Differential receptor-mediated drug targeting to the diseased brain

Expert Opinion on Drug Delivery

Volumn 6, Issue 3, 2009, Pages 227-237

  Rip, J ^a   Schenk, G J ^a   De Boer, A G ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Blood brain barrier; Disease induced targeting; Protein and gene delivery; Receptor mediated targeting

Indexed keywords

ANGIOPEP 2; CARRIER PROTEINS AND BINDING PROTEINS; CHOLINERGIC RECEPTOR; DIPHTHERIA TOXIN RECEPTOR; DRUG RECEPTOR; GLUTATHIONE TRANSPORTER; GLYCOPHORIN A; INSULIN RECEPTOR; LIPOPROTEIN RECEPTOR; PEPTIDE; SCAVENGER RECEPTOR; TMEM30A PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CENTRAL NERVOUS SYSTEM AGENTS; DRUG CARRIER;

BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN DISEASE; BRAIN TUMOR; CENTRAL NERVOUS SYSTEM DISEASE; DRUG DELIVERY SYSTEM; DRUG RECEPTOR BINDING; DRUG TARGETING; ENDOCYTOSIS; HUMAN; NONHUMAN; PINOCYTOSIS; PROTEIN TARGETING; REVIEW; ANIMAL; BRAIN; DRUG ADMINISTRATION ROUTE; DRUG EFFECT; METABOLISM;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CENTRAL NERVOUS SYSTEM AGENTS; CENTRAL NERVOUS SYSTEM DISEASES; DRUG ADMINISTRATION ROUTES; DRUG CARRIERS; HUMANS; RECEPTORS, CELL SURFACE;

EID: 66149130750     PISSN: 17425247     EISSN: None     Source Type: Journal    
DOI: 10.1517/17425240902806383     Document Type: Review

References (93)

1. de Boer AG, Gaillard PJ. Drug targeting to the brain. Annu Rev Pharmacol Toxicol 2007;47:323-355
2. Ehrlich P. Das Sauerstoff-Bedurfnis des Organismus: eine farbenanalytische Studie. 2008
3. Goldman EE. Vitalfarbung am Zentralnervensystem. 2008
4. Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006;86:849-899
5. de Boer AG, van der Sandt IC, Gaillard PJ. The role of drug transporters at the blood-brain barrier. Annu Rev Pharmacol Toxicol 2003;43:629-656
6. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003;422:37-44
7. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005;6:79-87
8. Hanson LR, Frey WH. Intranasal delivery bypasses the blood-brain barrier to target therapeutic agents to the central nervous system and treat neurodegenerative disease. BMC Neurosci 2008;9(Suppl 3):S5
9. Bickel U, Yoshikawa T, Pardridge WM. Delivery of peptides and proteins through the blood-brain barrier. Adv Drug Deliv Rev 2001;46:247-279
10. Pardridge WM. Drug targeting to the brain. Pharm Res 2007;24:1733-1744
11. Pardridge WM. shRNA and siRNA delivery to the brain. Adv Drug Deliv Rev 2007;59:141-152
12. Pardridge WM. Blood-brain barrier delivery. Drug Discov Today 2007;12:54-61
13. Schlachetzki F, Zhang Y, Boado RJ, Pardridge WM. Gene therapy of the brain: the trans-vascular approach. Neurology 2004;62:1275-1281
14. Pardridge WM. Drug and gene delivery to the brain: the vascular route. Neuron 2002;36:555-558
15. Xia CF, Boado RJ, Zhang Y, et al. Intravenous glial-derived neurotrophic factor gene therapy of experimental Parkinson's disease with Trojan horse liposomes and a tyrosine hydroxylase promoter. J Gene Med 2008;10:306-315
16. Zhang Y, Pardridge WM. Blood-brain barrier targeting of BDNF improves motor function in rats with middle cerebral artery occlusion. Brain Res 2006;1111:227-229
17. Zhang Y, Wang Y, Boado RJ, Pardridge WM. Lysosomal enzyme replacement of the brain with intravenous non-viral gene transfer. Pharm Res 2008;25:400-406
18. Dehouck B, Fenart L, Dehouck MP, et al. A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J Cell Biol 1997;138:877-889
19. Bu G, Maksymovitch EA, Nerbonne JM, Schwartz AL. Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J Biol Chem 1994;269:18521-18528
20. Fillebeen C, Descamps L, Dehouck MP, et al. Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J Biol Chem 1999;274:7011-7017
21. Ji B, Maeda J, Higuchi M, et al. Pharmacokinetics and brain uptake of lactoferrin in rats. Life Sci 2006;78:851-855
22. Demeule M, Poirier J, Jodoin J, et al. High transcytosis of melanotransferrin (P97) across the blood-brain barrier. J Neurochem 2002;83:924-933
23. Richardson DR, Morgan EH. The transferrin homologue, melanotransferrin (p97), is rapidly catabolized by the liver of the rat and does not effectively donate iron to the brain. Biochim Biophys Acta 2004;1690:124-133
24. Demeule M, Currie JC, Bertrand Y, et al. Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector angiopep-2. J Neurochem 2008;106:1534-1544
25. Regina A, Demeule M, Che C, et al. Antitumour activity of ANG1005, a conjugate between paclitaxel and the new brain delivery vector Angiopep-2. Br J Pharmacol 2008;155:185-197
26. Goti D, Hrzenjak A, Levak-Frank S, et al. Scavenger receptor class B, type I is expressed in porcine brain capillary endothelial cells and contributes to selective uptake of HDL-associated vitamin E. J Neurochem 2001;76:498-508
27. Kratzer I, Wernig K, Panzenboeck U, et al. Apolipoprotein A-I coating of protamine-oligonucleotide nanoparticles increases particle uptake and transcytosis in an in vitro model of the blood-brain barrier. J Control Release 2007;117:301-311
28. Abulrob A, Sprong H, Bergen en HP, Stanimirovic D. The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells. J Neurochem 2005;95:1201-1214
29. Abulrob A, Baumann E, Brunette E, et al. TMEM30A - A Novel Blood-Brain Barrier Receptor That Undergoes Receptor-Mediated Transcytosis. 2008
30. Kumar P, Wu H, McBride JL, et al. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007;448:39-43
31. Raab G, Klagsbrun M. Heparin-binding EGF-like growth factor. Biochim Biophys Acta 1997;1333:F179-99
32. Mishima K, Higashiyama S, Nagashima Y, et al. Regional distribution of heparin-binding epidermal growth factor-like growth factor mRNA and protein in adult rat forebrain. Neurosci Lett 1996;213:153-156
33. Kawahara N, Mishima K, Higashiyama S, et al. The gene for heparin-binding epidermal growth factor-like growth factor is stress-inducible: its role in cerebral ischemia. J Cereb Blood Flow Metab 1999;19:307-320
34. Tanaka N, Sasahara M, Ohno M, et al. Heparin-binding epidermal growth factor-like growth factor mRNA expression in neonatal rat brain with hypoxic/ischemic injury. Brain Res 1999;827:130-138
35. Opanashuk LA, Mark RJ, Porter J, et al. Heparin-binding epidermal growth factor-like growth factor in hippocampus: modulation of expression by seizures and anti-excitotoxic action. J Neurosci 1999;19:133-146
36. Buzzi S, Rubboli D, Buzzi G, et al. CRM197 (nontoxic diphtheria toxin): effects on advanced cancer patients. Cancer Immunol Immunother 2004;53:1041-1048
37. Anderson P. Antibody responses to Haemophilus influenzae type b and diphtheria toxin induced by conjugates of oligosaccharides of the type b capsule with the nontoxic protein CRM197. Infect Immun 1983;39:233-238
38. Gaillard PJ, de Boer AG. 2B-Trans technology: targeted drug delivery across the blood-brain barrier. Methods Mol Biol 2008;437:161-175
39. Gaillard PJ, de Boer AG. A novel opportunity for targeted drug delivery to the brain. J Control Release 2006;116:e60-2
40. Kannan R, Kuhlenkamp JF, Jeandidier E, et al. Evidence for carrier-mediated transport of glutathione across the blood-brain barrier in the rat. J Clin Invest 1990;85:2009-2013
41. Gaillard PJ. Targeted Intracellular Delivery of Antiviral Agents. 2008
42. More SS, Vince R. Design, synthesis and biological evaluation of glutathione peptidomimetics as components of anti-Parkinson prodrugs. J Med Chem 2008;51:4581-4588
43. Sadoshima S, Fujishima M, Ogata J, et al. Disruption of blood-brain barrier following bilateral carotid artery occlusion in spontaneously hypertensive rats. A quantitative study. Stroke 1983;14:876-882
44. Sage JI, Van Uitert RL, Duffy TE. Early changes in blood-brain barrier permeability to small molecules after transient cerebral ischemia. Stroke 1984;15:46-50
45. Desai BS, Monahan AJ, Carvey PM, Hendey B. Blood-brain barrier pathology in Alzheimer's and Parkinson's disease: implications for drug therapy. Cell Transplant 2007;16:285-299
46. Trojano M, Manzari C, Livrea P. Blood-brain barrier changes in multiple sclerosis. Ital J Neurol Sci 1992;13:55-64
47. Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 2005;46:1724-1743
48. Abbott NJ. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol 2000;20:131-147
49. Brabers NA, Nottet HS. Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur J Clin Invest 2006;36:447-458
50. Gaillard PJ, de Boer AB, Breimer DD. Pharmacological investigations on lipopolysaccharide-induced permeability changes in the blood-brain barrier in vitro. Microvasc Res 2003;65:24-31
51. Lo EH, Singhal AB, Torchilin VP, Abbott NJ. Drug delivery to damaged brain. Brain Res Brain Res Rev 2001;38:140-148
52. Reichel A. The role of blood-brain barrier studies in the pharmaceutical industry. Curr Drug Metab 2006;7:183-203
53. Krizbai IA, Bauer H, Bresgen N, et al. Effect of oxidative stress on the junctional proteins of cultured cerebral endothelial cells. Cell Mol Neurobiol 2005;25:129-139
54. Chiba H, Osanai M, Murata M, et al. Transmembrane proteins of tight junctions. Biochim Biophys Acta 2008;1778:588-600
55. Easton AS, Abbott NJ. Bradykinin increases permeability by calcium and 5-lipoxygenase in the ECV304/C6 cell culture model of the blood-brain barrier. Brain Res 2002;953:157-169
56. Burke-Gaffney A, Keenan AK. Modulation of human endothelial cell permeability by combinations of the cytokines interleukin-1 alpha/beta, tumor necrosis factor-alpha and interferon-gamma. Immunopharmacology 1993;25:1-9
57. Burke-Gaffney A, Keenan AK. Does TNF-alpha directly increase endothelial cell monolayer permeability? Agents Actions 1993;38 Spec No:C83-5
58. Deli MA, Descamps L, Dehouck MP, et al. Exposure of tumor necrosis factor-alpha to luminal membrane of bovine brain capillary endothelial cells cocultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J Neurosci Res 1995;41:717-726
59. Huynh HK, Dorovini-Zis K. Effects of interferon-gamma on primary cultures of human brain microvessel endothelial cells. Am J Pathol 1993;142:1265-1278
60. Maruo N, Morita I, Shirao M, Murota S. IL-6 increases endothelial permeability in vitro. Endocrinology 1992;131:710-714
61. Tunkel AR, Rosser SW, Hansen EJ, Scheld WM. Blood-brain barrier alterations in bacterial meningitis: development of an in vitro model and observations on the effects of lipopolysaccharide. In Vitro Cell Dev Biol 1991;27A:113-120
62. Wong D, Dorovini-Zis K, Vincent SR. Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp Neurol 2004;190:446-455
63. Fischer S, Clauss M, Wiesnet M, et al. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am J Physiol 1999;276:C812-20
64. Witt KA, Mark KS, Huber J, Davis TP. Hypoxia-inducible factor and nuclear factor kappa-B activation in blood-brain barrier endothelium under hypoxic/reoxygenation stress. J Neurochem 2005;92:203-214
65. Abraham CS, Deli MA, Joo F, et al. Intracarotid tumor necrosis factor-alpha administration increases the blood-brain barrier permeability in cerebral cortex of the newborn pig: quantitative aspects of double-labelling studies and confocal laser scanning analysis. Neurosci Lett 1996;208:85-88
66. Gardenfors A, Nilsson F, Skagerberg G, et al. Cerebral physiological and biochemical changes during vasogenic brain oedema induced by intrathecal injection of bacterial lipopolysaccharides in piglets. Acta Neurochir (Wien) 2002;144:601-608
67. Banks WA, Terrell B, Farr SA, et al. Passage of amyloid beta protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease. Peptides 2002;23:2223-2226
68. Yang GY, Gong C, Qin Z, et al. Tumor necrosis factor alpha expression produces increased blood-brain barrier permeability following temporary focal cerebral ischemia in mice. Brain Res Mol Brain Res 1999;69:135-143
69. Schroeter M, Kury P, Jander S. Inflammatory gene expression in focal cortical brain ischemia: differences between rats and mice. Brain Res Mol Brain Res 2003;117:1-7
70. Olsen AL, Morrey JD, Smee DF, Sidwell RW. Correlation between breakdown of the blood-brain barrier and disease outcome of viral encephalitis in mice. Antiviral Res 2007;75:104-112
71. Kanmogne GD, Primeaux C, Grammas P. HIV-1 gp120 proteins alter tight junction protein expression and brain endothelial cell permeability: implications for the pathogenesis of HIV-associated dementia. J Neuropathol Exp Neurol 2005;64:498-505
72. Stolp HB, Dziegielewska KM, Ek CJ, et al. Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur J Neurosci 2005;22:2805-2816
73. Nonaka N, Hileman SM, Shioda S, et al. Effects of lipopolysaccharide on leptin transport across the blood-brain barrier. Brain Res 2004;1016:58-65
74. Leech S, Kirk J, Plumb J, McQuaid S. Persistent endothelial abnormalities and blood-brain barrier leak in primary and secondary progressive multiple sclerosis. Neuropathol Appl Neurobiol 2007;33:86-98
75. Kirk J, Plumb J, Mirakhur M, McQuaid S. Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J Pathol 2003;201:319-327
76. Langford D, Masliah E. Crosstalk between components of the blood brain barrier and cells of the CNS in microglial activation in AIDS. Brain Pathol 2001;11:306-312
77. Tanabe S, Shimohigashi Y, Nakayama Y, et al. In vivo and in vitro evidence of blood-brain barrier transport of a novel cationic arginine-vasopressin fragment 4-9 analog. J Pharmacol Exp Ther 1999;290:561-568
78. Kumagai AK, Eisenberg JB, Pardridge WM. Absorptive-mediated endocytosis of cationized albumin and a beta-endorphincationized albumin chimeric peptide by isolated brain capillaries. Model system of blood-brain barrier transport. J Biol Chem 1987;262:15214-15219
79. Duchini A, Govindarajan S, Santucci M, et al. Effects of tumor necrosis factor-alpha and interleukin-6 on fluid-phase permeability and ammonia diffusion in CNS-derived endothelial cells. J Investig Med 1996;44:474-482
80. Cipolla MJ, Crete R, Vitullo L, Rix RD. Transcellular transport as a mechanism of blood-brain barrier disruption during stroke. Front Biosci 2004;9:777-785
81. Burdo JR, Connor JR. Brain iron uptake and homeostatic mechanisms: an overview. Biometals 2003;16:63-75
82. Messier C, Teutenberg K. The role of insulin, insulin growth factor, and insulin-degrading enzyme in brain aging and Alzheimer's disease. Neural Plast 2005;12:311-328
83. Jeynes B, Provias J. Evidence for altered LRP/RAGE expression in Alzheimer lesion pathogenesis. Curr Alzheimer Res 2008;5:432-437
84. Gaultier A, Arandjelovic S, Niessen S, et al. Regulation of tumor necrosis factor receptor-1 and the IKK-NF-kappaB pathway by LDL receptor-related protein explains the anti-inflammatory activity of this receptor. Blood 2008;111:5316-5325
85. Herholz K. Acetylcholine esterase activity in mild cognitive impairment and Alzheimer's disease. Eur J Nucl Med Mol Imaging 2008;35(Suppl 1):S25-9
86. Mishima K, Higashiyama S, Asai A, et al. Heparin-binding epidermal growth factor-like growth factor stimulates mitogenic signaling and is highly expressed in human malignant gliomas. Acta Neuropathol 1998;96:322-328
87. Sims NR, Nilsson M, Muyderman H. Mitochondrial glutathione: a modulator of brain cell death. J Bioenerg Biomembr 2004;36:329-333
88. Valko M, Leibfritz D, Moncol J, et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84
89. Fillebeen C, Dehouck B, Benaissa M, et al. Tumor necrosis factor-alpha increases lactoferrin transcytosis through the blood-brain barrier. J Neurochem 1999;73:2491-2500
90. Kreuter J. Nanoparticulate systems for brain delivery of drugs. Adv Drug Deliv Rev 2001;47:65-81
91. Kreuter J, Shamenkov D, Petrov V, et al. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood-brain barrier. J Drug Target 2002;10:317-325
92. de Boer AG, Gaillard PJ. Strategies to improve drug delivery across the blood-brain barrier. Clin Pharmacokinet 2007;46:553-576
93. More SS, Vince R. Design, synthesis and biological evaluation of glutathione peptidomimetics as components of anti-Parkinson prodrugs. J Med Chem 2008;51:4581-4588