Stability of orthogonal arrays of particles in murine skeletal muscle and astrocytes after circulatory arrest, and human gliomas

Neuhaus, Jochen; Schmid, Eva-Maria; Wolburg, Hartwig

doi:10.1016/0304-3940(90)90556-o

Cited by 22 publications

(15 citation statements)

References 17 publications

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“…The more efficient internalization of large amounts of AQP4 with square arrays would thus increase dynamic regulation of AQP4 in vivo, and therefore we may have revealed the first functional rationale for maintaining the elaborate square arrays. Disruption of square arrays in the glial endfeet within minutes after the onset of cerebral ischemia has indeed been demonstrated [47][48][49], although a conflicting study identifies square arrays present in the astrocytic endfeet 60 min after the onset of hypoxia [50]. One may speculate whether the putative hypoxia-induced disruption of square arrays may be indicative of phosphorylation-dependent internalization of AQP4, i.e., via the G-protein coupled vasopressin receptor, V1 a R [35].…”

Section: Discussionmentioning

confidence: 99%

Differential water permeability and regulation of three aquaporin 4 isoforms

Fenton

Moeller

Zelenina

et al. 2009

Cell. Mol. Life Sci.

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Aquaporin 4 (AQP4) is expressed in the perivascular glial endfeet and is an important pathway for water during formation and resolution of brain edema. In this study, we examined the functional properties and relative unit water permeability of three functional isoforms of AQP4 expressed in the brain (M1, M23, Mz). The M23 isoform gave rise to square arrays when expressed in Xenopus laevis oocytes. The relative unit water permeability differed significantly between the isoforms in the order of M1 > Mz > M23. None of the three isoforms were permeable to small osmolytes nor were they affected by changes in external K(+) concentration. Upon protein kinase C (PKC) activation, oocytes expressing the three isoforms demonstrated rapid reduction of water permeability, which correlated with AQP4 internalization. The M23 isoform was more sensitive to PKC regulation than the longer isoforms and was internalized significantly faster. Our results suggest a specific role for square array formation.

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Section: Discussionmentioning

confidence: 99%

Differential water permeability and regulation of three aquaporin 4 isoforms

Fenton

Moeller

Zelenina

et al. 2009

Cell. Mol. Life Sci.

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“…The arrays were reported to disassemble under various metabolic and osmotic conditions (14,29,30) and may vary with tissue preservation conditions and even between adjacent astrocytes (24,31). Because mechanisms regulating AQP4 array assembly are unknown, we explored the possibility that AQP4 isoforms M1 and M23 may be determinants.…”

Section: Discussionmentioning

confidence: 99%

Aquaporin-4 square array assembly: Opposing actions of M1 and M23 isoforms

Furman

Gorelick-Feldman

Davidson

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

286

287

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Osmotic homeostasis in the brain involves movement of water through aquaporin-4 (AQP4) membrane channels. Perivascular astrocyte end-feet contain distinctive orthogonal lattices (square arrays) assembled from 4-to 6-nm intramembrane particles (IMPs) corresponding to individual AQP4 tetramers. Two isoforms of AQP4 result from translation initiation at methionine residues M1 and M23, but no functional differences are known. In this study, Chinese hamster ovary cells were transfected with M1, M23, or M1؉M23 isoforms, and AQP4 expression was confirmed by immunoblotting, immunocytochemistry, and immunogold labeling. Square array organization was examined by freeze-fracture electron microscopy. In astrocyte end-feet, >90% of 4-to 6-nm IMPs were found in square arrays, with 65% in arrays of 13-30 IMPs. In cells transfected with M23, 95% of 4-to 6-nm IMPs were in large assemblies (rafts), 85% of which contained >100 IMPs. However, in M1 cells, >95% of 4-to 6-nm IMPs were present as singlets, with <5% in incipient arrays of 2-12 IMPs. In A quaporins are specialized water transport channels in plasma membranes of water-permeable tissues (1). Aquaporins 1 and 4 (AQP1 and AQP4) are most important to fluid movements in mammalian brain. AQP4 exists as two isoforms, differing at their N termini, because of translation initiation at the first methionine (M1, 323 aa) or the second methionine (M23, 301 aa) (2, 3). Both isoforms are present in brain, but M23 is at least 3-fold more abundant (4, 5). Endogenous AQP4 is a tetramer usually containing M1 and M23 subunits. The water permeabilities of M1 and M23 are similar, and functional differences are not known (3, 4).Fluid movements are precisely orchestrated within the rigid cranium to prevent physical damage from swelling or shrinkage. Interfaces between brain parenchyma and cerebrospinal fluid occur around the ventricles, surrounding blood vessels, and at the brain surface. AQP1 is expressed in rat choroid plexus, the site of cerebrospinal fluid secretion (6), whereas AQP4 is enriched in rat astrocyte end-feet surrounding brain capillaries (7,8). Astrocyte processes forming the glia limitans at brain surfaces, ependymal cells lining brain ventricles, and Müller cells facing the vitreous body and retinal blood vessels all have abundant AQP4 (9). AQP4 in perivascular membranes of astrocyte end-feet has been implicated in neurological disorders, including acute hyponatremic edema, postischemic injury, and epileptic seizures (10-13).Perivascular membranes of astrocyte end-feet contain numerous strikingly regular arrays of intramembrane particles (IMPs) in freeze-fracture electron micrographs. These IMP arrays have been referred to as square arrays, assemblies, or orthogonally arranged particles (OAPs) (14). In early freeze-fracture images of astrocyte end-feet (15), square arrays were resolved as 6-nm IMP protrusions in P-face images (protoplasmic leaflets) or as smaller pits in E-faces (extraplasmic leaflets). The sizes and shapes of square arrays vary, but the IMPs and pits have un...

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“…This hypothesis was later confirmed in AQP4-transfected Chinese Hamster Ovary (CHO) cells (Yang et al, 1996) and transgenic knock-out AQP4 mice (Verbavatz et al, 1997) and by direct immunogold labeling (Rash et al, 1998). Modification of the membrane density of these OAPs has been reported for several pathological states, including brain ischemia (Suzuki et al, 1984;Neuhaus et al, 1990), epilepsy (Hatton and Ellisman, 1984), and muscular dystrophy (Wakayama et al, 1989).…”

Section: Introductionmentioning

confidence: 86%