739
   PubMed Web of Science ®Google Scholar
• Ali T, Kim T, Rehman SU, et al. Natural dietary supplementation of anthocyanins via PI3K/Akt/Nrf2/HO-1 pathways mitigate oxidative stress, neurodegeneration, and memory impairment in a mouse model of Alzheimer’s disease. Mol Neurobiol. 2018;55(7):6076–6093. doi:10.1007/s12035-017-0798-6
   PubMed Web of Science ®Google Scholar
• Thangapandiyan S, Ramesh M, Miltonprabu S, Hema T, Jothi GB, Nandhini V. Sulforaphane potentially attenuates arsenic-induced nephrotoxicity via the PI3K/Akt/Nrf2 pathway in albino Wistar rats. Environ Sci Pollut Res Int. 2019;26(12):12247–12263. doi:10.1007/s11356-019-04502-w
   PubMed Web of Science ®Google Scholar
• de Vries HE, Witte M, Hondius D, et al. Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med. 2008;45(10):1375–1383. doi:10.1016/j.freeradbiomed.2008.09.001
   PubMed Web of Science ®Google Scholar
• Hayes JD, Dinkova-Kostova AT. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci. 2014;39(4):199–218. doi:10.1016/j.tibs.2014.02.002
   PubMed Web of Science ®Google Scholar
• Tong G, Liang Y, Xue M, et al. The protective role of bFGF in myocardial infarction and hypoxia cardiomyocytes by reducing oxidative stress via Nrf2. Biochem Biophys Res Commun. 2020;527(1):15–21. doi:10.1016/j.bbrc.2020.04.053
   PubMed Web of Science ®Google Scholar