Abstract
The microvessels of the brain represent around 3–4 % of the brain compartment but constitute the most important length (400 miles) and surface of exchange (20 m2) between the blood and the parenchyma of brain. Under influence of surrounding tissues, the brain microvessel endothelium expresses a specific phenotype that regulates and restricts the entry of compounds and cells from blood to brain, and defined the so-called blood–brain barrier (BBB). Evidences that alkaline phosphatase (AP) is a characteristic feature of the BBB phenotype that allows differentiating capillary endothelial cells from brain to those of the periphery have rapidly emerge. Thenceforth, AP has been rapidly used as a biomarker of the blood-brain barrier phenotype. In fact, brain capillary endothelial cells (BCECs) express exclusively tissue non-specific alkaline phosphatase (TNAP). There are several lines of evidence in favour of an important role for TNAP in brain function. TNAP is thought to be responsible for the control of transport of some compounds across the plasma membrane of the BCECs. Here, we report that levamisole-mediated inhibition of TNAP provokes an increase of the permeability to Lucifer Yellow of the endothelial monolayer. Moreover, we illustrate the disruption of the cytoskeleton organization. Interestingly, all observed effects were reversible 24 h after levamisole removal and correlated with the return of a full activity of the TNAP. This reversible effect remains to be studied in details to evaluate the potentiality of a levamisole treatment to enhance the entry of drugs in the brain parenchyma.
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References
Abbott NJ (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25:5–23. doi:10.1007/s10571-004-1374-y
Abbott NJ, Hughes CC, Revest PA, Greenwood J (1992) Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood-brain barrier. J Cell Sci 103(Pt 1):23–37
Abbott NJ, Patabendige AA, Dolman DE et al (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37:13–25
Abbott NJ, Ronnback L, Hansson E, Rönnbäck L (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41–53. doi:10.1038/nrn1824
Adams SE, Melnykovych G (1985) Synergistic stimulation of alkaline phosphatase activity in bovine aortic endothelial cells grown in the presence of retinoids and glucocorticoids. J Cell Physiol 124:120–124. doi:10.1002/jcp.1041240119
Albrecht J, Szumanska G, Gadamski R, Gajkowska B (1994) Changes of activity and ultrastructural localization of alkaline phosphatase in cerebral cortical microvessels of rat after single intraperitoneal administration of mercuric chloride. Neurotoxicology 15:897–902
Alvarez JI, Dodelet-Devillers A, Kebir H et al (2011) The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 334:1727–1731. doi:10.1126/science.1206936
Alvarez JI, Katayama T, Prat A (2013) Glial influence on the blood brain barrier. Glia 61:1939–1958. doi:10.1002/glia.22575
Andreeva aY, Krause E, Müller EC et al (2001) Protein kinase C regulates the phosphorylation and cellular localization of occludin. J Biol Chem 276:38480–38486. doi:10.1074/jbc.M104923200
Anstrom JA, Brown WR, Moody DM et al (2002) Temporal expression pattern of cerebrovascular endothelial cell alkaline phosphatase during human gestation. J Neuropathol Exp Neurol 61:76–84
Armulik A, Genove G, Mae M et al (2010) Pericytes regulate the blood-brain barrier. Nature 468:557–561
Balabanov R, Dore-Duffy P (1998) Role of the CNS microvascular pericyte in the blood-brain barrier. J Neurosci Res 53:637–644
Ballabh P, Braun A, Nedergaard M (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 16:1–13
Ballabh P, Hu F, Kumarasiri M et al (2005) Development of tight junction molecules in blood vessels of germinal matrix, cerebral cortex, and white matter. Pediatr Res 58:791–798. doi:10.1203/01.PDR.0000180535.14093.FB
Bär T (1980) The vascular system of the cerebral cortex. Adv Anat Embryol Cell Biol 59:I–VI, 1–62
Beck DW, Roberts RL, Olson JJ (1986) Glial cells influence membrane-associated enzyme activity at the blood-brain barrier. Brain Res 381:131–137
Bell MA, Ball MJ (1985) Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 335:139–143
Bell RD, Winkler EA, Sagare AP et al (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68:409–427. doi:10.1016/j.neuron.2010.09.043
Bessey O, Lowry OH, Brock MJ (1946) A method for the rapid determination of alkaline phosphates with five cubic millimeters of serum. J Biol Chem 164:321–329
Betz AL, Firth JA, Goldstein GW (1980) Polarity of the blood-brain barrier: distribution of enzymes between the luminal and antiluminal membranes of brain capillary endothelial cells. Brain Res 192:17–28
Beuckmann C, Hellwig S, Galla HJ (1995) Induction of the blood/brain-barrier-associated enzyme alkaline phosphatase in endothelial cells from cerebral capillaries is mediated via cAMP. Eur J Biochem 229:641–644
Blasig IE, Giese H, Schroeter ML et al (2001) *NO and oxyradical metabolism in new cell lines of rat brain capillary endothelial cells forming the blood-brain barrier. Microvasc Res 62:114–127
Boado RJ (2003) Blood-brain barrier genomics. Methods Mol Med 89:401–418. doi:10.1385/1-59259-419-0:401
Bonkowski D, Katyshev V, Balabanov RD et al (2011) The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS 8:8. doi:10.1186/2045-8118-8-8
Brunel C, Cathala G, Saintot M (1969) Purification and properties of alkaline phosphatase from beef brain. Biochim Biophys Acta 191:621–635
Brun-Heath I, Ermonval M, Chabrol E et al (2011) Differential expression of the bone and the liver tissue non-specific alkaline phosphatase isoforms in brain tissues. Cell Tissue Res 343:521–536. doi:10.1007/s00441-010-1111-4
Calabria AR, Shusta EV (2006) Blood-brain barrier genomics and proteomics: elucidating phenotype, identifying disease targets and enabling brain drug delivery. Drug Discov Today 11:792–799. doi:10.1016/j.drudis.2006.07.006
Calabria AR, Shusta EV (2008) A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab 28:135–148. doi:10.1038/sj.jcbfm.9600518
Calabria AR, Shusta EV (2009) A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. Blood 28:135–148. doi:10.1038/sj.jcbfm.9600518.A
Calhau C, Martel F, Soares-da-Silva P et al (2002) Regulation of [(3)H]MPP(+) transport by phosphorylation/dephosphorylation pathways in RBE4 cells: role of ecto-alkaline phosphatase. Naunyn Schmiedebergs Arch Pharmacol 365:349–356. doi:10.1007/s00210-002-0542-1
Cardelli-Cangiano P, Fiori A, Cangiano C et al (1987) Isolated brain microvessels as in vitro equivalents of the blood-brain barrier: selective removal by collagenase of the A-system of neutral amino acid transport. J Neurochem 49:1667–1675
Chan JR, Stinson Ra (1986) Dephosphorylation of phosphoproteins of human liver plasma membranes by endogenous and purified liver alkaline phosphatases. J Biol Chem 261:7635–7639
Chu C, Li JY, Boado RJ et al (2008) Blood-brain barrier genomics and cloning of a novel organic anion transporter. J Cereb Blood Flow Metab 28:291–301. doi:10.1038/sj.jcbfm.9600538
Ciani F, Contestabile A, Minelli G, Quaglia A (1973) Ultrastructural localization of alkaline phosphatase in cultures of nervous tissue in vitro. J Neurocytol 2:105–116
Couraud P, Greenwood J, Roux F, Adamson P (2003) Development and characterization of immortalized cerebral endothelial cell lines. Methods Mol Med 89:349–364
Daneman R (2012) The blood-brain barrier in health and disease. Ann Neurol 72:648–672. doi:10.1002/ana.23648
Daneman R, Zhou L, Agalliu D, et al (2010a) The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells. 5:1–16. doi:10.1371/journal.pone.0013741
Daneman R, Zhou L, Kebede A, Barres BA (2010b) Pericytes are required for blood–brain barrier integrity during embryogenesis. 468:562–566. doi:10.1038/nature09513.Pericytes
Dehouck MP, Meresse S, Delorme P et al (1990) An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. J Neurochem 54:1798–1801
Deli MA, Abrahám CS, Kataoka Y et al (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25:59–127
DePierre JW, Karnovsky ML (1974) Ecto-enzymes of the guinea pig polymorphonuclear leukocyte. I. Evidence for an ecto-adenosine monophosphatase, adenosine triphosphatase, and -p-nitrophenyl phosphates. J Biol Chem 249:7111–7120
Deracinois B, Duban-Deweer S, Karamanos Y et al (2012) TNAP and EHD1 are over-expressed in bovine brain capillary endothelial cells after the re-induction of blood-brain barrier properties. PLoS ONE 7:e48428. doi:10.1371/journal.pone.0048428
Díaz-Hernández M, Gómez-Ramos A, Rubio A et al (2010) Tissue-nonspecific alkaline phosphatase promotes the neurotoxicity effect of extracellular tau. J Biol Chem 285:32539–32548. doi:10.1074/jbc.M110.145003
Djuricić BM, Rogac L, Spatz M et al (1978) Brain microvessels. I. Enzymic activities. Adv Neurol 20:197–205
Ehrlich P (1885) Das Sauerstoff-bedürfniss des Organismus. Ein farbenanalytische Studie. Hirschwald, Berlin
Ehrlich YH, Davis TB, Bock E et al (1986) Ecto-protein kinase activity on the external surface of neural cells. Nature 320:67–70. doi:10.1038/320067a0
Enerson BE, Drewes LR (2006) The rat blood-brain barrier transcriptome. J Cereb Blood Flow Metab 26:959–973. doi:10.1038/sj.jcbfm.9600249
Engelhardt B (2003) Development of the blood-brain barrier. Cell Tissue Res 314:119–129
Ermonval M, Baudry A, Baychelier F et al (2009) The cellular prion protein interacts with the tissue non-specific alkaline phosphatase in membrane microdomains of bioaminergic neuronal cells. PLoS ONE 4:e6497. doi:10.1371/journal.pone.0006497
Farkas-Bargeton E, Arsenio-Nunes ML (1970) Maturation of enzymatic equipment in the vessel walls of the nervous system. Histochemical study. Acta Neuropathol 15:251–271
Farley JR, Joel L, Baylink DJ (1980) Human Skeletal Alkaline Phosphatase. J Biol Chem 10:4680–4686
Fedde KN, Michel MP, Whyte MP (1993) Evidence against a role for alkaline phosphatase in the dephosphorylation of plasma membrane proteins: hypophosphatasia fibroblast study. J Cell Biochem 53:43–50. doi:10.1002/jcb.240530106
Fleming A, Diekmann H, Goldsmith P (2013) Functional characterisation of the maturation of the blood-brain barrier in larval zebrafish. PLoS ONE 8:e77548. doi:10.1371/journal.pone.0077548
Fonta C, Imbert M (2002) Vascularization in the primate visual cortex during development. Cereb Cortex 12:199–211
Fonta C, Negyessy L, Renaud L, Barone P (2005) Postnatal development of alkaline phosphatase activity correlates with the maturation of neurotransmission in the cerebral cortex. J Comp Neurol 486:179–196. doi:10.1002/cne.20524
Fonta C, Négyessy L, Renaud L, Barone P (2004) Areal and subcellular localization of the ubiquitous alkaline phosphatase in the primate cerebral cortex: evidence for a role in neurotransmission. Cereb Cortex 14:595–609. doi:10.1093/cercor/bhh021
Frangakis MV, Kimelberg HK (1984) Dissociation of neonatal rat brain by dispase for preparation of primary astrocyte cultures. Neurochem Res 9:1689–1698
Fukushima H, Fujimoto M, Ide M (1990) Quantitative detection of blood-brain barrier-associated enzymes in cultured endothelial cells of porcine brain microvessels. Vitro Cell Dev Biol 26:612–620
Ginsbourg M, Foncin JF, Le Beau J (1973) Vascular abnormalities in cerebral tumours. A comparative study of enzyme activity and permeability to fluorescent tracers. Rev Neurol (Paris) 129:275–288
Ginsbourg M, Le Beau J (1975) Histochemical correlations of vascular permeability and enzyme activity in the choroid plexus in man. C R Seances Soc Biol Fil 169:518–521
Goldmann E (1913) Vitalfärbung am zentral nerven System. Bietrag zur Physio-Pathologie des Plexus Choroidus und der Hirnhuate. Abhandlungen der koniglich preubischen Akademie der Wissenschaften. Physikalisch-Mathematische Classe 1:1–64
Goldstein GW (1988) Endothelial cell-astrocyte interactions. A cellular model of the blood-brain barrier. Ann N Y Acad Sci 529:31–39
Grammas P, Martinez J, Miller B (2011) Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases. Expert Rev Mol Med 13:e19. doi:10.1017/S1462399411001918
Haseloff RF, Blasig IE, Bauer HC, Bauer H (2005) In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitro. Cell Mol Neurobiol 25:25–39
Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173–185. doi:10.1124/pr.57.2.4.173
Hurst RD, Fritz IB (1996) Properties of an immortalised vascular endothelial/glioma cell co-culture model of the blood-brain barrier. J Cell Physiol 167:81–88. doi:10.1002/(SICI)1097-4652(199604)167:1<81:AID-JCP9>3.0.CO;2-8
Inomata K, Yoshioka T, Nasu F, Mayahara H (1984) Ultracytochemical studies of capillary endothelial cells in the rat central nervous system. Acta Anat (Basel) 118:243–248
Isobe I, Watanabe T, Yotsuyanagi T, et al (1996) Astrocytic contributions to blood-brain barrier (BBB) formation by endothelial cells: a possible use of aortic endothelial cell for in vitro BBB model. Neurochem Int 28:523–33
Jancsó G, Tóth L, Karcsú S (1975) Histochemical localization of capillary enzyme activities in brain smears. Z Mikrosk Anat Forsch 89:983–990
Janzer RC, Raff MC (1987) Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325:253–257. doi:10.1038/325253a0
Jeong J-Y, Kwon H-B, Ahn J-C et al (2008) Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res Bull 75:619–628. doi:10.1016/j.brainresbull.2007.10.043
Joo F (1993) The blood-brain barrier in vitro: the second decade. Neurochem Int 23:499–521
Joó F, Karnushina I (1973) A procedure for the isolation of capillaries from rat brain. Cytobios 8:41–48
Kamiie J, Ohtsuki S, Iwase R et al (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 25:1469–1483
Kondo T, Imaizumi S, Kato I, Yoshimoto T (1994) Isolation and culture of brain endothelial cells and establishment of in vitro blood-brain barrier model. Cell Transplant 3(Suppl 1):S35–S37
Kozlenkov A, Le Du MH, Cuniasse P et al (2004) Residues determining the binding specificity of uncompetitive inhibitors to tissue-nonspecific alkaline phosphatase. J Bone Miner Res 19:1862–1872. doi:10.1359/JBMR.040608
Latker CH, Shinowara NL, Miller JC, Rapoport SI (1987) Differential localization of alkaline phosphatase in barrier tissues of the frog and rat nervous systems: a cytochemical and biochemical study. J Comp Neurol 264:291–302. doi:10.1002/cne.902640302
Lazzari M, Franceschini V, Ciani F, Minelli G (1989) Cytochemical localization of alkaline phosphatase and Na+, K+-ATPase activities in the blood-brain barrier of Rana esculenta. Basic Appl Histochem 33:113–120
Lechardeur D, Schwartz B, Paulin D, Scherman D (1995) Induction of blood-brain barrier differentiation in a rat brain-derived endothelial cell line. Exp Cell Res 220:161–170. doi:10.1006/excr.1995.1302
Leduc EH, Wislocki GB (1952) The histochemical localization of acid and alkaline phosphatases, non-specific esterase and succinic dehydrogenase in the structures comprising the hemato-encephalic barrier of the rat. J Comp Neurol 97:241–279
Lev R, Griffiths WC (1982) Colonic and small intestinal alkaline phosphatase. A histochemical and biochemical study. Gastroenterology 82:1427–1435
Lewandowsky M (1900) Zur lehre von der Cerebrospinalflüssigkeit. Z Klin Med 480–494
Li JY, Boado RJ, Pardridge WM (2001) Blood-brain barrier genomics. J Cereb Blood Flow Metab 21:61–68
Li JY, Boado RJ, Pardridge WM (2002) Rat blood-brain barrier genomics. II. J Cereb Blood Flow Metab 22:1319–1326. doi:10.1097/00004647-200211000-00005
Lippmann ES, Weidenfeller C, Svendsen CN, Shusta EV (2011) Blood-brain barrier modeling with co-cultured neural progenitor cell-derived astrocytes and neurons. J Neurochem 119:507–520. doi:10.1111/j.1471-4159.2011.07434.x
Liu HC, Lee JC, Bakay L (1979) Experimental cerebral concussion. A histochemical study. Acta Neurochir (Wien) 47:105–122
Liu S, Agalliu D, Yu C, Fisher M (2012) The role of pericytes in blood-brain barrier function and stroke. Curr Pharm Des 18:3653–3662
Mabry CC, Bautista A, Kirk RF et al (1970) Familial hyperphosphatase with mental retardation, seizures, and neurologic deficits. J Pediatr 77:74–85
Mebarek S, Hamade E, Thouverey C et al (2011) Ankylosing spondylitis, late osteoarthritis, vascular calcification, chondrocalcinosis and pseudo gout: toward a possible drug therapy. Curr Med Chem 18:2196–2203
Meresse S, Dehouck MP, Delorme P et al (1989) Bovine brain endothelial cells express tight junctions and monoamine oxidase activity in long-term culture. J Neurochem 53:1363–1371
Meunier MT, Bouchaud C (1978) Histoenzymological contribution to the study of the rat blood-brain barrier. Arch Anat Microsc Morphol Exp 67:81–98
Meyer J, Mischeck U, Veyhl M et al (1990) Blood-brain barrier characteristic enzymatic properties in cultured brain capillary endothelial cells. Brain Res 514:305–309
Meyer J, Rauh J, Galla HJ (1991) The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferative state. J Neurochem 57:1971–1977
Millán JL (2006) Alkaline Phosphatases: structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2:335–341. doi:10.1007/s11302-005-5435-6
Mizuguchi H, Fujii A, Utoguchi N et al (1995) Glial-conditioned medium elevates alkaline phosphatase activity in cultured bovine aortic endothelial cells. Microvasc Res 50:129–132
Mizuguchi H, Hashioka Y, Utoguchi N et al (1994) A comparison of drug transport through cultured monolayers of bovine brain capillary and bovine aortic endothelial cells. Biol Pharm Bull 17:1385–1390
Mulkins MA, Allison AC (1987) Recombinant human interleukin-1 inhibits the induction by dexamethasone of alkaline phosphatase activity in murine capillary endothelial cells. J Cell Physiol 133:539–545. doi:10.1002/jcp.1041330315
Nag S (2011) Morphology and properties of brain endothelial cells. Methods Mol Biol 686:3–47
Nakazato H, Deguchi M, Fujimoto M, Fukushima H (1997) Alkaline phosphatase expression in cultured endothelial cells of aorta and brain microvessels: induction by interleukin-6-type cytokines and suppression by transforming growth factor betas. Science 80(61):2065–2072
Neuhaus J, Risau W, Wolburg H (1991) Induction of blood-brain barrier characteristics in bovine brain endothelial cells by rat astroglial cells in transfilter coculture. Ann N Y Acad Sci 633:578–580
Nishio S, Egami H, Fukui M et al (1986) Ultrastructural and cytochemical study of microvascular enzyme activity in experimental brain tumors of rat. Neurol Med Chir (Tokyo) 26:527–533
Norman MG, O’Kusky JR (1986) The growth and development of microvasculature in human cerebral cortex. J Neuropathol Exp Neurol 45:222–232
Nosjean O, Koyama I, Goseki M, et al (1997) Human tissue non-specific alkaline phosphatases: sugar-moiety-induced enzymic and antigenic modulations and genetic aspects. Biochem J 321(Pt 2):297–303
Oby E, Janigro D (2006) The blood-brain barrier and epilepsy. Epilepsia 47:1761–1774
Oldendorf WH, Cornford ME, Brown WJ (1977) The large apparent work capability of the blood-brain barrier: a study of the mitochondrial content of capillary endothelial cells in brain and other tissues of the rat. Ann Neurol 1:409–417. doi:10.1002/ana.410010502
Palmer AM (2010) The role of the blood-CNS barrier in CNS disorders and their treatment. Neurobiol Dis 37:3–12. doi:10.1016/j.nbd.2009.07.029
Paolinelli R, Corada M, Orsenigo F, Dejana E (2011) The molecular basis of the blood brain barrier differentiation and maintenance. Is it still a mystery? Pharmacol Res 63:165–171. doi:10.1016/j.phrs.2010.11.012
Pardridge WM (2002) Drug and gene targeting to the brain with molecular Trojan horses. Nat Rev Drug Discov 1:131–139
Pardridge WM (2007) Blood-brain barrier delivery. Drug Discov Today 12:54–61
Pardridge WM, Oldendorf WH (1977) Transport of metabolic substrates through the blood-brain barrier. J Neurochem 28:5–12
Persidsky Y, Heilman D, Haorah J et al (2006) Rho-mediated regulation of tight junctions during monocyte migration across the blood-brain barrier in HIV-1 encephalitis (HIVE). Blood 107:4770–4780. doi:10.1182/blood-2005-11-4721
Plesner L (1995) Ecto-ATPases: identities and functions. Int Rev Cytol 158:141–214
Pottiez G, Flahaut C, Cecchelli R, Karamanos Y (2009) Understanding the blood-brain barrier using gene and protein expression profiling technologies. Brain Res Rev 62:83–98. doi:10.1016/j.brainresrev.2009.09.004
Prat A, Biernacki K, Wosik K, Antel JP (2001) Glial cell influence on the human blood-brain barrier. Glia 36:145–155
Ramsauer M, Krause D, Dermietzel R (2002) Angiogenesis of the blood-brain barrier in vitro and the function of cerebral pericytes. FASEB J 16:1274–1276. doi:10.1096/fj.01-0814fje
Rauh J, Meyer J, Beuckmann C, Galla HJ (1992) Development of an in vitro cell culture system to mimic the blood-brain barrier. Prog Brain Res 91:117–121
Reichel A, Begley DJ, Abbott NJ (2003) An overview of in vitro techniques for blood-brain barrier studies. blood brain barrier. Biol Res Protoc 89:307–324
Renkawek K, Murray MR, Spatz M, Klatzo I (1976) Distinctive histochemical characteristics of brain capillaries in organotypic culture. Exp Neurol 50:194–206
Risau W, Hallmann R, Albrecht U (1986) Differentiation-dependent expression of proteins in brain endothelium during development of the blood-brain barrier. Dev Biol 117:537–545
Roux F, Durieu-Trautmann O, Chaverot N et al (1994) Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J Cell Physiol 159:101–113. doi:10.1002/jcp.1041590114
Rubin LL (1991) The blood-brain barrier in and out of cell culture. Curr Opin Neurobiol 1:360–363
Rubin LL, Hall DE, Porter S et al (1991) A cell culture model of the blood-brain barrier. J Cell Biol 115:1725–1735
Sakakibara A, Furuse M, Saitou M et al (1997) Possible involvement of phosphorylation of occludin in tight junction formation. J Cell Biol 137:1393–1401
Sánchez del Pino MM, Hawkins RA, Peterson DR (1995) Biochemical discrimination between luminal and abluminal enzyme and transport activities of the blood-brain barrier. J Biol Chem 270:14907–14912
Schiffer D, Vesco C, Piazza L (1962) Contribution to the histochemical demonstration and distribution of phosphatases and non-specific esterase in human nervous tissue. Psychiatr Neurol (Basel) 144:34–47
Sessa G, Perez MM (1975) Biochemical changes in rat brain associated with the development of the blood-brain barrier. J Neurochem 25:779–782
Shi F, Audus KL (1994) Biochemical characteristics of primary and passaged cultures of primate brain microvessel endothelial cells. Neurochem Res 19:427–433
Shusta EV, Boado RJ, Mathern GW, Pardridge WM (2002) Vascular genomics of the human brain. J Cereb Blood Flow Metab 22:245–252. doi:10.1097/00004647-200203000-00001
Siddharthan V, Kim YV, Liu S, Kim KS (2007) Human astrocytes/astrocyte-conditioned medium and shear stress enhance the barrier properties of human brain microvascular endothelial cells. Brain Res 1147:39–50. doi:10.1016/j.brainres.2007.02.029
Sidique S, Ardecky R, Su Y et al (2009) Design and synthesis of pyrazole derivatives as potent and selective inhibitors of tissue-nonspecific alkaline phosphatase (TNAP). Bioorg Med Chem Lett 19:222–225. doi:10.1016/j.bmcl.2008.10.107
Smith M, Weiss MJ, Griffin CA et al (1988) Regional assignment of the gene for human liver/bone/kidney alkaline phosphatase to chromosome 1p36.1–p34. Genomics 2:139–143
Sobue K, Yamamoto N, Yoneda K et al (1999) Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci Res 35:155–164
Soma T, Chiba H, Kato-Mori Y et al (2004) Thr(207) of claudin-5 is involved in size-selective loosening of the endothelial barrier by cyclic AMP. Exp Cell Res 300:202–212. doi:10.1016/j.yexcr.2004.07.012
Stanness KA, Neumaier JF, Sexton TJ et al (1999) A new model of the blood–brain barrier: co-culture of neuronal, endothelial and glial cells under dynamic conditions. Neuroreport 10:3725–3731
Stewart PA, Wiley MJ (1981) Structural and histochemical features of the avian blood-brain barrier. J Comp Neurol 202:157–167. doi:10.1002/cne.902020203
Sundstrom JM, Tash BR, Murakami T et al (2009) Identification and analysis of occludin phosphosites: a combined mass spectrometry and bioinformatics approach. J Proteome Res 8:808–817. doi:10.1021/pr7007913
Takemoto H, Kaneda K, Hosokawa M, et al (1994) Conditioned media of glial cell lines induce alkaline phosphatase in cultured artery endothelial cells of interleukin-6 as an induction factor activity Identification. 350:99–103
Tao-Cheng J, Nagy Z, Brightman M (1987) Tight junctions astroglia of brain endothelium in vitro are enhanced by astroglia. J Neurosci 7:3293–3299
Tatsuta T, Naito M, Oh-hara T et al (1992) Functional involvement of P-glycoprotein in blood-brain barrier. J Biol Chem 267:20383–20391
Tio S, Deenen M, Marani E (1990) Astrocyte-mediated induction of alkaline phosphatase activity in human umbilical cord vein endothelium: an in vitro model. Eur J Morphol 28:289–300
Tontsch U, Bauer HC (1991) Glial cells and neurons induce blood-brain barrier related enzymes in cultured cerebral endothelial cells. Brain Res 539:247–253
Torack R, Barrnett R (1964) The fine structural localization of nucleoside phosphatase activity in the blood-brain barrier. J Neuropathol Exp Neurol 23:46–59
Uchida Y, Ohtsuki S, Katsukura Y et al (2011) Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem 117:333–345. doi:10.1111/j.1471-4159.2011.07208.x
Van Belle H (1976) Alkaline phosphatase. I. Kinetics and inhibition by levamisole of purified isoenzymes from humans. Clin Chem 22:972–976
Vandenhaute E, Culot M, Gosselet F et al (2012) Brain pericytes from stress-susceptible pigs increase blood-brain barrier permeability in vitro. Fluids Barriers CNS 9:11. doi:10.1186/2045-8118-9-11
Vardy ERLC, Kellett KAB, Cocklin SL, Hooper NM (2012) Alkaline phosphatase is increased in both brain and plasma in Alzheimer’s disease. Neurodegener Dis 9:31–37. doi:10.1159/000329722
Vinters HV, Reave S, Costello P et al (1987) Isolation and culture of cells derived from human cerebral microvessels. Cell Tissue Res 249:657–667
Vorbrodt aW, Trowbridge RS (1991) Ultracytochemical characteristics of cultured goat brain microvascular endothelial cells [corrected]. J Histochem Cytochem 39:1555–1563. doi:10.1177/39.11.1655877
Vorbrodt AW, Lossinsky AS, Wisniewski HM et al (1981) Ultrastructural cytochemical studies of cerebral microvasculature in scrapie infected mice. Acta Neuropathol 53:203–211
Vorbrodt AW, Lossinsky AS, Wisniewski HM (1986) Localization of alkaline phosphatase activity in endothelia of developing and mature mouse blood-brain barrier. Dev Neurosci 8:1–13
Vorbrodt AW, Lossinsky AS, Wisniewski HM et al (1985) Ultrastructural observations on the transvascular route of protein removal in vasogenic brain edema. Acta Neuropathol 66:265–273
Vorbrodt AW, Lossinsky AS, Wisniewski HM (1983) Enzyme cytochemistry of blood-brain barrier (BBB) disturbances. Acta Neuropathol Suppl 8:43–57
Wakai S, Hirokawa N (1978) Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tissue Res 195:195–203
Whyte MP (1994) Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. Endocr Rev 15:439–461
Williams SK, Gillis JF, Matthews MA et al (1980) Isolation and characterization of brain endothelial cells: morphology and enzyme activity. J Neurochem 35:374–381
Wisniewski HM, Lossinsky AS, Moretz RC et al (1983) Increased blood-brain barrier permeability in scrapie-infected mice. J Neuropathol Exp Neurol 42:615–626
Wollscheid B, Bausch-Fluck D, Henderson C et al (2009) Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 27:378–386. doi:10.1038/nbt.1532
Wong AD, Ye M, Levy AF et al (2013) The blood-brain barrier: an engineering perspective. Front Neuroeng 6:7. doi:10.3389/fneng.2013.00007
Wong V (1997) Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am J Physiol 273:C1859–C1867
Yu S, Guo Z, Johnson C, et al (2013) Recent progress in synthetic and biological studies of GPI anchors and GPI-anchored proteins. Curr Opin Chem Biol 1–8. doi:10.1016/j.cbpa.2013.09.016
Zhou H, Manji SS, Findlay DM et al (1994) Novel action of retinoic acid. Stabilization of newly synthesized alkaline phosphatase transcripts. J Biol Chem 269:22433–22439
Zoellner HF, Hunter N (1989) Histochemical identification of the vascular endothelial isoenzyme of alkaline phosphatase. J Histochem Cytochem 37:1893–1898. doi:10.1177/37.12.2584695
Acknowledgments
This research was funded by the Ministère de la Recherche et de l’Enseignement Supérieur. We are also grateful to Johan Hachani for his technical expertise and continuous help of every day.
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The authors declare no conflict of interest.
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Deracinois, B., Lenfant, AM., Dehouck, MP., Flahaut, C. (2015). Tissue Non-specific Alkaline Phosphatase (TNAP) in Vessels of the Brain. In: Fonta, C., Négyessy, L. (eds) Neuronal Tissue-Nonspecific Alkaline Phosphatase (TNAP). Subcellular Biochemistry, vol 76. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7197-9_7
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