Blood-brain barrier alterations in ageing and dementia

Journal of the Neurological Sciences - Tập 283 - Trang 99-106 - 2009
Bogdan O. Popescu1,2, Emil C. Toescu3, Laurenţiu M. Popescu1, Ovidiu Bajenaru2, Dafin F. Muresanu4, Marianne Schultzberg5, Nenad Bogdanovic6
1Laboratory of Molecular Medicine, ‘Victor Babeş’ National Institute of Pathology, Bucharest 050096, Romania
2Department of Neurology, University Hospital Bucharest, ‘Carol Davila’ University of Medicine and Pharmacy, Bucharest 050098, Romania
3Department of Physiology, Division of Medical Sciences, The Medical School, University of Birmingham, Birmingham B15 2TT, UK
4Department of Neurology, ‘Iuliu Hatieganu’ University of Medicine and Pharmacy, Cluj Napoca 400023, Romania
5Division of Neurodegeneration, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Stockholm SE-141 86, Sweden
6Alzheimer's Disease Research Center, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Stockholm SE-141 86, Sweden

Tài liệu tham khảo

Bandopadhyay, 2001, Contractile proteins in pericytes at the blood-brain and blood-retinal barriers, J Neurocytol, 30, 35, 10.1023/A:1011965307612 Abbott, 2006, Astrocyte–endothelial interactions at the blood-brain barrier, Nat Rev Neurosci, 7, 41, 10.1038/nrn1824 Kniesel, 2000, Tight junctions of the blood-brain barrier, Cell Mol Neurobiol, 20, 57, 10.1023/A:1006995910836 Furuse, 1993, Occludin: a novel integral membrane protein localizing at tight junctions, J Cell Biol, 123, 1777, 10.1083/jcb.123.6.1777 Furuse, 1998, Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin, J Cell Biol, 141, 1539, 10.1083/jcb.141.7.1539 Martìn-Padura, 1998, Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration, J Cell Biol, 142, 117, 10.1083/jcb.142.1.117 Persidsky, 2006, Blood-brain barrier: structural components and function under physiologic and pathologic conditions, J Neuroimmunol Pharmacol, 1, 223, 10.1007/s11481-006-9025-3 Butt, 1990, Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study, J Physiol, 429, 47, 10.1113/jphysiol.1990.sp018243 Thuerauf, 2006, The role of the transporter P-glycoprotein for disposition and effects of centrally acting drugs and for the pathogenesis of CNS diseases, Eur Arch Psychiatry Clin Neurosci, 256, 281, 10.1007/s00406-006-0662-6 Nielsen, 1997, Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain, J Neurosci, 17, 171, 10.1523/JNEUROSCI.17-01-00171.1997 Yool, 2007, Aquaporins: multiple roles in the central nervous system, Neuroscientist, 13, 470, 10.1177/1073858407303081 Minn, 1991, Drug metabolizing enzymes in the brain and cerebral microvessels, Brain Res Brain Res Rev, 16, 65, 10.1016/0165-0173(91)90020-9 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 Ramsauer, 2002, Angiogenesis of the blood-brain barrier in vitro and the function of cerebral pericytes, FASEB J, 16, 1274, 10.1096/fj.01-0814fje Kose, 2007, Altered expression of basement membrane-related molecules in rat brain pericyte, endothelial, and astrocyte cell lines after transforming growth factor-beta1 treatment, Drug Metab Pharmacokinet, 22, 255, 10.2133/dmpk.22.255 Góra-Kupilas, 2005, The neuroprotective function of vascular endothelial growth factor (VEGF), Folia Neuropathol, 43, 31 Su, 2006, Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings, J Neurol Sci, 243, 21, 10.1016/j.jns.2005.11.006 Sobue, 1999, Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors, Neurosci Res, 35, 155, 10.1016/S0168-0102(99)00079-6 Utsumi, 2000, Expression of GFRalpha-1, receptor for GDNF, in rat brain capillary during postnatal development of the BBB, Am J Physiol Cell Physiol, 279, C361, 10.1152/ajpcell.2000.279.2.C361 Braet, 2004, Calcium signal communication in the central nervous system, Biol Cell, 96, 79, 10.1016/j.biolcel.2003.10.007 Simard, 2003, Signaling at the gliovascular interface, J Neurosci, 23, 9254, 10.1523/JNEUROSCI.23-27-09254.2003 Wosik, 2007, Death receptor expression and function at the human blood brain barrier, J Neurol Sci, 259, 53, 10.1016/j.jns.2006.08.018 Yu, 2007, TNF activates P-glycoprotein in cerebral microvascular endothelial cells, Cell Physiol Biochem, 20, 853, 10.1159/000110445 Simpson, 2007, White matter lesions in an unselected cohort of the elderly: astrocytic, microglial and oligodendrocyte precursor cell responses, Neuropathol Appl Neurobiol, 33, 410, 10.1111/j.1365-2990.2007.00828.x Frisoni, 2007, The effect of white matter lesions on cognition in the elderly—small but detectable, Nat Clin Pract Neurol, 3, 620, 10.1038/ncpneuro0638 Farrall, 2007, Blood-brain barrier: ageing and microvascular disease — systematic review and meta-analysis, Neurobiol Aging Hosokawa, 1999, Aging of blood-brain barrier and neuronal cells of eye and ear in SAM mice, Neurobiol Aging, 20, 117, 10.1016/S0197-4580(99)00029-9 Vorbrodt, 1995, A quantitative immunocytochemical study of blood-brain barrier to endogenous albumin in cerebral cortex and hippocampus of senescence-accelerated mice (SAM), Folia Histochem Cytobiol, 33, 229 Pelegrí, 2007, Increased permeability of blood-brain barrier on the hippocampus of a murine model of senescence, Mech Ageing Dev, 128, 522, 10.1016/j.mad.2007.07.002 Yasui, 2003, Brain lipid hydroperoxide level increases in senescence-accelerated mice at an early age, Neurosci Lett, 350, 66, 10.1016/S0304-3940(03)00827-9 Alvarez-García, 2006, Elevated oxidative stress in the brain of senescence-accelerated mice at 5 months of age, Biogerontology, 7, 43, 10.1007/s10522-005-6041-2 Kurokawa, 2001, Age-related changes in manganese superoxide dismutase activity in the cerebral cortex of senescence-accelerated prone and resistant mouse, Neurosci Lett, 298, 135, 10.1016/S0304-3940(00)01755-9 Okatani, 2002, Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse, Neurobiol Aging, 23, 639, 10.1016/S0197-4580(02)00005-2 Morley, 2000, Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory, Peptides, 21, 1761, 10.1016/S0196-9781(00)00342-9 Chan-Ling, 2007, Inflammation and breakdown of the blood-retinal barrier during “physiological aging” in the rat retina: a model for CNS aging, Microcirculation, 14, 63, 10.1080/10739680601073451 Dringen, 2005, Oxidative and antioxidative potential of brain microglial cells, Antioxid Redox Signal, 7, 1223, 10.1089/ars.2005.7.1223 Banks, 2001, Regional transport of TNF-alpha across the blood-brain barrier in young ICR and young and aged SAMP8 mice, Neurobiol Aging, 22, 671, 10.1016/S0197-4580(01)00220-2 McLay, 2000, Passage of interleukin-1-beta across the blood-brain barrier is reduced in aged mice: a possible mechanism for diminished fever in aging, Neuroimmunomodulation, 8, 148, 10.1159/000054275 Vorbrodt, 1999, Immunogold study of regional differences in the distribution of glucose transporter (GLUT-1) in mouse brain associated with physiological and accelerated aging and scrapie infection, J Neurocytol, 28, 711, 10.1023/A:1007034003114 Gschanes, 2000, The drug cerebrolysin and its peptide fraction E021 increase the abundance of the blood-brain barrier GLUT1 glucose transporter in brains of young and old rats, Histochem J, 32, 71, 10.1023/A:1004003008683 Connor, 1990, Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains, J Neurosci Res, 27, 595, 10.1002/jnr.490270421 Jeong, 2006, Age-related changes in iron homeostasis and cell death in the cerebellum of ceruloplasmin-deficient mice, J Neurosci, 26, 9810, 10.1523/JNEUROSCI.2922-06.2006 Aisen, 2001, Chemistry and biology of eukaryotic iron metabolism, Int J Biochem Cell Biol, 33, 940, 10.1016/S1357-2725(01)00063-2 Moos, 2001, Expression of transferrin mRNA in rat oligodendrocytes is iron-independent and changes with increasing age, Nutr Neurosci, 4, 15, 10.1080/1028415X.2001.11747347 Dringen, 2007, The pivotal role of astrocytes in the metabolism of iron in the brain, Neurochem Res, 32, 1884, 10.1007/s11064-007-9375-0 Toornvliet, 2006, Effect of age on functional P-glycoprotein in the blood-brain barrier measured by use of (R)-[(11)C]verapamil and positron emission tomography, Clin Pharmacol Ther, 79, 540, 10.1016/j.clpt.2006.02.004 Bake, 2004, 17beta-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats, Endocrinology, 145, 5471, 10.1210/en.2004-0984 Gustafson, 2007, Mid-life adiposity factors relate to blood-brain barrier integrity in late life, J Intern Med, 262, 643, 10.1111/j.1365-2796.2007.01869.x Dietrich, 2007, Megalin mediates the transport of leptin across the blood-CSF barrier, Neurobiol Aging Banks, 2003, Impaired transport of leptin across the blood-brain barrier in obesity is acquired and reversible, Am J Physiol Endocrinol Metab, 285, E10, 10.1152/ajpendo.00468.2002 Muzumdar, 2006, Central resistance to the inhibitory effects of leptin on stimulated insulin secretion with aging, Neurobiol Aging, 27, 1308, 10.1016/j.neurobiolaging.2005.07.007 Messier, 2005, The role of insulin, insulin growth factor, and insulin-degrading enzyme in brain aging and Alzheimer's disease, Neural Plast, 12, 311, 10.1155/NP.2005.311 Shiiki, 2004, Brain insulin impairs amyloid-beta(1–40) clearance from the brain, J Neurosci, 24, 9632, 10.1523/JNEUROSCI.2236-04.2004 Korczyn, 2007, The prevention of the dementia epidemic, J Neurol Sci, 257, 2, 10.1016/j.jns.2007.01.081 Hajjar, 2005, Antihypertensive agents for aging patients who are at risk for cognitive dysfunction, Curr Hypertens Rep, 7, 466, 10.1007/s11906-005-0043-y Wardlaw, 2003, Is breakdown of the blood-brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia?, Stroke, 34, 806, 10.1161/01.STR.0000058480.77236.B3 Hom, 2007, Comparative changes in the blood-brain barrier and cerebral infarction of SHR and WKY rats, Am J Physiol Regul Integr Comp Physiol, 292, R1881, 10.1152/ajpregu.00761.2005 Qi, 2008, Sustained pharmacological inhibition of deltaPKC protects against hypertensive encephalopathy through prevention of blood-brain barrier breakdown in rats, J Clin Invest, 118, 173 Chou, 2008, Hypertensive encephalopathy and the blood-brain barrier: is deltaPKC a gatekeeper?, J Clin Invest, 118, 17, 10.1172/JCI34516 Bright, 2007, DeltaPKC mediates microcerebrovascular dysfunction in acute ischemia and in chronic hypertensive stress in vivo, Brain Res, 1144, 146, 10.1016/j.brainres.2007.01.113 Siflinger-Birnboim, 2003, Protein kinase C modulates pulmonary endothelial permeability: a paradigm for acute lung injury, Am J Physiol Lung Cell Mol Physiol, 284, L435, 10.1152/ajplung.00106.2002 Ramírez, 1996, Protein kinase C modulates microvascular permeability through nitric oxide synthase, Am J Physiol, 271, H1702 Euser, 2008, Magnesium sulphate treatment decreases blood-brain barrier permeability during acute hypertension in pregnant rats, Exp Physiol, 93, 254, 10.1113/expphysiol.2007.039966 Muresanu, 2007, Chronic hypertension aggravates heat stress induced cognitive dysfunction and brain pathology: an experimental study in the rat, using growth hormone therapy for possible neuroprotection, Ann N Y Acad Sci, 1122, 1, 10.1196/annals.1403.001 Ott, 1996, Association of diabetes mellitus and dementia: the Rotterdam Study, Diabetologia, 39, 1392, 10.1007/s001250050588 Yoshitake, 1995, Incidence and risk factors of vascular dementia and Alzheimer's disease in a defined elderly Japanese population: the Hisayama Study, Neurology, 45, 1161, 10.1212/WNL.45.6.1161 Hawkins, 2008, Pathophysiology of the blood-brain barrier: animal models and methods, Curr Top Dev Biol, 80, 277, 10.1016/S0070-2153(07)80007-X Hou, 2007, Influence of blood glucose on the expression of glucose trans-porter proteins 1 and 3 in the brain of diabetic rats, Chin Med J (Engl), 120, 1704, 10.1097/00029330-200710010-00013 Maeng, 2007, Functional induction of P-glycoprotein in the blood-brain barrier of streptozotocin-induced diabetic rats: evidence for the involvement of nuclear factor-kappaB, a nitrosative stress-sensitive transcription factor, in the regulation, Drug Metab Dispos, 35, 1996, 10.1124/dmd.107.015800 Hawkins, 2007, Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases, Diabetologia, 50, 202, 10.1007/s00125-006-0485-z Romanitan, 2007, Occludin is overexpressed in Alzheimer's disease and vascular dementia, J Cell Mol Med, 11, 569, 10.1111/j.1582-4934.2007.00047.x Huber, 2006, Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats, Am J Physiol Heart Circ Physiol, 291, H2660, 10.1152/ajpheart.00489.2006 Savidge, 2007, Starring roles for astroglia in barrier pathologies of gut and brain, Lab Invest, 87, 731, 10.1038/labinvest.3700600 Stella, 2007, Risk factors for vascular dementia in elderly psychiatric outpatients with preserved cognitive functions, J Neurol Sci, 257, 247, 10.1016/j.jns.2007.01.035 Björkhem, 2004, Brain cholesterol: long secret life behind a barrier, Arterioscler Thromb Vasc Biol, 24, 806, 10.1161/01.ATV.0000120374.59826.1b Pfrieger, 2003, Cholesterol homeostasis and function in neurons of the central nervous system, Cell Mol Life Sci, 60, 1158, 10.1007/s00018-003-3018-7 Björkhem, 2006, Crossing the barrier: oxysterols as cholesterol transporters and metabolic modulators in the brain, J Intern Med, 260, 493, 10.1111/j.1365-2796.2006.01725.x Ghribi, 2006, Deposition of iron and beta-amyloid plaques is associated with cortical cellular damage in rabbits fed with long-term cholesterol-enriched diets, J Neurochem, 99, 438, 10.1111/j.1471-4159.2006.04079.x Crisby, 2004, Effects of high cholesterol diet on gliosis in apolipoprotein E knockout mice. Implications for Alzheimer's disease and stroke, Neurosci Lett, 369, 87, 10.1016/j.neulet.2004.05.057 Rahman, 2005, High cholesterol diet results in increased expression of interleukin-6 and caspase-1 in the brain of apolipoprotein E knockout and wild type mice, J Neuroimmunol, 169, 59, 10.1016/j.jneuroim.2005.07.018 Rahman, 2005, High cholesterol diet induces tau hyperphosphorylation in apolipoprotein E deficient mice, FEBS Lett, 579, 6411, 10.1016/j.febslet.2005.10.024 Mooradian, 2005, Statins ameliorate endothelial barrier permeability changes in the cerebral tissue of streptozotocin-induced diabetic rats, Diabetes, 54, 2977, 10.2337/diabetes.54.10.2977 Prasad, 2005, Inhibition of phosphoinositide 3 kinase-Akt (protein kinase B)-nuclear factor-kappa B pathway by lovastatin limits endothelial–monocyte cell interaction, J Neurochem, 94, 204, 10.1111/j.1471-4159.2005.03182.x Hempel, 1999, Calcium antagonists ameliorate ischemia-induced endothelial cell permeability by inhibiting protein kinase C, Circulation, 99, 2523, 10.1161/01.CIR.99.19.2523 Abbruscato, 1999, Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity, J Pharmacol Exp Ther, 289, 668 Brown, 2002, Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke, Stroke, 33, 1706, 10.1161/01.STR.0000016405.06729.83 Volpe, 2000, Abnormalities of endothelial function in the pathogenesis of stroke: the importance of endothelin, J Cardiovasc Pharmacol, 35, S45, 10.1097/00005344-200000002-00011 McCarron, 2006, Endothelial-mediated regulation of cerebral microcirculation, J Physiol Pharmacol, 57, 133 Zinkel, 2006, Postischemic reperfusion: ultrastructural blood-brain barrier and hemodynamic correlative changes in an awake model of transient forebrain ischemia, Neurosurgery, 59, E1152, 10.1227/01.NEU.0000252884.42686.6E Lee, 2007, Vascular permeability precedes spontaneous intracerebral hemorrhage in stroke-prone spontaneously hypertensive rats, Stroke, 38, 3289, 10.1161/STROKEAHA.107.491621 Popescu, 2007, Still debating a cause and diagnostic criteria for Alzheimer's disease, J Cell Mol Med, 11, 1225, 10.1111/j.1582-4934.2007.00149.x Cedazo-Mínguez, 2007, Apolipoprotein E and Alzheimer's disease: molecular mechanisms and therapeutic opportunities, J Cell Mol Med, 11, 1227, 10.1111/j.1582-4934.2007.00130.x Oprica, 2007, Studies on brain volume, Alzheimer-related proteins and cytokines in mice with chronic overexpression of IL-1 receptor antagonist, J Cell Mol Med, 11, 810, 10.1111/j.1582-4934.2007.00074.x Reid, 2007, Alzheimer's disease: cholesterol, membrane rafts, isoprenoids and statins, J Cell Mol Med, 11, 383, 10.1111/j.1582-4934.2007.00054.x Forero, 2006, Synaptic dysfunction and oxidative stress in Alzheimer's disease: emerging mechanisms, J Cell Mol Med, 10, 796, 10.1111/j.1582-4934.2006.tb00439.x Popescu, 2004, Gamma-secretase activity of presenilin 1 regulates acetylcholine muscarinic receptor-mediated signal transduction, J Biol Chem, 279, 6455, 10.1074/jbc.M306041200 Popescu, 2004, Mechanisms of cell death in Alzheimer's disease: role of presenilins, J Alzheimers Dis, 6, 123, 10.3233/JAD-2004-6203 Desai, 2007, Blood-brain barrier pathology in Alzheimer's and Parkinson's disease: implications for drug therapy, Cell Transplant, 16, 285, 10.3727/000000007783464731 Deane, 2004, RAGE (yin) versus LRP (yang) balance regulates Alzheimer amyloid beta-peptide clearance through transport across the blood-brain barrier, Stroke, 35, 2628, 10.1161/01.STR.0000143452.85382.d1 Deane, 2003, RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain, Nat Med, 9, 907, 10.1038/nm890 Zlokovic, 2004, Clearing amyloid through the blood-brain barrier, J Neurochem, 89, 807, 10.1111/j.1471-4159.2004.02385.x Deane, 2005, IgG-assisted age-dependent clearance of Alzheimer's amyloid beta peptide by the blood-brain barrier neonatal Fc receptor, J Neurosci, 25, 11495, 10.1523/JNEUROSCI.3697-05.2005 Cirrito, 2005, P-glycoprotein deficiency at the blood-brain barrier increases amyloid-β deposition in an Alzheimer disease mouse model, J Neurosci, 25, 11495 Ujiie, 2003, Blood-brain barrier permeability precedes senile plaque formation in an Alzheimer disease model, Microcirculation, 10, 463 Banks, 2002, Passage of amyloid beta protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease, Peptides, 23, 2223, 10.1016/S0196-9781(02)00261-9 Methia, 2001, ApoE deficiency compromises the blood brain barrier especially after injury, Mol Med, 7, 810, 10.1007/BF03401973 Hafezi-Moghadam, 2007, ApoE deficiency leads to a progressive age-dependent blood-brain barrier leakage, Am J Physiol Cell Physiol, 292, C1256, 10.1152/ajpcell.00563.2005 Mulder, 2001, Apolipoprotein E protects against neuropathology induced by a high-fat diet and maintains the integrity of the blood-brain barrier during aging, Lab Invest, 81, 953, 10.1038/labinvest.3780307 Shibata, 2000, Clearance of Alzheimer's amyloid-ss(1–40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier, J Clin Invest, 106, 1489, 10.1172/JCI10498 Algotsson, 2007, The integrity of the blood-brain barrier in Alzheimer's disease, Acta Neurol Scand, 115, 403, 10.1111/j.1600-0404.2007.00823.x Bowman, 2007, Blood-brain barrier impairment in Alzheimer disease: stability and functional significance, Neurology, 68, 1809, 10.1212/01.wnl.0000262031.18018.1a Forman, 2005, Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration, J Neurosci, 25, 3539, 10.1523/JNEUROSCI.0081-05.2005 Dickstein, 2006, Abeta peptide immunization restores blood-brain barrier integrity in Alzheimer disease, FASEB J, 20, 426, 10.1096/fj.05-3956com Schiera, 2007, Neurons produce FGF2 and VEGF and secrete them at least in part by shedding extracellular vesicles, J Cell Mol Med, 11, 1384, 10.1111/j.1582-4934.2007.00100.x Lok, 2007, Cell–cell signaling in the neurovascular unit, Neurochem Res, 32, 2032, 10.1007/s11064-007-9342-9 Rite, 2007, Blood-brain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons, J Neurochem, 101, 1567, 10.1111/j.1471-4159.2007.04567.x Whitton, 2007, Inflammation as a causative factor in the aetiology of Parkinson's disease, Br J Pharmacol, 150, 963, 10.1038/sj.bjp.0707167 Kortekaas, 2005, Blood-brain barrier dysfunction in parkinsonian midbrain in vivo, Ann Neurol, 57, 176, 10.1002/ana.20369 Yokel, 2006, Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration, J Alzheimers Dis, 10, 223, 10.3233/JAD-2006-102-309 Toescu, 2005, Normal brain ageing: models and mechanisms, Philos Trans R Soc Lond B Biol Sci, 360, 2347, 10.1098/rstb.2005.1771