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. 2011 Jan 18;8(1):3.
doi: 10.1186/2045-8118-8-3.

Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences

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Free PMC article

Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences

Zoran Redzic. Fluids Barriers CNS. .
Free PMC article

Abstract

Efficient processing of information by the central nervous system (CNS) represents an important evolutionary advantage. Thus, homeostatic mechanisms have developed that provide appropriate circumstances for neuronal signaling, including a highly controlled and stable microenvironment. To provide such a milieu for neurons, extracellular fluids of the CNS are separated from the changeable environment of blood at three major interfaces: at the brain capillaries by the blood-brain barrier (BBB), which is localized at the level of the endothelial cells and separates brain interstitial fluid (ISF) from blood; at the epithelial layer of four choroid plexuses, the blood-cerebrospinal fluid (CSF) barrier (BCSFB), which separates CSF from the CP ISF, and at the arachnoid barrier. The two barriers that represent the largest interface between blood and brain extracellular fluids, the BBB and the BCSFB, prevent the free paracellular diffusion of polar molecules by complex morphological features, including tight junctions (TJs) that interconnect the endothelial and epithelial cells, respectively. The first part of this review focuses on the molecular biology of TJs and adherens junctions in the brain capillary endothelial cells and in the CP epithelial cells. However, normal function of the CNS depends on a constant supply of essential molecules, like glucose and amino acids from the blood, exchange of electrolytes between brain extracellular fluids and blood, as well as on efficient removal of metabolic waste products and excess neurotransmitters from the brain ISF. Therefore, a number of specific transport proteins are expressed in brain capillary endothelial cells and CP epithelial cells that provide transport of nutrients and ions into the CNS and removal of waste products and ions from the CSF. The second part of this review concentrates on the molecular biology of various solute carrier (SLC) transport proteins at those two barriers and underlines differences in their expression between the two barriers. Also, many blood-borne molecules and xenobiotics can diffuse into brain ISF and then into neuronal membranes due to their physicochemical properties. Entry of these compounds could be detrimental for neural transmission and signalling. Thus, BBB and BCSFB express transport proteins that actively restrict entry of lipophilic and amphipathic substances from blood and/or remove those molecules from the brain extracellular fluids. The third part of this review concentrates on the molecular biology of ATP-binding cassette (ABC)-transporters and those SLC transporters that are involved in efflux transport of xenobiotics, their expression at the BBB and BCSFB and differences in expression in the two major blood-brain interfaces. In addition, transport and diffusion of ions by the BBB and CP epithelium are involved in the formation of fluid, the ISF and CSF, respectively, so the last part of this review discusses molecular biology of ion transporters/exchangers and ion channels in the brain endothelial and CP epithelial cells.

Figures

Figure 1
Morphology of choroid plexus epithelium (CPE) in situ and in primary culture. A. Ultrastructure: CP from lateral ventricle of an adult Sprague-Dawley rat. Apical membrane (CSF-facing) shows numerous microvilli (Mv) and many intracellular mitochondria (M). J refers to the tight junction welding two cells at their apical poles. C: centriole. G and ER: Golgi apparatus and endoplasmic reticulum. Nucleus (Nu) is oval and has a nucleolus. Arrowheads point to basal lamina at the plasma face of the epithelial cell; the basal lamina separates the CPE above from the interstitial fluid below. Basal labyrinth (BL) is the intertwining of basolateral membranes of adjacent cells. Choroidal morphology resembles proximal tubule, consistent with both cell types rapidly turning over fluid. Scale bar = 2 μm, reproduced from [248] with permission. B. Phase-contrast micrographs of 8d-old sheep CPE cells cultured on laminin-coated filters shows a typical cobblestone arrangement of polygonal cells (scale bar 20 μm). C. Eight-day-old sheep CPE cells grown on laminin-coated filters were stained with primary antibodies against occludin and then with FITC conjugated secondary antibodies. A continuous circumferential distribution of fluorescence consistent with the establishment of TJs in CPEC monolayer is shown. Scale bar 20 μm. Images B and C reproduced from [257].
Figure 2
Schematic representation of tight junctions between two adjacent cells. In general, TJs at the BBB and in the CP epithelium are similar, but they express different claudins (that are not shown in this figure). This is probably an important structural difference underlying the lower values of TEER across CP epithelium compared to TEER values across the brain endothelium.
Figure 3
Solute carrier transporters (SLCs) in the BECs (A) and in the CP epithelial cells (B). Only SLC involved in transport of monosaccharides, amino-acids, monocarboxylic acids and peptides are shown. A. A proposed model of SLCs distribution in BECs. A question mark with MCT8 transporter indicates that in BECs this transporter is detected at the transcript level, but its cellular localization is not clear. Also, there are conflicting data on LAT2 expression, also indicated by a question mark. Members of the peptide transporters family (PTR) are not present in BECs. B. A proposed model of SLCs distribution in CPE cells. A question mark indicates that there is conflicting data about presence of SGLT1 in CPE cells. Symbols in superscript indicate: a -GLUT1 is present in the apical membrane of the CPE cells, but it is much less abundant in that membrane than in the basolateral membrane; b - System y+ was detected at the transcript level in CPE cells and functional uptake studies indicated that it was located in the basolateral membrane; c - Uptake studies in the rat in vivo indicated that EAAT1 substrates aspartate and glutamate were taken by CPE from CSF side by a saturable and stereospecific mechanism that did not show cross-inhibition with neutral amino acid. However, EAAT1 is not expressed in normal CPE in humans and is expressed in dedifferentiated CPE cells in CP tumors; d-CPE cells express MCT 1, but at much lower level than BECs and cellular localization of this isoform includes both basolateral and apical membranes. CPE cells also express a lysosomal AA transporter LYAAT1, which is located intracellularly.
Figure 4
Distribution of ABC-transporters, organic anion/cation transporters and organic anion transporting polypeptide expression in the BECs (A) and in the CP epithelium (B). Members of the ABC family are presented in red, while SLC members are presented in various tones of blue. Some data indicate that in the BECs Mrp1 and P-gp may also be present in organelles and nuclear envelope. Membrane localization of Mrp1 in BECs is not completely clear, with some reports indicating that it is present at the luminal side, while others indicating that it is scarce and probably located at the abluminal side. Mrp5 was detected in the CPE cells at the transcript level, but there are no functional or immunocytochemical data so far, indicating its cellular localization (asterisk). The same stands for Oat2, Oct1-3 and Oatp9.
Figure 5
Distribution of ion transporters and channels in the BECs (A) and in the CP epithelium (B). Only those transporters and channels that play a role in vectorial transport of Na+, Cl-, HCO3- and K+ are shown. These include Na+, K+-ATPase, potassium channels Kir and Kv, chloride/bicarbonate channel Clir and members of the SLC: Na+, HCO3- cotransporters 1 and 2 (NBCn1 and 2), Cl-, HCO3- exchangers 1 and 2 (Ae 1 (in the BBB, figure A) and Ae2 (in the CP, figure B), Na+, H+ exchanger 1 and 2 (Nhe1 and Nhe2), K+-Cl--cotransporters 3 and 4 (KCC3 and 4, in the CP, figure B), Na+-K+-2Cl- cotransporter 1 (NKCC1, in the BBB, figure A) and electrogenic Na+, HCO3- exchanger (NBCe2, in the CP, figure B). In addition, localization of two carbonic anhydrase isoenzymes in the CP epithelium (figure B), CA2 and CA12 are shown, as well as localization of aquaporin 1 (AQP1). Symbol * indicates that NBCn1 was detected in CPE, but it probably does not play a role in vectorial transport of these two ions.

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