The blood-brain barrier in systemic inflammation

Abbott, 2000, Inflammatory mediators and modulation of blood-brain barrier permeability, Cell. Mol. Neurobiol., 20, 131, 10.1023/A:1007074420772 Agrawal, 2006, Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis, J. Exp. Med., 203, 1007, 10.1084/jem.20051342 Ahn, 2008, Human microglial cells synthesize albumin in brain, PLoS ONE, 3, e2829, 10.1371/journal.pone.0002829 Akaishi, 2015, Importance of the quotient of albumin, quotient of immunoglobulin G and Reibergram in inflammatory neurological disorders with disease-specific patterns of blood-brain barrier permeability, Neurol. Clin. Neurosci., 3, 94, 10.1111/ncn3.158 Akanuma, 2011, Attenuation of prostaglandin E2 elimination across the mouse blood-brain barrier in lipopolysaccharide-induced inflammation and additive inhibitory effect of cefmetazole, Fluids Barriers CNS, 8, 24, 10.1186/2045-8118-8-24 Allen, 1965, The effect of bacterial pyrogen on the blood-brain barrier for trypan blue, J. Pathol. Bacteriol., 89, 481, 10.1002/path.1700890205 Alvarez, 2015, Focal disturbances in the blood–brain barrier are associated with formation of neuroinflammatory lesions, Neurobiol. Dis., 74, 14, 10.1016/j.nbd.2014.09.016 Asgari, 2015, Cerebrospinal fluid aquaporin-4-immunoglobulin G disrupts blood brain barrier, Ann. Clin. Transl. Neurol., 2, 857, 10.1002/acn3.221 Banks, 2005, Blood-brain barrier transport of cytokines: a mechanism for neuropathology, Curr. Pharm. Des., 11, 973, 10.2174/1381612053381684 Banks, 1999, Adsorptive endocytosis of HIV-1gp120 by blood-brain barrier is enhanced by lipopolysaccharide, Exp. Neurol., 156, 165, 10.1006/exnr.1998.7011 Banks, 2012, Pharmacokinetics and modeling of immune cell trafficking: quantifying differential influences of target tissues versus lymphocytes in SJL and lipopolysaccharide-treated mice, J. Neuroinflammation, 9, 231, 10.1186/1742-2094-9-231 Banks, 2015, Lipopolysaccharide-induced blood-brain barrier disruption: roles of cyclooxygenase, oxidative stress, neuroinflammation, and elements of the neurovascular unit, J. Neuroinflammation, 12, 223, 10.1186/s12974-015-0434-1 Barkalow, 1996, Brain endothelium lack one of two pathways of P-selectin-mediated neutrophil adhesion, Blood, 88, 4585, 10.1182/blood.V88.12.4585.bloodjournal88124585 Bechmann, 2007, What is the blood–brain barrier (not)?, Trends Immunol., 28, 5, 10.1016/j.it.2006.11.007 Bickel, 1998, No increase in blood-brain barrier permeability after intraperitoneal injection of endotoxin in the rat, J. Neuroimmunol., 85, 131, 10.1016/S0165-5728(98)00004-6 Biesmans, 2013, Systemic immune activation leads to neuroinflammation and sickness behavior in mice, Mediators Inflamm., 5, 271359 Blom, 2015, Human severe sepsis cytokine mixture increases β2-integrin-dependent polymorphonuclear leukocyte adhesion to cerebral microvascular endothelial cells in vitro, Crit. Care, 19, 149, 10.1186/s13054-015-0883-z Bö, 1996, Distribution of immunoglobulin superfamily members ICAM-1, -2, -3, and the beta 2 integrin LFA-1 in multiple sclerosis lesions, J. Neuropathol. Exp. Neurol., 55, 1060, 10.1097/00005072-199655100-00006 Bohatschek, 2001, Systemic LPS injection leads to granulocyte influx into normal and injured brain: effects of ICAM-1 deficiency, Exp. Neurol., 172, 137, 10.1006/exnr.2001.7764 Booth, 2012, Characterization of a microfluidic in vitro model of the blood-brain barrier (μBBB), Lab Chip, 12, 1784, 10.1039/c2lc40094d Buljevac, 2002, Prospective study on the relationship between infections and multiple sclerosis exacerbations, Brain, 125, 952, 10.1093/brain/awf098 Bush, 1999, Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice, Neuron, 23, 297, 10.1016/S0896-6273(00)80781-3 Cao, 1995, Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain; its possible role in the febrile response, Brain Res., 697, 187, 10.1016/0006-8993(95)00839-I Cardoso, 2010, Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches, Brain Res. Rev., 64, 328, 10.1016/j.brainresrev.2010.05.003 Cardoso, 2012, Exposure to lipopolysaccharide and/or unconjugated bilirubin impair the integrity and function of brain microvascular endothelial cells, PLoS ONE, 7, e35919, 10.1371/journal.pone.0035919 Cardoso, 2015, Systemic inflammation in early neonatal mice induces transient and lasting neurodegenerative effects, J. Neuroinflammation, 12, 82, 10.1186/s12974-015-0299-3 Carvalho-Tavares, 2000, A role for platelets and endothelial selectins in tumor necrosis factor-alpha-induced leukocyte recruitment in the brain microvasculature, Circ. Res., 87, 1141, 10.1161/01.RES.87.12.1141 Chappell, 2008, Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx, Biol. Chem., 389, 79, 10.1515/BC.2008.005 Choi, 1986, Phenylalanine transport at the human blood-brain barrier. Studies with isolated human brain capillaries, J. Biol. Chem., 261, 6536, 10.1016/S0021-9258(19)84595-7 Chui, 2010, Regulation of CCL2 and CCL3 expression in human brain endothelial cells by cytokines and lipopolysaccharide, J. Neuroinflammation, 7, 1, 10.1186/1742-2094-7-1 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, 2006, The risk of relapses in multiple sclerosis during systemic infections, Neurology, 67, 652, 10.1212/01.wnl.0000233834.09743.3b Cramer, 2014, Abnormal blood-brain barrier permeability in normal appearing white matter in multiple sclerosis investigated by MRI., Neuroimage Clin., 4, 182, 10.1016/j.nicl.2013.12.001 Daniels, 2014, Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals, mBio, 5, 10.1128/mBio.01476-14 de Vries, 1996, Effect of endotoxin on permeability of bovine cerebral endothelial cell layers in vitro, J. Pharmacol. Exp. Ther., 277, 1418 de Vries, 1996, The influence of cytokines on the integrity of the blood-brain barrier in vitro, J. Neuroimmunol., 64, 37, 10.1016/0165-5728(95)00148-4 Denes, 2011, Systemic inflammatory challenges compromise survival after experimental stroke via augmenting brain inflammation, blood- brain barrier damage and brain oedema independently of infarct size, J. Neuroinflammation, 8, 164, 10.1186/1742-2094-8-164 Dinges, 2001, Comparative analysis of lipopolysaccharide-induced tumor necrosis factor alpha activity in serum and lethality in mice and rabbits pretreated with the staphylococcal superantigen toxic shock syndrome toxin 1, Infect. Immun., 69, 7169, 10.1128/IAI.69.11.7169-7172.2001 Dohgu, 2008, Lipopolysaccharide-enhanced transcellular transport of HIV-1 across the blood-brain barrier is mediated by the p38 mitogen-activated protein kinase pathway, Exp. Neurol., 210, 740, 10.1016/j.expneurol.2007.12.028 Dohgu, 2013, Brain pericytes increase the lipopolysaccharide-enhanced transcytosis of HIV-1 free virus across the in vitro bloodbrain barrier: evidence for cytokine-mediated pericyte-endothelial cell crosstalk, Fluids Barriers CNS, 10, 1, 10.1186/2045-8118-10-23 Dohgu, 2011, Lipopolysaccharide-enhanced transcellular transport of HIV-1 across the blood-brain barrier is mediated by luminal microvessel IL-6 and GM-CSF, J. Neuroinflammation, 8, 167, 10.1186/1742-2094-8-167 Doll, 2015, Mitochondrial crisis in cerebrovascular endothelial cells opens the blood-brain barrier, Stroke, 46, 1681, 10.1161/STROKEAHA.115.009099 du Moulin, 1985, E. coli peritonitis and bacteremia cause increased blood-brain barrier permeability, Brain Res., 340, 261, 10.1016/0006-8993(85)90922-9 Erickson, 2013, Blood-brain barrier dysfunction as a cause and consequence of Alzheimer’s disease, J. Cereb. Blood Flow Metab., 33, 1500, 10.1038/jcbfm.2013.135 Erickson, 2012, Lipopolysaccharide impairs amyloid β efflux from brain: altered vascular sequestration, cerebrospinal fluid reabsorption, peripheral clearance and transporter function at the blood-brain barrier, J. Neuroinflammation, 9, 150, 10.1186/1742-2094-9-150 Ericsson, 1995, Type 1 interleukin-1 receptor in the rat brain: distribution, regulation, and relationship to sites of IL-1-induced cellular activation, J. Comp. Neurol., 361, 681, 10.1002/cne.903610410 Fabis, 2007, Loss of blood-brain barrier integrity in the spinal cord is common to experimental allergic encephalomyelitis in knockout mouse models, PNAS, 104, 5656, 10.1073/pnas.0701252104 Fan, 2014, Systemic inflammation induces a profound long term brain cell injury in rats, Acta. Neurobiol. Exp. (Wars.), 74, 298 Farkas, 1998, Experimental acute pancreatitis results in increased blood–brain barrier permeability in the rat: a potential role for tumor necrosis factor and interleukin 6, Neuroscience, 242, 147 Förster, 2008, Differential effects of hydrocortisone and TNFalpha on tight junction proteins in an in vitro model of the human blood-brain barrier, J. Physiol. (Lond.), 586, 1937, 10.1113/jphysiol.2007.146852 Gaillard, 2003, Pharmacological investigations on lipopolysaccharide-induced permeability changes in the blood-brain barrier in vitro, Microvasc. Res., 65, 24, 10.1016/S0026-2862(02)00009-2 Gregorius, 1976, Pathologenesis of hematogenous bacterial meningitis in rabbits, J. Neurosurg., 45, 561, 10.3171/jns.1976.45.5.0561 Han, 2016, Clematichinenoside protects blood brain barrier against ischemic stroke superimposed on systemic inflammatory challenges through up-regulating A20, Brain Behav. Immun., 51, 56, 10.1016/j.bbi.2015.07.025 Hart, 1988, Biological basis of the behavior of sick animals, Neurosci. Biobehav. Rev., 12, 123, 10.1016/S0149-7634(88)80004-6 Hartz, 2006, Rapid modulation of P-glycoprotein-mediated transport at the blood-brain barrier by tumor necrosis factor-alpha and lipopolysaccharide, Mol. Pharmacol., 69, 462, 10.1124/mol.105.017954 Hathaway, 1999, Experimental colitis increases blood-brain barrier permeability in rabbits, Am. J. Physiol., 276, G1174 He, 2011, RhoA and NF-κB are involved in lipopolysaccharide-induced brain microvascular cell line hyperpermeability, Neuroscience, 188, 35, 10.1016/j.neuroscience.2011.04.025 He, 2014, Cell-culture models of the blood-brain barrier, Stroke, 45, 2514, 10.1161/STROKEAHA.114.005427 Helms, 2016, In vitro models of the blood-brain barrier: an overview of commonly used brain endothelial cell culture models and guidelines for their use., J. Cereb. Blood Flow Metab., 10.1177/0271678X16630991 Herkenham, 1998, Temporal and spatial patterns of c-fos mRNA induced by intravenous interleukin-1: a cascade of non-neuronal cellular activation at the blood-brain barrier, J. Comp. Neurol., 400, 175, 10.1002/(SICI)1096-9861(19981019)400:2<175::AID-CNE2>3.0.CO;2-6 Hill, 2000, Biochemical markers in acute ischemic stroke, CMAJ, 162, 1139 Hofer, 2008, Injury of the blood brain barrier and up-regulation of icam-1 in polymicrobial sepsis, J. Surg. Res., 146, 276, 10.1016/j.jss.2007.07.021 Holmes, 2009, Systemic inflammation and disease progression in Alzheimer disease, Neurology, 73, 768, 10.1212/WNL.0b013e3181b6bb95 Hoyer, 1991, Angiotensin II, vasopressin and GTP[gamma-S] inhibit inward-rectifying K+ channels in porcine cerebral capillary endothelial cells, J. Membr. Biol., 123, 55, 10.1007/BF01993963 Huber, 2002, Blood-brain barrier tight junctions are altered during a 72-h exposure to λ-carrageenan-induced inflammatory pain, Am. J. Physiol. Heart Circ. Physiol., 283, H1531, 10.1152/ajpheart.00027.2002 Iannotti, 1987, Simplified, noninvasive PET measurement of blood-brain barrier permeability, J. Comput. Assist. Tomogr., 11, 390, 10.1097/00004728-198705000-00004 Iwase, 2000, Induction of endothelial nitric-oxide synthase in rat brain astrocytes by systemic lipopolysaccharide treatment, J. Biol. Chem., 275, 11929, 10.1074/jbc.275.16.11929 Jaeger, 2009, Lipopolysaccharide alters the blood–brain barrier transport of amyloid β protein: a mechanism for inflammation in the progression of Alzheimer’s disease, Brain Behav. Immun., 23, 507, 10.1016/j.bbi.2009.01.017 Jeong, 2010, Systemic LPS administration induces brain inflammation but not dopaminergic neuronal death in the substantia nigra, Exp. Mol. Med., 42, 10.3858/emm.2010.42.12.085 Junker, 2009, MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47, Brain, 132, 3342, 10.1093/brain/awp300 Kapural, 2002, Serum S-100beta as a possible marker of blood-brain barrier disruption, Brain Res., 940, 102, 10.1016/S0006-8993(02)02586-6 Karahashi, 2009, Lipopolysaccharide-induced apoptosis in transformed bovine brain endothelial cells and human dermal microvessel endothelial cells: the role of JNK, J. Immunol., 182, 7280, 10.4049/jimmunol.0801376 Kastin, 2001, Validity of multiple-time regression analysis in measurement of tritiated and iodinated leptin crossing the blood-brain barrier: meaningful controls, Peptides, 22, 2127, 10.1016/S0196-9781(01)00569-1 Kerfoot, 2002, Overlapping roles of P-selectin and alpha 4 integrin to recruit leukocytes to the central nervous system in experimental autoimmune encephalomyelitis, J. Immunol., 169, 1000, 10.4049/jimmunol.169.2.1000 Knudsen, 1994, Application of the double-indicator technique for measurement of blood-brain barrier permeability in humans, Cerebrovasc. Brain Metab. Rev., 6, 1 Krumbholz, 2006, Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment, Brain, 129, 200, 10.1093/brain/awh680 Lee, 1991, Fluid replacement protection of rabbits challenged subcutaneous with toxic shock syndrome toxins, Infect. Immun., 59, 879, 10.1128/IAI.59.3.879-884.1991 Lipowsky, 2012, The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases, Ann. Biomed. Eng., 40, 840, 10.1007/s10439-011-0427-x Lopez-Ramirez, 2014, MicroRNA-155 negatively affects blood-brain barrier function during neuroinflammation, FASEB, 28, 2551, 10.1096/fj.13-248880 Lossinsky, 2004, Structural pathways for macromolecular and cellular transport across the blood-brain barrier during inflammatory conditions, Histol. Histopathol., 19, 535 Lustig, 1992, Viral neuroinvasion and encephalitis induced by lipopolysaccharide and its mediators, J. Exp. Med., 176, 707, 10.1084/jem.176.3.707 Maggioli, 2016, Estrogen protects the blood-brain barrier from inflammation-induced disruption and increased lymphocyte trafficking, Brain Behav. Immun., 51, 212, 10.1016/j.bbi.2015.08.020 Mato, 1998, Ultrastructural and immunohistochemical changes of fluorescent granular perithelial cells and the interaction of FGP cells to microglia after lipopolysaccharide administration, Anat. Rec., 251, 330, 10.1002/(SICI)1097-0185(199807)251:3<330::AID-AR8>3.0.CO;2-Z Minagar, 2003, Interferon (IFN)-beta 1a and IFN-beta 1b block IFN-gamma-induced disintegration of endothelial junction integrity and barrier, Endothelium, 10, 299, 10.1080/10623320390272299 Minami, 1998, Roles of nitric oxide and prostaglandins in the increased permeability of the blood-brain barrier caused by lipopolysaccharide, Environ. Toxicol. Pharmacol., 5, 35, 10.1016/S1382-6689(97)10004-7 Moore, 1988, Eicosanoid metabolism in cerebromicrovascular endothelium, Am. J. Physiol., 254, 37, 10.1152/ajpcell.1988.254.1.C37 Moreno, 2011, Systemic inflammation induces axon injury during brain inflammation, Ann. Neurol., 70, 932, 10.1002/ana.22550 Moseley, 1997, Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes, Biochim. Biophys. Acta, 1362, 221, 10.1016/S0925-4439(97)00083-5 Nadeau, 1999, Regulation of the gene encoding tumor necrosis factor alpha (TNF-alpha) in the rat brain and pituitary in response in different models of systemic immune challenge, J. Neuropathol. Exp. Neurol., 58, 61, 10.1097/00005072-199901000-00008 Natah, 2005, Disruption of the blood-brain barrier during TNBS colitis, Neurogastroenterol. Motil., 17, 433, 10.1111/j.1365-2982.2005.00654.x Nonaka, 2004, Effects of lipopolysaccharide on leptin transport across the blood–brain barrier, Brain Res., 1016, 58, 10.1016/j.brainres.2004.04.066 Nonaka, 2005, Effect of lipopolysaccharide on the transport of pituitary adenylate cyclase activating polypeptide across the blood-brain barrier, Exp. Neurol., 191, 137, 10.1016/j.expneurol.2004.09.013 Osburg, 2002, Effect of endotoxin on expression of TNF receptors and transport of TNF-α at the blood-brain barrier of the rat, Am. J. Physiol. Endocrinol. Metab., 283, E899, 10.1152/ajpendo.00436.2001 Oshima, 2009, Penetration of oseltamivir and its active metabolite into the brain after lipopolysaccharide-induced inflammation in mice, J. Pharm. Pharmacol., 61, 1397, 10.1211/jpp.61.10.0018 Ott, 2012, The viral mimetic polyinosinic:polycytidylic acid (poly I:C) induces cellular responses in primary cultures from rat brain sites with an incomplete blood-brain barrier, Neurosci. Lett., 530, 64, 10.1016/j.neulet.2012.09.038 Palasik, 2005, Assessment of relations between clinical outcome of ischemic stroke and activity of inflammatory processes in the acute phase based on examination of selected parameters, Eur. Neurol., 53, 188, 10.1159/000086355 Pan, 1996, Differential permeability of the BBB in acute EAE: enhanced transport of TNT-alpha, Am. J. Physiol., 271, E636 Pan, 2008, Neuroinflammation facilitates LIF entry into brain: role of TNF, Am. J. Physiol. Cell Physiol., 294, C1436, 10.1152/ajpcell.00489.2007 Papadopoulos, 1999, Faecal peritonitis causes oedema and neuronal injury in pig cerebral cortex, Clin. Sci., 96, 461, 10.1042/cs0960461 Pardridge, 1997, Brain microvascular and astrocyte localization of P-glycoprotein, J. Neurochem., 68, 1278, 10.1046/j.1471-4159.1997.68031278.x Patlak, 1983, Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data, J. Cereb. Blood Flow Metab., 3, 1, 10.1038/jcbfm.1983.1 Perry, 2014, Microglial priming in neurodegenerative disease, Nat. Rev. Neurol., 10, 217, 10.1038/nrneurol.2014.38 Pieper, 2013, Pericytes support neutrophil transmigration via interleukin-8 across a porcine co-culture model of the blood–brain barrier, Brain Res., 1524, 1, 10.1016/j.brainres.2013.05.047 Prat, 2005, Th1 and Th2 lymphocyte migration across the human BBB is specifically regulated by interferon β and copolymer-1, J. Autoimmun., 24, 119, 10.1016/j.jaut.2005.01.004 Qin, 2015, LPS induces occludin dysregulation in cerebral microvascular endothelial cells via MAPK signaling and augmenting MMP-2 levels, Oxid. Med. Cell. Longev., 10.1155/2015/120641 Quan, 2003, Endothelial activation is an intermediate step for peripheral lipopolysaccharide induced activation of paraventricular nucleus, Brain Res. Bull., 59, 447, 10.1016/S0361-9230(02)00951-6 Raj, 2015, Enhanced microglial pro-inflammatory response to lipopolysaccharide correlates with brain infiltration and blood-brain barrier dysregulation in a mouse model of telomere shortening, Aging Cell, 14, 1003, 10.1111/acel.12370 Sánchez del Pino, 1992, Neutral amino acid transport by the blood-brain barrier. Membrane vesicle studies, J. Biol. Chem., 267, 25951, 10.1016/S0021-9258(18)35701-6 Sandoval, 2008, Blood-brain barrier tight junction permeability and ischemic stroke, Neurobiol. Dis., 32, 200, 10.1016/j.nbd.2008.08.005 Serres, 2009, Systemic inflammatory response reactivates immune-mediated lesions in rat brain, J. Neurosci., 29, 4820, 10.1523/JNEUROSCI.0406-09.2009 Sharshar, 2007, Brain lesions in septic shock: a magnetic resonance imaging study, Intensive Care Med., 33, 798, 10.1007/s00134-007-0598-y Skelly, 2013, A systematic analysis of the peripheral and CNS effects of systemic LPS, IL-1B, TNF-α and IL-6 challenges in C57BL/6 mice, PLoS ONE, 8, 10.1371/journal.pone.0069123 Sofroniew, 2015, Astrocyte barriers to neurotoxic inflammation, Nat. Rev. Neurosci., 16, 249, 10.1038/nrn3898 Stanness, 1997, Morphological and functional characterization of an in vitro blood-brain barrier model, Brain Res., 771, 329, 10.1016/S0006-8993(97)00829-9 Stolp, 2005, Breakdown of the blood-brain barrier to proteins in white matter of the developing brain following systemic inflammation, Cell Tissue Res., 320, 369, 10.1007/s00441-005-1088-6 Takeda, 2013, Increased blood-brain barrier vulnerability to systemic inflammation in an Alzheimer disease mouse model, Neurobiol. Aging, 34, 2064, 10.1016/j.neurobiolaging.2013.02.010 Tarbell, 2010, Shear stress and the endothelial transport barrier, Cardiovasc. Res., 87, 320, 10.1093/cvr/cvq146 Tran, 1998, Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice, J. Immunol., 161, 3767, 10.4049/jimmunol.161.7.3767 Tsao, 2001, Tumour necrosis factor-alpha causes an increase in blood-brain barrier permeability during sepsis, J. Med. Microbiol., 50, 812, 10.1099/0022-1317-50-9-812 Tunkel, 1991, Blood-brain barrier alterations in bacterial meningitis: development of an in vitro model and observations on the effects of lipopolysaccharide, Vitro Cell Dev. Biol., 27, 113, 10.1007/BF02630996 Urayama, 2015, Pharmacologic manipulation of lysosomal enzyme transport across the blood-brain barrier, J. Cereb. Blood Flow Metab. Vallières, 1997, Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta, J. Neurochem., 69, 1668, 10.1046/j.1471-4159.1997.69041668.x van Vliet, 2007, Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy, Brain, 130, 521, 10.1093/brain/awl318 Vasilache, 2015, Immune challenge by intraperitoneal administration of lipopolysaccharide directs gene expression in distinct blood-brain barrier cells toward enhanced prostaglandin E2 signalling, Brain Behav. Immun., 48, 31, 10.1016/j.bbi.2015.02.003 Wang, 2004, Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis, Nat. Med., 10, 1366, 10.1038/nm1140 Wang, 2008, Human immunodeficiency virus type 1 infection increases the in vivo capacity of peripheral monocytes to cross the blood-brain barrier into the brain and the in vivo sensitivity of the blood-brain barrier to disruption by lipopolysaccharide, J. Virol., 82, 7591, 10.1128/JVI.00768-08 Weintraub, 2014, Peripheral administration of poly I: C leads to increased hippocampal amyloid-beta and cognitive deficits in a non-transgenic mouse, Behav. Brain Res., 266, 183, 10.1016/j.bbr.2014.03.009 Wiesinger, 2013, Nanomechanics of the endothelial glycocalyx during experimental sepsis, PLoS ONE, 8, 10.1371/journal.pone.0080905 Wittmann, 2015, Parallel regulation of thyroid hormone transporters OATP1c1 and MCT8 during and after endotoxemia at the blood-brain barrier of male rodents, Endocrinology, 156, 1552, 10.1210/en.2014-1830 Wittmann, 2015, Endotoxin-induced inflammation down-regulates l-type amino acid transporter 1 (LAT1) expression at the blood–brain barrier of male rats and mice, Fluids Barriers CNS, 12, 21, 10.1186/s12987-015-0016-8 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 Neuropathol., 105, 586, 10.1007/s00401-003-0688-z Wolburg, 2005, Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact, Acta Neuropathol., 109, 181, 10.1007/s00401-004-0928-x Wong, 2004, Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier, Exp. Neurol., 190, 446, 10.1016/j.expneurol.2004.08.008 Woodcock, 2012, Revised Starling equation and the glycocalyx model of transvascular fluid exchange: an improved paradigm for prescribing intravenous fluid therapy, Br. J. Anaesth., 108, 384, 10.1093/bja/aer515 Wu, 2015, Effects of lipopolysaccharide on the expression of plasma membrane monoamine transporter (PMAT) at the blood-brain barrier and its implications to the transport of neurotoxins, J. Neurochem., 135, 1178, 10.1111/jnc.13363 Xaio, 2001, Effect of LPS on the permeability of the blood-brain barrier to insulin, Brain Res., 896, 36, 10.1016/S0006-8993(00)03247-9 Yan, 2004, Cerebrovascular responses in the fetal sheep brain to low-dose endotoxin, Pediatr. Res., 55, 855, 10.1203/01.PDR.0000115681.95957.D4 Yang, 2015, Simvastatin attenuates sepsis-induced blood-brain barrier integrity loss, J. Surg. Res., 194, 591, 10.1016/j.jss.2014.11.030 Young, 1992, The electroencephalogram in sepsis-associated encephalopathy, J. Clin. Neurophysiol., 9, 145, 10.1097/00004691-199201000-00016 Yu, 2015, Activation of AMPK improves lipopolysaccharide-induced dysfunction of the blood-brain barrier in mice, Brain Inj., 29, 777, 10.3109/02699052.2015.1004746 Zamanian, 2012, Genomic analysis of reactive astrogliosis, J. Neurosci., 32, 6391, 10.1523/JNEUROSCI.6221-11.2012 Zhou, 2006, A requirement for microglial TLR4 in leukocyte recruitment into brain in response to lipopolysaccharide, J. Immunol., 177, 8103, 10.4049/jimmunol.177.11.8103 Zhou, 2009, Role of endothelial TLR4 for neutrophil recruitment into central nervous system microvessels in systemic inflammation, J. Immunol., 183, 5244, 10.4049/jimmunol.0901309 Zhou, 2014, Blood-brain barrier dysfunction in mice induced by lipopolysaccharide is attenuated by dapsone, Biochem. Biophys. Res. Commun., 453, 419, 10.1016/j.bbrc.2014.09.093 Zimmer, 2011, Activation of endothelial toll-like receptor 3 impairs endothelial function, Circ. Res., 108, 1358, 10.1161/CIRCRESAHA.111.243246