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Aquaporin-4 in Astroglial Cells in the CNS and Supporting Cells of Sensory Organs — A Comparative Perspective

View Article: PubMed Central - PubMed

ABSTRACT

The main water channel of the brain, aquaporin-4 (AQP4), is one of the classical water-specific aquaporins. It is expressed in many epithelial tissues in the basolateral membrane domain. It is present in the membranes of supporting cells in most sensory organs in a specifically adapted pattern: in the supporting cells of the olfactory mucosa, AQP4 occurs along the basolateral aspects, in mammalian retinal Müller cells it is highly polarized. In the cochlear epithelium of the inner ear, it is expressed basolaterally in some cells but strictly basally in others. Within the central nervous system, aquaporin-4 (AQP4) is expressed by cells of the astroglial family, more specifically, by astrocytes and ependymal cells. In the mammalian brain, AQP4 is located in high density in the membranes of astrocytic endfeet facing the pial surface and surrounding blood vessels. At these locations, AQP4 plays a role in the maintenance of ionic homeostasis and volume regulation. This highly polarized expression has not been observed in the brain of fish where astroglial cells have long processes and occur mostly as radial glial cells. In the brain of the zebrafish, AQP4 immunoreactivity is found along the radial extent of astroglial cells. This suggests that the polarized expression of AQP4 was not present at all stages of evolution. Thus, a polarized expression of AQP4 as part of a control mechanism for a stable ionic environment and water balanced occurred at several locations in supporting and glial cells during evolution. This initially basolateral membrane localization of AQP4 is shifted to highly polarized expression in astrocytic endfeet in the mammalian brain and serves as a part of the neurovascular unit to efficiently maintain homeostasis.

No MeSH data available.


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(a) Freeze fracture replica of rat brain tissue surrounding a capillary: the fracture plane goes through the lumen (L) of a capillary and the bordering endothelial cell (End). This is surrounded by astrocytes A1 and A2. The membrane of A1 indicated by the square is shown at higher magnification in b; (b) High densities of orthogonal arrays of particles (OAP) are found on astrocytic endfeet facing a basal lamina. The circled area is magnified further showing OAPs on the P-face (Pf) If: intermediate filaments; (c) Ependymal cells lining the ventricle; and (d), hippocampal astrocytes in rat brain stained for glial fibrillary acidic protein (GFAP, red) and AQP4 (green). Ependymal cells are positive for AQP4 at their basolateral membranes, bearing cilia apically (arrows). Brain astrocytes in d show high AQP4 binding at their endfeet surrounding capillaries (arrows). Scale bars: (a) 1 µm; (b) 0.1 µm; (c) 5 µm; (d) 20 µm; (a,b) are modified from [24].
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ijms-17-01411-f001: (a) Freeze fracture replica of rat brain tissue surrounding a capillary: the fracture plane goes through the lumen (L) of a capillary and the bordering endothelial cell (End). This is surrounded by astrocytes A1 and A2. The membrane of A1 indicated by the square is shown at higher magnification in b; (b) High densities of orthogonal arrays of particles (OAP) are found on astrocytic endfeet facing a basal lamina. The circled area is magnified further showing OAPs on the P-face (Pf) If: intermediate filaments; (c) Ependymal cells lining the ventricle; and (d), hippocampal astrocytes in rat brain stained for glial fibrillary acidic protein (GFAP, red) and AQP4 (green). Ependymal cells are positive for AQP4 at their basolateral membranes, bearing cilia apically (arrows). Brain astrocytes in d show high AQP4 binding at their endfeet surrounding capillaries (arrows). Scale bars: (a) 1 µm; (b) 0.1 µm; (c) 5 µm; (d) 20 µm; (a,b) are modified from [24].

Mentions: The history of the discovery of aquaporins in the mammalian brain is curiously remarkable in the respect that the main water channel in the CNS, aquaporin-4 (AQP4), was investigated on ultra-morphological grounds before the first reports on the existence of specific water channels were published. So-called orthogonal arrays of particles (OAPs) were found in membranes of astrocytes by the freeze fracture method employing electron microscopy [10,11]. These OAPs occurred especially in high densities at places where astrocytes faced the basal lamina and therefore extracellular fluid spaces as is the case around blood vessels (Figure 1a,b) and under the pia mater, at the superficial glia limitans [12]. Before it became known that OAPs consist of AQP4, there were many speculations on their functional involvement ranging from ion channels [13] to regeneration, and even a role for water transport, reviewed in Wolburg [12]. The suggestion for a role in regeneration resulted from comparisons of various brain structures across different species, reviewed in [14]. Within the brain, OAPs were also found in membranes of ependymal cells, the cells that line the ventricular surface [15], and of course in many cells outside the CNS [16].


Aquaporin-4 in Astroglial Cells in the CNS and Supporting Cells of Sensory Organs — A Comparative Perspective
(a) Freeze fracture replica of rat brain tissue surrounding a capillary: the fracture plane goes through the lumen (L) of a capillary and the bordering endothelial cell (End). This is surrounded by astrocytes A1 and A2. The membrane of A1 indicated by the square is shown at higher magnification in b; (b) High densities of orthogonal arrays of particles (OAP) are found on astrocytic endfeet facing a basal lamina. The circled area is magnified further showing OAPs on the P-face (Pf) If: intermediate filaments; (c) Ependymal cells lining the ventricle; and (d), hippocampal astrocytes in rat brain stained for glial fibrillary acidic protein (GFAP, red) and AQP4 (green). Ependymal cells are positive for AQP4 at their basolateral membranes, bearing cilia apically (arrows). Brain astrocytes in d show high AQP4 binding at their endfeet surrounding capillaries (arrows). Scale bars: (a) 1 µm; (b) 0.1 µm; (c) 5 µm; (d) 20 µm; (a,b) are modified from [24].
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Related In: Results  -  Collection

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Show All Figures
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ijms-17-01411-f001: (a) Freeze fracture replica of rat brain tissue surrounding a capillary: the fracture plane goes through the lumen (L) of a capillary and the bordering endothelial cell (End). This is surrounded by astrocytes A1 and A2. The membrane of A1 indicated by the square is shown at higher magnification in b; (b) High densities of orthogonal arrays of particles (OAP) are found on astrocytic endfeet facing a basal lamina. The circled area is magnified further showing OAPs on the P-face (Pf) If: intermediate filaments; (c) Ependymal cells lining the ventricle; and (d), hippocampal astrocytes in rat brain stained for glial fibrillary acidic protein (GFAP, red) and AQP4 (green). Ependymal cells are positive for AQP4 at their basolateral membranes, bearing cilia apically (arrows). Brain astrocytes in d show high AQP4 binding at their endfeet surrounding capillaries (arrows). Scale bars: (a) 1 µm; (b) 0.1 µm; (c) 5 µm; (d) 20 µm; (a,b) are modified from [24].
Mentions: The history of the discovery of aquaporins in the mammalian brain is curiously remarkable in the respect that the main water channel in the CNS, aquaporin-4 (AQP4), was investigated on ultra-morphological grounds before the first reports on the existence of specific water channels were published. So-called orthogonal arrays of particles (OAPs) were found in membranes of astrocytes by the freeze fracture method employing electron microscopy [10,11]. These OAPs occurred especially in high densities at places where astrocytes faced the basal lamina and therefore extracellular fluid spaces as is the case around blood vessels (Figure 1a,b) and under the pia mater, at the superficial glia limitans [12]. Before it became known that OAPs consist of AQP4, there were many speculations on their functional involvement ranging from ion channels [13] to regeneration, and even a role for water transport, reviewed in Wolburg [12]. The suggestion for a role in regeneration resulted from comparisons of various brain structures across different species, reviewed in [14]. Within the brain, OAPs were also found in membranes of ependymal cells, the cells that line the ventricular surface [15], and of course in many cells outside the CNS [16].

View Article: PubMed Central - PubMed

ABSTRACT

The main water channel of the brain, aquaporin-4 (AQP4), is one of the classical water-specific aquaporins. It is expressed in many epithelial tissues in the basolateral membrane domain. It is present in the membranes of supporting cells in most sensory organs in a specifically adapted pattern: in the supporting cells of the olfactory mucosa, AQP4 occurs along the basolateral aspects, in mammalian retinal Müller cells it is highly polarized. In the cochlear epithelium of the inner ear, it is expressed basolaterally in some cells but strictly basally in others. Within the central nervous system, aquaporin-4 (AQP4) is expressed by cells of the astroglial family, more specifically, by astrocytes and ependymal cells. In the mammalian brain, AQP4 is located in high density in the membranes of astrocytic endfeet facing the pial surface and surrounding blood vessels. At these locations, AQP4 plays a role in the maintenance of ionic homeostasis and volume regulation. This highly polarized expression has not been observed in the brain of fish where astroglial cells have long processes and occur mostly as radial glial cells. In the brain of the zebrafish, AQP4 immunoreactivity is found along the radial extent of astroglial cells. This suggests that the polarized expression of AQP4 was not present at all stages of evolution. Thus, a polarized expression of AQP4 as part of a control mechanism for a stable ionic environment and water balanced occurred at several locations in supporting and glial cells during evolution. This initially basolateral membrane localization of AQP4 is shifted to highly polarized expression in astrocytic endfeet in the mammalian brain and serves as a part of the neurovascular unit to efficiently maintain homeostasis.

No MeSH data available.


Related in: MedlinePlus