Structure and function of the blood–brain barrier

Neurobiology of Disease - Tập 37 Số 1 - Trang 13-25 - 2010
N. Joan Abbott1, Adjanie Patabendige1, Diana E. M. Dolman1, Siti R. Yusof1, David J. Begley1
1King's College London, Blood–Brain Barrier Group, Pharmaceutical Science Division, Hodgkin Building, Guy's Campus, London SE1 1UL, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Abbott, 1992, Comparative physiology of the blood–brain barrier, 371

Abbott, 1998, Role of intracellular calcium in regulation of brain endothelial permeability, 345

Abbott, 2002, Astrocyte–endothelial interactions and blood–brain barrier permeability, J. Anat., 200, 629, 10.1046/j.1469-7580.2002.00064.x

Abbott, 2004, Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology, Neurochem. Int., 45, 545, 10.1016/j.neuint.2003.11.006

Abbott, 2005, Dynamics of CNS barriers: evolution, differentiation, and modulation, Cell. Mol. Neurobiol., 25, 5, 10.1007/s10571-004-1374-y

Abbott, 2006, Astrocyte–endothelial interactions at the blood–brain barrier, Nature Rev. Neurosci., 7, 41, 10.1038/nrn1824

Abbott, 2002, Drug resistance in epilepsy: the role of the blood–brain barrier, 38

Anthony, 1997, Age-related effects of interleukin-β on polymorphonuclear neutrophil-dependent increases in blood–brain barrier permeability in rats, Brain, 120, 435, 10.1093/brain/120.3.435

Balda, 1991, Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin, J. Membr. Biol., 122, 193, 10.1007/BF01871420

Balda, 2009, Tight junctions and the regulation of gene expression, Biochim. Biophys. Acta, 1788, 761, 10.1016/j.bbamem.2008.11.024

Ballabh, 2004, The blood–brain barrier: an overview: structure, regulation, and clinical implications, Neurobiol. Disease, 16, 1, 10.1016/j.nbd.2003.12.016

Banks, 2002, Leptin transport across the blood–brain barrier of the Koletsky rat is not mediated by a product of the leptin receptor gene, Brain Res., 950, 130, 10.1016/S0006-8993(02)03013-5

Banks, 2004, The source of cerebral insulin, Eur. J. Pharmacol., 490, 5, 10.1016/j.ejphar.2004.02.040

Bartels, 2008, Decreased blood–brain barrier P-glycoprotein function in the progression of Parkinson's disease, PSP and MSA, J. Neural Transm., 115, 1001, 10.1007/s00702-008-0030-y

Bauer, 2004, Proteins of the tight junction in the blood brain barrier, 1

Bechmann, 2005, Circulating monocytic cells infiltrate layers of anterograde axonal degeneration where they transform into microglia, FASEB J., 19, 647, 10.1096/fj.04-2599fje

Bechmann, 2001, Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages, Eur. J. Neurosci., 14, 1651, 10.1046/j.0953-816x.2001.01793.x

Begley, 1996, The blood–brain barrier: principles for targeting peptides and drugs to the central nervous system, J. Pharm. Pharmacol., 48, 136, 10.1111/j.2042-7158.1996.tb07112.x

Begley, 2004, Delivery of therapeutic agents to the central nervous system: the problems and the possibilities, Pharmacol. Ther., 104, 29, 10.1016/j.pharmthera.2004.08.001

Begley, 2004, ABC transporters and the blood–brain barrier, Curr. Pharm. Des., 10, 1295, 10.2174/1381612043384844

Begley, 2007, Structure and function of the blood–brain barrier, 575

Begley, 2003, Structural and functional aspects of the blood–brain barrier, Progr. Drug Res., 61, 39

Begley, 2008, Lysosomal storage diseases and the blood–brain barrier, Curr. Pharm. Des., 14, 1566, 10.2174/138161208784705504

Bell, 2009, Neurovascular mechanisms and blood–brain barrier disorder in Alzheimer's disease, Acta Neuropathol., 118, 103, 10.1007/s00401-009-0522-3

Berger, 2004, The blood brain barrier in HIV infection, Front. Biosci., 9, 2680, 10.2741/1427

Bernacki, 2008, Physiology and pharmacological role of the blood–brain barrier, Pharmacol. Rep., 60, 600

Berzin, 2000, Agrin and microvascular damage in Alzheimer's disease, Neurobiol. Aging, 21, 349, 10.1016/S0197-4580(00)00121-4

Betz, 1980, Polarity of the blood–brain barrier: distribution of enzymes between the luminal and abluminal membranes of brain capillary endothelial cells, Brain Res., 192, 17, 10.1016/0006-8993(80)91004-5

Bodor, 2003, Brain-targeted drug delivery: experiences to date, Am. J. Drug Targ., 1, 13, 10.2165/00137696-200301010-00002

Bolton, 1998, Loss of tight junction proteins occludin and zonula-occludens-1 from cerebral vascular endothelium during neutrophil-induced blood–brain barrier breakdown in vivo, Neuroscience, 86, 1245, 10.1016/S0306-4522(98)00058-X

Bouldin, 1975, Differential permeability of cerebral capillary and choroid plexus to lanthanum ion, Brain Res., 99, 444, 10.1016/0006-8993(75)90053-0

Bradbury, 1963, The distribution of potassium, sodium, chloride and urea between lumbar cerebrospinal fluid and blood serum in human subjects, Clin. Sci., 25, 97

Brightman, 1969, Junctions between intimately apposed cell membranes in the vertebrate brain, J. Cell Biol., 40, 648, 10.1083/jcb.40.3.648

Broadwell, 1988, Transcytotic pathway for blood–borne protein through the blood–brain barrier, Proc. Natl. Acad. Sci. U. S. A., 85, 632, 10.1073/pnas.85.2.632

Bronger, 2005, ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood–tumor barrier, Cancer Res, 65, 11419, 10.1158/0008-5472.CAN-05-1271

Brown, 2004, Molecular mechanisms of cerebrospinal fluid production, Neuroscience, 129, 957, 10.1016/j.neuroscience.2004.07.003

Buckner, 2006, Neuroimmunity and the blood–brain barrier: molecular regulation of leukocyte transmigration and viral entry into the nervous system with a focus on NeuroAIDS, J. Neuroimmune Pharmacol., 1, 160, 10.1007/s11481-006-9017-3

Butt, 1990, Electrical resistance across the blood–brain barrier in anaesthetised rats: a developmental study, J. Physiol., 429, 47, 10.1113/jphysiol.1990.sp018243

Butt, 1995, Effect of inflammatory agents on electrical resistance across the blood–brain barrier in pial microvessels of anaesthetised rats, Brain Res, 696, 145, 10.1016/0006-8993(95)00811-4

Carman, 2008, Trans-cellular migration: cell–cell contacts get intimate, Curr. Opin. Cell Biol., 20, 533, 10.1016/j.ceb.2008.05.007

Cirrito, 2005, P-glycoprotein deficiency at the blood–brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model, J. Clin. Invest., 115, 3285, 10.1172/JCI25247

Clark, 2003, In silico prediction of blood–brain barrier permeation, Drug Discov. Today, 8, 927, 10.1016/S1359-6446(03)02827-7

Claudio, 1989, Increased vesicular transport and decreased mitochondrial content in blood–brain barrier endothelial cells during experimental autoimmune encephalomyelitis, Am. J. Pathol., 135, 1157

Correale, 2007, The blood–brain-barrier in multiple sclerosis: functional roles and therapeutic targeting, Autoimmunity, 40, 148, 10.1080/08916930601183522

Cserr, 1981, Efflux of radiolabeled polyethylene glycol and albumin from rat brain, Am. J. Physiol., 240, F319

Cserr, 1992, Secretion and bulk flow of interstitial fluid, 245

Dahlin, 2009, Expression profiling of the solute carrier gene family in the mouse brain, J. Pharmacol. Exp. Ther., 329, 558, 10.1124/jpet.108.149831

Dallas, 2006, Multidrug resistance-associated proteins: expression and function in the central nervous system, Pharmacol. Rev., 58, 140, 10.1124/pr.58.2.3

Dallasta, 1999, Blood–brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis, Am. J. Pathol., 155, 1915, 10.1016/S0002-9440(10)65511-3

Dauchy, 2008, ABC transporters, cytochromes P450 and their main transcription factors: expression at the human blood–brain barrier, J. Neurochem., 107, 1518, 10.1111/j.1471-4159.2008.05720.x

Dauchy, 2009, Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells, Biochem. Pharmacol., 77, 897, 10.1016/j.bcp.2008.11.001

Davies, 2002, Blood–brain barrier breakdown in septic encephalopathy and brain tumours, J. Anat., 200, 639, 10.1046/j.1469-7580.2002.00065.x

Davoust, 2008, From bone marrow to microglia: barriers and avenues, Trends Immunol., 29, 227, 10.1016/j.it.2008.01.010

Davson, 1995

Dean, 2001, The human ATP-binding cassette (ABC) transporter superfamily, Genome Res., 11, 1156, 10.1101/gr.GR-1649R

Deane, 2004, RAGE (Yin) versus LRP (Yang) balance regulates Alzheimer amyloid β-peptide clearance through transport across the blood–brain barrier, Stroke, 35, 2628, 10.1161/01.STR.0000143452.85382.d1

Demeule, 2002, High transcytosis of melanotransferrin (P97) across the blood–brain barrier, J. Neurochem., 83, 924, 10.1046/j.1471-4159.2002.01201.x

Desai, 2007, Blood–brain barrier pathology in Alzheimer's and Parkinson's disease: implications for drug therapy, Cell Trans., 16, 285, 10.3727/000000007783464731

Dogrukol-Ak, 2009, Isolation of peptide transport system-6 from brain endothelial cells: therapeutic effects with antisense inhibition in Alzheimer and stroke models, J. Cereb. Blood Flow Metab., 29, 411, 10.1038/jcbfm.2008.131

Dolman, 2005, Induction of aquaporin 1 but not aquaporin 4 messenger RNA in rat primary brain microvessel endothelial cells in culture, J. Neurochem., 93, 825, 10.1111/j.1471-4159.2005.03111.x

Drin, 2003, Studies on the internalisation mechanism of cationic cell-penetrating peptides, J. Biol. Chem., 278, 31192, 10.1074/jbc.M303938200

Eilers, 2008, MRP (ABCC) transporters-mediated efflux of anti-HIV drugs, saquinavir and zidovudine, from human endothelial cells, Exp. Biol. Med. (Maywood)., 233, 1149, 10.3181/0802-RM-59

Engelhardt, 2007, Development of the blood–brain interface, 11

Engelhardt, 2004, Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house?, Eur. J. Immunol., 34, 2955, 10.1002/eji.200425327

Fabis, 2007, Loss of blood–brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models, Proc. Natl. Acad. Sci. U. S. A., 104, 5656, 10.1073/pnas.0701252104

Förster, 2008, Tight junctions and the modulation of barrier function in disease, Histochem. Cell Biol., 130, 55, 10.1007/s00418-008-0424-9

Förster, 2008, Compound profiling for ABCC2 (MRP2) using a fluorescent microplate assay system, Eur. J. Pharm. Biopharm., 69, 396, 10.1016/j.ejpb.2007.10.003

Gaillard, 2005, Targeted delivery across the blood–brain barrier, Expert Opin. Drug Deliv., 2, 299, 10.1517/17425247.2.2.299

Gaillard, 2003, Pharmacological investigations on lipopolysaccharide-induced permeability changes in the blood–brain in vitro, Microvasc. Res., 65, 24, 10.1016/S0026-2862(02)00009-2

Gingrich, 2000, Potentiation of NMDA receptor function by the serine protease thrombin, J. Neurosci., 20, 4582, 10.1523/JNEUROSCI.20-12-04582.2000

Gingrich, 2000, Serine proteases and brain damage — is there a link?, Trends Neurosci., 23, 399, 10.1016/S0166-2236(00)01617-9

Giri, 2008, Investigation of the role of breast cancer resistance protein (Bcrp/Abcg2) on pharmacokinetics and central nervous system penetration of abacavir and zidovudine in the mouse, Drug Metab. Dispos., 36, 1476, 10.1124/dmd.108.020974

Gleeson, 2008, Generation of a set of simple, interpretable ADMET rules of thumb, J. Med. Chem., 51, 817, 10.1021/jm701122q

Glezer, 2007, Neuroprotective role of the innate immune system by microglia, Neuroscience, 147, 867, 10.1016/j.neuroscience.2007.02.055

Grieshaber, 2007, Does the blood–brain barrier play a role in glaucoma?, Surv. Ophthalmol., 52, S115, 10.1016/j.survophthal.2007.08.005

Grontoft, 1954, Intracranial haemorrhage and blood–brain barrier problems in the new-born: a pathologico-anatomical and experimental investigation, Acta Pathol. Microbiol. Scand. Suppl., 100, 8

Hamm, 2004, Astrocyte mediated modulation of blood–brain barrier permeability does not correlate with loss of tight junction proteins from the cellular contacts, Cell Tiss. Res., 315, 157, 10.1007/s00441-003-0825-y

Hansen, 1985, Effect of anoxia on ion distribution in the brain, Physiol. Rev., 65, 101, 10.1152/physrev.1985.65.1.101

Herz, 2003, Coaxing the LDL receptor family into the fold, Cell, 112, 289, 10.1016/S0092-8674(03)00073-4

Hess, 2004, Hematopoietic origin of microglial and perivascular cells in brain, Exp. Neurol., 186, 134, 10.1016/j.expneurol.2003.11.005

Huber, 2001, Inflammatory pain alters blood–brain barrier permeability and tight junctional protein expression, Am. J. Physiol. Heart Circ. Physiol., 280, H1241, 10.1152/ajpheart.2001.280.3.H1241

Jeong, 2006, Changes in magnesium concentration in the serum and cerebrospinal fluid of neuropathic rats, Acta Anaesthesiol. Scand., 50, 211, 10.1111/j.1399-6576.2006.00925.x

Jones, 1992, The development of ion regulation at the blood–brain barrier, Prog. Brain Res., 91, 123, 10.1016/S0079-6123(08)62326-2

Kalaria, 1999, The blood–brain barrier and cerebrovascular pathology in Alzheimer's disease, Ann. N. Y. Acad. Sci., 893, 113, 10.1111/j.1749-6632.1999.tb07821.x

Kamiie, 2008, Quantitative atlas of membrane transporter proteins: development and application of a highly sensitive simultaneous LC/MS/MS method combined with novel in-silico peptide selection criteria, Pharm. Res., 25, 69, 10.1007/s11095-008-9532-4

Kandel, 2000, 1294

Kastin, 2003, Peptide transport across the blood–brain barrier, Prog. Drug Res., 61, 79

Kaur, 2008, Blood brain barrier in hypoxic–ischemic conditions, Curr. Neurovasc. Res., 5, 71, 10.2174/156720208783565645

Keep, 1995, Developmental changes in blood–brain barrier potassium permeability in the rat: relation to brain growth, J. Physiol., 488, 439, 10.1113/jphysiol.1995.sp020978

Konsman, 2007, (Peri)vascular production and action of pro-inflammatory cytokines in brain pathology, Clin. Sci. (Lond), 112, 1, 10.1042/CS20060043

Kortekaas, 2005, Blood–brain barrier dysfunction in parkinsonian midbrain in vivo, Ann. Neurol., 57, 176, 10.1002/ana.20369

Krämer, 1999, Absorption prediction from physicochemical parameters, Pharm. Sci. Technol. Today, 2, 373, 10.1016/S1461-5347(99)00188-1

Lazarowski, 2007, ABC transporters during epilepsy and mechanisms underlying multidrug resistance in refractory epilepsy, Epilepsia, 48, 140, 10.1111/j.1528-1167.2007.01302.x

Lee, 2003, SSeCKS regulates angiogenesis and tight junction formation in blood–brain barrier, Nat. Med, 9, 900, 10.1038/nm889

Liebner, 2000, Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme, Acta Neuropathol, 100, 323, 10.1007/s004010000180

Liebner, 2008, Wnt/beta-catenin signaling controls development of the blood–brain barrier, J. Cell Biol., 183, 409, 10.1083/jcb.200806024

Lim, 2007, The adult neural stem cell niche: lessons for future neural cell replacement strategies, Neurosurg. Clin. N. Am., 18, 81, 10.1016/j.nec.2006.10.002

Liu, 2004, Development of a computational approach to predict blood–brain barrier permeability, Drug Metab. Dispos., 32, 132, 10.1124/dmd.32.1.132

Lo, 2003, Mechanisms, challenges and opportunities in stroke, Nature Rev. Neurosci., 4, 399, 10.1038/nrn1106

Lyck, 2009, Culture-induced changes in blood–brain barrier transcriptome: implications for amino-acid transporters in vivo, J. Cereb. Blood Flow Metab., 10.1038/jcbfm.2009.72

Marroni, 2003, Vascular and parenchymal mechanisms in multiple drug resistance: a lesson from human epilepsy, Curr. Drug Targets, 4, 297, 10.2174/1389450033491109

Matsuoka, 1999, Developmental expression of P-glycoprotein (multidrug resistance gene product) in rat brain, J. Neurobiol., 39, 383, 10.1002/(SICI)1097-4695(19990605)39:3<383::AID-NEU5>3.0.CO;2-4

McQuaid, 2009, The effects of blood–brain barrier disruption on glial cell function in multiple sclerosis, Biochem. Soc. Trans., 37, 329, 10.1042/BST0370329

Mellman, 1996, Endocytosis and molecular sorting, Annu. Rev. Cell Dev. Biol., 12, 575, 10.1146/annurev.cellbio.12.1.575

Mertsch, 2002, Blood–brain barrier penetration and drug development from an industrial point of view, Curr. Med. Chem. – Central Nervous System Agents, 2, 187, 10.2174/1568015023358067

Milhorat, 1971, Cerebrospinal fluid production by the choroid plexus and brain, Science, 173, 330, 10.1126/science.173.3994.330

Minagar, 2003, Blood–brain barrier disruption in multiple sclerosis, Mult. Scler., 9, 540, 10.1191/1352458503ms965oa

Mitic, 2000, Molecular physiology and pathophysiology of tight junctions. I. Tight junction structure and function: lessons from mutant animals and proteins, Am. J. Physiol. Gastrointest. Liver. Physiol., 297, G250, 10.1152/ajpgi.2000.279.2.G250

Moos, 1993, Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages, Neuropathol. Applied. Neurobiol., 19, 120, 10.1111/j.1365-2990.1993.tb00416.x

Mukherjee, 1997, Endocytosis, Phys. Rev., 77, 759

Nadal, 1995, Plasma albumin is a potent trigger of calcium signals and DNA synthesis in astrocytes, Proc. Natl. Acad. Sci. U. S. A., 92, 1426, 10.1073/pnas.92.5.1426

Nag, 2005, Blood–brain barrier, exchange of metabolites and gases, 22

Nakagawa, 2009, A new blood–brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes, Neurochem. Int., 54, 253, 10.1016/j.neuint.2008.12.002

Neuhaus, 1991, Induction of blood–brain barrier characteristics in bovine brain endothelial cells by rat astroglial cells in transfilter coculture, Ann. N.Y. Acad. Sci., 633, 578, 10.1111/j.1749-6632.1991.tb15667.x

Nischwitz, 2008, Speciation analysis of selected metals and determination of their total contents in paired serum and cerebrospinal fluid samples: an approach to investigate the permeability of the human blood–cerebrospinal fluid-barrier, Anal. Chim. Acta, 627, 258, 10.1016/j.aca.2008.08.018

Nitta, 2003, Size-selective loosening of the blood–brain barrier in claudin-5 deficient mice, J. Cell Biol., 161, 653, 10.1083/jcb.200302070

Ohno, 1978, Lower limits of cerebrovascular permeability to nonelectrolytes in the conscious rat, Am. J. Physiol., 235, H299

Ohtsuki, 2007, Contribution of carrier-mediated transport systems to the blood–brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development, Pharm. Res., 24, 1745, 10.1007/s11095-007-9374-5

Oki, 2004, Increased ability of peripheral blood lymphocytes to degrade laminin in multiple sclerosis, J. Neurol. Sci., 222, 7, 10.1016/j.jns.2004.03.026

Olsson, 1968, Blood–brain barrier to albumin in embryonic new born and adult rats, Acta Neuropathol., 10, 117, 10.1007/BF00691305

Pan, 2000, Saturable entry of leukemia inhibitory factor from blood to the central nervous system, J. Neuroimmunol., 106, 172, 10.1016/S0165-5728(00)00241-1

Pan, 1999, Entry of EGF into brain is rapid and saturable, Peptides, 20, 1091, 10.1016/S0196-9781(99)00094-7

Pan, 2002, TNFα transport across the blood–brain barrier is abolished in receptor knockout mice, Exp. Neurol., 174, 193, 10.1006/exnr.2002.7871

Papadopoulos, 2004, Molecular mechanisms of brain tumor edema, Neuroscience, 129, 1011, 10.1016/j.neuroscience.2004.05.044

Pardridge, 1990, Evaluation of cationised rat albumin as a potential blood–brain barrier drug transport vector, Exp. Neurol., 255, 893

Persidsky, 2006, Blood–brain barrier: structural components and function under physiologic and pathologic conditions, J. Neuroimmune Pharmacol., 1, 223, 10.1007/s11481-006-9025-3

Polli, 2009, Drug Metab. Dispos., 37, 439, 10.1124/dmd.108.024646

Preston, 1995, Permeability of the developing blood–brain barrier to 14C-mannitol using the rat in situ brain perfusion technique, Brain Res. Dev. Brain Res., 87, 69, 10.1016/0165-3806(95)00060-Q

Reiber, 2001, Dynamics of brain-derived proteins in cerebrospinal fluid, Clin. Chem. Acta, 310, 173, 10.1016/S0009-8981(01)00573-3

Remy, 2006, Molecular and cellular mechanisms of pharmacoresistance in epilepsy, Brain, 129, 18, 10.1093/brain/awh682

Rennels, 1983, Innervation of capillaries by local neurones in the cat hypothalamus: a light microscopic study with horseradish peroxidise, J. Cereb. Blood Flow Metab., 3, 535, 10.1038/jcbfm.1983.82

Roberts, 2008, A critical overview of the influence of inflammation and infection on P-glycoprotein expression and activity in the brain, Expert Opin. Drug Metab. Toxicol., 4, 1245, 10.1517/17425255.4.10.1245

Roberts, 2008, Subcellular localization of transporters along the rat blood–brain barrier and blood–cerebral–spinal fluid barrier by in vivo biotinylation, Neuroscience, 155, 423, 10.1016/j.neuroscience.2008.06.015

Rosenberg, 2007, Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia, Neurosurg. Focus., 22, E4, 10.3171/foc.2007.22.5.5

Rubin, 1991, Differentiation of brain endothelial cells in cell culture, Ann. N.Y. Acad. Sci., 633, 420, 10.1111/j.1749-6632.1991.tb15631.x

Sauer, 2005, An apolipoprotein E-derived peptide mediates uptake of sterically stabilized liposomes into brain capillary endothelial cells, Biochemistry, 44, 2021, 10.1021/bi048080x

Saunders, 1992, Development of the blood–brain barrier to macromolecules, 128

Saunders, 2000, Barriers in the immature brain, Cell Mol. Neurobiol., 20, 29, 10.1023/A:1006991809927

Scheingold, 2001, Multidrug resistance gene expression during the murine ontogeny, Mech. Ageing Dev., 122, 255, 10.1016/S0047-6374(00)00223-2

Scholz, 2007, Neutrophils and the blood–brain barrier dysfunction after trauma, Med. Res. Rev., 27, 401, 10.1002/med.20064

Schwaninger, 1999, Bradykinin induces interleukin-6 expression in astrocytes through activation of nuclear factor-KB, J. Neurochem., 73, 1461, 10.1046/j.1471-4159.1999.0731461.x

Schwartz, 2006, Microglial phenotype: is the commitment reversible?, Trends Neurosci, 29, 68, 10.1016/j.tins.2005.12.005

Shimizu, 2008, Peripheral nerve pericytes originating from the blood–nerve barrier expresses tight junctional molecules and transporters as barrier-forming cells, J. Cell Physiol., 217, 388, 10.1002/jcp.21508

Somjen, 2004

Stern, 2002, Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings, Adv. Drug Deliv. Rev., 54, 1615, 10.1016/S0169-409X(02)00160-6

Stewart, 2000, Endothelial vesicles in the blood–brain barrier: are they related to permeability?, Cell. Mol. Neurobiol., 20, 149, 10.1023/A:1007026504843

Tai, 2009, P-glycoprotein and breast cancer resistance protein restrict apical-to-basolateral permeability of human brain endothelium to amyloid-β, J. Cereb. Blood Flow Metab., 29, 1079, 10.1038/jcbfm.2009.42

Talukder, 2003, Receptor-mediated transport of lactoferrin into the cerebrospinal fluid via plasma in young calves, J. Vet. Med. Sci., 65, 957, 10.1292/jvms.65.957

Tauc, 1984, Evidence for the effectiveness of the blood–CSF barrier in the fetal rat choroid plexus. A freeze-fracture and peroxidase diffusion study, Tissue Cell, 16, 65, 10.1016/0040-8166(84)90019-3

Tomás-Camardiel, 2005, Blood–brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals, J. Neurosci. Res., 80, 235, 10.1002/jnr.20443

Tran, 1999, Transforming growth factor-β mediates astrocyte-specific regulation of brain endothelial anticoagulant factors, Stroke, 30, 1671, 10.1161/01.STR.30.8.1671

Vakili, 2005, Role of arginine vasopressin V(1) and V(2) receptors for brain damage after transient focal cerebral ischemia, J. Cereb. Blood Flow Metab., 25, 1012, 10.1038/sj.jcbfm.9600097

Veldhuis, 2003, Interferon-beta prevents cytokine-induced neutrophil infiltration and attenuates blood–brain barrier disruption, J. Cereb. Blood Flow Metab., 23, 1060, 10.1097/01.WCB.0000080701.47016.24

Virgintino, 2004, Immunolocalisation of tight junction proteins in the adult and developing human brain, Histochem. Cell Biol., 122, 51, 10.1007/s00418-004-0665-1

Visser, 2004, Characterisation of the transferrin receptor on brain capillary endothelial cells, Pharm. Res., 21, 761, 10.1023/B:PHAM.0000026425.69874.8e

Volkov, 1997, Two mechanisms of permeation of small neutral molecules and hydrated ions across phospholipid bilayers, Bioelectrochem. Bioenergetics, 42, 153, 10.1016/S0302-4598(96)05097-0

Waterhouse, 2003, Determination of lipophilicity and its use as a predictor of blood–brain barrier penetration of molecular imaging agents, Molec. Imag. Biol., 5, 376, 10.1016/j.mibio.2003.09.014

Warth, 2004, Redistribution of aquaporin-4 in human glioblastoma correlates with loss of agrin immunoreactivity from brain capillary basal laminae, Acta Neuropath., 107, 311, 10.1007/s00401-003-0812-0

Willis, 2008, Chronic inflammatory pain and the neurovascular unit: a central role for glia in maintaining BBB integrity?, Curr. Pharm. Des., 14, 1625, 10.2174/138161208784705414

Wolburg, 2006, The endothelial frontier, 77

Wolburg, 2002, Tight junctions of the blood–brain barrier: development, composition and regulation, Vascul. Pharmacol., 38, 323, 10.1016/S1537-1891(02)00200-8

Wolburg, 2009, Brain endothelial cells and the glio–vascular complex, Cell Tissue Res., 335, 75, 10.1007/s00441-008-0658-9

Wolburg, 2005, Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves the tight junctions intact, Acta Neuropathol., 109, 181, 10.1007/s00401-004-0928-x

Wolburg, 2003, Localization of claudin-3 in tight junctions of the blood–brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme, Acta Neuropath., 105, 586, 10.1007/s00401-003-0688-z

Zhang, 2002, Structural biology and function of solute transporters: implications for identifying and designing substrates, Drug Metab. Rev., 34, 709, 10.1081/DMR-120015692

Zlokovic, 2008, The blood–brain barrier in health and chronic neurodegenerative disorders, Neuron, 57, 178, 10.1016/j.neuron.2008.01.003

Zlokovic, 1990, A saturable mechanism for transport of immunoglobulin G across the blood–brain barrier of the guinea pig, Exp. Neurol., 107, 263, 10.1016/0014-4886(90)90144-H

Zlokovic, 2005, Neurovascular mechanisms of Alzheimer's neurodegeneration, Trends Neurosci., 28, 202, 10.1016/j.tins.2005.02.001