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Choroid Plexus and the Blood–Cerebrospinal Fluid Barrier in Disease

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Choroid Plexus and the Blood–Cerebrospinal Fluid Barrier in Disease Solár et al. Fluids Barriers CNS (2020) 17:35 https://doi.org/10.1186/s12987-020-00196-2 Fluids and Barriers of the CNS REVIEW Open Access Choroid plexus and the blood–cerebrospinal fuid barrier in disease Peter Solár1,2†, Alemeh Zamani1†, Lucie Kubíčková1, Petr Dubový1 and Marek Joukal1* Abstract The choroid plexus (CP) forming the blood–cerebrospinal fuid (B-CSF) barrier is among the least studied structures of the central nervous system (CNS) despite its clinical importance. The CP is an epithelio-endothelial convolute comprising a highly vascularized stroma with fenestrated capillaries and a continuous lining of epithelial cells joined by apical tight junctions (TJs) that are crucial in forming the B-CSF barrier. Integrity of the CP is critical for maintain- ing brain homeostasis and B-CSF barrier permeability. Recent experimental and clinical research has uncovered the signifcance of the CP in the pathophysiology of various diseases afecting the CNS. The CP is involved in penetra- tion of various pathogens into the CNS, as well as the development of neurodegenerative (e.g., Alzheimer´s disease) and autoimmune diseases (e.g., multiple sclerosis). Moreover, the CP was shown to be important for restoring brain homeostasis following stroke and trauma. In addition, new diagnostic methods and treatment of CP papilloma and carcinoma have recently been developed. This review describes and summarizes the current state of knowledge with regard to the roles of the CP and B-CSF barrier in the pathophysiology of various types of CNS diseases and sets up the foundation for further avenues of research. Keywords: Choroid plexus, Blood–cerebrospinal fuid barrier, Infammatory diseases, Neurodegenerative disease, Autoimmune disease, Stroke, Carcinoma Background the B-CSF barrier allows blood-borne pathogenic com- Te central nervous system (CNS) is protected against ponents to enter the CSF, they would contribute to harmful substances contained in the blood by the blood– neurotoxicity and neuronal dysfunction. On the other brain barrier (BBB) and the blood–cerebrospinal (B-CSF) hand, reduction in the efux of waste products (and the barrier [1–3]. Even though the B-CSF barrier is more consequent presence of neurotoxic residues inside the accessible than the BBB for many foreign invaders, the brain), could interfere with neurotransmission, and lead BBB has received more attention regarding CNS pathol- to various disorders. Te mechanism(s) by which a dys- ogy. Nevertheless, there is a growing body of evidence functioning B-CSF barrier contributes to pathogenesis showing that the B-CSF barrier plays a crucial role in is still poorly understood. Terefore, we aim to review the spread of infammatory reactions from the periph- recent knowledge of the changes and regulation of the ery to the CNS and contributes to the pathogenesis and B-CSF barrier in diferent diseases. A better understand- progression of various neurological disorders [4–7]. If ing of the role played by the B-CSF barrier in CNS dis- eases can shed light on identifying therapeutic targets in neuropathology. *Correspondence: [email protected] †Peter Solár and Alemeh Zamani contributed equally to this work 1 Department of Anatomy, Cellular and Molecular Neurobiology Research Group, Faculty of Medicine, Masaryk University, CZ-625 00 Brno, Czech Republic Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Solár et al. Fluids Barriers CNS (2020) 17:35 Page 2 of 29 Morphology and physiology of the B‑CSF barrier KCC3, Na+-HCO3− cotransporters (NBCn1 and NCBE/ Te B-CSF barrier is localized in the choroid plexus (CP) NBCn2), Cl−/HCO3− exchanger (AE2), glucose trans- of the brain ventricles. Te CP is an epithelio-endothelial porter-1 (GLUT1) and AQP1 [18, 32–36]. convolute, comprising a highly vascularized stroma with NKCC1 that is expressed in the apical membrane of CP connective tissue, and epithelial cells [8–11]. Te stroma may contribute as much as half of the CSF production, comprises fenestrated capillaries with 60 to 80 nm fen- via ion-mediated cotransport of water [37, 38]. estrations surrounded by connective tissue stroma with Transcellular water transport is supported by a fam- immune cells. Te ventricular side of the stroma is cov- ily of AQPs. AQP1 is expressed in the basolateral mem- ered by a single layer of cuboidal epithelial cells [10, 11]. brane of the CP epithelial cells but at much lower levels Epiplexus (Kolmer) cells (KCs) with phagocytic activ- than those in the apical membrane [39–41]. Based on ity adhere to the ventricular side of epithelial cells [12] experimental fndings, it seems that AQP1 contributes (Fig. 1). Te KCs communicate with epithelial cells of the to the production of 20–25% of the CSF [42]. AQP4 is through pannexin-1 channels and seem to be the scaven- expressed in the cytoplasm but not in the apical or baso- gers of the brain ventricular system [13, 14]. Te CP of lateral membrane of CP epithelial cells. Difuse cyto- the lateral ventricle is a thin undulating veil while in the plasmic distribution of AQP4 and AQP5 suggests their fourth ventricle it is highly lobulated and more complex. possible expression in the membranes of intracellular Te CP in the third ventricle is much smaller in size and organelles. Evidence of AQP7 in the apical membrane has an intermediate appearance [10]. of the CP cells suggests a possible cooperation of AQP7 Te primary function of the CP is to produce CSF with AQP1 in CSF secretion [38, 43–45]. It was also sug- and form the B-CSF barrier. Besides these roles, it has gested that GLUT1 may increase the permeability of the recently been described that the CP might be a part of basal membrane of CP epithelial cells to water [19, 38]. the circadian regulatory system [15]. It has also been CSF secretion is infuenced by the action of the auto- shown that the B-CSF barrier expresses chemosensory nomic nervous system. Te capillaries and cuboidal receptors such as odorant receptors, vomeronasal recep- epithelial cells are innervated by adrenergic nerve fb- tors, and taste receptors. Tese receptors could help to ers arising from the superior cervical ganglia [46, 47]. In monitor the composition of blood, CSF and interstitial addition, CP capillaries and cuboidal epithelial cells are fuid, and, through transporters upon ligand-binding, to also innervated by parasympathetic nerve fbers probably control alterations in brain fuid composition [16]. related to the glossopharyngeal and vagus nerves [48, 49]. Parasympathetic stimulation reduces Na +-K+ ATPase Cerebrospinal fuid production and transport systems activity mediated by nitric oxide formation, and results in the B‑CSF barrier in reduced CSF secretion [50]. Moreover, serotoninergic A classic and widely-accepted hypothesis claims that the and peptidergic fbers in the CP also possibly infuence primary function of CP epithelial cells is secretion of cer- CSF production [48, 51, 52]. ebrospinal fuid (CSF) into the brain ventricles. Much lit- Specifc transport mechanisms employing a variety of erature has been produced pointing to the likelihood that transmembrane proteins that enable selective passage of indeed the CP may produce more than 50% of total CSF molecules form important components of the B-CSF bar- [17–23]. Te remaining CSF is derived from the intersti- rier. Tey are crucial for the exchange of metabolites and tial fuid of the brain which is produced by the BBB and xenobiotics between blood and CSF. Tese transporters the ependymal cells lining the ventricles [18, 24–26]. Te mainly belong to the ATP-binding cassette (ABC) trans- total volume of CSF in humans is about 140 ml, and every porter and solute carrier (SLC) super-families [21]. Two day about 600 ml CSF is produced [27]. main types of ATP-biding cassette (ABC) transporters Te formation of CSF in CP depends mainly on Na+, are expressed in the CP; the multidrug resistance-related + − 3− K , Cl , HCO and H2O transport. Te osmotic gradi- proteins (MRPs) and multidrug transporters P-glycopro- ent created by ion movement drives the secretion of water tein (PgP) [53]. Te MRPs are selectively expressed on [28–31]. A number of transporters were found on the the apical or basolateral side of the epithelial cells, and apical membrane of the CP epithelial cells, including K + move metabolic waste products and harmful molecules channels (Kv1.3; Kv1.1 and Kir7.1), Na+-HCO3− cotrans- out of the CNS. Te MRP1 protein transporter contrib- porter (NBCe2), Na+-K+-2Cl− cotransporter (NKCC1), utes to the protection of the B-CSF barrier against heavy the K+-Cl− cotransporter KCC4, Na +/H+ exchanger metal ions, toxins, and various xenobiotics [54–56]. On (NHE1), Cl− channels (VRAC and Clir), Na+-K+-ATPase the other hand, PgP is localized on the apical side of CP and aquaporin (AQP1).
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