Targeting cerebral diseases with enhanced delivery of therapeutic proteins across the blood-brain barrier

References

• Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. DOI:10.3322/caac.21708
   PubMed Web of Science ®Google Scholar
• Erkkinen MG, Kim MO, Geschwind MD. Clinical neurology and epidemiology of the major neurodegenerative diseases. Cold Spring Harb Perspect Biol. 2018;10(4):a033118.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Treatment of Alzheimer’s disease and blood-brain barrier drug delivery. Pharmaceuticals (Basel). 2020;13(11):394.
   PubMedGoogle Scholar
• Kopeček J, Yang J. Polymer nanomedicines. Adv Drug Deliv Rev. 2020;156:40–64.
   PubMed Web of Science ®Google Scholar
• Yang J, Li L, Kopeček J. Biorecognition: a key to drug-free macromolecular therapeutics. Biomaterials. 2019;190-191:11–23.
   PubMed Web of Science ®Google Scholar
• Raucher D, Dragojevic S, Ryu J. Macromolecular drug carriers for targeted glioblastoma therapy: preclinical Studies, challenges, and future perspectives. Front Oncol. 2018;8:624.
   PubMed Web of Science ®Google Scholar
• Banks WA. From blood-brain barrier to blood-brain interface: new opportunities for CNS drug delivery. Nat Rev Drug Discov. 2016;15(4):275–292.
   PubMed Web of Science ®Google Scholar
• Bajracharya R, Caruso AC, Vella LJ, et al. Current and emerging strategies for enhancing antibody delivery to the brain. Pharmaceutics. 2021;13(12):2014. DOI:10.3390/pharmaceutics13122014
   PubMed Web of Science ®Google Scholar
• Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol. 2015;7(1):a020412.
   PubMed Web of Science ®Google Scholar
• Profaci CP, Munji RN, Pulido RS, et al. The blood-brain barrier in health and disease: important unanswered questions. J Exp Med. 2020;217(4):e20190062. DOI:10.1084/jem.20190062
   PubMed Web of Science ®Google Scholar
• Hajal C, Le Roi B, Kamm RD, et al. Biology and models of the blood-brain barrier. Annu Rev Biomed Eng. 2021;23:359–384.
   PubMed Web of Science ®Google Scholar
• Pandit R, Chen L, Götz J. The blood-brain barrier: physiology and strategies for drug delivery. Adv Drug Deliv Rev. 2020;165-166:1–14. . 10.1016/j.addr.2019.11.009
   PubMed Web of Science ®Google Scholar
• Kadry H, Noorani B, Cucullo L. A blood-brain barrier overview on structure, function, impairment, and biomarkers of integrity. Fluids Barriers CNS. 2020;17(1):69.
   PubMed Web of Science ®Google Scholar
• Liebner S, Dijkhuizen RM, Reiss Y, et al. Functional morphology of the blood-brain barrier in health and disease. Acta Neuropathol. 2018;135(3):311–336. DOI:10.1007/s00401-018-1815-1
   PubMed Web of Science ®Google Scholar
• Arvanitis CD, Ferraro GB, Jain RK. The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat Rev Cancer. 2020;201:26–4110.1038/s41568-019-0205-x
   PubMed Web of Science ®Google Scholar
• Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat Med. 2013;19(12):1584–1596.
   PubMed Web of Science ®Google Scholar
• Alahmari A, Wu L-J. Blood-brain barrier overview: structural and functional correlation. Neural Plast. 2021;2021:6564585.
   PubMedGoogle Scholar
• Sanchez-Cano F, Hernández-Kelly LC, Ortega A. The blood-brain barrier: much more than a selective access to the brain. Neurotox Res. 2021;39(6):2154–2174.
   PubMed Web of Science ®Google Scholar
• Ronaldson PT, Davis TP. Regulation of blood-brain barrier integrity by microglia in health and disease: a therapeutic opportunity. J Cereb Blood Flow Metab. 2020;40(1_suppl):S6–24.
   PubMed Web of Science ®Google Scholar
• Xu L, Nirwane A, Yao Y. Basement membrane and blood–brain barrier. Stroke Vasc Neurol. 2019;4(2):78–82.
   PubMedGoogle Scholar
• Sweeney MD, Zhao Z, Montagne A, et al. Blood-brain barrier: from physiology to disease and back. Physiol Rev. 2019;99(1):21–78. DOI:10.1152/physrev.00050.2017
   PubMed Web of Science ®Google Scholar
• Patching SG. Glucose transporters at the blood-brain barrier: function, regulation and gateways for drug delivery. Mol Neurobiol. 2017;54(2):1046–1077.
   PubMed Web of Science ®Google Scholar
• Moura RP, Martins C, Pinto S, et al. Blood-brain barrier receptors and transporters: an insight on their function and how to exploit them through nanotechnology. Expert Opin Drug Deliv. 2019;16(3):271–285. DOI:10.1080/17425247.2019.1583205
   PubMed Web of Science ®Google Scholar
• Hladky SB, Barrand MA. Fluid and ion transfer across the blood-brain and blood-cerebrospinal fluid barriers; a comparative account of mechanisms and roles. Fluids Barriers CNS. 2016;13(1):19.
   PubMed Web of Science ®Google Scholar
• Hladky SB, Barrand MA. Elimination of substances from the brain parenchyma: efflux via perivascular pathways and via the blood-brain barrier. Fluids Barriers CNS. 2018;15(1):30.
   PubMedGoogle Scholar
• Chen L, Zeng D, Xu N, et al. Blood-brain barrier- and blood-brain tumor barrier-penetrating peptide-derived targeted therapeutics for glioma and malignant tumor brain metastases. ACS Appl Mater Interfaces. 2019;11(45):41889–41897. DOI:10.1021/acsami.9b14046
   PubMed Web of Science ®Google Scholar
• Song J, Lu C, Leszek J, et al. Design and development of nanomaterial-based drug carriers to overcome the blood–brain barrier by using different transport mechanisms. Int J Mol Sci. 2021;22(18):10118. DOI:10.3390/ijms221810118
   PubMed Web of Science ®Google Scholar
• Cockerill I, Oliver JA, Xu H, et al. Blood-brain barrier integrity and clearance of amyloid-β from the BBB. Adv Exp Med Biol. 2018;1097:261–278.
   PubMed Web of Science ®Google Scholar
• Villaseñor R, Lampe J, Schwaninger M, et al. Intracellular transport and regulation of transcytosis across the blood-brain barrier. Cell Mol Life Sci. 2019;76(6):1081–1092. DOI:10.1007/s00018-018-2982-x
   PubMed Web of Science ®Google Scholar
• Ayloo S, Gu C. Transcytosis at the blood-brain barrier. Curr Opin Neurobiol. 2019;57:32–38.
   PubMed Web of Science ®Google Scholar
• Lajoie JM, Shusta EV. Targeting receptor-mediated transport for delivery of biologics across the blood-brain barrier. Annu Rev Pharmacol Toxicol. 2015;55(1):613–631.
   PubMed Web of Science ®Google Scholar
• Lu W. Adsorptive-mediated brain delivery systems. Curr Pharm Biotechnol. 2012;13(12):2340–2348.
   PubMed Web of Science ®Google Scholar
• Patel MM, Patel BM. Crossing the blood-brain barrier: recent advances in drug delivery to the brain. CNS Drugs. 2017;31(2):109–133.
   PubMed Web of Science ®Google Scholar
• Terstappen GC, Meyer AH, Bell RD, et al. Strategies for delivering therapeutics across the blood-brain barrier. Nat Rev Drug Discov. 2021;20(5):362–383. DOI:10.1038/s41573-021-00139-y. .
   PubMed Web of Science ®Google Scholar
• Ferraris C, Cavalli R, Panciani PP, et al. Overcoming the blood-brain barrier: successes and challenges in developing nanoparticle-mediated drug delivery systems for the treatment of brain tumours. Int J Nanomedicine. 2020;15:2999–3022.
   PubMed Web of Science ®Google Scholar
• Ding S, Khan AI, Cai X, et al. Overcoming blood-brain barrier transport: advances in nanoparticle-based drug delivery strategies. Mater Today (Kidlington). 2020;37:112–125.
   PubMedGoogle Scholar
• Elgundi Z, Reslan M, Cruz E, et al. The state-of-play and future of antibody therapeutics. Adv Drug Deliv Rev. 2017;122:2–19.
   PubMed Web of Science ®Google Scholar
• Shim H. Bispecific antibodies and antibody-drug conjugates for cancer therapy: technological considerations. Biomolecules. 2020;10(3):360.
   PubMed Web of Science ®Google Scholar
• Parola C, Neumeier D, Reddy ST. Integrating high-throughput screening and sequencing for monoclonal antibody discovery and engineering. Immunology. 2018;153(1):31–41.
   PubMed Web of Science ®Google Scholar
• Carter PJ, Lazar GA. Next generation antibody drugs: pursuit of the ‘high-hanging fruit’. Nat Rev Drug Discov. 2018;17(3):197–223.
   PubMed Web of Science ®Google Scholar
• Jones AR, Shusta EV. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res. 2007;24(9):1759–1771.
   PubMed Web of Science ®Google Scholar
• Barar J, Rafi MA, Pourseif MM, et al. Blood-brain barrier transport machineries and targeted therapy of brain diseases. Bioimpacts. 2016;6(4):225–248. DOI:10.15171/bi.2016.30
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Blood-brain barrier drug targeting: the future of brain drug development. Mol Interv. 2003;3(2):90–105, 51.
   PubMedGoogle Scholar
• Pardridge WM. Molecular Trojan horses for blood-brain barrier drug delivery. Curr Opin Pharmacol. 2006;6(5):494–500.
   PubMed Web of Science ®Google Scholar
• Pardridge WM, Boado RJ. Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier. Methods Enzymol. 2012;503:269–292.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Delivery of biologics across the blood-brain barrier with molecular Trojan Horse technology. BioDrugs. 2017;31(6):503–519.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Blood–brain barrier drug delivery of IgG fusion proteins with a transferrin receptor monoclonal antibody. Expert Opin Drug Delivery. 2015;12(2):207–222.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Targeted delivery of protein and gene medicines through the blood-brain barrier. Clin Pharmacol Ther. 2015;97(4):347–361.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Re-engineering therapeutic antibodies for Alzheimer’s disease as blood-brain barrier penetrating bi-specific antibodies. Expert Opin Biol Ther. 2016;16(12):1455–1468.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Blood-brain barrier and delivery of protein and gene therapeutics to brain. Front Aging Neurosci. 2019;11:373.
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Blood-brain barrier delivery for lysosomal storage disorders with IgG-lysosomal enzyme fusion proteins. Adv Drug Deliv Rev. 2022;184:114234. . 10.1016/j.addr.2022.114234
   PubMed Web of Science ®Google Scholar
• Johnsen KB, Burkhart A, Thomsen LB, et al. Targeting the transferrin receptor for brain drug delivery. Prog Neurobiol. 2019;181:101665.
   PubMed Web of Science ®Google Scholar
• Chang R, Knox J, Chang J, et al. Blood-brain barrier penetrating biologic TNF-α inhibitor for Alzheimer’s disease. Mol Pharm. 2017;14(7):2340–2349. DOI:10.1021/acs.molpharmaceut.7b00200
   PubMed Web of Science ®Google Scholar
• Chang R, Al Maghribi A, Vanderpoel V, et al. Brain penetrating bifunctional erythropoietin-transferrin receptor antibody fusion protein for Alzheimer’s disease. Mol Pharm. 2018;15(11):4963–4973. DOI:10.1021/acs.molpharmaceut.8b00594
   PubMedGoogle Scholar
• Sumbria RK, Boado RJ, Pardridge WM. Combination stroke therapy in the mouse with blood-brain barrier penetrating IgG-GDNF and IgG-TNF decoy receptor fusion proteins. Brain Res. 2013;1507:91–96.
   PubMed Web of Science ®Google Scholar
• Boado RJ, Lu JZ, Hui EK, et al. Reduction in brain heparan sulfate with systemic administration of an IgG Trojan Horse-sulfamidase fusion protein in the mucopolysaccharidosis type IIIA mouse. Mol Pharm. 2018;15(2):602–608. DOI:10.1021/acs.molpharmaceut.7b00958
   PubMedGoogle Scholar
• Boado RJ, Hui EK, Lu JZ, et al. Blood-brain barrier molecular trojan horse enables imaging of brain uptake of radioiodinated recombinant protein in the rhesus monkey. Bioconjug Chem. 2013;24(10):1741–1749. DOI:10.1021/bc400319d
   PubMed Web of Science ®Google Scholar
• Boado RJ, Lu JZ, Hui EK, et al. Bi-functional IgG-lysosomal enzyme fusion proteins for brain drug delivery. Sci Rep. 2019;9(1):18632. DOI:10.1038/s41598-019-55136-4
   PubMedGoogle Scholar
• Boado RJ, Hui EK, Lu JZ, et al. AGT-181: expression in CHO cells and pharmacokinetics, safety, and plasma iduronidase enzyme activity in Rhesus monkeys. J Biotechnol. 2009;144(2):135–141. DOI:10.1016/j.jbiotec.2009.08.019
   PubMed Web of Science ®Google Scholar
• Giugliani R, Giugliani L, de Oliveira Poswar F, et al. Neurocognitive and somatic stabilization in pediatric patients with severe Mucopolysaccharidosis Type I after 52 weeks of intravenous brain-penetrating insulin receptor antibody-iduronidase fusion protein (valanafusp alpha): an open label phase 1-2 trial. Orphanet J Rare Dis. 2018;13(1):110. DOI:10.1186/s13023-018-0849-8
   PubMedGoogle Scholar
• Kariolis MS, Wells RC, Getz JA, et al. Brain delivery of therapeutic proteins using an Fc fragment blood-brain barrier transport vehicle in mice and monkeys. Sci Transl Med. 2020;12(545):eaay1359. DOI:10.1126/scitranslmed.aay1359
   PubMed Web of Science ®Google Scholar
• Ullman JC, Arguello A, Getz JA, et al. Brain delivery and activity of a lysosomal enzyme using a blood-brain barrier transport vehicle in mice. Sci Transl Med. 2020;12(545):eaay1163. DOI:10.1126/scitranslmed.aay1163
   PubMed Web of Science ®Google Scholar
• Arguello A, Mahon CS, Calvert MEK, et al. Molecular architecture determines brain delivery of a transferrin receptor-targeted lysosomal enzyme. J Exp Med. 2022;219(3):e20211057. DOI:10.1084/jem.20211057
   PubMed Web of Science ®Google Scholar
• Sehlin D, Stocki P, Gustavsson T, et al. Brain delivery of biologics using a cross-species reactive transferrin receptor 1 VNAR shuttle. Faseb J. 2020;34(10):13272–13283. DOI:10.1096/fj.202000610RR
   PubMed Web of Science ®Google Scholar
• Stocki P, Szary J, Rasmussen CLM, et al. Blood-brain barrier transport using a high affinity, brain-selective VNAR antibody targeting transferrin receptor 1. Faseb J. 2021;35(2):e21172. DOI:10.1096/fj.202001787R
   PubMed Web of Science ®Google Scholar
• Spencer B, Williams S, Rockenstein E, et al. α-synuclein conformational antibodies fused to penetratin are effective in models of Lewy body disease. Ann Clin Transl Neurol. 2016;3(8):588–606. DOI:10.1002/acn3.321
   PubMed Web of Science ®Google Scholar
• Dupont E, Prochiantz A, Joliot A. Penetratin story: an overview. Methods Mol Biol. 2015;1324:29–37.
   PubMedGoogle Scholar
• Skrlj N, Drevenšek G, Hudoklin S, et al. Recombinant single-chain antibody with the Trojan peptide penetratin positioned in the linker region enables cargo transfer across the blood-brain barrier. Appl Biochem Biotechnol. 2013;169(1):159–169. DOI:10.1007/s12010-012-9962-7
   PubMed Web of Science ®Google Scholar
• Watts RJ, Dennis MS. Bispecific antibodies for delivery into the brain. Curr Opin Chem Biol. 2013;17(3):393–399.
   PubMed Web of Science ®Google Scholar
• Yu YJ, Atwal JK, Zhang Y, et al. Therapeutic bispecific antibodies cross the blood-brain barrier in nonhuman primates. Sci Transl Med. 2014;6(261):261ra154. DOI:10.1126/scitranslmed.3009835
   PubMed Web of Science ®Google Scholar
• Sumbria RK, Hui EK, Lu JZ, et al. Disaggregation of amyloid plaque in brain of Alzheimer’s disease transgenic mice with daily subcutaneous administration of a tetravalent bispecific antibody that targets the transferrin receptor and the Abeta amyloid peptide. Mol Pharm. 2013;10(9):3507–3513. DOI:10.1021/mp400348n
   PubMed Web of Science ®Google Scholar
• Niewoehner J, Bohrmann B, Collin L, et al. Increased brain penetration and potency of a therapeutic antibody using a monovalent molecular shuttle. Neuron. 2014;81(1):49–60. DOI:10.1016/j.neuron.2013.10.061
   PubMed Web of Science ®Google Scholar
• Hultqvist G, Syvänen S, Fang XT, et al. Bivalent brain shuttle increases antibody uptake by monovalent binding to the transferrin receptor. Theranostics. 2017;7(2):308–318. DOI:10.7150/thno.17155
   PubMed Web of Science ®Google Scholar
• Englund H, Sehlin D, Johansson AS, et al. Sensitive ELISA detection of amyloid-beta protofibrils in biological samples. J Neurochem. 2007;103(1):334–345. DOI:10.1111/j.1471-4159.2007.04759.x
   PubMed Web of Science ®Google Scholar
• Tucker S, Möller C, Tegerstedt K, et al. The murine version of BAN2401 (mAb158) selectively reduces amyloid-β protofibrils in brain and cerebrospinal fluid of tg-ArcSwe mice. J Alzheimers Dis. 2015;43(2):575–588. DOI:10.3233/JAD-140741
   PubMed Web of Science ®Google Scholar
• Magnusson K, Sehlin D, Syvänen S, et al. Specific uptake of an amyloid-β protofibril-binding antibody-tracer in AβPP transgenic mouse brain. J Alzheimers Dis. 2013;37(1):29–40. DOI:10.3233/JAD-130029
   PubMed Web of Science ®Google Scholar
• van Dyck Ch, Swanson CJ, Aisen P, et al. Lecanemab in early Alzheimer’s disease. N Engl J Med. 2023;388(1):9–21. DOI:10.1056/NEJMoa2212948
   PubMed Web of Science ®Google Scholar
• Song C, Shi J, Zhang P, et al. Immunotherapy for Alzheimer’s disease: targeting β-amyloid and beyond. Transl Neurodegener. 2022;11(1):18. DOI:10.1186/s40035-022-00292-3
   PubMed Web of Science ®Google Scholar
• DeMattos RB, Bales KR, Cummins DJ, et al. Peripheral anti-A beta antibody alters CNS and plasma a beta clearance and decreases brain a beta burden in a mouse model of Alzheimer’s disease. Proc Natl Acad Sci U S A. 2001;98(15):8850–8855. DOI:10.1073/pnas.151261398
   PubMed Web of Science ®Google Scholar
• Zuchero YJ, Chen X, Bien-Ly N, et al. Discovery of novel blood-brain barrier targets to enhance brain uptake of therapeutic antibodies. Neuron. 2016;89(1):70–82. DOI:10.1016/j.neuron.2015.11.024
   PubMed Web of Science ®Google Scholar
• Edavettal S, Cejudo-Martin P, Dasgupta B, et al. Enhanced delivery of antibodies across the blood-brain barrier via TEMs with inherent receptor-mediated phagocytosis. Med (N Y). 2022;3(12):860–882.e15. DOI:10.1016/j.medj.2022.09.007
   PubMedGoogle Scholar
• Deuschle FC, Schiefner A, Brandt C, et al. Design of a surrogate Anticalin protein directed against CD98hc for preclinical studies in mice. Protein Sci. 2020;29(8):1774–1783. DOI:10.1002/pro.3894
   PubMed Web of Science ®Google Scholar
• Farrington GK, Caram-Salas N, Haqqani AS, et al. A novel platform for engineering blood-brain barrier-crossing bispecific biologics. Faseb J. 2014;28(11):4764–4778. DOI:10.1096/fj.14-253369
   PubMed Web of Science ®Google Scholar
• Hovelsø N, Sotty F, Montezinho LP, et al. Therapeutic potential of metabotropic glutamate receptor modulators. Curr Neuropharmacol. 2012;10(1):12–48. DOI:10.2174/157015912799362805
   PubMed Web of Science ®Google Scholar
• Webster CI, Caram-Salas N, Haqqani AS, et al. Brain penetration, target engagement, and disposition of the blood-brain barrier-crossing bispecific antibody antagonist of metabotropic glutamate receptor type 1. Faseb J. 2016;30(5):1927–1940. DOI:10.1096/fj.201500078
   PubMed Web of Science ®Google Scholar
• Wu S, Lu L, Zhou J, et al. All-stage targeted therapy for glioblastoma based on lipid membrane coated cabazitaxel nanocrystals. J Control Release. 2022;345:685–695.
   PubMed Web of Science ®Google Scholar
• Guo H, Wang R, Wang D, et al. Deliver anti-PD-L1 into brain by p-hydroxybenzoic acid to enhance immunotherapeutic effect for glioblastoma. J Control Release. 2020;320:63–72.
   PubMed Web of Science ®Google Scholar
• Sánchez-Navarro M, Giralt E, Teixidó M. Blood-brain barrier peptide shuttles. Curr Opin Chem Biol. 2017;38:134–140.
   PubMed Web of Science ®Google Scholar
• Ruan H, Chai Z, Shen Q, et al. A novel peptide ligand RAP12 of LRP1 for glioma targeted drug delivery. J Control Release. 2018;279:306–315.
   PubMed Web of Science ®Google Scholar
• Wang D, El-Amouri SS, Dai M, et al. Engineering a lysosomal enzyme with a derivative of receptor-binding domain of apoE enables delivery across the blood-brain barrier. Proc Natl Acad Sci U S A. 2013;110(8):2999–3004. DOI:10.1073/pnas.1222742110
   PubMed Web of Science ®Google Scholar
• Zhan C, Li B, Hu L, et al. Micelle-based brain-targeted drug delivery enabled by a nicotine acetylcholine receptor ligand. Angew Chem Int Ed Engl. 2011;50(24):5482–5485. DOI:10.1002/anie.201100875
   PubMed Web of Science ®Google Scholar
• Bao Q, Hu P, Xu Y, et al. Simultaneous blood-brain barrier crossing and protection for stroke treatment based on edaravone-loaded ceria nanoparticles. ACS Nano. 2018;12(7):6794–6805. DOI:10.1021/acsnano.8b01994
   PubMed Web of Science ®Google Scholar
• Jafari B, Pourseif MM, Barar J, et al. Peptide-mediated drug delivery across the blood-brain barrier for targeting brain tumors. Expert Opin Drug Deliv. 2019;16(6):583–605. DOI:10.1080/17425247.2019.1614911
   PubMed Web of Science ®Google Scholar
• Suárez VM, Vispo NS, Ramos OS. Application of the phage display technology for the development of peptide-mediated drug delivery systems through the blood-brain barrier. Curr Pharm Biotechnol. 2021;22(11):1394–1403.
   PubMed Web of Science ®Google Scholar
• Cavaco M, Valle J, da Silva R, et al. (D)peph3, an improved peptide shuttle for receptor-independent transport across the blood-brain barrier. Curr Pharm Des. 2020;26(13):1495–1506. DOI:10.2174/1381612826666200213094556
   PubMed Web of Science ®Google Scholar
• Zolotarev YA, Mitkevich VA, Shram SI, et al. Pharmacokinetics and molecular modeling indicate nAchrα4-derived peptide HAEE goes through the blood-brain barrier. Biomolecules. 2021;11(6):909. DOI:10.3390/biom11060909
   PubMed Web of Science ®Google Scholar
• Majerova P, Hanes J, Olesova D, et al. Novel blood-brain barrier shuttle peptides discovered through the phage display method. Molecules. 2020;25(4):874. DOI:10.3390/molecules25040874
   PubMed Web of Science ®Google Scholar
• Kumar V, Patiyal S, Kumar R, et al. B3pdb: an archive of blood-brain barrier-penetrating peptides. Brain Struct Funct. 2021;226(8):2489–2495. DOI:10.1007/s00429-021-02341-5
   PubMed Web of Science ®Google Scholar
• Regina A, Demeule M, Tripathy S, et al. ANG4043, a novel brain-penetrant peptide-mAb conjugate, is efficacious against HER2-positive intracranial tumors in mice. Mol Cancer Ther. 2015;14(1):129–140. DOI:10.1158/1535-7163.MCT-14-0399
   PubMed Web of Science ®Google Scholar
• Yang T, Mochida Y, Liu X, et al. Conjugation of glucosylated polymer chains to checkpoint blockade antibodies augments their efficacy and specificity for glioblastoma. Nat Biomed Eng. 2021;5(11):1274–1287. DOI:10.1038/s41551-021-00803-z. .
   PubMed Web of Science ®Google Scholar
• Filipczak N, Pan J, Yalamarty SSK, et al. Recent advancements in liposome technology. Adv Drug Deliv Rev. 2020;156:4–22.
   PubMed Web of Science ®Google Scholar
• Zamani P, Penson PE, Barreto GE, et al. Recent advancements in liposome-based strategies for effective drug delivery to the brain. Curr Med Chem. 2021;28(21):4152–4171. DOI:10.2174/0929867328666201218121728
   PubMed Web of Science ®Google Scholar
• Agrawal M, Ajazuddin TD, Tripathi DK, et al. Recent advancements in liposomes targeting strategies to cross blood-brain barrier (BBB) for the treatment of Alzheimer’s disease. J Control Release. 2017;260:61–77.
   PubMed Web of Science ®Google Scholar
• Lindqvist A, Rip J, Gaillard PJ, et al. Enhanced brain delivery of the opioid peptide DAMGO in glutathione pegylated liposomes: a microdialysis study. Mol Pharm. 2013;10(5):1533–1541. DOI:10.1021/mp300272a
   PubMedGoogle Scholar
• Gaillard PJ, Appeldoorn CC, Rip J, et al. Enhanced brain delivery of liposomal methylprednisolone improved therapeutic efficacy in a model of neuroinflammation. J Control Release. 2012;164(3):364–369. DOI:10.1016/j.jconrel.2012.06.022
   PubMed Web of Science ®Google Scholar
• Rotman M, Welling MM, Bunschoten A, et al. Enhanced glutathione PEGylated liposomal brain delivery of an anti-amyloid single domain antibody fragment in a mouse model for Alzheimer’s disease. JControlled Release. 2015;203:40–50.
   PubMed Web of Science ®Google Scholar
• Morais M, Cantante C, Gano L, et al. Biodistribution of a (67)ga-labeled anti-TNF VHH single-domain antibody containing a bacterial albumin-binding domain (Zag). Nucl Med Biol. 2014;41:e44–8.
   PubMed Web of Science ®Google Scholar
• Yin W, Zhao Y, Kang X, et al. BBB-penetrating codelivery liposomes treat brain metastasis of non-small cell lung cancer with EGFR(T790M) mutation. Theranostics. 2020;10(14):6122–6135. DOI:10.7150/thno.42234
   PubMed Web of Science ®Google Scholar
• Böttger D, Ullrich C, Humpel C. Monocytes deliver bioactive nerve growth factor through a brain capillary endothelial cell-monolayer in vitro and counteract degeneration of cholinergic neurons. Brain Res. 2010;1312:108–119.
   PubMed Web of Science ®Google Scholar
• Kuo YC, Wang CT. Protection of SK-N-MC cells against β-amyloid peptide-induced degeneration using neuron growth factor-loaded liposomes with surface lactoferrin. Biomaterials. 2014;35(22):5954–5964.
   PubMed Web of Science ®Google Scholar
• Kuo YC, Chou PR. Neuroprotection against degeneration of sk-N-mc cells using neuron growth factor-encapsulated liposomes with surface cereport and transferrin. J Pharmaceut sci. 2014;103(8):2484–2497.
   PubMed Web of Science ®Google Scholar
• Kreuter J, Alyautdin RN, Kharkevich DA, et al. Passage of peptides through the blood-brain barrier with colloidal polymer particles (nanoparticles). Brain Res. 1995;674(1):171–174. DOI:10.1016/0006-8993(95)00023-J
   PubMed Web of Science ®Google Scholar
• Alyautdin RN, Tezikov EB, Ramge P, et al. Significant entry of tubocurarine into the brain of rats by adsorption to polysorbate 80-coated polybutylcyanoacrylate nanoparticles: an in situ brain perfusion study. J Microencapsul. 1998;15(1):67–74. DOI:10.3109/02652049809006836
   PubMed Web of Science ®Google Scholar
• Alyautdin RN, Petrov VE, Langer K, et al. Delivery of loperamide across the blood-brain barrier with polysorbate 80-coated polybutylcyanoacrylate nanoparticles. Pharm Res. 1997;14(3):325–328. DOI:10.1023/A:1012098005098
   PubMed Web of Science ®Google Scholar
• Friese A, Seiller E, Quack G, et al. Increase of the duration of the anticonvulsive activity of a novel NMDA receptor antagonist using poly(butylcyanoacrylate) nanoparticles as a parenteral controlled release system. Eur J Pharm Biopharm. 2000;49(2):103–109. DOI:10.1016/S0939-6411(99)00073-9
   PubMed Web of Science ®Google Scholar
• Tian XH, Lin XN, Wei F, et al. Enhanced brain targeting of temozolomide in polysorbate-80 coated polybutylcyanoacrylate nanoparticles. Int J Nanomedicine. 2011;6:445–452.
   PubMed Web of Science ®Google Scholar
• Reimold I, Domke D, Bender J, et al. Delivery of nanoparticles to the brain detected by fluorescence microscopy. Eur J Pharm Biopharm. 2008;70(2):627–632. DOI:10.1016/j.ejpb.2008.05.007
   PubMed Web of Science ®Google Scholar
• Kuo YC, Chung CY. Transcytosis of CRM197-grafted polybutylcyanoacrylate nanoparticles for delivering zidovudine across human brain-microvascular endothelial cells. Colloids Surf B Biointerfaces. 2012;91:242–249.
   PubMed Web of Science ®Google Scholar
• Wilson B. Brain targeting PBCA nanoparticles and the blood-brain barrier. Nanomedicine (Lond). 2009;4(5):499–502.
   PubMed Web of Science ®Google Scholar
• Ramge P, Unger RE, Oltrogge JB, et al. Polysorbate-80 coating enhances uptake of polybutylcyanoacrylate (PBCA)-nanoparticles by human and bovine primary brain capillary endothelial cells. Eur J Neurosci. 2000;12(6):1931–1940. DOI:10.1046/j.1460-9568.2000.00078.x
   PubMed Web of Science ®Google Scholar
• Koffie RM, Farrar CT, Saidi LJ, et al. Nanoparticles enhance brain delivery of blood-brain barrier-impermeable probes for in vivo optical and magnetic resonance imaging. Proc Natl Acad Sci U S A. 2011;108(46):18837–18842. DOI:10.1073/pnas.1111405108
   PubMed Web of Science ®Google Scholar
• Wang Y, Jia F, Lin Y. Poly(butyl cyanoacrylate) nanoparticles-deliveredβ-nerve growth factor promotes the neurite outgrowth and reduces the mortality in the rat after traumatic brain injury. Nanotechnology. 2022;33(13). DOI:10.1088/1361-6528/ac44e8
   Web of Science ®Google Scholar
• Wei J, Wu D, Shao Y, et al. ApoE-mediated systemic nanodelivery of granzyme B and CpG for enhanced glioma immunotherapy. J Control Release. 2022;347:68–77.
   PubMed Web of Science ®Google Scholar
• Khalin I, Alyautdin R, Wong TW, et al. Brain-derived neurotrophic factor delivered to the brain using poly (lactide-co-glycolide) nanoparticles improves neurological and cognitive outcome in mice with traumatic brain injury. Drug Deliv. 2016;23(9):3520–3528. DOI:10.1080/10717544.2016.1199609
   PubMed Web of Science ®Google Scholar
• Tosi G, Duskey JT, Kreuter J. Nanoparticles as carriers for drug delivery of macromolecules across the blood-brain barrier. Expert Opin Drug Deliv. 2020;17(1):23–32.
   PubMed Web of Science ®Google Scholar
• Lackington WA, Kočí Z, Alekseeva T, et al. Controlling the dose-dependent, synergistic and temporal effects of NGF and GDNF by encapsulation in PLGA microparticles for use in nerve guidance conduits for the repair of large peripheral nerve defects. J Control Release. 2019;304:51–64.
   PubMed Web of Science ®Google Scholar
• Harris NM, Ritzel R, Mancini NS, et al. Nano-particle delivery of brain derived neurotrophic factor after focal cerebral ischemia reduces tissue injury and enhances behavioral recovery. Pharmacol Biochem Behav. 2016;150-151:48–56.
   PubMed Web of Science ®Google Scholar
• Garbayo E, Ansorena E, Lana H, et al. Brain delivery of microencapsulated GDNF induces functional and structural recovery in parkinsonian monkeys. Biomaterials. 2016;110:11–23.
   PubMed Web of Science ®Google Scholar
• Pinkernelle J, Raffa V, Calatayud MP, et al. Growth factor choice is critical for successful functionalization of nanoparticles. Front Neurosci. 2015;9:305.
   PubMed Web of Science ®Google Scholar
• D’souza A, Dave KM, Stetler RA, et al. Targeting the blood-brain barrier for the delivery of stroke therapies. Adv Drug Deliv Rev. 2021;171:332–351.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Fay JM, Poon CD, et al. Nanoformulation of brain-derived neurotrophic factor with target receptor-triggered-release in the central nervous system. Adv Funct Mater. 2018;28(6):1703982. DOI:10.1002/adfm.201703982
   PubMed Web of Science ®Google Scholar
• Pilakka-Kanthikeel S, Atluri VS, Sagar V, et al. Targeted brain derived neurotropic factors (BDNF) delivery across the blood-brain barrier for neuro-protection using magnetic nano carriers: an in-vitro study. PLoS ONE. 2013;8(4):e62241. DOI:10.1371/journal.pone.0062241
   PubMed Web of Science ®Google Scholar
• Schuster T, Mühlstein A, Yaghootfam C, et al. Potential of surfactant-coated nanoparticles to improve brain delivery of arylsulfatase a. J Control Release. 2017;253:1–10.
   PubMed Web of Science ®Google Scholar
• Rigon L, Salvalaio M, Pederzoli F, et al. Targeting brain disease in MPSII: preclinical evaluation of IDS-loaded PLGA nanoparticles. Int J Mol Sci. 2019;20(8):2014. DOI:10.3390/ijms20082014
   PubMed Web of Science ®Google Scholar
• Kim JY, Choi WI, Kim YH, et al. Brain-targeted delivery of protein using chitosan- and RVG peptide-conjugated, pluronic-based nano-carrier. Biomaterials. 2013;34(4):1170–1178. DOI:10.1016/j.biomaterials.2012.09.047
   PubMed Web of Science ®Google Scholar
• Wyatt EA, Davis ME. Nanoparticles containing a combination of a drug and an antibody for the treatment of breast cancer brain metastases. Mol Pharm. 2020;17(2):717–721.
   PubMedGoogle Scholar
• Johnsen KB, Bak M, Kempen PJ, et al. Antibody affinity and valency impact brain uptake of transferrin receptor-targeted gold nanoparticles. Theranostics. 2018;8(12):3416–3436. DOI:10.7150/thno.25228
   PubMed Web of Science ®Google Scholar
• Fan K, Jia X, Zhou M, et al. Ferritin nanocarrier traverses the blood brain barrier and kills glioma. ACS Nano. 2018;12(5):4105–4115. DOI:10.1021/acsnano.7b06969
   PubMed Web of Science ®Google Scholar
• Rizzuto MA, Dal Magro R, Barbieri L, et al. H-Ferritin nanoparticle-mediated delivery of antibodies across a BBB in vitro model for treatment of brain malignancies. Biomater Sci. 2021;9(6):2032–2042. DOI:10.1039/D0BM01726D
   PubMed Web of Science ®Google Scholar
• Jin Z, Piao L, Sun G, et al. Dual functional nanoparticles efficiently across the blood-brain barrier to combat glioblastoma via simultaneously inhibit the PI3K pathway and NKG2A axis. J Drug Target. 2021;29(3):323–335. DOI:10.1080/1061186X.2020.1841214
   PubMed Web of Science ®Google Scholar
• Yin T, Fan Q, Hu F, et al. Engineered macrophage-membrane-coated nanoparticles with enhanced PD-1 expression induce immunomodulation for a synergistic and targeted antiglioblastoma activity. Nano Lett. 2022;22(16):6606–6614. DOI:10.1021/acs.nanolett.2c01863
   PubMed Web of Science ®Google Scholar
• He CS, Li JS, Cai P, et al. Two-step targeted hybrid nanoconstructs increase brain penetration and efficacy of the therapeutic antibody trastuzumab against brain metastasis of HER2-positive breast cancer. Adv Funct Mater. 2018;28(9):1705668. DOI:10.1002/adfm.201705668
   Web of Science ®Google Scholar
• Wei X, Zhan C, Shen Q, et al. A D-peptide ligand of nicotine acetylcholine receptors for brain-targeted drug delivery. Angew Chem Int Ed Engl. 2015;54(10):3023–3027. DOI:10.1002/anie.201411226
   PubMed Web of Science ®Google Scholar
• Han L, Liu C, Qi H, et al. Systemic delivery of monoclonal antibodies to the central nervous system for brain tumor therapy. Adv Mater. 2019;31(19):e1805697. DOI:10.1002/adma.201805697
   PubMed Web of Science ®Google Scholar
• Wang H, Chao Y, Zhao H, et al. Smart nanomedicine to enable crossing blood-brain barrier delivery of checkpoint blockade antibody for immunotherapy of glioma. ACS Nano. 2022;16(1):664–674. DOI:10.1021/acsnano.1c08120. .
   PubMed Web of Science ®Google Scholar
• Vella LJ, Hill AF, Cheng L. Focus on extracellular vesicles: exosomes and their role in protein trafficking and biomarker potential in Alzheimer’s and Parkinson’s disease. Int J Mol Sci. 2016;17(2):173.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Bi J, Huang J, et al. Exosome: a review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomedicine. 2020;15:6917–6934.
   PubMed Web of Science ®Google Scholar
• Wu P, Zhang B, Ocansey DKW, et al. Extracellular vesicles: a bright star of nanomedicine. Biomaterials. 2021;269:120467.
   PubMed Web of Science ®Google Scholar
• Liang Y, Duan L, Lu J, et al. Engineering exosomes for targeted drug delivery. Theranostics. 2021;11(7):3183–3195. DOI:10.7150/thno.52570
   PubMed Web of Science ®Google Scholar
• Cully M. Exosome-based candidates move into the clinic. Nat Rev Drug Discov. 2021;20(1):6–7.
   PubMed Web of Science ®Google Scholar
• Chen H, Wang L, Zeng X, et al. Exosomes, a New Star for Targeted Delivery. Front Cell Dev Biol. 2021;9:751079.
   PubMed Web of Science ®Google Scholar
• Shao J, Zaro J, Shen Y. Advances in exosome-based drug delivery and tumor targeting: from tissue distribution to intracellular fate. Int J Nanomedicine. 2020;15:9355–9371.
   PubMed Web of Science ®Google Scholar
• Saint-Pol J, Gosselet F, Duban-Deweer S, et al. Targeting and crossing the blood-brain barrier with extracellular vesicles. Cells. 2020;9(4):851. DOI:10.3390/cells9040851
   PubMed Web of Science ®Google Scholar
• Joshi BS, Zuhorn IS. Heparan sulfate proteoglycan-mediated dynamin-dependent transport of neural stem cell exosomes in an in vitro blood-brain barrier model. Eur J Neurosci. 2021;53(3):706–719.
   PubMed Web of Science ®Google Scholar
• Haney MJ, Klyachko NL, Zhao Y, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.
   PubMed Web of Science ®Google Scholar
• Haney MJ, Zhao Y, Li S, et al. Cell-mediated transfer of catalase nanoparticles from macrophages to brain endothelial, glial and neuronal cells. Nanomedicine (Lond). 2011;6(7):1215–1230. DOI:10.2217/nnm.11.32
   PubMed Web of Science ®Google Scholar
• Haney MJ, Suresh P, Zhao Y, et al. Blood-borne macrophage-neural cell interactions hitchhike on endosome networks for cell-based nanozyme brain delivery. Nanomedicine (Lond). 2012;7(6):815–833. DOI:10.2217/nnm.11.156
   PubMed Web of Science ®Google Scholar
• Haney MJ, Zhao Y, Harrison EB, et al. Specific transfection of inflamed brain by macrophages: a new therapeutic strategy for neurodegenerative diseases. PLoS ONE. 2013;8(4):e61852. DOI:10.1371/journal.pone.0061852
   PubMed Web of Science ®Google Scholar
• Yuan D, Zhao Y, Banks WA, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 2017;142:1–12.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Haney MJ, Gupta R, et al. GDNF-transfected macrophages produce potent neuroprotective effects in Parkinson’s disease mouse model. PLoS ONE. 2014;9(9):e106867. DOI:10.1371/journal.pone.0106867
   PubMed Web of Science ®Google Scholar
• Woods S, O’brien LM, Butcher W, et al. Glucosamine-NISV delivers antibody across the blood-brain barrier: optimization for treatment of encephalitic viruses. J Control Release. 2020;324:644–656.
   PubMed Web of Science ®Google Scholar
• Galstyan A, Markman JL, Shatalova ES, et al. Blood-brain barrier permeable nano immunoconjugates induce local immune responses for glioma therapy. Nat Commun. 2019;10(1):3850. DOI:10.1038/s41467-019-11719-3
   PubMedGoogle Scholar
• Santana-Armas ML, Tros de Ilarduya C. Strategies for cancer gene-delivery improvement by non-viral vectors. Int J Pharm. 2021;596:120291.
   PubMedGoogle Scholar
• Bexell D, Svensson A, Bengzon J. Stem cell-based therapy for malignant glioma. Cancer Treat Rev. 2013;39(4):358–365.
   PubMed Web of Science ®Google Scholar
• Razpotnik R, Novak N, Čurin Šerbec V, et al. Targeting malignant brain tumors with antibodies. Front Immunol. 2017;8:1181.
   PubMed Web of Science ®Google Scholar
• Zhao D, Najbauer J, Garcia E, et al. Neural stem cell tropism to glioma: critical role of tumor hypoxia. Mol Cancer Res. 2008;6(12):1819–1829. DOI:10.1158/1541-7786.MCR-08-0146
   PubMed Web of Science ®Google Scholar
• Kanojia D, Balyasnikova MR IV, Morshed RA, et al. Neural stem cells secreting anti-HER2 antibody improve survival in a preclinical model of HER2 overexpressing breast cancer brain metastases. Stem Cells. 2015;33(10):2985–2994. DOI:10.1002/stem.2109
   PubMed Web of Science ®Google Scholar
• van de Water Ja, Bagci-Onder T, Agarwal AS, et al. Therapeutic stem cells expressing variants of EGFR-specific nanobodies have antitumor effects. Proc Natl Acad Sci U S A. 2012;109(41):16642–16647. DOI:10.1073/pnas.1202832109
   PubMed Web of Science ®Google Scholar
• Balyasnikova IV, Prasol MS, Ferguson SD, et al. Intranasal delivery of mesenchymal stem cells significantly extends survival of irradiated mice with experimental brain tumors. Mol Ther. 2014;22(1):140–148. DOI:10.1038/mt.2013.199
   PubMed Web of Science ®Google Scholar
• Dave KM, Zhao W, Hoover C, et al. Extracellular vesicles derived from a human brain endothelial cell line increase cellular ATP levels. AAPS Pharm Sci Tech. 2021;22(1):18. DOI:10.1208/s12249-020-01892-w
   PubMed Web of Science ®Google Scholar
• Kojima R, Bojar D, Rizzi G, et al. Designer exosomes produced by implanted cells intracerebrally deliver therapeutic cargo for Parkinson’s disease treatment. Nat Commun. 2018;9(1):1305. DOI:10.1038/s41467-018-03733-8
   PubMedGoogle Scholar
• Abulimiti A, Lai MS, Chang RC. Applications of adeno-associated virus vector-mediated gene delivery for neurodegenerative diseases and psychiatric diseases: progress, advances, and challenges. Mech Ageing Dev. 2021;199:111549.
   PubMed Web of Science ®Google Scholar
• Chen W, Yao S, Wan J, et al. BBB-crossing adeno-associated virus vector: an excellent gene delivery tool for CNS disease treatment. J Control Release. 2021;333:129–138.
   PubMed Web of Science ®Google Scholar
• Wang D, Li S, Gessler DJ, et al. A rationally engineered capsid variant of AAV9 for systemic CNS-directed and peripheral tissue-detargeted gene delivery in neonates. Mol Ther Methods Clin Dev. 2018;9:234–246.
   PubMed Web of Science ®Google Scholar
• Wirth B. Spinal muscular atrophy: in the challenge lies a solution. Trends Neurosci. 2021;44(4):306–322.
   PubMed Web of Science ®Google Scholar
• Stevens D, Claborn MK, Gildon BL, et al. Onasemnogene Abeparvovec-xioi: gene therapy for spinal muscular atrophy. Ann Pharmacother. 2020;54(10):1001–1009. DOI:10.1177/1060028020914274
   PubMed Web of Science ®Google Scholar
• Al-Zaidy SA, Mendell JR. From clinical trials to clinical practice: practical considerations for gene replacement therapy in SMA type 1. Pediatr Neurol. 2019;100:3–11.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med. 2017;377(18):1713–1722. DOI:10.1056/NEJMoa1706198
   PubMed Web of Science ®Google Scholar
• Zhao L, Gottesdiener AJ, Parmar M, et al. Intracerebral adeno-associated virus gene delivery of apolipoprotein E2 markedly reduces brain amyloid pathology in Alzheimer’s disease mouse models. Neurobiol Aging. 2016;44:159–172.
   PubMed Web of Science ®Google Scholar
• d’Abramo C, Acker CM, Jimenez H, et al. Passive immunization in JNPL3 transgenic mice using an array of phospho-tau specific antibodies. PLoS ONE. 2015;10(8):e0135774. DOI:10.1371/journal.pone.0135774
   PubMed Web of Science ®Google Scholar
• Liu W, Zhao L, Blackman B, et al. Vectored intracerebral immunization with the anti-tau monoclonal antibody PHF1 markedly reduces tau pathology in mutant tau transgenic mice. J Neurosci. 2016;36(49):12425–12435. DOI:10.1523/JNEUROSCI.2016-16.2016
   PubMed Web of Science ®Google Scholar
• Sacramento CB, Sondhi D, Rosenberg JB, et al. Anti-phospho-tau gene therapy for chronic traumatic encephalopathy. Hum Gene Ther. 2020;31(1–2):57–69. DOI:10.1089/hum.2019.174
   PubMed Web of Science ®Google Scholar
• Maguire CA, Balaj L, Sivaraman S, et al. Microvesicle-associated AAV vector as a novel gene delivery system. Mol Ther. 2012;20(5):960–971. DOI:10.1038/mt.2011.303
   PubMed Web of Science ®Google Scholar
• Hudry E, Martin C, Gandhi S, et al. Exosome-associated AAV vector as a robust and convenient neuroscience tool. Gene Ther. 2016;23(4):380–392. DOI:10.1038/gt.2016.11
   PubMed Web of Science ®Google Scholar
• Cheng M, Dietz L, Gong Y, et al. Neutralizing antibody evasion and transduction with purified extracellular vesicle-enveloped adeno-associated virus vectors. Hum Gene Ther. 2021;32(23–24):1457–1470. DOI:10.1089/hum.2021.122
   PubMed Web of Science ®Google Scholar
• Kurokawa Y, Osaka H, Kouga T, et al. Gene therapy in a mouse model of Niemann-Pick disease type C1. Hum Gene Ther. 2021;32(11–12):589–598. DOI:10.1089/hum.2020.175
   PubMed Web of Science ®Google Scholar
• Jiang D, Lee H, Pardridge WM. Plasmid DNA gene therapy of the Niemann-Pick C1 mouse with transferrin receptor-targeted Trojan horse liposomes. Sci Rep. 2020;10(1):13334.
   PubMed Web of Science ®Google Scholar
• Jackson KL, Dayton RD, Deverman BE, et al. Better targeting, better efficiency for wide-scale neuronal transduction with the synapsin promoter and AAV-PHP.B. Front Mol Neurosci. 2016;9:116.
   PubMed Web of Science ®Google Scholar
• O’keeffe E, Campbell M. Modulating the paracellular pathway at the blood-brain barrier: current and future approaches for drug delivery to the CNS. Drug Discov Today Technol. 2016;20:35–39.
   PubMedGoogle Scholar
• Chen KT, Wei KC, Liu HL. Theranostic strategy of focused ultrasound induced blood-brain barrier opening for CNS disease treatment. Front Pharmacol. 2019;10:86.
   PubMed Web of Science ®Google Scholar
• Rezai AR, Ranjan M, D’haese PF, et al. Noninvasive hippocampal blood-brain barrier opening in Alzheimer’s disease with focused ultrasound. Proc Natl Acad Sci U S A. 2020;117(17):9180–9182. DOI:10.1073/pnas.2002571117
   PubMed Web of Science ®Google Scholar
• Chen KT, Chai WY, Lin YJ, et al. Neuronavigation-guided focused ultrasound for transcranial blood-brain barrier opening and immunostimulation in brain tumors. Sci Adv. 2021;7(6).
   Web of Science ®Google Scholar
• Beccaria K, Canney M, Bouchoux G, et al. Ultrasound-induced blood-brain barrier disruption for the treatment of gliomas and other primary CNS tumors. Cancer Lett. 2020;479:13–22.
   PubMed Web of Science ®Google Scholar
• Brighi C, Salimova E, de Veer M, et al. Translation of focused ultrasound for blood-brain barrier opening in glioma. J Control Release. 2022;345:443–463. .
   PubMed Web of Science ®Google Scholar
• Chai WY, Chu PC, Tsai MY, et al. Magnetic-resonance imaging for kinetic analysis of permeability changes during focused ultrasound-induced blood-brain barrier opening and brain drug delivery. J Control Release. 2014;192:1–9.
   PubMed Web of Science ®Google Scholar
• Curley CT, Sheybani ND, Bullock TN, et al. Focused ultrasound immunotherapy for central nervous system pathologies: challenges and opportunities. Theranostics. 2017;7(15):3608–3623. DOI:10.7150/thno.21225
   PubMed Web of Science ®Google Scholar
• Fishman PS, Fischell JM. Focused ultrasound mediated opening of the blood-brain barrier for neurodegenerative diseases. Front Neurol. 2021;12:749047.
   PubMed Web of Science ®Google Scholar
• Chen PY, Hsieh HY, Huang CY, et al. Focused ultrasound-induced blood–brain barrier opening to enhance interleukin-12 delivery for brain tumor immunotherapy: a preclinical feasibility study. J Transl Med. 2015;13(1):93. DOI:10.1186/s12967-015-0451-y
   PubMedGoogle Scholar
• Park EJ, Zhang YZ, Vykhodtseva N, et al. Ultrasound-mediated blood-brain/blood-tumor barrier disruption improves outcomes with trastuzumab in a breast cancer brain metastasis model. J Control Release. 2012;163(3):277–284. DOI:10.1016/j.jconrel.2012.09.007
   PubMed Web of Science ®Google Scholar
• Kobus T, Zervantonakis IK, Zhang Y, et al. Growth inhibition in a brain metastasis model by antibody delivery using focused ultrasound-mediated blood-brain barrier disruption. J Control Release. 2016;238:281–288.
   PubMed Web of Science ®Google Scholar
• Liu HL, Hsu PH, Lin CY, et al. Focused ultrasound enhances central nervous system delivery of bevacizumab for malignant glioma treatment. Radiology. 2016;281(1):99–108. DOI:10.1148/radiol.2016152444
   PubMed Web of Science ®Google Scholar
• Sun T, Shi Q, Zhang Y, et al. Focused ultrasound with anti-pGlu3 Aβ enhances efficacy in Alzheimer’s disease-like mice via recruitment of peripheral immune cells. J Control Release. 2021;336:443–456.
   PubMed Web of Science ®Google Scholar
• Nisbet RM, Van der Jeugd A, Leinenga G, et al. Combined effects of scanning ultrasound and a tau-specific single chain antibody in a tau transgenic mouse model. Brain. 2017;140(5):1220–1230. DOI:10.1093/brain/awx052
   PubMedGoogle Scholar
• Janowicz PW, Leinenga G, Götz J, et al. Ultrasound-mediated blood-brain barrier opening enhances delivery of therapeutically relevant formats of a tau-specific antibody. Sci Rep. 2019;9(1):9255. DOI:10.1038/s41598-019-45577-2
   PubMedGoogle Scholar
• Leinenga G, Koh WK, Götz J. A comparative study of the effects of Aducanumab and scanning ultrasound on amyloid plaques and behavior in the APP23 mouse model of Alzheimer disease. Alzheimers Res Ther. 2021;13(1):76.
   PubMed Web of Science ®Google Scholar
• Leinenga G, Bodea LG, Koh WK, et al. Delivery of antibodies into the brain using focused scanning ultrasound. J Vis Exp. 2020;2020(161).
   Google Scholar
• Wang F, Shi Y, Lu L, et al. Targeted delivery of GDNF through the blood-brain barrier by MRI-guided focused ultrasound. PLoS ONE. 2012;7(12):e52925. DOI:10.1371/journal.pone.0052925
   PubMed Web of Science ®Google Scholar
• Samiotaki G, Acosta C, Wang S, et al. Enhanced delivery and bioactivity of the neurturin neurotrophic factor through focused ultrasound-mediated blood-brain barrier opening in vivo. J Cereb Blood Flow Metab. 2015;35(4):611–622. DOI:10.1038/jcbfm.2014.236
   PubMed Web of Science ®Google Scholar
• Åslund AKO, Berg S, Hak S, et al. Nanoparticle delivery to the brain–by focused ultrasound and self-assembled nanoparticle-stabilized microbubbles. J Control Release. 2015;220(Pt A):287–294. DOI:10.1016/j.jconrel.2015.10.047
   PubMedGoogle Scholar
• Fan CH, Ting CY, Lin CY, et al. Noninvasive, Targeted and Non-Viral Ultrasound-Mediated GDNF-Plasmid Delivery for Treatment of Parkinson’s Disease. Sci Rep. 2016;6(1):19579. DOI:10.1038/srep19579
   PubMedGoogle Scholar
• Mead BP, Kim N, Miller GW, et al. Novel focused ultrasound gene therapy approach noninvasively restores dopaminergic neuron function in a rat Parkinson’s disease model. Nano Lett. 2017;17(6):3533–3542. DOI:10.1021/acs.nanolett.7b00616
   PubMed Web of Science ®Google Scholar
• Thévenot E, Jordão JF, O’reilly MA, et al. Targeted delivery of self-complementary adeno-associated virus serotype 9 to the brain, using magnetic resonance imaging-guided focused ultrasound. Hum Gene Ther. 2012;23(11):1144–1155. DOI:10.1089/hum.2012.013
   PubMed Web of Science ®Google Scholar
• Alonso A, Reinz E, Leuchs B, et al. Focal delivery of AAV2/1-transgenes into the rat brain by localized ultrasound-induced BBB opening. Mol Ther Nucleic Acids. 2013;2(2):e73. DOI:10.1038/mtna.2012.64
   PubMedGoogle Scholar
• Karakatsani ME, Wang S, Samiotaki G, et al. Amelioration of the nigrostriatal pathway facilitated by ultrasound-mediated neurotrophic delivery in early Parkinson’s disease. J Control Release. 2019;303:289–301.
   PubMed Web of Science ®Google Scholar
• Hsu PH, Wei KC, Huang CY, et al. Noninvasive and targeted gene delivery into the brain using microbubble-facilitated focused ultrasound. PLoS ONE. 2013;8(2):e57682. DOI:10.1371/journal.pone.0057682
   PubMed Web of Science ®Google Scholar
• Morse SV, Mishra A, Chan TG, et al. Liposome delivery to the brain with rapid short-pulses of focused ultrasound and microbubbles. J Control Release. 2022;341:605–615.
   PubMed Web of Science ®Google Scholar
• Bien-Ly N, Yu YJ, Bumbaca D, et al. Transferrin receptor (TfR) trafficking determines brain uptake of TfR antibody affinity variants. J Exp Med. 2014;211(2):233–244. DOI:10.1084/jem.20131660
   PubMed Web of Science ®Google Scholar
• Voigt N, Henrich-Noack P, Kockentiedt S, et al. Toxicity of polymeric nanoparticles in vivo and in vitro. J Nanopart Res. 2014;16(6):2379. DOI:10.1007/s11051-014-2379-1
   PubMed Web of Science ®Google Scholar
• Zhou Y, Peng Z, Seven ES, et al. Crossing the blood-brain barrier with nanoparticles. J Control Release. 2018;270:290–303.
   PubMed Web of Science ®Google Scholar
• Körbelin J, Dogbevia G, Michelfelder S, et al. A brain microvasculature endothelial cell-specific viral vector with the potential to treat neurovascular and neurological diseases. EMBO Mol Med. 2016;8(6):609–625. DOI:10.15252/emmm.201506078
   PubMed Web of Science ®Google Scholar