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ISSN (Online): 1873-4286

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Review Article

Brain Drug Delivery: Overcoming the Blood-brain Barrier to Treat Tauopathies

Author(s): Jozef Hanes*, Eva Dobakova and Petra Majerova

Volume 26, Issue 13, 2020

Page: [1448 - 1465] Pages: 18

DOI: 10.2174/1381612826666200316130128

Price: $65

Abstract

Tauopathies are neurodegenerative disorders characterized by the deposition of abnormal tau protein in the brain. The application of potentially effective therapeutics for their successful treatment is hampered by the presence of a naturally occurring brain protection layer called the blood-brain barrier (BBB). BBB represents one of the biggest challenges in the development of therapeutics for central nervous system (CNS) disorders, where sufficient BBB penetration is inevitable. BBB is a heavily restricting barrier regulating the movement of molecules, ions, and cells between the blood and the CNS to secure proper neuronal function and protect the CNS from dangerous substances and processes. Yet, these natural functions possessed by BBB represent a great hurdle for brain drug delivery. This review is concentrated on summarizing the available methods and approaches for effective therapeutics’ delivery through the BBB to treat neurodegenerative disorders with a focus on tauopathies. It describes the traditional approaches but also new nanotechnology strategies emerging with advanced medical techniques. Their limitations and benefits are discussed.

Keywords: CNS, blood-brain barrier (BBB), Alzheimer's disease, brain drug delivery, drug targeting, Tauopathies.

« Previous Next »
[1]
Banks WA. From blood-brain barrier to blood-brain interface: new opportunities for CNS drug delivery. Nat Rev Drug Discov 2016; 15(4): 275-92.
[http://dx.doi.org/10.1038/nrd.2015.21] [PMID: 26794270]
[2]
Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005; 2(1): 3-14.
[http://dx.doi.org/10.1602/neurorx.2.1.3] [PMID: 15717053]
[3]
Kovacs GG. Tauopathies. Handb Clin Neurol 2017; 145: 355-68.
[http://dx.doi.org/10.1016/B978-0-12-802395-2.00025-0] [PMID: 28987182]
[4]
Irwin DJ. Tauopathies as clinicopathological entities. Parkinsonism Relat Disord 2016; 22(Suppl. 1): S29-33.
[http://dx.doi.org/10.1016/j.parkreldis.2015.09.020] [PMID: 26382841]
[5]
Williams DR. Tauopathies: classification and clinical update on neurodegenerative diseases associated with microtubule-associated protein tau. Intern Med J 2006; 36(10): 652-60.
[http://dx.doi.org/10.1111/j.1445-5994.2006.01153.x] [PMID: 16958643]
[6]
Iqbal K, Liu F, Gong CX. Alzheimer disease therapeutics: focus on the disease and not just plaques and tangles. Biochem Pharmacol 2014; 88(4): 631-9.
[http://dx.doi.org/10.1016/j.bcp.2014.01.002] [PMID: 24418409]
[7]
Gong CX, Iqbal K. Hyperphosphorylation of microtubule-associated protein tau: a promising therapeutic target for Alzheimer disease. Curr Med Chem 2008; 15(23): 2321-8.
[http://dx.doi.org/10.2174/092986708785909111] [PMID: 18855662]
[8]
Gendron TF, Petrucelli L. The role of tau in neurodegeneration. Mol Neurodegener 2009; 4: 13.
[http://dx.doi.org/10.1186/1750-1326-4-13] [PMID: 19284597]
[9]
Fong TG, Tulebaev SR, Inouye SK. Delirium in elderly adults: diagnosis, prevention and treatment. Nat Rev Neurol 2009; 5(4): 210-20.
[http://dx.doi.org/10.1038/nrneurol.2009.24] [PMID: 19347026]
[10]
Beyreuther K, Bush AI, Dyrks T, et al. Mechanisms of amyloid deposition in Alzheimer’s disease. Ann N Y Acad Sci 1991; 640: 129-39.
[http://dx.doi.org/10.1111/j.1749-6632.1991.tb00204.x] [PMID: 1776729]
[11]
Selkoe DJ. Cell biology of protein misfolding: the examples of Alzheimer’s and Parkinson’s diseases. Nat Cell Biol 2004; 6(11): 1054-61.
[http://dx.doi.org/10.1038/ncb1104-1054] [PMID: 15516999]
[12]
Wong KH, Riaz MK, Xie Y, et al. Review of current strategies for delivering alzheimer’s disease drugs across the blood-brain barrier. Int J Mol Sci 2019; 20(2): E381
[http://dx.doi.org/10.3390/ijms20020381] [PMID: 30658419]
[13]
Hardy JA, Higgins GA. Alzheimer’s disease: the amyloid cascade hypothesis. Science 1992; 256(5054): 184-5.
[http://dx.doi.org/10.1126/science.1566067] [PMID: 1566067]
[14]
Gray EG, Paula-Barbosa M, Roher A. Alzheimer’s disease: paired helical filaments and cytomembranes. Neuropathol Appl Neurobiol 1987; 13(2): 91-110.
[http://dx.doi.org/10.1111/j.1365-2990.1987.tb00174.x] [PMID: 3614544]
[15]
Anderson RM, Hadjichrysanthou C, Evans S, Wong MM. Why do so many clinical trials of therapies for Alzheimer’s disease fail? Lancet 2017; 390(10110): 2327-9.
[http://dx.doi.org/10.1016/S0140-6736(17)32399-1] [PMID: 29185425]
[16]
Mullard A. BACE inhibitor bust in Alzheimer trial. Nat Rev Drug Discov 2017; 16(3): 155.
[PMID: 28248932]
[17]
Karthivashan G, Ganesan P, Park SY, Kim JS, Choi DK. Therapeutic strategies and nano-drug delivery applications in management of ageing Alzheimer’s disease. Drug Deliv 2018; 25(1): 307-20.
[http://dx.doi.org/10.1080/10717544.2018.1428243] [PMID: 29350055]
[18]
Logsdon AF, Erickson MA, Rhea EM, Salameh TS, Banks WA. Gut reactions: How the blood-brain barrier connects the microbiome and the brain. Exp Biol Med 2018; 243(2): 159-65.
[http://dx.doi.org/10.1177/1535370217743766] [PMID: 29169241]
[19]
He Q, Liu J, Liang J, et al. Towards improvements for penetrating the blood-brain barrier-recent progress from a material and pharmaceutical perspective. Cells 2018; 7(4): E24
[http://dx.doi.org/10.3390/cells7040024] [PMID: 29570659]
[20]
Gabathuler R. Approaches to transport therapeutic drugs across the blood-brain barrier to treat brain diseases. Neurobiol Dis 2010; 37(1): 48-57.
[http://dx.doi.org/10.1016/j.nbd.2009.07.028] [PMID: 19664710]
[21]
Pardridge WM. Blood-brain barrier delivery. Drug Discov Today 2007; 12(1-2): 54-61.
[http://dx.doi.org/10.1016/j.drudis.2006.10.013] [PMID: 17198973]
[22]
Bickel U, Yoshikawa T, Pardridge WM. Delivery of peptides and proteins through the blood-brain barrier. Adv Drug Deliv Rev 2001; 46(1-3): 247-79.
[http://dx.doi.org/10.1016/S0169-409X(00)00139-3] [PMID: 11259843]
[23]
Pardridge WM. Vector-mediated drug delivery to the brain. Adv Drug Deliv Rev 1999; 36(2-3): 299-321.
[http://dx.doi.org/10.1016/S0169-409X(98)00087-8] [PMID: 10837722]
[24]
Soppimath KS, Aminabhavi TM, Kulkarni AR, Rudzinski WE. Biodegradable polymeric nanoparticles as drug delivery devices. J Control Release 2001; 70(1-2): 1-20.
[http://dx.doi.org/10.1016/S0168-3659(00)00339-4] [PMID: 11166403]
[25]
Koziara JM, Lockman PR, Allen DD, Mumper RJ. The blood-brain barrier and brain drug delivery. J Nanosci Nanotechnol 2006; 6(9-10): 2712-35.
[http://dx.doi.org/10.1166/jnn.2006.441] [PMID: 17048477]
[26]
Chen Y, Liu L. Modern methods for delivery of drugs across the blood-brain barrier. Adv Drug Deliv Rev 2012; 64(7): 640-65.
[http://dx.doi.org/10.1016/j.addr.2011.11.010] [PMID: 22154620]
[27]
Dalpiaz A, Filosa R, de Caprariis P, et al. Molecular mechanism involved in the transport of a prodrug dopamine glycosyl conjugate. Int J Pharm 2007; 336(1): 133-9.
[http://dx.doi.org/10.1016/j.ijpharm.2006.11.051] [PMID: 17184941]
[28]
Bonina F, Puglia C, Rimoli MG, et al. Glycosyl derivatives of dopamine and L-dopa as anti-Parkinson prodrugs: synthesis, pharmacological activity and in vitro stability studies. J Drug Target 2003; 11(1): 25-36.
[http://dx.doi.org/10.1080/10611860305553] [PMID: 12852438]
[29]
Müller T. Drug therapy in patients with Parkinson’s disease. Transl Neurodegener 2012; 1(1): 10.
[http://dx.doi.org/10.1186/2047-9158-1-10] [PMID: 23211041]
[30]
Winkler EA, Nishida Y, Sagare AP, et al. GLUT1 reductions exacerbate Alzheimer’s disease vasculo-neuronal dysfunction and degeneration. Nat Neurosci 2015; 18(4): 521-30.
[http://dx.doi.org/10.1038/nn.3966] [PMID: 25730668]
[31]
Sanjo N, Kuwahara H, Nagata T, et al. Molecular imaging and treatment of alzheimer’s disease by developing amyloid-β oligomer antibodies that cross the blood-brain barrier. Alzheimers Dement 2018; 14(7): 687.
[http://dx.doi.org/10.1016/j.jalz.2018.06.739]
[32]
Serlin Y, Shelef I, Knyazer B, Friedman A. Anatomy and physiology of the blood-brain barrier. Semin Cell Dev Biol 2015; 38: 2-6.
[http://dx.doi.org/10.1016/j.semcdb.2015.01.002] [PMID: 25681530]
[33]
Simpson IA, Vannucci SJ, DeJoseph MR, Hawkins RA. Glucose transporter asymmetries in the bovine blood-brain barrier. J Biol Chem 2001; 276(16): 12725-9.
[http://dx.doi.org/10.1074/jbc.M010897200] [PMID: 11278779]
[34]
Huttunen J, Peltokangas S, Gynther M, et al. L-type amino acid transporter 1 (LAT1/Lat1)-utilizing prodrugs can improve the delivery of drugs into neurons, astrocytes and microglia. Sci Rep 2019; 9(1): 12860.
[http://dx.doi.org/10.1038/s41598-019-49009-z] [PMID: 31492955]
[35]
Peura L, Malmioja K, Huttunen K, et al. Design, synthesis and brain uptake of LAT1-targeted amino acid prodrugs of dopamine. Pharm Res 2013; 30(10): 2523-37.
[http://dx.doi.org/10.1007/s11095-012-0966-3] [PMID: 24137801]
[36]
Thiele NA, Kärkkäinen J, Sloan KB, Rautio J, Huttunen KM. Secondary carbamate linker can facilitate the sustained release of dopamine from brain-targeted prodrug. Bioorg Med Chem Lett 2018; 28(17): 2856-60.
[http://dx.doi.org/10.1016/j.bmcl.2018.07.030] [PMID: 30055889]
[37]
Vellonen KS, Ihalainen J, Boucau MC, et al. Disease-induced alterations in brain drug transporters in animal models of alzheimer’s disease: theme: drug discovery, development and delivery in alzheimer’s disease. Pharm Res 2017; 34: (12): 2652-62.
[38]
Gynther M, Puris E, Peltokangas S, et al. Alzheimer’s disease phenotype or inflammatory insult does not alter function of l-type amino acid transporter 1 in mouse blood-brain barrier and primary astrocytes. Pharm Res 2018; 36(1): 17.
[http://dx.doi.org/10.1007/s11095-018-2546-7] [PMID: 30488131]
[39]
Allen DD, Lockman PR, Roder KE, Dwoskin LP, Crooks PA. Active transport of high-affinity choline and nicotine analogs into the central nervous system by the blood-brain barrier choline transporter. J Pharmacol Exp Ther 2003; 304(3): 1268-74.
[http://dx.doi.org/10.1124/jpet.102.045856] [PMID: 12604705]
[40]
Pardridge WM. Recent developments in peptide drug delivery to the brain. Pharmacol Toxicol 1992; 71(1): 3-10.
[http://dx.doi.org/10.1111/j.1600-0773.1992.tb00512.x] [PMID: 1523192]
[41]
Vivès E, Brodin P, Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 1997; 272(25): 16010-7.
[http://dx.doi.org/10.1074/jbc.272.25.16010] [PMID: 9188504]
[42]
Lockman PR, Koziara JM, Mumper RJ, Allen DD. Nanoparticle surface charges alter blood-brain barrier integrity and permeability. J Drug Target 2004; 12(9-10): 635-41.
[http://dx.doi.org/10.1080/10611860400015936] [PMID: 15621689]
[43]
van Rooy I, Cakir-Tascioglu S, Hennink WE, Storm G, Schiffelers RM, Mastrobattista E. In vivo methods to study uptake of nanoparticles into the brain. Pharm Res 2011; 28(3): 456-71.
[http://dx.doi.org/10.1007/s11095-010-0291-7] [PMID: 20924653]
[44]
Lajoie JM, Shusta EV. Targeting receptor-mediated transport for delivery of biologics across the blood-brain barrier. Annu Rev Pharmacol Toxicol 2015; 55: 613-31.
[http://dx.doi.org/10.1146/annurev-pharmtox-010814-124852] [PMID: 25340933]
[45]
Pardridge WM. Delivery of biologics across the blood-brain barrier with molecular trojan horse technology. BioDrugs 2017; 31(6): 503-19.
[http://dx.doi.org/10.1007/s40259-017-0248-z] [PMID: 29067674]
[46]
Mills E, Dong XP, Wang F, Xu H. Mechanisms of brain iron transport: insight into neurodegeneration and CNS disorders. Future Med Chem 2010; 2(1): 51-64.
[http://dx.doi.org/10.4155/fmc.09.140] [PMID: 20161623]
[47]
Descamps L, Dehouck MP, Torpier G, Cecchelli R. Receptor-mediated transcytosis of transferrin through blood-brain barrier endothelial cells. Am J Physiol 1996; 270(4 Pt 2): H1149-58.
[PMID: 8967351]
[48]
Crowe A, Morgan EH. Iron and transferrin uptake by brain and cerebrospinal fluid in the rat. Brain Res 1992; 592(1-2): 8-16.
[http://dx.doi.org/10.1016/0006-8993(92)91652-U] [PMID: 1450923]
[49]
Morgan EH, Moos T. Mechanism and developmental changes in iron transport across the blood-brain barrier. Dev Neurosci 2002; 24(2-3): 106-13.
[http://dx.doi.org/10.1159/000065699] [PMID: 12401948]
[50]
Shin SU, Friden P, Moran M, et al. Transferrin-antibody fusion proteins are effective in brain targeting. Proc Natl Acad Sci USA 1995; 92(7): 2820-4.
[http://dx.doi.org/10.1073/pnas.92.7.2820] [PMID: 7708731]
[51]
Mishra V, Mahor S, Rawat A, et al. Targeted brain delivery of AZT via transferrin anchored pegylated albumin nanoparticles. J Drug Target 2006; 14(1): 45-53.
[http://dx.doi.org/10.1080/10611860600612953] [PMID: 16603451]
[52]
Ulbrich K, Hekmatara T, Herbert E, Kreuter J. Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB). Eur J Pharm Biopharm 2009; 71(2): 251-6.
[http://dx.doi.org/10.1016/j.ejpb.2008.08.021] [PMID: 18805484]
[53]
Qian ZM, Li H, Sun H, Ho K. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol Rev 2002; 54(4): 561-87.
[http://dx.doi.org/10.1124/pr.54.4.561] [PMID: 12429868]
[54]
Jefferies WA, Brandon MR, Hunt SV, Williams AF, Gatter KC, Mason DY. Transferrin receptor on endothelium of brain capillaries. Nature 1984; 312(5990): 162-3.
[http://dx.doi.org/10.1038/312162a0] [PMID: 6095085]
[55]
Kissel K, Hamm S, Schulz M, Vecchi A, Garlanda C, Engelhardt B. Immunohistochemical localization of the murine transferrin receptor (TfR) on blood-tissue barriers using a novel anti-TfR monoclonal antibody. Histochem Cell Biol 1998; 110(1): 63-72.
[http://dx.doi.org/10.1007/s004180050266] [PMID: 9681691]
[56]
Lee HJ, Engelhardt B, Lesley J, Bickel U, Pardridge WM. Targeting rat anti-mouse transferrin receptor monoclonal antibodies through blood-brain barrier in mouse. J Pharmacol Exp Ther 2000; 292(3): 1048-52.
[PMID: 10688622]
[57]
Zhang Y, Pardridge WM. Blood-brain barrier targeting of BDNF improves motor function in rats with middle cerebral artery occlusion. Brain Res 2006; 1111(1): 227-9.
[http://dx.doi.org/10.1016/j.brainres.2006.07.005] [PMID: 16884698]
[58]
Wu D, Pardridge WM. Central nervous system pharmacologic effect in conscious rats after intravenous injection of a biotinylated vasoactive intestinal peptide analog coupled to a blood-brain barrier drug delivery system. J Pharmacol Exp Ther 1996; 279(1): 77-83.
[PMID: 8858978]
[59]
Song BW, Vinters HV, Wu D, Pardridge WM. Enhanced neuroprotective effects of basic fibroblast growth factor in regional brain ischemia after conjugation to a blood-brain barrier delivery vector. J Pharmacol Exp Ther 2002; 301(2): 605-10.
[http://dx.doi.org/10.1124/jpet.301.2.605] [PMID: 11961063]
[60]
Kordower JH, Charles V, Bayer R, et al. Intravenous administration of a transferrin receptor antibody-nerve growth factor conjugate prevents the degeneration of cholinergic striatal neurons in a model of Huntington disease. Proc Natl Acad Sci USA 1994; 91(19): 9077-80.
[http://dx.doi.org/10.1073/pnas.91.19.9077] [PMID: 8090772]
[61]
Lyons MK, Anderson RE, Meyer FB. Basic fibroblast growth factor promotes in vivo cerebral angiogenesis in chronic forebrain ischemia. Brain Res 1991; 558(2): 315-20.
[http://dx.doi.org/10.1016/0006-8993(91)90784-S] [PMID: 1723639]
[62]
Paterson J, Webster CI. Exploiting transferrin receptor for delivering drugs across the blood-brain barrier. Drug Discov Today Technol 2016; 20: 49-52.
[http://dx.doi.org/10.1016/j.ddtec.2016.07.009] [PMID: 27986223]
[63]
Lee HJ, Boado RJ, Braasch DA, Corey DR, Pardridge WM. Imaging gene expression in the brain in vivo in a transgenic mouse model of Huntington’s disease with an antisense radiopharmaceutical and drug-targeting technology. J Nucl Med 2002; 43(7): 948-56.
[PMID: 12097468]
[64]
Friden PM, Walus LR, Musso GF, Taylor MA, Malfroy B, Starzyk RM. Anti-transferrin receptor antibody and antibody-drug conjugates cross the blood-brain barrier. Proc Natl Acad Sci USA 1991; 88(11): 4771-5.
[http://dx.doi.org/10.1073/pnas.88.11.4771] [PMID: 2052557]
[65]
Unger JW, Livingston JN, Moss AM. Insulin receptors in the central nervous system: localization, signalling mechanisms and functional aspects. Prog Neurobiol 1991; 36(5): 343-62.
[http://dx.doi.org/10.1016/0301-0082(91)90015-S] [PMID: 1887067]
[66]
Banks WA, Owen JB, Erickson MA. Insulin in the brain: there and back again. Pharmacol Ther 2012; 136(1): 82-93.
[http://dx.doi.org/10.1016/j.pharmthera.2012.07.006] [PMID: 22820012]
[67]
Werner H, LeRoith D. Insulin and insulin-like growth factor receptors in the brain: physiological and pathological aspects. Eur Neuropsychopharmacol 2014; 24(12): 1947-53.
[http://dx.doi.org/10.1016/j.euroneuro.2014.01.020] [PMID: 24529663]
[68]
Havrankova J, Brownstein M, Roth J. Insulin and insulin receptors in rodent brain. Diabetologia 1981; 20(Suppl. ): 268-73.
[http://dx.doi.org/10.1007/BF00254492]
[69]
Smith MW, Gumbleton M. Endocytosis at the blood-brain barrier: from basic understanding to drug delivery strategies. J Drug Target 2006; 14(4): 191-214.
[http://dx.doi.org/10.1080/10611860600650086] [PMID: 16777679]
[70]
Duffy KR, Pardridge WM. Blood-brain barrier transcytosis of insulin in developing rabbits. Brain Res 1987; 420(1): 32-8.
[http://dx.doi.org/10.1016/0006-8993(87)90236-8] [PMID: 3315116]
[71]
Pardridge WM. Receptor-mediated peptide transport through the blood-brain barrier. Endocr Rev 1986; 7(3): 314-30.
[http://dx.doi.org/10.1210/edrv-7-3-314] [PMID: 3017689]
[72]
Pardridge WM, Kang YS, Buciak JL, Yang J. Human insulin receptor monoclonal antibody undergoes high affinity binding to human brain capillaries in vitro and rapid transcytosis through the blood-brain barrier in vivo in the primate. Pharm Res 1995; 12(6): 807-16.
[http://dx.doi.org/10.1023/A:1016244500596] [PMID: 7667183]
[73]
Pardridge WM. Transport of small molecules through the blood-brain barrier: biology and methodology. Adv Drug Deliv Rev 1995; 15(1-3): 5-36.
[http://dx.doi.org/10.1016/0169-409X(95)00003-P]
[74]
Wu D, Yang J, Pardridge WM. Drug targeting of a peptide radiopharmaceutical through the primate blood-brain barrier in vivo with a monoclonal antibody to the human insulin receptor. J Clin Invest 1997; 100(7): 1804-12.
[http://dx.doi.org/10.1172/JCI119708] [PMID: 9312181]
[75]
Boado RJ, Zhang Y, Zhang Y, Pardridge WM. Humanization of anti-human insulin receptor antibody for drug targeting across the human blood-brain barrier. Biotechnol Bioeng 2007; 96(2): 381-91.
[http://dx.doi.org/10.1002/bit.21120] [PMID: 16937408]
[76]
Coloma MJ, Lee HJ, Kurihara A, et al. Transport across the primate blood-brain barrier of a genetically engineered chimeric monoclonal antibody to the human insulin receptor. Pharm Res 2000; 17(3): 266-74.
[http://dx.doi.org/10.1023/A:1007592720793] [PMID: 10801214]
[77]
Hwang WY, Foote J. Immunogenicity of engineered antibodies. Methods 2005; 36(1): 3-10.
[http://dx.doi.org/10.1016/j.ymeth.2005.01.001] [PMID: 15848070]
[78]
Bondy CA, Lee WH, Zhou J. Ontogeny and cellular distribution of brain glucose transporter gene expression. Mol Cell Neurosci 1992; 3(4): 305-14.
[http://dx.doi.org/10.1016/1044-7431(92)90027-Y] [PMID: 19912873]
[79]
Alberini CM, Chen DY. Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci 2012; 35(5): 274-83.
[http://dx.doi.org/10.1016/j.tins.2011.12.007] [PMID: 22341662]
[80]
Urayama A, Grubb JH, Sly WS, Banks WA. Developmentally regulated mannose 6-phosphate receptor-mediated transport of a lysosomal enzyme across the blood-brain barrier. Proc Natl Acad Sci USA 2004; 101(34): 12658-63.
[http://dx.doi.org/10.1073/pnas.0405042101] [PMID: 15314220]
[81]
Duffy KR, Pardridge WM, Rosenfeld RG. Human blood-brain barrier insulin-like growth factor receptor. Metabolism 1988; 37(2): 136-40.
[http://dx.doi.org/10.1016/S0026-0495(98)90007-5] [PMID: 2963191]
[82]
Nedelkov D, Nelson RW, Kiernan UA, Niederkofler EE, Tubbs KA. Detection of bound and free IGF-1 and IGF-2 in human plasma via biomolecular interaction analysis mass spectrometry. FEBS Lett 2003; 536(1-3): 130-4.
[http://dx.doi.org/10.1016/S0014-5793(03)00042-5] [PMID: 12586351]
[83]
Gaillard PJ, Visser CC, de Boer AG. Targeted delivery across the blood-brain barrier. Expert Opin Drug Deliv 2005; 2(2): 299-309.
[http://dx.doi.org/10.1517/17425247.2.2.299] [PMID: 16296755]
[84]
Demeule M, Poirier J, Jodoin J, et al. High transcytosis of melanotransferrin (P97) across the blood-brain barrier. J Neurochem 2002; 83(4): 924-33.
[http://dx.doi.org/10.1046/j.1471-4159.2002.01201.x] [PMID: 12421365]
[85]
Gabathuler R, Arthur G, Kennard M, Chen Q, Tsai S, Yang J, et al. Development of a potential protein vector (NeuroTrans) to deliver drugs across the blood-brain barrier. Int Congr Ser 2005; 1277: 171-84.
[http://dx.doi.org/10.1016/j.ics.2005.02.021]
[86]
Wang Z, Zhao Y, Jiang Y, et al. Enhanced anti-ischemic stroke of ZL006 by T7-conjugated PEGylated liposomes drug delivery system. Sci Rep 2015; 5: 12651.
[http://dx.doi.org/10.1038/srep12651] [PMID: 26219474]
[87]
Xin H, Sha X, Jiang X, et al. The brain targeting mechanism of Angiopep-conjugated poly(ethylene glycol)-co-poly(ε-caprolactone) nanoparticles. Biomaterials 2012; 33(5): 1673-81.
[http://dx.doi.org/10.1016/j.biomaterials.2011.11.018] [PMID: 22133551]
[88]
Liu Y, He X, Kuang Y, et al. A bacteria deriving peptide modified dendrigraft poly-l-lysines (DGL) self-assembling nanoplatform for targeted gene delivery. Mol Pharm 2014; 11(10): 3330-41.
[http://dx.doi.org/10.1021/mp500084s] [PMID: 24964270]
[89]
Thomas FC, Taskar K, Rudraraju V, et al. Uptake of ANG1005, a novel paclitaxel derivative, through the blood-brain barrier into brain and experimental brain metastases of breast cancer. Pharm Res 2009; 26(11): 2486-94.
[http://dx.doi.org/10.1007/s11095-009-9964-5] [PMID: 19774344]
[90]
Régina A, Demeule M, Ché C, et al. Antitumour activity of ANG1005, a conjugate between paclitaxel and the new brain delivery vector Angiopep-2. Br J Pharmacol 2008; 155(2): 185-97.
[http://dx.doi.org/10.1038/bjp.2008.260] [PMID: 18574456]
[91]
Kumthekar P, Lawrence B, Iordanova V, Ibrahim N, Mazanet R, Eds. ANG1005 in leptomeningeal disease (ANGLeD) trial: A randomized, open-label, phase 3 study of ANG1005 compared with physician’s best choice in HER2-negative breast cancer patients with newly diagnosed leptomeningeal carcinomatosis and previously treated brain metastases. Sant antonio breast cancer symposium 2019 December 4-8, 2018;. San Antonio, Texas, USA: American Association for Cancer Research. Avaialble at:. https://clinicaltrials.gov/ct2/show/NCT03613181
[http://dx.doi.org/10.1158/1538-7445.SABCS18-OT1-06-01]
[92]
Bu G. Apolipoprotein E and its receptors in Alzheimer’s disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 2009; 10(5): 333-44.
[http://dx.doi.org/10.1038/nrn2620] [PMID: 19339974]
[93]
Lambert JC, Ibrahim-Verbaas CA, Harold D, et al. European Alzheimer’s disease initiative (EADI); genetic and environmental risk in alzheimer’s disease; alzheimer’s disease genetic consortium; cohorts for heart and aging research in genomic epidemiology.. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer’s disease. Nat Genet 2013; 45(12): 1452-8.
[http://dx.doi.org/10.1038/ng.2802] [PMID: 24162737]
[94]
Liu CC, Liu CC, Kanekiyo T, Xu H, Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol 2013; 9(2): 106-18.
[http://dx.doi.org/10.1038/nrneurol.2012.263] [PMID: 23296339]
[95]
Laskowitz DT, Thekdi AD, Thekdi SD, et al. Downregulation of microglial activation by apolipoprotein E and apoE-mimetic peptides. Exp Neurol 2001; 167(1): 74-85.
[http://dx.doi.org/10.1006/exnr.2001.7541] [PMID: 11161595]
[96]
Rao KS, Reddy MK, Horning JL, Labhasetwar V. TAT-conjugated nanoparticles for the CNS delivery of anti-HIV drugs. Biomaterials 2008; 29(33): 4429-38.
[http://dx.doi.org/10.1016/j.biomaterials.2008.08.004] [PMID: 18760470]
[97]
Kreuter J, Shamenkov D, Petrov V, et al. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood-brain barrier. J Drug Target 2002; 10(4): 317-25.
[http://dx.doi.org/10.1080/10611860290031877] [PMID: 12164380]
[98]
Michaelis K, Hoffmann MM, Dreis S, et al. Covalent linkage of apolipoprotein e to albumin nanoparticles strongly enhances drug transport into the brain. J Pharmacol Exp Ther 2006; 317(3): 1246-53.
[http://dx.doi.org/10.1124/jpet.105.097139] [PMID: 16554356]
[99]
Hülsermann U, Hoffmann MM, Massing U, Fricker G. Uptake of apolipoprotein E fragment coupled liposomes by cultured brain microvessel endothelial cells and intact brain capillaries. J Drug Target 2009; 17(8): 610-8.
[http://dx.doi.org/10.1080/10611860903105986] [PMID: 19694613]
[100]
Buch T, Heppner FL, Tertilt C, et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat Methods 2005; 2(6): 419-26.
[http://dx.doi.org/10.1038/nmeth762] [PMID: 15908920]
[101]
Pereira MM, Mahú I, Seixas E, et al. A brain-sparing diphtheria toxin for chemical genetic ablation of peripheral cell lineages. Nat Commun 2017; 8: 14967.
[http://dx.doi.org/10.1038/ncomms14967] [PMID: 28367972]
[102]
Anderson P, Pichichero ME, Insel RA. Immunogens consisting of oligosaccharides from the capsule of Haemophilus influenzae type b coupled to diphtheria toxoid or the toxin protein CRM197. J Clin Invest 1985; 76(1): 52-9.
[http://dx.doi.org/10.1172/JCI111976] [PMID: 3874882]
[103]
Gaillard PJ, de Boer AG. A novel opportunity for targeted drug delivery to the brain. J Control Release 2006; 116(2): e60-2.
[http://dx.doi.org/10.1016/j.jconrel.2006.09.050] [PMID: 17718973]
[104]
Edis BO, Haciosmanoglu E, Varol B, Bektas M. Intracellular trafficking of diphtheria toxin and its mutated form, CRM197, in the endocytic pathway. North Clin Istanb 2018; 5(2): 89-95.
[PMID: 30374472]
[105]
Gosselet F, Saint-Pol J, Candela P, Fenart L. Amyloid-β peptides, Alzheimer’s disease and the blood-brain barrier. Curr Alzheimer Res 2013; 10(10): 1015-33.
[http://dx.doi.org/10.2174/15672050113106660174] [PMID: 24156262]
[106]
Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011; 1(1): a006189
[http://dx.doi.org/10.1101/cshperspect.a006189] [PMID: 22229116]
[107]
Zhang M, Schmitt-Ulms G, Sato C, et al. Drug repositioning for alzheimer’s disease based on systematic ‘omics’ data mining. PLoS One 2016; 11(12): e0168812
[http://dx.doi.org/10.1371/journal.pone.0168812] [PMID: 28005991]
[108]
Lleó A. Current therapeutic options for Alzheimer’s disease. Curr Genomics 2007; 8(8): 550-8.
[http://dx.doi.org/10.2174/138920207783769549] [PMID: 19415128]
[109]
Swanson SJ. Minimally invasive surgery is best treatment for early lung cancer. J Thorac Dis 2018; 10(Suppl. 17): S1998-9.
[http://dx.doi.org/10.21037/jtd.2018.04.171] [PMID: 30023102]
[110]
Cummings JL, Morstorf T, Zhong K. Alzheimer’s disease drug-development pipeline: few candidates, frequent failures. Alzheimers Res Ther 2014; 6(4): 37.
[http://dx.doi.org/10.1186/alzrt269] [PMID: 25024750]
[111]
Crucho CIC, Barros MT. Polymeric nanoparticles: A study on the preparation variables and characterization methods. Mater Sci Eng C 2017; 80: 771-84.
[http://dx.doi.org/10.1016/j.msec.2017.06.004] [PMID: 28866227]
[112]
Mathew A, Fukuda T, Nagaoka Y, et al. Curcumin loaded-PLGA nanoparticles conjugated with Tet-1 peptide for potential use in Alzheimer’s disease. PLoS One 2012; 7(3): e32616
[http://dx.doi.org/10.1371/journal.pone.0032616] [PMID: 22403681]
[113]
Anand P, Nair HB, Sung B, et al. Design of curcumin-loaded PLGA nanoparticles formulation with enhanced cellular uptake, and increased bioactivity in vitro and superior bioavailability in vivo. Biochem Pharmacol 2010; 79(3): 330-8.
[http://dx.doi.org/10.1016/j.bcp.2009.09.003] [PMID: 19735646]
[114]
Tiwari SK, Agarwal S, Seth B, et al. Curcumin-loaded nanoparticles potently induce adult neurogenesis and reverse cognitive deficits in Alzheimer’s disease model via canonical Wnt/β-catenin pathway. ACS Nano 2014; 8(1): 76-103.
[http://dx.doi.org/10.1021/nn405077y] [PMID: 24467380]
[115]
Huang N, Lu S, Liu XG, Zhu J, Wang YJ, Liu RT. PLGA nanoparticles modified with a BBB-penetrating peptide co-delivering Aβ generation inhibitor and curcumin attenuate memory deficits and neuropathology in Alzheimer’s disease mice. Oncotarget 2017; 8(46): 81001-13.
[http://dx.doi.org/10.18632/oncotarget.20944] [PMID: 29113362]
[116]
Sánchez-López E, Ettcheto M, Egea MA, et al. New potential strategies for Alzheimer’s disease prevention: pegylated biodegradable dexibuprofen nanospheres administration to APPswe/PS1dE9. Nanomedicine 2017; 13(3): 1171-82.
[http://dx.doi.org/10.1016/j.nano.2016.12.003] [PMID: 27986603]
[117]
Carradori D, Balducci C, Re F, et al. Antibody-functionalized polymer nanoparticle leading to memory recovery in Alzheimer’s disease-like transgenic mouse model. Nanomedicine 2018; 14(2): 609-18.
[http://dx.doi.org/10.1016/j.nano.2017.12.006] [PMID: 29248676]
[118]
Lai F, Fadda AM, Sinico C. Liposomes for brain delivery. Expert Opin Drug Deliv 2013; 10(7): 1003-22.
[http://dx.doi.org/10.1517/17425247.2013.766714] [PMID: 23373728]
[119]
Vieira DB, Gamarra LF. Getting into the brain: liposome-based strategies for effective drug delivery across the blood-brain barrier. Int J Nanomedicine 2016; 11: 5381-414.
[http://dx.doi.org/10.2147/IJN.S117210] [PMID: 27799765]
[120]
Redzic ZB, Segal MB. The structure of the choroid plexus and the physiology of the choroid plexus epithelium. Adv Drug Deliv Rev 2004; 56(12): 1695-716.
[http://dx.doi.org/10.1016/j.addr.2004.07.005] [PMID: 15381330]
[121]
Chen ZL, Huang M, Wang XR, et al. Transferrin-modified liposome promotes α-mangostin to penetrate the blood-brain barrier. Nanomedicine 2016; 12(2): 421-30.
[http://dx.doi.org/10.1016/j.nano.2015.10.021] [PMID: 26711963]
[122]
Yao Y, Han DD, Zhang T, Yang Z. Quercetin improves cognitive deficits in rats with chronic cerebral ischemia and inhibits voltage-dependent sodium channels in hippocampal CA1 pyramidal neurons. Phytother Res 2010; 24(1): 136-40.
[http://dx.doi.org/10.1002/ptr.2902] [PMID: 19688719]
[123]
Manach C, Morand C, Crespy V, et al. Quercetin is recovered in human plasma as conjugated derivatives which retain antioxidant properties. FEBS Lett 1998; 426(3): 331-6.
[http://dx.doi.org/10.1016/S0014-5793(98)00367-6] [PMID: 9600261]
[124]
Emerich DF, Dean RL, Marsh J, et al. Intravenous cereport (RMP-7) enhances delivery of hydrophilic chemotherapeutics and increases survival in rats with metastatic tumors in the brain. Pharm Res 2000; 17(10): 1212-9.
[http://dx.doi.org/10.1023/A:1026462629438] [PMID: 11145226]
[125]
Kawamata T, Tooyama I, Yamada T, Walker DG, McGeer PL. Lactotransferrin immunocytochemistry in Alzheimer and normal human brain. Am J Pathol 1993; 142(5): 1574-85.
[PMID: 8494052]
[126]
Huang RQ, Ke WL, Qu YH, Zhu JH, Pei YY, Jiang C. Characterization of lactoferrin receptor in brain endothelial capillary cells and mouse brain. J Biomed Sci 2007; 14(1): 121-8.
[http://dx.doi.org/10.1007/s11373-006-9121-7] [PMID: 17048089]
[127]
Kuo YC, Tsao CW. Neuroprotection against apoptosis of SK-N-MC cells using RMP-7- and lactoferrin-grafted liposomes carrying quercetin. Int J Nanomedicine 2017; 12: 2857-69.
[http://dx.doi.org/10.2147/IJN.S132472] [PMID: 28435263]
[128]
Sun D, Li N, Zhang W, et al. Design of PLGA-functionalized quercetin nanoparticles for potential use in Alzheimer’s disease. Colloids Surf B Biointerfaces 2016; 148: 116-29.
[http://dx.doi.org/10.1016/j.colsurfb.2016.08.052] [PMID: 27591943]
[129]
Jose S, Sowmya S, Cinu TA, Aleykutty NA, Thomas S, Souto EB. Surface modified PLGA nanoparticles for brain targeting of Bacoside-A. Eur J Pharm Sci 2014; 63: 29-35.
[http://dx.doi.org/10.1016/j.ejps.2014.06.024]
[130]
Aalinkeel R, Kutscher HL, Singh A, et al. Neuroprotective effects of a biodegradable poly(lactic-co-glycolic acid)-ginsenoside Rg3 nanoformulation: a potential nanotherapy for Alzheimer’s disease? J Drug Target 2018; 26(2): 182-93.
[http://dx.doi.org/10.1080/1061186X.2017.1354002] [PMID: 28697660]
[131]
Li J, Zhou L, Ye D, et al. Choline-derivate-modified nanoparticles for brain-targeting gene delivery. Adv Mater 2011; 23(39): 4516-20.
[http://dx.doi.org/10.1002/adma.201101899] [PMID: 21898606]
[132]
Ali M, Khan T, Fatima K, et al. Selected hepatoprotective herbal medicines: Evidence from ethnomedicinal applications, animal models, and possible mechanism of actions. Phytother Res 2018; 32(2): 199-215.
[http://dx.doi.org/10.1002/ptr.5957] [PMID: 29047177]
[133]
Xu MF, Xiong YY, Liu JK, Qian JJ, Zhu L, Gao J. Asiatic acid, a pentacyclic triterpene in Centella asiatica, attenuates glutamate-induced cognitive deficits in mice and apoptosis in SH-SY5Y cells. Acta Pharmacol Sin 2012; 33(5): 578-87.
[http://dx.doi.org/10.1038/aps.2012.3] [PMID: 22447225]
[134]
Röcker C, Pötzl M, Zhang F, Parak WJ, Nienhaus GU. A quantitative fluorescence study of protein monolayer formation on colloidal nanoparticles. Nat Nanotechnol 2009; 4(9): 577-80.
[http://dx.doi.org/10.1038/nnano.2009.195] [PMID: 19734930]
[135]
Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V. Time evolution of the nanoparticle protein corona. ACS Nano 2010; 4(7): 3623-32.
[http://dx.doi.org/10.1021/nn901372t] [PMID: 20553005]
[136]
Mirshafiee V, Kim R, Park S, Mahmoudi M, Kraft ML. Impact of protein pre-coating on the protein corona composition and nanoparticle cellular uptake. Biomaterials 2016; 75: 295-304.
[http://dx.doi.org/10.1016/j.biomaterials.2015.10.019] [PMID: 26513421]
[137]
Zhang Z, Guan J, Jiang Z, et al. Brain-targeted drug delivery by manipulating protein corona functions. Nat Commun 2019; 10(1): 3561.
[http://dx.doi.org/10.1038/s41467-019-11593-z] [PMID: 31395892]
[138]
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001; 46(1-3): 3-26.
[http://dx.doi.org/10.1016/S0169-409X(00)00129-0] [PMID: 11259830]
[139]
Tosi G, Bortot B, Ruozi B, et al. Potential use of polymeric nanoparticles for drug delivery across the blood-brain barrier. Curr Med Chem 2013; 20(17): 2212-25.
[http://dx.doi.org/10.2174/0929867311320170006] [PMID: 23458620]
[140]
Lu CT, Zhao YZ, Wong HL, Cai J, Peng L, Tian XQ. Current approaches to enhance CNS delivery of drugs across the brain barriers. Int J Nanomedicine 2014; 9: 2241-57.
[http://dx.doi.org/10.2147/IJN.S61288] [PMID: 24872687]
[141]
Sawada GA, Williams LR, Lutzke BS, Raub TJ. Novel, highly lipophilic antioxidants readily diffuse across the blood-brain barrier and access intracellular sites. J Pharmacol Exp Ther 1999; 288(3): 1327-33.
[PMID: 10027874]
[142]
Batrakova EV, Kabanov AV. Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. J Control Release 2008; 130(2): 98-106.
[http://dx.doi.org/10.1016/j.jconrel.2008.04.013] [PMID: 18534704]
[143]
Sanchez-Covarrubias L, Slosky LM, Thompson BJ, Davis TP, Ronaldson PT. Transporters at CNS barrier sites: obstacles or opportunities for drug delivery? Curr Pharm Des 2014; 20(10): 1422-49.
[http://dx.doi.org/10.2174/13816128113199990463] [PMID: 23789948]
[144]
Scarpa M, Bellettato CM, Lampe C, Begley DJ. Neuronopathic lysosomal storage disorders: Approaches to treat the central nervous system. Best Pract Res Clin Endocrinol Metab 2015; 29(2): 159-71.
[http://dx.doi.org/10.1016/j.beem.2014.12.001] [PMID: 25987170]
[145]
Bellettato CM, Scarpa M. Possible strategies to cross the blood-brain barrier. Ital J Pediatr 2018; 44(Suppl. 2): 131.
[http://dx.doi.org/10.1186/s13052-018-0563-0] [PMID: 30442184]
[146]
Blasberg RG, Patlak C, Fenstermacher JD. Intrathecal chemotherapy: brain tissue profiles after ventriculocisternal perfusion. J Pharmacol Exp Ther 1975; 195(1): 73-83.
[PMID: 810575]
[147]
Cohen-Pfeffer JL, Gururangan S, Lester T, et al. Intracerebroventricular Delivery as a Safe, long-term route of drug administration. Pediatr Neurol 2017; 67: 23-35.
[http://dx.doi.org/10.1016/j.pediatrneurol.2016.10.022] [PMID: 28089765]
[148]
Eriksdotter Jönhagen M, Nordberg A, Amberla K, et al. Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer’s disease. Dement Geriatr Cogn Disord 1998; 9(5): 246-57.
[http://dx.doi.org/10.1159/000017069] [PMID: 9701676]
[149]
Nutt JG, Burchiel KJ, Comella CL, et al. ICV GDNF Study Group. Implanted intracerebroventricular. Glial cell line-derived neurotrophic factor. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 2003; 60(1): 69-73.
[http://dx.doi.org/10.1212/WNL.60.1.69] [PMID: 12525720]
[150]
Patel NK, Bunnage M, Plaha P, Svendsen CN, Heywood P, Gill SS. Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: a two-year outcome study. Ann Neurol 2005; 57(2): 298-302.
[http://dx.doi.org/10.1002/ana.20374] [PMID: 15668979]
[151]
Beck M, Flachenecker P, Magnus T, et al. Autonomic dysfunction in ALS: a preliminary study on the effects of intrathecal BDNF. Amyotroph Lateral Scler Other Motor Neuron Disord 2005; 6(2): 100-3.
[http://dx.doi.org/10.1080/14660820510028412] [PMID: 16036433]
[152]
Duma C, Kopyov O, Kopyov A, et al. Human intracerebroventricular (ICV) injection of autologous, non-engineered, adipose-derived stromal vascular fraction (ADSVF) for neurodegenerative disorders: results of a 3-year phase 1 study of 113 injections in 31 patients. Mol Biol Rep 2019; 46(5): 5257-72.
[http://dx.doi.org/10.1007/s11033-019-04983-5] [PMID: 31327120]
[153]
Lieberman DM, Laske DW, Morrison PF, Bankiewicz KS, Oldfield EH. Convection-enhanced distribution of large molecules in gray matter during interstitial drug infusion. J Neurosurg 1995; 82(6): 1021-9.
[http://dx.doi.org/10.3171/jns.1995.82.6.1021] [PMID: 7539062]
[154]
Bobo RH, Laske DW, Akbasak A, Morrison PF, Dedrick RL, Oldfield EH. Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci USA 1994; 91(6): 2076-80.
[http://dx.doi.org/10.1073/pnas.91.6.2076] [PMID: 8134351]
[155]
Strasser JF, Fung LK, Eller S, Grossman SA, Saltzman WM. Distribution of 1,3-bis(2-chloroethyl)-1-nitrosourea and tracers in the rabbit brain after interstitial delivery by biodegradable polymer implants. J Pharmacol Exp Ther 1995; 275(3): 1647-55.
[PMID: 8531140]
[156]
Kroin JS, Penn RD. Intracerebral chemotherapy: chronic microinfusion of cisplatin. Neurosurgery 1982; 10(3): 349-54.
[http://dx.doi.org/10.1227/00006123-198203000-00009] [PMID: 7200201]
[157]
Sendelbeck SL, Urquhart J. Spatial distribution of dopamine, methotrexate and antipyrine during continuous intracerebral microperfusion. Brain Res 1985; 328(2): 251-8.
[http://dx.doi.org/10.1016/0006-8993(85)91036-4] [PMID: 4039212]
[158]
Vandergrift WA, Patel SJ, Nicholas JS, Varma AK. Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. Neurosurg Focus 2006; 20(4): E13
[http://dx.doi.org/10.3171/foc.2006.20.4.8] [PMID: 16709018]
[159]
Bors L, Erdő F. Overcoming the blood-brain barrier. Challenges and tricks for CNS drug delivery. Sci Pharm 2019; 87(1): 6.
[http://dx.doi.org/10.3390/scipharm87010006]
[160]
Westphal M, Hilt DC, Bortey E, et al. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro-oncol 2003; 5(2): 79-88.
[http://dx.doi.org/10.1093/neuonc/5.2.79] [PMID: 12672279]
[161]
Vukelja SJ, Anthony SP, Arseneau JC, et al. Phase 1 study of escalating-dose OncoGel (ReGel/paclitaxel) depot injection, a controlled-release formulation of paclitaxel, for local management of superficial solid tumor lesions. Anticancer Drugs 2007; 18(3): 283-9.
[http://dx.doi.org/10.1097/CAD.0b013e328011a51d] [PMID: 17264760]
[162]
Herzog CD, Dass B, Holden JE, et al. Striatal delivery of CERE-120, an AAV2 vector encoding human neurturin, enhances activity of the dopaminergic nigrostriatal system in aged monkeys. Mov Disord 2007; 22(8): 1124-32.
[http://dx.doi.org/10.1002/mds.21503] [PMID: 17443702]
[163]
Marks WJ Jr, Ostrem JL, Verhagen L, et al. Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson’s disease: an open-label, phase I trial. Lancet Neurol 2008; 7(5): 400-8.
[http://dx.doi.org/10.1016/S1474-4422(08)70065-6] [PMID: 18387850]
[164]
Dong X. Current strategies for brain drug delivery. Theranostics 2018; 8(6): 1481-93.
[http://dx.doi.org/10.7150/thno.21254] [PMID: 29556336]
[165]
Gray SJ, Woodard KT, Samulski RJ. Viral vectors and delivery strategies for CNS gene therapy. Ther Deliv 2010; 1(4): 517-34.
[http://dx.doi.org/10.4155/tde.10.50] [PMID: 22833965]
[166]
Alberch J, Pérez-Navarro E, Canals JM. Neuroprotection by neurotrophins and GDNF family members in the excitotoxic model of Huntington’s disease. Brain Res Bull 2002; 57(6): 817-22.
[http://dx.doi.org/10.1016/S0361-9230(01)00775-4] [PMID: 12031278]
[167]
Tenenbaum L, Humbert-Claude M. Glial cell line-derived neurotrophic factor gene delivery in parkinson’s disease: a delicate balance between neuroprotection, trophic effects, and unwanted compensatory mechanisms. Front Neuroanat 2017; 11: 29.
[http://dx.doi.org/10.3389/fnana.2017.00029] [PMID: 28442998]
[168]
Hollon T. Researchers and regulators reflect on first gene therapy death. Am J Ophthalmol 2000; 129(5): 701.
[http://dx.doi.org/10.1016/S0002-9394(00)00442-6] [PMID: 10844080]
[169]
Check E. Gene therapy put on hold as third child develops cancer. Nature 2005; 433(7026): 561.
[http://dx.doi.org/10.1038/433561a] [PMID: 15703711]
[170]
Neuwelt EA. Mechanisms of disease: the blood-brain barrier. Neurosurgery 2004; 54(1): 131-40.
[http://dx.doi.org/10.1227/01.NEU.0000097715.11966.8E] [PMID: 14683550]
[171]
Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery 1998; 42(5): 1083-99.
[http://dx.doi.org/10.1097/00006123-199805000-00082] [PMID: 9588554]
[172]
Hendricks BK, Cohen-Gadol AA, Miller JC. Novel delivery methods bypassing the blood-brain and blood-tumor barriers. Neurosurg Focus 2015; 38(3): E10
[http://dx.doi.org/10.3171/2015.1.FOCUS14767] [PMID: 25727219]
[173]
Neuwelt EA, Frenkel EP, Diehl JT, et al. Osmotic blood-brain barrier disruption: a new means of increasing chemotherapeutic agent delivery. Trans Am Neurol Assoc 1979; 104: 256-60.
[PMID: 121949]
[174]
Rapoport SI, Fredericks WR, Ohno K, Pettigrew KD. Quantitative aspects of reversible osmotic opening of the blood-brain barrier. Am J Physiol 1980; 238(5): R421-31.
[PMID: 7377381]
[175]
Boockvar JA, Tsiouris AJ, Hofstetter CP, et al. Safety and maximum tolerated dose of superselective intraarterial cerebral infusion of bevacizumab after osmotic blood-brain barrier disruption for recurrent malignant glioma. Clinical article. J Neurosurg 2011; 114(3): 624-32.
[http://dx.doi.org/10.3171/2010.9.JNS101223] [PMID: 20964595]
[176]
Guillaume DJ, Doolittle ND, Gahramanov S, Hedrick NA, Delashaw JB, Neuwelt EA. Intra-arterial chemotherapy with osmotic blood-brain barrier disruption for aggressive oligodendroglial tumors: results of a phase I study. Neurosurgery 2010; 66(1): 48-58.
[PMID: 20023537]
[177]
Gutman M, Laufer R, Eisenthal A, et al. Increased microvascular permeability induced by prolonged interleukin-2 administration is attenuated by the oxygen-free-radical scavenger dimethylthiourea. Cancer Immunol Immunother 1996; 43(4): 240-4.
[http://dx.doi.org/10.1007/s002620050328] [PMID: 9003470]
[178]
Black KL, Chio CC. Increased opening of blood-tumour barrier by leukotriene C4 is dependent on size of molecules. Neurol Res 1992; 14(5): 402-4.
[http://dx.doi.org/10.1080/01616412.1992.11740093] [PMID: 1282688]
[179]
Côté J, Bovenzi V, Savard M, et al. Induction of selective blood-tumor barrier permeability and macromolecular transport by a biostable kinin B1 receptor agonist in a glioma rat model. PLoS One 2012; 7(5): e37485
[http://dx.doi.org/10.1371/journal.pone.0037485] [PMID: 22629405]
[180]
Ford J, Osborn C, Barton T, Bleehen NM. A phase I study of intravenous RMP-7 with carboplatin in patients with progression of malignant glioma. Eur J Cancer 1998; 34(11): 1807-11.
[http://dx.doi.org/10.1016/S0959-8049(98)00155-5] [PMID: 9893673]
[181]
Lopez-Ramirez MA, Fischer R, Torres-Badillo CC, et al. Role of caspases in cytokine-induced barrier breakdown in human brain endothelial cells. J Immunol 2012; 189(6): 3130-9.
[http://dx.doi.org/10.4049/jimmunol.1103460] [PMID: 22896632]
[182]
Nakano S, Matsukado K, Black KL. Increased brain tumor microvessel permeability after intracarotid bradykinin infusion is mediated by nitric oxide. Cancer Res 1996; 56(17): 4027-31.
[PMID: 8752174]
[183]
Inamura T, Nomura T, Bartus RT, Black KL. Intracarotid infusion of RMP-7, a bradykinin analog: a method for selective drug delivery to brain tumors. J Neurosurg 1994; 81(5): 752-8.
[http://dx.doi.org/10.3171/jns.1994.81.5.0752] [PMID: 7931623]
[184]
Bartus RT, Snodgrass P, Marsh J, Agostino M, Perkins A, Emerich DF. Intravenous cereport (RMP-7) modifies topographic uptake profile of carboplatin within rat glioma and brain surrounding tumor, elevates platinum levels, and enhances survival. J Pharmacol Exp Ther 2000; 293(3): 903-11.
[PMID: 10869391]
[185]
Prados MD, Schold SC Jr, Fine HA, et al. A randomized, double-blind, placebo-controlled, phase 2 study of RMP-7 in combination with carboplatin administered intravenously for the treatment of recurrent malignant glioma. Neuro-oncol 2003; 5(2): 96-103.
[http://dx.doi.org/10.1093/neuonc/5.2.96] [PMID: 12672281]
[186]
Hynynen K, Clement GT, McDannold N, et al. 500-element ultrasound phased array system for noninvasive focal surgery of the brain: a preliminary rabbit study with ex vivo human skulls. Magn Reson Med 2004; 52(1): 100-7.
[http://dx.doi.org/10.1002/mrm.20118] [PMID: 15236372]
[187]
Huang Q, Deng J, Xie Z, et al. Effective gene transfer into central nervous system following ultrasound-microbubbles-induced opening of the blood-brain barrier. Ultrasound Med Biol 2012; 38(7): 1234-43.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2012.02.019] [PMID: 22677255]
[188]
Snipstad S, Sulheim E, de Lange Davies C, et al. Sonopermeation to improve drug delivery to tumors: from fundamental understanding to clinical translation. Expert Opin Drug Deliv 2018; 15(12): 1249-61.
[http://dx.doi.org/10.1080/17425247.2018.1547279] [PMID: 30415585]
[189]
Jung NY, Park CK, Kim M, Lee PH, Sohn YH, Chang JW. The efficacy and limits of magnetic resonance-guided focused ultrasound pallidotomy for Parkinson’s disease: a Phase I clinical trial. J Neurosurg 2018; 1-9.
[PMID: 30095337]
[190]
Meng Y, MacIntosh BJ, Shirzadi Z, et al. Resting state functional connectivity changes after MR-guided focused ultrasound mediated blood-brain barrier opening in patients with Alzheimer’s disease. Neuroimage 2019; 200: 275-80.
[http://dx.doi.org/10.1016/j.neuroimage.2019.06.060] [PMID: 31254646]
[191]
Lidar Z, Mardor Y, Jonas T, et al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J Neurosurg 2004; 100(3): 472-9.
[http://dx.doi.org/10.3171/jns.2004.100.3.0472] [PMID: 15035283]
[192]
Kunwar S, Prados MD, Chang SM, et al. Cintredekin Besudotox Intraparenchymal Study Group. Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the cintredekin besudotox intraparenchymal study group. J Clin Oncol 2007; 25(7): 837-44.
[http://dx.doi.org/10.1200/JCO.2006.08.1117] [PMID: 17327604]
[193]
Patel SJ, Shapiro WR, Laske DW, et al. Safety and feasibility of convection-enhanced delivery of Cotara for the treatment of malignant glioma: initial experience in 51 patients. Neurosurgery 2005; 56(6): 1243-52.
[http://dx.doi.org/10.1227/01.NEU.0000159649.71890.30] [PMID: 15918940]
[194]
Carpentier A, Laigle-Donadey F, Zohar S, et al. Phase 1 trial of a CpG oligodeoxynucleotide for patients with recurrent glioblastoma. Neuro-oncol 2006; 8(1): 60-6.
[http://dx.doi.org/10.1215/S1522851705000475] [PMID: 16443949]
[195]
Carpentier A, Metellus P, Ursu R, et al. Intracerebral administration of CpG oligonucleotide for patients with recurrent glioblastoma: a phase II study. Neuro-oncol 2010; 12(4): 401-8.
[http://dx.doi.org/10.1093/neuonc/nop047] [PMID: 20308317]
[196]
Weber F, Asher A, Bucholz R, et al. Safety, tolerability, and tumor response of IL4-Pseudomonas exotoxin (NBI-3001) in patients with recurrent malignant glioma. J Neurooncol 2003; 64(1-2): 125-37.
[http://dx.doi.org/10.1007/BF02700027] [PMID: 12952293]
[197]
Laske DW, Youle RJ, Oldfield EH. Tumor regression with regional distribution of the targeted toxin TF-CRM107 in patients with malignant brain tumors. Nat Med 1997; 3(12): 1362-8.
[http://dx.doi.org/10.1038/nm1297-1362] [PMID: 9396606]
[198]
Weaver M, Laske DW. Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas. J Neurooncol 2003; 65(1): 3-13.
[http://dx.doi.org/10.1023/A:1026246500788] [PMID: 14649881]
[199]
Hersh DS, Wadajkar AS, Roberts N, et al. Evolving drug delivery strategies to overcome the blood brain barrier. Curr Pharm Des 2016; 22(9): 1177-93.
[http://dx.doi.org/10.2174/1381612822666151221150733] [PMID: 26685681]
[200]
Drappatz J, Brenner A, Wong ET, et al. Phase I study of GRN1005 in recurrent malignant glioma. Clin Cancer Res 2013; 19(6): 1567-76.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-2481] [PMID: 23349317]
[201]
Gregor A, Lind M, Newman H, et al. Phase II studies of RMP-7 and carboplatin in the treatment of recurrent high grade glioma. RMP-7 European Study Group. J Neurooncol 1999; 44(2): 137-45.
[http://dx.doi.org/10.1023/A:1006379332212] [PMID: 10619497]
[202]
Angelov L, Doolittle ND, Kraemer DF, et al. Blood-brain barrier disruption and intra-arterial methotrexate-based therapy for newly diagnosed primary CNS lymphoma: a multi-institutional experience. J Clin Oncol 2009; 27(21): 3503-9.
[http://dx.doi.org/10.1200/JCO.2008.19.3789] [PMID: 19451444]
[203]
Neuwelt EA, Wiliams PC, Mickey BE, Frenkel EP, Henner WD. Therapeutic dilemma of disseminated CNS germinoma and the potential of increased platinum-based chemotherapy delivery with osmotic blood-brain barrier disruption. Pediatr Neurosurg 1994; 21(1): 16-22.
[http://dx.doi.org/10.1159/000120809] [PMID: 7947304]
[204]
Gumerlock MK, Belshe BD, Madsen R, Watts C. Osmotic blood-brain barrier disruption and chemotherapy in the treatment of high grade malignant glioma: patient series and literature review. J Neurooncol 1992; 12(1): 33-46.
[http://dx.doi.org/10.1007/BF00172455] [PMID: 1541977]
[205]
Krasovitski B, Frenkel V, Shoham S, Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc Natl Acad Sci USA 2011; 108(8): 3258-63.
[http://dx.doi.org/10.1073/pnas.1015771108] [PMID: 21300891]
[206]
Neuwelt EA, Frenkel EP, Rapoport S, Barnett P. Effect of osmotic blood-brain barrier disruption on methotrexate pharmacokinetics in the dog. Neurosurgery 1980; 7(1): 36-43.
[http://dx.doi.org/10.1227/00006123-198007000-00006] [PMID: 6774280]
[207]
Inamura T, Black KL. Bradykinin selectively opens blood-tumor barrier in experimental brain tumors. J Cereb Blood Flow Metab 1994; 14(5): 862-70.
[http://dx.doi.org/10.1038/jcbfm.1994.108] [PMID: 8063881]
[208]
Kovacs Z, Werner B, Rassi A, Sass JO, Martin-Fiori E, Bernasconi M. Prolonged survival upon ultrasound-enhanced doxorubicin delivery in two syngenic glioblastoma mouse models. J Control Release 2014; 187: 74-82.
[http://dx.doi.org/10.1016/j.jconrel.2014.05.033] [PMID: 24878186]
[209]
Kim GY, Tyler BM, Tupper MM, et al. Resorbable polymer microchips releasing BCNU inhibit tumor growth in the rat 9L flank model. J Control Release 2007; 123(2): 172-8.
[http://dx.doi.org/10.1016/j.jconrel.2007.08.003] [PMID: 17884232]

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