Targeted Delivery of Macrophage Membrane Biomimetic Liposomes Through Intranasal Administration for Treatment of Ischemic Stroke

References

• Bhaskar S, Stanwell P, Cordato D, Attia J, Levi C. Reperfusion therapy in acute ischemic stroke: dawn of a new era? BMC Neurol. 2018;18(1):8. doi:10.1186/s12883-017-1007-y
   PubMedGoogle Scholar
• Yoo AJ, Pulli B, Gonzalez RG. Imaging-based treatment selection for intravenous and intra-arterial stroke therapies: a comprehensive review. Expert Rev Cardiovasc Ther. 2011;9(7):857–876. doi:10.1586/erc.11.56
   Google Scholar
• Campbell BCV, De Silva DA, Macleod MR, et al. Ischaemic stroke. Nat Rev Dis Primers. 2019;5(1):5. doi:10.1038/s41572-019-0118-8
   Google Scholar
• Jurcau A, Simion A. Neuroinflammation in cerebral ischemia and ischemia/reperfusion injuries: from pathophysiology to therapeutic strategies. Int J Mol Sci. 2022;23(1). doi:10.3390/ijms23010014
   Web of Science ®Google Scholar
• Selvaraj K, Gowthamarajan K, Karri V. Nose to brain transport pathways an overview: potential of nanostructured lipid carriers in nose to brain targeting. Artif Cells Nanomed Biotechnol. 2018;46(8):2088–2095. doi:10.1080/21691401.2017.1420073
   PubMed Web of Science ®Google Scholar
• Yu S, Li D, Shi A, et al. Multidrug-loaded liposomes prevent ischemic stroke through intranasal administration. Biomed Pharmacother. 2023:162. doi:10.1016/j.biopha.2023.114542
   Web of Science ®Google Scholar
• Alavian F, Shams N. Oral and intra-nasal administration of nanoparticles in the cerebral ischemia treatment in animal experiments: considering its advantages and disadvantages open access plus. Curr Clin Pharmacol. 2020;15(1):20–29. doi:10.2174/1574884714666190704115345
   Web of Science ®Google Scholar
• Laffleur F, Bauer B. Progress in nasal drug delivery systems. Int J Pharmaceut. 2021;607. doi:10.1016/j.ijpharm.2021.120994
   Google Scholar
• Hanson LR, Frey WH. Intranasal delivery bypasses the blood-brain barrier to target therapeutic agents to the central nervous system and treat neurodegenerative disease. BMC Neurosci. 2008;9. doi:10.1186/1471-2202-9-S3-S5
   Web of Science ®Google Scholar
• Kim M, Lee Y, Lee M. Hypoxia-specific anti-RAGE exosomes for nose-to-brain delivery of anti-miR-181a oligonucleotide in an ischemic stroke model. Nanoscale. 2021;13(33):14166–14178. doi:10.1039/d0nr07516g
   PubMed Web of Science ®Google Scholar
• Schaefer ML, Böttger B, Silver WL, Finger TE. Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol. 2002;444(3):221–226. doi:10.1002/cne.10143
   PubMed Web of Science ®Google Scholar
• Wang SY, Li MH, Guo Y, et al. Effects of Panax notoginseng ginsenoside Rb1 on abnormal hippocampal microenvironment in rats. J Ethnopharmacol. 2017;202:138–146. doi:10.1016/j.jep.2017.01.005
   Web of Science ®Google Scholar
• Feng LD, Han F, Zhou L, et al. Efficacy and safety of (Xueshuantong) in patients with acute ischemic stroke (EXPECT) trial: rationale and design. Front Pharmacol. 2021:12. doi:10.3389/fphar.2021.648921
   Google Scholar
• Zou S, Zhang MX, Feng LM, et al. Protective effects of notoginsenoside R1 on cerebral ischemia-reperfusion injury in rats. Exp Ther Med. 2017;14(6):6012–6016. doi:10.3892/etm.2017.5268
   Web of Science ®Google Scholar
• Wu T, Jia ZH, Dong SF, et al. Saponins ameliorate leukocyte adherence and cerebrovascular endothelial barrier breakdown upon ischemia-reperfusion in mice. J Vasc Res. 2019;56(1):1–10. doi:10.1159/000494935
   Web of Science ®Google Scholar
• Im DS. Pro-resolving effect of ginsenosides as an anti-inflammatory mechanism of panax ginseng. Biomolecules. 2020;10(3):444. doi:10.3390/biom10030444
   PubMed Web of Science ®Google Scholar
• Cheng ZK, Zhang M, Ling CL, et al. Neuroprotective effects of ginsenosides against cerebral ischemia. Molecules. 2019;24(6):1102. doi:10.3390/molecules24061102
   PubMed Web of Science ®Google Scholar
• Wang J, Zeng L, Zhang Y, et al. Pharmacological properties, molecular mechanisms and therapeutic potential of ginsenoside Rg3 as an antioxidant and anti-inflammatory agent. Front Pharmacol. 2022:13. doi:10.3389/fphar.2022.975784
   Web of Science ®Google Scholar
• Li MY, Du CY, Guo N, et al. Composition design and medical application of liposomes. Eur J Med Chem. 2019;164:640–653. doi:10.1016/j.ejmech.2019.01.007
   PubMed Web of Science ®Google Scholar
• Ajeeshkumar KK, Aneesh PA, Raju N, et al. Advancements in liposome technology: preparation techniques and applications in food, functional foods, and bioactive delivery: a review. Compr Rev Food Sci F. 2021;20(2):1280–1306. doi:10.1111/1541-4337.12725
   Google Scholar
• Guimaraes D, Cavaco-Paulo A, Nogueira E. Design of liposomes as drug delivery system for therapeutic applications. Int J Pharmaceut. 2021;601. doi:10.1016/j.ijpharm.2021.120571
   Google Scholar
• Liu B, Zhang J, Liu Z, et al. Research on the preparation process of the cytarabine/daunorubicin dual-encapsulation liposome and its physicochemical properties and performances in vitro/vivo. Int J Pharm. 2023;646:123500. doi:10.1016/j.ijpharm.2023.123500
   Google Scholar
• Li YJ, Wu JY, Liu JH, et al. From blood to brain: blood cell-based biomimetic drug delivery systems. Drug Deliv. 2021;28(1):1214–1225. doi:10.1080/10717544.2021.1937384
   PubMed Web of Science ®Google Scholar
• Koupenova M, Kehrel BE, Corkrey HA, Freedman JE. Thrombosis and platelets: an update. Eur Heart J. 2017;38(11):785–791. doi:10.1093/eurheartj/ehw550
   PubMed Web of Science ®Google Scholar
• Fang RH, Kroll AV, Gao WW, Zhang LF. Cell membrane coating nanotechnology. Adv Mater. 2018;30(23). doi:10.1002/adma.201706759
   Web of Science ®Google Scholar
• Li RX, He YW, Zhang SY, Qin J, Wang JX. Cell membrane-based nanoparticles: a new biomimetic platform for tumor diagnosis and treatment. Acta Pharm Sin B. 2018;8(1):14–22. doi:10.1016/j.apsb.2017.11.009
   PubMed Web of Science ®Google Scholar
• Pang L, Zhang C, Qin J, et al. A novel strategy to achieve effective drug delivery: exploit cells as carrier combined with nanoparticles. Drug Deliv. 2017;24(1):83–91. doi:10.1080/10717544.2016.1230903
   PubMed Web of Science ®Google Scholar
• Wu HH, Zhang TY, Li N, Gao JQ. Cell membrane-based biomimetic vehicles for effective central nervous system target delivery: insights and challenges. J Control Release. 2023;360:169–184. doi:10.1016/j.jconrel.2023.06.023
   Web of Science ®Google Scholar
• Feng LS, Dou CR, Xia YG, et al. Neutrophil-like cell-membrane-coated nanozyme therapy for ischemic brain damage and long-term neurological functional recovery. Acs Nano. 2021;15(2):2263–2280. doi:10.1021/acsnano.0c07973
   PubMed Web of Science ®Google Scholar
• Yan JJ, Fei WD, Song QQ, et al. Cell membrane-camouflaged PLGA biomimetic system for diverse biomedical application. Drug Deliv. 2022;29(1):2296–2319. doi:10.1080/10717544.2022.2100010
   PubMed Web of Science ®Google Scholar
• Zhang RT, Wu SQ, Ding Q, et al. Recent advances in cell membrane-camouflaged nanoparticles for inflammation therapy. Drug Deliv. 2021;28(1):1109–1119. doi:10.1080/10717544.2021.1934188
   PubMed Web of Science ®Google Scholar
• Li C, Zhao ZH, Luo YF, et al. Macrophage-disguised manganese dioxide nanoparticles for neuroprotection by reducing oxidative stress and modulating inflammatory microenvironment in acute ischemic stroke. Adv Sci. 2021;8(20). doi:10.1002/advs.202101526
   Web of Science ®Google Scholar
• Jian ZH, Liu R, Zhu XQ, et al. The involvement and therapy target of immune cells after ischemic stroke. Front Immunol. 2019;10:10. doi:10.3389/fimmu.2019.02167
   Web of Science ®Google Scholar
• Gelderblom M, Leypoldt F, Steinbach K, et al. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke. 2009;40(5):1849–1857. doi:10.1161/Strokeaha.108.534503
   PubMed Web of Science ®Google Scholar
• Cai W, Hu MY, Li CY, et al. FOXP3+macrophage represses acute ischemic stroke-induced neural inflammation. Autophagy. 2023;19(4):1144–1163. doi:10.1080/15548627.2022.2116833
   PubMed Web of Science ®Google Scholar
• Zhang H. Thin-Film hydration followed by extrusion method for liposome preparation. Methods Mol Biol. 2017;1522:17–22. doi:10.1007/978-1-4939-6591-5_2
   PubMedGoogle Scholar
• Wu HH, Jiang XC, Li YS, et al. Engineering stem cell derived biomimetic vesicles for versatility and effective targeted delivery. Adv Funct Mater. 2020;30(49). doi:10.1002/adfm.202006169
   Web of Science ®Google Scholar
• Hayes BH, Tsai RK, Dooling LJ, et al. Macrophages show higher levels of engulfment after disruption of interactions between CD47 and the checkpoint receptor SIRPα. J Cell Sci. 2020;133(5). doi:10.1242/jcs.237800
   Web of Science ®Google Scholar
• Perego C, Fumagalli S, Zanier ER, et al. Macrophages are essential for maintaining a M2 protective response early after ischemic brain injury. Neurobiol Dis. 2016;96:284–293. doi:10.1016/j.nbd.2016.09.017
   Web of Science ®Google Scholar
• Liu W, Lu HW, Rao XY, et al. Enhanced treatment for cerebral ischemia-reperfusion injury of puerarin loading liposomes through neutrophils-mediated targeted delivery. Nano Res. 2021;14(12):4634–4643. doi:10.1007/s12274-021-3395-y
   Web of Science ®Google Scholar
• Jiang YY, Liu CQ, Zhai WC, et al. The optimization design of lactoferrin loaded HupA nanoemulsion for targeted drug transport via intranasal route. Int J Nanomed. 2019;14:9217–9234. doi:10.2147/Ijn.S214657
   PubMed Web of Science ®Google Scholar
• Askarizadeh A, Barreto GE, Henney NC, Majeed M, Sahebkar A. Neuroprotection by curcumin: a review on brain delivery strategies. Int J Pharmaceut. 2020;585. doi:10.1016/j.ijpharm.2020.119476
   Web of Science ®Google Scholar
• Alexander A, Agrawal M, Uddin A, et al. Recent expansions of novel strategies towards the drug targeting into the brain. Int J Nanomed. 2019;14:5895–5909. doi:10.2147/Ijn.S210876
   PubMed Web of Science ®Google Scholar
• Brown RC, Morris AP, O’Neil RG. Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells. Brain Res. 2007;1130(1):17–30. doi:10.1016/j.brainres.2006.10.083
   PubMed Web of Science ®Google Scholar
• Li GL, Simon MJ, Cancel LM, et al. Permeability of endothelial and astrocyte cocultures: blood-brain barrier models for drug delivery studies. Ann Biomed Eng. 2010;38(8):2499–2511. doi:10.1007/s10439-010-0023-5
   Web of Science ®Google Scholar
• Zhang YD, He JL, Shen L, et al. Brain-targeted delivery of obidoxime, using aptamer-modified liposomes, for detoxification of organophosphorus compounds. J Control Release. 2021;329:1117–1128. doi:10.1016/j.jconrel.2020.10.039
   PubMed Web of Science ®Google Scholar
• Jiang YY, Jiang YC, Ding ZY, Yu Q. Investigation of the “Nose-to-Brain” pathways in intranasal HupA nanoemulsions and evaluation of their in vivo pharmacokinetics and brain-targeting ability. Int J Nanomed. 2022;17. doi:10.2147/Ijn.S369978
   Web of Science ®Google Scholar
• Li Y, Zhang MM, Li SY, et al. Selective ischemic-hemisphere targeting Ginkgolide B liposomes with improved solubility and therapeutic efficacy for cerebral ischemia-reperfusion injury. Asian J Pharm Sci. 2023;18(2). doi:10.1016/j.ajps.2023.100783
   Web of Science ®Google Scholar
• Wang C, Yang XW, Jiang YX, et al. Targeted delivery of fat extract by platelet membrane-cloaked nanocarriers for the treatment of ischemic stroke. J Nanobiotechnol. 2022;20(1). doi:10.1186/s12951-022-01461-2
   Web of Science ®Google Scholar
• Yilmaz G, Granger DN. Leukocyte recruitment and ischemic brain injury. Neuromolecular Med. 2010;12(2):193–204. doi:10.1007/s12017-009-8074-1
   Web of Science ®Google Scholar
• Arumugam TV, Salter JW, Chidlow JH, et al. Contributions of LFA-1 and Mac-1 to brain injury and microvascular dysfunction induced by transient middle cerebral artery occlusion. Am J Physiol-Heart C. 2004;287(6):H2555–H2560. doi:10.1152/ajpheart.00588.2004
   Web of Science ®Google Scholar
• Han Y, Gao C, Wang H, et al. Macrophage membrane-coated nanocarriers Co-Modified by RVG29 and TPP improve brain neuronal mitochondria-targeting and therapeutic efficacy in Alzheimer’s disease mice. Bioact Mater. 2021;6(2):529–542. doi:10.1016/j.bioactmat.2020.08.017
   PubMed Web of Science ®Google Scholar
• Tang H, Xie YZ, Zhu M, et al. Estrone-conjugated PEGylated liposome co-loaded paclitaxel and carboplatin improve anti-tumor efficacy in ovarian cancer and reduce acute toxicity of chemo-drugs. Int J Nanomed. 2022;17:3013–3041. doi:10.2147/Ijn.S362263
   PubMed Web of Science ®Google Scholar
• Keller LA, Merkel O, Popp A. Intranasal drug delivery: opportunities and toxicologic challenges during drug development. Drug Deliv Transl Re. 2022;12(4):735–757. doi:10.1007/s13346-020-00891-5
   PubMed Web of Science ®Google Scholar
• Xiang Y, Long Y, Yang QY, et al. Pharmacokinetics, pharmacodynamics and toxicity of Baicalin liposome on cerebral ischemia reperfusion injury rats via intranasal administration. Brain Res. 2020:1726. doi:10.1016/j.brainres.2019.146503
   Web of Science ®Google Scholar
• Lu JQ, Li R, Mu BS, et al. Multiple targeted doxorubicin-lonidamine liposomes modified with -hydroxybenzoic acid and triphenylphosphonium to synergistically treat glioma. Eur J Med Chem. 2022:230. doi:10.1016/j.ejmech.2021.114093
   Web of Science ®Google Scholar
• Benedek A, Móricz K, Jurányi Z, et al. Use of TTC staining for the evaluation of tissue injury in the early phases of reperfusion after focal cerebral ischemia in rats. Brain Res. 2006;1116(1):159–165. doi:10.1016/j.brainres.2006.07.123
   PubMedGoogle Scholar
• Tirandi A, Sgura C, Carbone F, Montecucco F, Liberale L. Inflammatory biomarkers of ischemic stroke. Intern Emerg Med. 2023;18(3):723–732. doi:10.1007/s11739-023-03201-2
   Web of Science ®Google Scholar
• Yang CJ, Hawkins KE, Doré S, Candelario-Jalil E. Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am J Physiol-Cell Ph. 2019;316(2):C135–C153. doi:10.1152/ajpcell.00136.2018
   PubMed Web of Science ®Google Scholar
• Han WX, Song Y, Rocha M, Shi YJ. Ischemic brain edema: emerging cellular mechanisms and therapeutic approaches. Neurobiol Dis. 2023;178. doi:10.1016/j.nbd.2023.106029
   Web of Science ®Google Scholar