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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.

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AQP4 localization fish brain and retina. (a) Immunostain in the brain (optic tectum) of a zebrafish (Danio rerio). AQP4 is expressed along radial glial fibers, but not particularly enhanced at the brain surface nor around blood vessels; (b) In the retina of the cichlid fish Astatotilapia burtoni punctate stain for AQP4 is detected along Müller cell fibers and endfeet at the inner limiting membrane (arrow heads); (c) Freeze fracture electron micrograph through Müller cell endfeet facing a basal lamina (BL). The square area shown at higher magnification in the lower panel reveals OAPs (circled). INL: inner nuclear layer, GCL: ganglion cell layer, NFL: nerve fiber layer. Scale bars 20 µm in (a,b), and 0.5 µm and 0.1 µm in (c).
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ijms-17-01411-f003: AQP4 localization fish brain and retina. (a) Immunostain in the brain (optic tectum) of a zebrafish (Danio rerio). AQP4 is expressed along radial glial fibers, but not particularly enhanced at the brain surface nor around blood vessels; (b) In the retina of the cichlid fish Astatotilapia burtoni punctate stain for AQP4 is detected along Müller cell fibers and endfeet at the inner limiting membrane (arrow heads); (c) Freeze fracture electron micrograph through Müller cell endfeet facing a basal lamina (BL). The square area shown at higher magnification in the lower panel reveals OAPs (circled). INL: inner nuclear layer, GCL: ganglion cell layer, NFL: nerve fiber layer. Scale bars 20 µm in (a,b), and 0.5 µm and 0.1 µm in (c).

Mentions: When stained for AQP4 by immunohistochemistry, radial glial cells in the zebrafish brain were positive but did not show the polarized distribution as it is known from mammalian astrocytes [74]. OAPs occurring in high density in mammalian perivascular astrocytic endfeet have never been found in the brain of fish. Thus, the expression pattern of AQP4 on radial glial cells and the lack of OAPs in fish brain resemble the situation of radial glial cells during cortical development. However, the radial glial (Müller) cells of the goldfish (Carassius auratus) retina have been reported to form OAPs at their endfeet facing the vitreous humor [76], a finding we could recently confirm in the retina of cichlid fish Astatotilapia burtoni (Figure 3). Thus, the formation of OAPs by AQP4 on glial cells is a trait that evolved prior to tetrapod evolution but is not prevalent in the fish brain.


Aquaporin-4 in Astroglial Cells in the CNS and Supporting Cells of Sensory Organs — A Comparative Perspective
AQP4 localization fish brain and retina. (a) Immunostain in the brain (optic tectum) of a zebrafish (Danio rerio). AQP4 is expressed along radial glial fibers, but not particularly enhanced at the brain surface nor around blood vessels; (b) In the retina of the cichlid fish Astatotilapia burtoni punctate stain for AQP4 is detected along Müller cell fibers and endfeet at the inner limiting membrane (arrow heads); (c) Freeze fracture electron micrograph through Müller cell endfeet facing a basal lamina (BL). The square area shown at higher magnification in the lower panel reveals OAPs (circled). INL: inner nuclear layer, GCL: ganglion cell layer, NFL: nerve fiber layer. Scale bars 20 µm in (a,b), and 0.5 µm and 0.1 µm in (c).
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ijms-17-01411-f003: AQP4 localization fish brain and retina. (a) Immunostain in the brain (optic tectum) of a zebrafish (Danio rerio). AQP4 is expressed along radial glial fibers, but not particularly enhanced at the brain surface nor around blood vessels; (b) In the retina of the cichlid fish Astatotilapia burtoni punctate stain for AQP4 is detected along Müller cell fibers and endfeet at the inner limiting membrane (arrow heads); (c) Freeze fracture electron micrograph through Müller cell endfeet facing a basal lamina (BL). The square area shown at higher magnification in the lower panel reveals OAPs (circled). INL: inner nuclear layer, GCL: ganglion cell layer, NFL: nerve fiber layer. Scale bars 20 µm in (a,b), and 0.5 µm and 0.1 µm in (c).
Mentions: When stained for AQP4 by immunohistochemistry, radial glial cells in the zebrafish brain were positive but did not show the polarized distribution as it is known from mammalian astrocytes [74]. OAPs occurring in high density in mammalian perivascular astrocytic endfeet have never been found in the brain of fish. Thus, the expression pattern of AQP4 on radial glial cells and the lack of OAPs in fish brain resemble the situation of radial glial cells during cortical development. However, the radial glial (Müller) cells of the goldfish (Carassius auratus) retina have been reported to form OAPs at their endfeet facing the vitreous humor [76], a finding we could recently confirm in the retina of cichlid fish Astatotilapia burtoni (Figure 3). Thus, the formation of OAPs by AQP4 on glial cells is a trait that evolved prior to tetrapod evolution but is not prevalent in the fish brain.

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