PMC:6194691 / 127170-136877
Annnotations
{"target":"http://pubannotation.org/docs/sourcedb/PMC/sourceid/6194691","sourcedb":"PMC","sourceid":"6194691","source_url":"https://www.ncbi.nlm.nih.gov/pmc/6194691","text":"Amino acid transporters at the blood–brain barrier\nThe transporters currently thought to be involved in amino acid transport across the blood–brain barrier are indicated in Fig. 19. These will be discussed below according to the categories of amino acids transported.\nFig. 19 Amino acid transporters thought to exist at the blood–brain barrier. Based on Nalecz [200]; Broer [393]; Mann et al. [520]; O’Kane et al. [657]; and Hawkins et al. [44]. #See [44, 398] but contrast [399, 400]\nAnionic amino acids, in particular glutamate, are transported by EAATs 1, 2 and/or 3 (coded by SLC1A3, 2, 1 respectively) which are found only in the abluminal membrane of the endothelial cells [387]. These EAATs mediate co-transport of the anionic amino acid together with 3 Na+ ions and 1 H+ ion followed by return transport of 1 K+ ion [388–390]. Because the electrochemical gradient for Na+ is directed from ISF into the endothelial cells and 3 Na+ ions are transported, this coupling renders the amino acid transport effectively unidirectional into the cells. Glutamate is also produced within the endothelial cells from breakdown of glutamine mediated by glutaminase [360]. Glutamate in the endothelial cells can then either be metabolized releasing NH4+, as argued by Helms and colleagues [391, 392], or be transported to blood plasma by a transporter other than an EAAT. Glutamate metabolism within endothelial cells is analogous to the extensive metabolism known to occur within gut epithelial cells (see e.g. [393]). Glutamate transport from brain endothelial cells to plasma has been demonstrated after sensory stimulation in vivo, which increases glutamate production [394]. This transport is likely to be via the glutamate/cystine exchanger, Xc− (SLC7A11 + SLC3A2), [200, 395]), though there is also evidence for a transporter, yet to be identified, that functions in the absence of cystine [396].\nCationic amino acids such as arginine and lysine are transported by CAT-1 (SLC7A1), which is known to exist in the abluminal membrane of the endothelial cells. Transport of these amino acids across the luminal membrane is less well-characterized but may be also via CAT-1 or possibly ATB0,+ (SLCA14). Transport of cationic amino acids by CAT-1 can involve exchange of one amino acid for another (trans-stimulation see Sect. 5.3.1), but this is not essential [397]. There may be at least one more transporter for cationic amino acids at the abluminal membrane (but see [398]). Hawkins et al. [44] reported that cationic amino-acid transport across both membranes can be inhibited by a number of neutral amino acids in the presence of Na+. CAT-1 is thought not to be so affected [397, 399, 400]. The additional transporter may be y+L [4F2hc (SLC3A2) + either y+LAT2 (SLC7A6) or y+LAT1 (SLC7A7)] [399, 400].\nNeutral amino acids are transported by several systems as indicated in Fig. 19.System L, primarily the heterodimer 4F2hc/Lat1 (Slc3a2 + Slc7a5) which is present in both membranes and functions independently of Na+;\nSystem A, primarily ATA2 (Slc38a2) in the abluminal membrane which because it is a Na+-linked transporter is biased towards transport from ISF into the endothelial cells;\nASC, primarily ASCT2 (Slc1a5), an obligatory exchanger that requires the presence of Na+-but is not driven by the Na+ gradient;\nSystem Na+-LNAA a Na+-linked system whose molecular basis is still unknown;\nATB0,+ (SLC6A14) which allows net fluxes without exchange;\nAnd possibly the y+L transporter [4F2hc (SLC3A2) + either y+LAT2 (SLC7A6) or y+LAT1 (SLC7A7)].\nThe large influxes of neutral amino acids from blood-to-brain seen in the early work and ascribed to system L have subsequently been shown to be mediated by 4F2hc/Lat1 [401–403]. The discovery that not only can this system mediate exchanges of amino acids [404, 405] but the exchange is obligatory [406–408] has far reaching consequences for amino acid transport at the blood–brain barrier [409]. It provides an important part of the explanation for how it is that there are large unidirectional fluxes (influx and efflux) but only small net fluxes. In order for system L to mediate a net inward flux of one amino acid, it must have net outward flux of another. An exchanger of neutral solutes, like system L, tends to equilibrate the concentration ratios for all of its substrates. Thus predicting the flux of any one of the amino acids across a membrane requires knowledge of the concentrations of all of the substrates on both sides of the membrane.20 Consumption of any system L substrate within the parenchyma will by reducing its ISF concentration tend to lead to net inward flux of that substrate and net outward flux of others. Similarly production of any system L substrate will tend to lead to its net outward flux together with net inward flux of others.\nThe function of 4F2hc/Lat1 (Slc3a2/Slc7a5), the principal component of system L, was explored in mice by Tarlungeanu et al. [410]. They compared the concentrations of amino acids in brain (amount per unit weight of brain) between a conditional Slc7a5 knockout [411] and normal controls. In adult mice they found that the levels of methionine, leucine and isoleucine in the knockouts were about 0.66 times the levels in normals, i.e. a reduction of about 35%. This suggests that there is normally a net inward flux of these amino acids via 4F2hc/Lat1 but that there are other routes at least as important. By contrast levels of phenylalanine, proline, glycine, threonine, and serine in the knockouts were about 1.3 times higher than in normals, i.e. an increase of about 30%. This suggests that for these amino acids there is normally a net outward flux via Lat1 but that there are other important routes for their elimination. More dramatically with histidine the level in knockouts was sevenfold higher, a 600% increase compared to normals. This suggests that 4F2hc/Lat1 is normally the main route for eliminating histidine from the parenchyma and that a net inward flux of histidine occurs by some route other than 4F2hc/Lat1. However, it is important to note that while these results show that 4F2hc/Lat1 is very important for the fluxes of histidine, they do not in themselves show that histidine efflux is a large fraction of the total efflux carried by 4F2hc/Lat1. Further evidence for exchanges involving histidine have been obtained using 4F2hc/Lat1 expressed in proteoliposomes. High concentrations of cysteine inside the vesicles can allow or drive influx of histidine and high concentrations of many amino acids outside of the vesicles can allow or drive efflux of histidine [412].\nIt has been tempting to propose that the combined net flux of neutral amino acids, inward or outward, is determined by their fluxes via systems other than system L and by their synthesis and breakdown in the parenchyma. System L is, however, still important, because it is the combined action of system L with the other transporters that determines which of the neutral amino acids move inwards and which outwards. A coherent overall account of the transport of neutral amino acids across the blood–brain barrier is still awaited.\nWith regard to glutamine, which is synthesized within the parenchyma, it has been tempting to propose that a substantial part of its efflux occurs via a system L mediated exchange for the essential large neutral amino acids such as leucine, isoleucine, valine and phenylalanine entering the parenchyma. Indeed such exchanges can be observed with isolated microvessels under experimental conditions [413, 414]. However, there is no evidence for this effect under conditions that exist in vivo.\nThe observation that there is a net efflux of glutamine is especially important because it is present at high concentration in plasma and ISF and it is the obvious sink for excess NH4+ in the brain. Glutamine is a substrate not only of 4F2hc/LAT1 (system L) as outlined above but also of Snat3 (SLC38A3) (system N), ATA2 (SLC38A2) (system A), and CAT (SLC7A1) (system y+) [200]. Of these the principal transport that has been observed is mediated by system N. Localization of system N has been controversial. Lee et al. [360] (see also [44]) found that vesicles prepared from abluminal membranes displayed a Na+-linked transport for glutamine while vesicles prepared from luminal membranes had only Na+-independent transport. This combination would explain net outward flux of glutamine from the brain. However, Ennis et al. [415] found marked Na+-dependent tracer influx of glutamine. While there are alternatives (see footnote 3 on p. 9 in [4]) the simplest interpretation is that there are Na+-linked transporters in both membranes. More recently immunohistochemical localization studies [416] have shown Snat3 primarily on the abluminal membrane but also on the luminal membrane of brain capillaries. It should be noted that while linking transport of glutamine to that of a single Na+ confers a bias towards transport into the endothelial cells, it does not preclude flux in the opposite direction via the same transporter and thus it is possible that Snat3 is responsible for the transport across both membranes.\nAs already mentioned, Lee et al. [360] found that brain endothelial cells have glutaminase activity, and thus following glutamine transport from ISF into the cells, at least some of the glutamine will be broken down to glutamate and NH4+. Helms et al. [391, 392] have suggested that some of the glutamate can be metabolized further releasing more NH4+. As a consequence of metabolism within the endothelial cells, glutamine removal from the parenchyma and glutamine appearance in plasma need not be the same. Glutamine net flux cannot be assessed in 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