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Review

Heterogeneity of the blood-brain barrier

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Article: e1143544 | Received 24 Nov 2015, Accepted 12 Jan 2016, Published online: 10 Mar 2016

References

  • Hill J, Rom S, Ramirez SH, Persidsky Y. Emerging roles of pericytes in the regulation of the neurovascular unit in health and disease. J Neuroimmune Pharmacol 2014; 9:591-605; PMID:25119834; http://dx.doi.org/10.1007/s11481-014-9557-x
  • Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci 2011; 14:1398-405; PMID:22030551; http://dx.doi.org/10.1038/nn.2946
  • Wilhelm I, Krizbai IA. In vitro models of the blood-brain barrier for the study of drug delivery to the brain. Mol Pharm 2014; 11:1949-63; PMID:24641309; http://dx.doi.org/10.1021/mp500046f
  • Shawahna R, Uchida Y, Declèves X, Ohtsuki S, Yousif S, Dauchy S, Jacob A, Chassoux F, Daumas-Duport C, Couraud PO, et al. Transcriptomic and quantitative proteomic analysis of transporters and drug metabolizing enzymes in freshly isolated human brain microvessels. Mol Pharm 2011; 8:1332-41; PMID:21707071; http://dx.doi.org/10.1021/mp200129p
  • Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7:41-53; PMID:16371949; http://dx.doi.org/10.1038/nrn1824
  • Schlageter KE, Molnar P, Lapin GD, Groothuis DR. Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties. Microvasc Res 1999; 58:312-28; PMID:10527772; http://dx.doi.org/10.1006/mvre.1999.2188
  • Borowsky IW, Collins RC. Metabolic anatomy of brain: a comparison of regional capillary density, glucose metabolism, and enzyme activities. J Comp Neurol 1989; 288:401-13; PMID:2551935; http://dx.doi.org/10.1002/cne.90288-0304
  • Murugesan N, Demarest TG, Madri JA, Pachter JS. Brain regional angiogenic potential at the neurovascular unit during normal aging. Neurobiol Aging 2012; 33:1004.e1-16; PMID:22019053; http://dx.doi.org/10.1016/j.neurobio-laging.2011.09.022
  • McCaslin AF, Chen BR, Radosevich AJ, Cauli B, Hillman EM. In vivo 3D morphology of astrocyte-vasculature interactions in the somatosensory cortex: implications for neurovascular coupling. J Cereb Blood Flow Metab 2011; 31:795-806; PMID:21139630; http://dx.doi.org/10.1038/jcbfm.2010.204
  • Cavaglia M, Dombrowski SM, Drazba J, Vasanji A, Bokesch PM, Janigro D. Regional variation in brain capillary density and vascular response to ischemia. Brain Res 2001; 910:81-93; PMID:11489257; http://dx.doi.org/10.1016/S0006-8993(01)02637-3
  • Gross PM, Sposito NM, Pettersen SE, Fenstermacher JD. Differences in function and structure of the capillary endothelium in gray matter, white matter and a circumventricular organ of rat brain. Blood Vessels 1986; 23:261-70; PMID:3790742
  • Zhao R, Pollack GM. Regional differences in capillary density, perfusion rate, and P-glycoprotein activity: a quantitative analysis of regional drug exposure in the brain. Biochem Pharmacol 2009; 78:1052-9; PMID:19523457; http://dx.doi.org/10.1016/j.bcp.2009.06.001
  • Janota CS, Brites D, Lemere CA, Brito MA. Glio-vascular changes during ageing in wild-type and Alzheimer's disease-like APP/PS1 mice. Brain Res 2015; 1620:153-68; PMID:25966615; http://dx.doi.org/10.1016/j.brainres.2015.04.056
  • Lundgaard I, Osório MJ, Kress BT, Sanggaard S, Nedergaard M. White matter astrocytes in health and disease. Neuroscience 2014; 276:161-73; PMID:24231735; http://dx.doi.org/10.1016/j.neuroscience.2013.10.050
  • Reichenbach A, Wolburg H. Astrocytes and ependymal glia. In: Kettenmann H, Ransom BR, eds. Neuroglia. United States of America: Oxford University Press, 2013:35-50.
  • Goursaud S, Kozlova EN, Maloteaux JM, Hermans E. Cultured astrocytes derived from corpus callosum or cortical gray matter show distinct glutamate handling properties. J Neurochem 2009; 108:1442-52; PMID:19222709; http://dx.doi.org/10.1111/j.1471-4159.2009.05889.x
  • Kaaijk P, Pals ST, Morsink F, Bosch DA, Troost D. Differential expression of CD44 splice variants in the normal human central nervous system. J Neuroimmunol 1997; 73:70-6; PMID:9058761; http://dx.doi.org/10.1016/S0165-5728(96)00167-1
  • Akiyama H, Tooyama I, Kawamata T, Ikeda K, McGeer PL. Morphological diversities of CD44 positive astrocytes in the cerebral cortex of normal subjects and patients with Alzheimer's disease. Brain Res 1993; 632:249-59; PMID:7511977; http://dx.doi.org/10.1016/0006-8993(93)91160-T
  • Girgrah N, Letarte M, Becker LE, Cruz TF, Theriault E, Moscarello MA. Localization of the CD44 glycoprotein to fibrous astrocytes in normal white matter and to reactive astrocytes in active lesions in multiple sclerosis. J Neuropathol Exp Neurol 1991; 50:779-92; PMID:1748883; http://dx.doi.org/10.1097/00005072-199111000-00009
  • Nagy JI, Rash JE. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Brain Res Rev 2000; 32:29-44; PMID:10751655; http://dx.doi.org/10.1016/S0165-0173(99)00066-1
  • Haas B, Schipke CG, Peters O, Söhl G, Willecke K, Kettenmann H. Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb Cortex 2006; 16:237-46; PMID:15930372; http://dx.doi.org/10.1093/cercor/bhi101
  • D'Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM, Janigro D. Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 1998; 18:4425-38; PMID:9614220
  • Liedtke W, Edelmann W, Bieri PL, Chiu FC, Cowan NJ, Kucherlapati R, Raine CS. GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 1996; 17:607-15; PMID:8893019; http://dx.doi.org/10.1016/S0896-6273(00)80194-4
  • Pekny M, Stanness KA, Eliasson C, Betsholtz C, Janigro D. Impaired induction of blood-brain barrier properties in aortic endothelial cells by astrocytes from GFAP-deficient mice. Glia 1998; 22:390-400; PMID:9517571; http://dx.doi.org/10.1002/(SICI)1098-1136(199804)22:4%3c390::AID-GLIA8%3e3.0.CO;2-7
  • Ballabh P. Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr Res 2010; 67:1-8; PMID:19816235; http://dx.doi.org/10.1203/PDR.0b013e3-181c1b176
  • Alvarez JI, Katayama T, Prat A. Glial influence on the blood brain barrier. Glia 2013; 61:1939-58; PMID:24123158; http://dx.doi.org/10.1002/glia.22575
  • Winkler EA, Sengillo JD, Bell RD, Wang J, Zlokovic BV. Blood-spinal cord barrier pericyte reductions contribute to increased capillary permeability. J Cereb Blood Flow Metab 2012; 32:1841-52; PMID:22850407; http://dx.doi.org/10.1038/jcbfm.2012.113
  • Winkler EA, Sengillo JD, Sullivan JS, Henkel JS, Appel SH, Zlokovic BV. Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol 2013; 125:111-20; PMID:22941226; http://dx.doi.org/10.1007/s00401-012-1039-8
  • Morita S, Hourai A, Miyata S. Changes in pericytic expression of NG2 and PDGFRB and vascular permeability in the sensory circumventricular organs of adult mouse by osmotic stimulation. Cell Biochem Funct 2014; 32:51-61; PMID:23629811; http://dx.doi.org/10.1002/cbf.2971
  • Montagne A, Barnes SR, Sweeney MD, Halliday MR, Sagare AP, Zhao Z, Toga AW, Jacobs RE, Liu CY, Amezcua L, et al. Blood-brain barrier breakdown in the aging human hippocampus. Neuron 2015; 85:296-302; PMID:25611508; http://dx.doi.org/10.1016/j.neuron.2014.12.032
  • Sengillo JD, Winkler EA, Walker CT, Sullivan JS, Johnson M, Zlokovic BV. Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease. Brain Pathol 2013; 23:303-10; PMID:23126372; http://dx.doi.org/10.1111/bpa.12004
  • Swift MR, Weinstein BM. Arterial-venous specification during development. Circ Res 2009; 104:576-88; PMID:19286613; http://dx.doi.org/10.1161/CIRCRESA-HA.108.188805
  • Macdonald JA, Murugesan N, Pachter JS. Endothelial cell heterogeneity of blood-brain barrier gene expression along the cerebral microvasculature. J Neurosci Res 2010; 88:1457-74; PMID:20025060
  • Ge S, Song L, Pachter JS. Where is the blood-brain barrier … really? J Neurosci Res 2005; 79:421-7; PMID:15635601; http://dx.doi.org/10.1002/jnr.20313
  • Nagy Z, Peters H, Hüttner I. Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab Invest 1984; 50:313-22; PMID:6422163
  • Paul D, Cowan AE, Ge S, Pachter JS. Novel 3D analysis of Claudin-5 reveals significant endothelial heterogeneity among CNS microvessels. Microvasc Res 2013; 86:1-10; PMID:23261753; http://dx.doi.org/10.1016/j.mvr.2012.12.001
  • Virgintino D, Robertson D, Errede M, Benagiano V, Girolamo F, Maiorano E, Roncali L, Bertossi M. Expression of P-glycoprotein in human cerebral cortex microvessels. J Histochem Cytochem 2002; 50:1671-6; PMID:12486090; http://dx.doi.org/10.1177/002215540205001212
  • Saubaméa B, Cochois-Guégan V, Cisternino S, Scherrmann JM. Heterogeneity in the rat brain vasculature revealed by quantitative confocal analysis of endothelial barrier antigen and P-glycoprotein expression. J Cereb Blood Flow Metab 2012; 32:81-92; http://dx.doi.org/10.1038/jcbfm.2011.109
  • Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. Signaling at the gliovascular interface. J Neurosci 2003; 23:9254-62; PMID:14534260
  • Xu H, Hu F, Sado Y, Ninomiya Y, Borza DB, Ungvari Z, Lagamma EF, Csiszar A, Nedergaard M, Ballabh P. Maturational changes in laminin, fibronectin, collagen IV, and perlecan in germinal matrix, cortex, and white matter and effect of betamethasone. J Neurosci Res 2008; 86:1482-500; PMID:18214989; http://dx.doi.org/10.1002/jnr.21618
  • Yasuda K, Cline C, Lin YS, Scheib R, Ganguly S, Thirumaran RK, Chaudhry A, Kim RB, Schuetz EG. In Vivo Imaging of Human MDR1 Transcription in the Brain and Spine of MDR1-Luciferase Reporter Mice. Drug Metab Dispos 2015; 43:1646-54; PMID:26281846; http://dx.doi.org/10.1124/dmd.115.065078
  • Kwan P, Li HM, Al-Jufairi E, Abdulla R, Gonzales M, Kaye AH, Szoeke C, Ng HK, Wong KS, O'Brien TJ. Association between temporal lobe P-glycoprotein expression and seizure recurrence after surgery for pharmacoresistant temporal lobe epilepsy. Neurobiol Dis 2010; 39:192-7; PMID:20403441; http://dx.doi.org/10.1016/j.nbd.2010.04.006
  • Matter K, Balda MS. Functional analysis of tight junctions. Methods 2003; 30:228-34; PMID:12798137; http://dx.doi.org/10.1016/S1046-2023(03)00029-X
  • Coomber BL, Stewart PA. Morphometric analysis of CNS microvascular endothelium. Microvasc Res 1985; 30:99-115; PMID:4021842; http://dx.doi.org/10.1016/0026-2862(85)90-042-1
  • Wang QP, Guan JL, Pan W, Kastin AJ, Shioda S. A diffusion barrier between the area postrema and nucleus tractus solitarius. Neurochem Res 2008; 33:2035-43; PMID:18373195; http://dx.doi.org/10.1007/s11064-008-9676-y
  • Morita S, Furube E, Mannari T, Okuda H, Tatsumi K, Wanaka A, Miyata S. Heterogeneous vascular permeability and alternative diffusion barrier in sensory circumventricular organs of adult mouse brain. Cell Tissue Res 2016 Feb;363(2):497-511; http://dx.doi.org/10.1007/s00441-015-2207-7
  • Petrov T, Howarth AG, Krukoff TL, Stevenson BR. Distribution of the tight junction-associated protein ZO-1 in circumventricular organs of the CNS. Brain Res Mol Brain Res 1994; 21:235-46; PMID:8170348; http://dx.doi.org/10.1016/0169-328X(94)90254-2
  • Seo Y, Takamata A, Ogino T, Morita H, Nakamura S, Murakami M. Water permeability of capillaries in the subfornical organ of rats determined by Gd-DTPA(2-) enhanced 1H magnetic resonance imaging. J Physiol 2002; 545:217-28; PMID:12433962; http://dx.doi.org/10.1113/jphysiol.2002.027227
  • Longatti P, Porzionato A, Basaldella L, Fiorindi A, De Caro P, Feletti A. The human area postrema: clear-cut silhouette and variations shown in vivo. J Neurosurg 2015; 122:989-95; PMID:25594320; http://dx.doi.org/10.3171/2014.11.JNS14482
  • Prockop LD, Naidu KA, Binard JE, Ransohoff J. Selective permeability of [3H]-D-mannitol and [14C]-carboxyl-inulin across the blood-brain barrier and blood-spinal cord barrier in the rabbit. J Spinal Cord Med 1995; 18:221-6; PMID:8591066
  • Watson PM, Paterson JC, Thom G, Ginman U, Lundquist S, Webster CI. Modelling the endothelial blood-CNS barriers: a method for the production of robust in vitro models of the rat blood-brain barrier and blood-spinal cord barrier. BMC Neurosci 2013; 14:59; PMID:23773766; http://dx.doi.org/10.1186/1471-2202-14-59
  • Ge S, Pachter JS. Isolation and culture of microvascular endothelial cells from murine spinal cord. J Neuroimmunol 2006; 177:209-14; PMID:16806499; http://dx.doi.org/10.1016/j.jneuroim.2006.05.012
  • Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M. The blood-spinal cord barrier: morphology and clinical implications. Ann Neurol 2011; 70:194-206; PMID:21674586; http://dx.doi.org/10.1002/ana.22421
  • Lee PD, Hintz RL, Sperry JB, Baxter RC, Powell DR. IGF binding proteins in growth-retarded children with chronic renal failure. Pediatr Res 1989; 26:308-15; PMID:2552387; http://dx.doi.org/10.1203/00006450-198910000-00005
  • Deli MA, Németh L, Falus A, Abrahám CS. Effects of N,N-diethyl-2-[4-(phenylmethyl)phenoxy]ethanamine on the blood-brain barrier permeability in the rat. Eur J Pharmacol 2000; 387:63-72; PMID:10633162; http://dx.doi.org/10.1016/S0014-2999(99)00796-7
  • Farkas G, Márton J, Nagy Z, Mándi Y, Takács T, Deli MA, Abrahám CS. Experimental acute pancreatitis results in increased blood-brain barrier permeability in the rat: a potential role for tumor necrosis factor and interleukin 6. Neurosci Lett 1998; 242:147-50; PMID:9530927; http://dx.doi.org/10.1016/S0304-3940(98)00060-3
  • van Vliet EA, Otte WM, Gorter JA, Dijkhuizen RM, Wadman WJ. Longitudinal assessment of blood-brain barrier leakage during epileptogenesis in rats. A quantitative MRI study. Neurobiol Dis 2014; 63:74-84; PMID:24321435; http://dx.doi.org/10.1016/j.nbd.2013.11.019
  • Bake S, Friedman JA, Sohrabji F. Reproductive age-related changes in the blood brain barrier: expression of IgG and tight junction proteins. Microvasc Res 2009; 78:413-24; PMID:19591848; http://dx.doi.org/10.1016/j.mvr.2009.06.009
  • Mendonça MC, Soares ES, de Jesus MB, Ceragioli HJ, Ferreira MS, Catharino RR, da Cruz-Höfling MA. Reduced graphene oxide induces transient blood-brain barrier opening: an in vivo study. J Nanobiotechnol-ogy 2015; 13:78; http://dx.doi.org/10.1186/s12951-015-0143-z

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