PMC:6194691 / 55603-68411 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/6194691","sourcedb":"PMC","sourceid":"6194691","source_url":"https://www.ncbi.nlm.nih.gov/pmc/6194691","text":"Transporters at the blood–brain barrier\nThe membranes of the endothelial cells that constitute the blood–brain barrier possess transporters for many different types of solutes. These transporters may be present on luminal, abluminal or both surfaces of the endothelial cells. Prominent among them are transporters for common nutrients and waste products of metabolism: GLUT1 for glucose, MCT1 for lactic acid and other small monocarboxylic acids, a range of transporters for amino acids, and several for nucleosides. There are also ion transporters involved in maintenance of the ionic composition of the brain fluids. Many of the transporters are specific and are involved in moving the normal constituents of brain extracellular fluid. Some of these are considered in Sect. 5. In addition there are also less specific transporters. Many of these can mediate efflux of a variety of other substrates including many exogenous substances and toxic occasional products of metabolism.\nEvidence concerning the presence and identity of many of these transporters has been reviewed elsewhere with studies being conducted primarily at the level of transcript [173–178], protein [31, 44, 58, 176, 179–188] and/or function [4, 20, 31, 46, 55–57, 179, 189–200]. The reports by Roberts et al. [180] and Kubo et al. [58] and reviews by Hawkins et al. [44], Redzic [31], Campos-Bedolla [57], Worzfeld and Schwaninger [187] and Nalecz [200] have been useful as sources of information about the localization of transporters to the luminal or abluminal membranes.\nThis review will not seek to provide yet another comprehensive survey. Extensive lists of transporters and substrates are available in many of the cited references and for SLC transporters at the BioParadigms website [201, 202].\n\nABC efflux transporters\nIt has long been appreciated that the brain represents a pharmacological sanctuary and is selectively “protected” from the toxic effects of many chemotherapeutic agents. These include vincristine and doxorubicin (aka adriamycin), which fail to penetrate the blood–brain barrier as well as their lipid solubilities would suggest [162]. A major part of this failure to penetrate has since been attributed to the presence of the multidrug transporter, P-glycoprotein. Absence of this transporter in knock-out mice was shown to allow entry of toxic agents including ivermectin [203]. P-glycoprotein was found to be located in the luminal membrane (see e.g. [204–209]) of the endothelial cells and is believed to act there to transport substrates out of the cells so rapidly that little remains to penetrate the abluminal membrane and enter the brain.\nIt is believed by many that P-glycoprotein, a transmembrane protein, acts by removing its lipophilic substrates from the lipid layer of the cell membrane, depositing them back into the blood [210–213]. Its structure has been investigated in both substrate-free and inhibitor bound conformations [213] and binding sites for various of its many substrates identified within the large cavity seen in the substrate-free conformation. It is the binding and hydrolysis of ATP that provides the motive force leading to a large conformational change in the P-glycoprotein and the transfer and expulsion of its substrates. There are two ATP binding sites located on the cytoplasmic side of the protein.\nP-glycoprotein, otherwise called ABCB1, is a member of the ABC (ATP-Binding Cassette) family of proteins many of which are primary active transporters that utilize the hydrolysis of ATP to fuel substrate transport. Since its discovery, other ABC active transporters with broad substrate profiles have been found in the luminal membrane of the endothelial cells. These include Breast Cancer Resistance Protein, BCRP (ABCG2) [180, 197, 214–218] and Multidrug Resistance Proteins, MRPs 4 and 5 (ABCC4 and 5) [180, 197, 209, 218–221]. MRP1 (ABCC1) has also been implicated but levels of this transporter are thought to be low in brain endothelial cells in situ and only increase in cultured brain endothelial cells once they are removed from the brain microenvironment [180, 184, 218, 222–226]. MRP1 and MRP2 are apparently upregulated and clearly expressed in epilepsy [227–229].\nThe role of efflux from endothelial cell to blood by ABC transporters in preventing influx of many substances from blood into the brain has been extensively reviewed (see e.g. [57, 196, 197, 199, 221, 230–234]. The regulation of P-glycoprotein, BCRP and MRP2 at the blood–brain barrier has been reviewed by Miller [221].\nThe role of ABC transporters in efflux from the brain parenchyma differs depending on the nature of the substrate. As described in Fig. 9, for substances that are sufficiently lipid soluble to cross the endothelial cell membranes rapidly by passive transport, the presence of ABC efflux transporters can greatly reduce blood-to-brain influx, as observed experimentally. However, as also explained in Fig. 9 the ABC transporters in the luminal membrane will have only a modest effect, e.g. a doubling, on the rate of brain-to-blood efflux. This may be of little consequence as the rate of efflux for lipid soluble substances is already high.\nFig. 9 The influence of ABC transporters on the movements of lipophilic substances. The substance is presumed to be able to enter and leave the endothelial cells by diffusion with rate constant kdiff., which for simplicity in this example is assumed to be same on both sides. The substance is expelled from the cell by ABC transporters on the luminal side at a rate, kactiveccell. With these assumptions the effect of the ABC transporters on influx can be calculated by setting cisf = 0 and the effect on efflux by setting cplasma = 0. In both sets of equations, the first line states that at steady-state the net flux into the cell on one side must equal the net flux out of the cell on the other. From the next to the last lines of both sets of equations, if the rate of ABC mediated expulsion from the cell is small or zero, the rate constants for both influx and efflux are (kdiff./2). By contrast from the last lines if the rate of ABC mediated expulsion is large, influx to the brain, J→, becomes very small, while efflux from the brain, J←, is doubled compared to the efflux with no ABC transporter\nThe role of ABC transporters for solutes with low passive permeability across the membranes is considered in the next section.\n\nEfflux mediated in part by SLC solute transporters\nMany of the SLC (solute carrier) transporters (see [202] for a list) are present in the membranes of the endothelial cells of the blood–brain barrier. Some are considered in connection with the transport of specific solutes in Sect. 5. Others, primarily from the SLC21 (OATPs, organic anion transporting polypeptides) and SLC22 (OATs and OCTs, organic anion transporters and organic cation transporters) families are associated with transport of a variety of organic anions and cations. These have been reviewed frequently and extensively [57, 176, 200, 218, 235–246]. (Uppercase labels, e.g. SLC or OAT, strictly refer to human sequences and proteins, while mixed-case labels, e.g. Slc or Oat, refer to any other species. In this review uppercase is also used when there is no intention to specify species).\nThere is little quantitative data on the efflux of organic anions and cations from the parenchyma in humans though many are known to be transported. In rodents more information is available for transfer of organic anions than cations. Table 1 lists some examples of organic anions/neutral molecules for which brain-to-blood transport rate constants have been determined. These are all believed to be substrates for Oat3 (Slc22a8) and/or one or more of the Oatp transporters present at the blood–brain barrier. In broad terms [238], small hydrophobic anions are substrates for Oats (Slc22 family) while larger amphipathic anions are substrates for Oatps (Slc21 family, whose member names start with Slco, see [247]). For comparison Table 1 also lists rate constants and clearances for examples of markers for perivascular efflux. It is clear that the rates of elimination of the Slc substrates are considerably greater than could be supported by perivascular efflux alone.\nTable 1 Comparison of rate constants for efflux and clearances for Slc22 and Slco substrates and the perivascular markers inulin, mannitol and sucrose\nkeff/min−1 t1/2/min Vd/mL/g CL/µL g−1 min−1 Ref # Notes\nSlc substrates Rat unless stated otherwise\n p-Aminohippuric acid (PAH) 0.059 12 0.80 47 [558] Influx much slower than efflux\n p-Aminohippuric acid (PAH) 0.039 18 [559] Abl. Oat3 based on inhibitors, lum. Mrp4 possible based on kidney [560]\n p-Aminohippuric acid (PAH) 0.0175 40 [131]\n Penicillin G, benzylpenicillin 0.043 16 [559] Oat3 based on inhibitors\n Taurocholate 0.023 30 [561]\n BQ-123 0.0078 100 [561]\n Estrone sulfate 0.066 9.9 1.1 75 [562]\n Estrone 0.061 11 3.3 227 [562]\n Dehydroepiandrosterone sulfate (DHEAS) 0.027 26 118 [563] Influx much slower than efflux, Oatp2\n Estradiol-17beta-glucuronide (E217betaG) 0.037 19 [564] Oatp2, 40% and Oat3 20%\n Pravastatin 0.060 12 0.99 59 [565] Oat3 (Slc22a8) and Oatp2 (Slco1a4) + others\n Pitavastatin 0.026 27 14 364 [565] Oat3, Oatp2 (Slco1a4) +others +diffusion\n Homovanillic acid 0.017 40.8 [566] Oat3 from inhibitors\n Indoxyl sulfate 0.011 64 [567] Oat3 and others\n Pemetrexed 0.018 39 0.62 11 [568] Mouse. Oat3 and unknown (not Mrp2 not Bcrp)\n Methotrexate 0.024 29 0.85 20 [568] Oat3 and Bcrp suggested\n Buprenorphine 0.025 27.5 6.1 154 [569] Pgp and unknown, possibly diffusion\n AZT, (3′-azido-3′-deoxythymidine) 0.032 22 [570] Oat3 from benzylpenicillin inhibition\n DDI, (2′,3′-dideoxyinosine) 0.253 2.8 [570] Oat3 from benzylpenicillin inhibition + diffusion\nMarkers for perivascular elimination\n Inulin 0.006 awake0.016 asleep 11543 0.2* 1.23.2 [128] Mouse\n Inulin 0.003 230 0.2* 0.6 [62] Mouse\n Inulin 0.005 135 0.2* 1 [131] Rat\n Mannitol 0.004 170 0.2* 0.8 [25] Mouse\n Sucrose 0.0028 awake0.0043 anesth. 245160 0.2* 0.560.86 [131] Rat\n Albumin 0.006 115 0.2* 1.2 [131] Rat\n Dextran-10K 0.0035 197 0.2* 0.7 [131] Rat\n Dextran-70K 0.004 170 0.2* 0.8 [131] Rat\nkeff rate constant for efflux determined from the time course of the decrease in concentration after injection of solute into the parenchyma (brain efflux index for the Slc substrates relative to inulin; these underestimate keff for values less than ~ 0.01 min−1 see [131]); t1/2 = 0.69/(rate constant) is the half-life; Vd, volume of distribution in the parenchyma determined using brain slices (ISF volume for inulin and mannitol); CL = Vd × keff, the clearance. For the Slc substrates more than one transporter in each membrane is likely to be involved in the transport\n* Assumed equal to ISF volume\nAs indicated in Fig. 10 transport from the parenchyma into the endothelial cells occurs via one or more of the SLC transporters, while exit from the endothelial cells to plasma occurs via either SLC or ABC transporters. For many of the anions efflux from brain to blood is clearly an active uphill process suggesting that the ABC route is dominant (for a caveat see.12) Transport across either membrane can be rate limiting and in many cases transport across each can occur by more than one route. As a consequence demonstration that a specific inhibitor of a transporter reduces the rate of efflux is evidence for involvement of that transporter, but failure to inhibit is relatively uninformative.\nFig. 10 Transport of organic anions across the blood–brain barrier. Organic anion transporters at the blood–brain barrier. The principal known transporters in the rat are shown. In human OAT3 is abluminal, while both OATP1A4 and OATP2B1 are present on both membranes. The ABC efflux pumps, P-gp, BCRP, MRP4 and MRP5, are all localized to the luminal, plasma facing, membrane. The Oat and Oatp transporters are exchangers (see Footnote 12). Localizations from [180] and the references in Table 1\nFor the SLC substrates in Table 1 the half-lives are shorter than the 1–2 h characteristic of markers eliminated from the parenchyma by perivascular efflux (see Sect. 3). As noted earlier, shorter half-lives imply that there are mechanisms for elimination other than perivascular. This is reinforced by noting that the clearances for those solutes for which volumes of distribution are available are much greater than the clearance associated with the perivascular route (see Sect. 3.2). There is ample further evidence (see the references for the entries in Table 1) for the importance of the Oat and Oatp transporters in the elimination of these solutes from the parenchyma including saturation, competition, the availability of transport inhibitors, and the rapid appearance of effluxed material in venous blood draining the 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