 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 1, Issue of January 1, 1997 pp. 171-180
Copyright ©1997 Society for NeuroscienceSpecialized Membrane Domains for Water Transport in Glial Cells: High-Resolution Immunogold Cytochemistry of Aquaporin-4 in Rat Brain
Received Aug. 16, 1996; revised Oct. 1, 1996; accepted Oct. 10, 1996.
Søren Nielsen1, , Erlend Arnulf Nagelhus2, , Mahmood Amiry-Moghaddam2, Charles Bourque3, Peter Agre4, and Ole Petter Ottersen2 1 Department of Cell Biology, Institute of Anatomy, University of Aarhus, 8000 Aarhus, Denmark, 2 Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, 0317 Oslo, Norway, 3 Centre for Research in Neuroscience, Montréal General Hospital and McGill University, Montréal, Québec, Canada H3G 1A4, and 4 Departments of Biological Chemistry and Medicine, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
Membrane water transport is critically involved in brain volume homeostasis and in the pathogenesis of brain edema. The cDNA encoding aquaporin-4 (AQP4) water channel protein was recently isolated from rat brain. We used immunocytochemistry and high-resolution immunogold electron microscopy to identify the cells and membrane domains that mediate water flux through AQP4. The AQP4 protein is abundant in glial cells bordering the subarachnoidal space, ventricles, and blood vessels. AQP4 is also abundant in osmosensory areas, including the supraoptic nucleus and subfornical organ. Immunogold analysis demonstrated that AQP4 is restricted to glial membranes and to subpopulations of ependymal cells. AQP4 is particularly strongly expressed in glial membranes that are in direct contact with capillaries and pia. The highly polarized AQP4 expression indicates that these cells are equipped with specific membrane domains that are specialized for water transport, thereby mediating the flow of water between glial cells and the cavities filled with CSF and the intravascular space.
Key words: aquaporin-4 water channel; brain water permeability; glial cells; ependymal cells; immunogold electron microscopy; CSF
This article has been cited by other articles:
A. Ablimit, T. Aoki, T. Matsuzaki, T. Suzuki, H. Hagiwara, S. Takami, and K. Takata
Immunolocalization of Water Channel Aquaporins in the Vomeronasal Organ of the Rat: Expression of AQP4 in Neuronal Sensory Cells
Chem Senses, June 1, 2008; 33(5): 481 - 488.
[Abstract] [Full Text] [PDF]
X. Yao, S. Hrabetova, C. Nicholson, and G. T. Manley
Aquaporin-4-Deficient Mice Have Increased Extracellular Space without Tortuosity Change
J. Neurosci., May 21, 2008; 28(21): 5460 - 5464.
[Abstract] [Full Text] [PDF]
M. J. Wiegman, L. V. Bullinger, M. M. Kohlmeyer, T. C. Hunter, and M. J. Cipolla
Regional Expression of Aquaporin 1, 4, and 9 in the Brain During Pregnancy
Reproductive Sciences, May 1, 2008; 15(5): 506 - 516.
[Abstract] [PDF]
L. R Mehta, M. K Samuelsson, A. K Kleiner, A. D Goodman, J. H Anolik, R J. Looney, and S. R Schwid
Neuromyelitis optica spectrum disorder in a patient with systemic lupus erythematosus and anti-phospholipid antibody syndrome
Multiple Sclerosis, April 1, 2008; 14(3): 425 - 427.
[Abstract] [PDF]
S. Saadoun, B. A. Bell, A. S. Verkman, and M. C. Papadopoulos
Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice
Brain, April 1, 2008; 131(4): 1087 - 1098.
[Abstract] [Full Text] [PDF]
D. Lovatt, U. Sonnewald, H. S. Waagepetersen, A. Schousboe, W. He, J. H.-C. Lin, X. Han, T. Takano, S. Wang, F. J. Sim, et al.
The Transcriptome and Metabolic Gene Signature of Protoplasmic Astrocytes in the Adult Murine Cortex
J. Neurosci., November 7, 2007; 27(45): 12255 - 12266.
[Abstract] [Full Text] [PDF]
A. J. Yool
Aquaporins: Multiple Roles in the Central Nervous System
Neuroscientist, October 1, 2007; 13(5): 470 - 485.
[Abstract] [PDF]
J. Ruiz-Ederra and A. S. Verkman
Aquaporin-1 Independent Microvessel Proliferation in a Neonatal Mouse Model of Oxygen-Induced Retinopathy
Invest. Ophthalmol. Vis. Sci., October 1, 2007; 48(10): 4802 - 4810.
[Abstract] [Full Text] [PDF]
K. Tanaka, T. Tani, M. Tanaka, T. Saida, J. Idezuka, M. Yamazaki, M. Tsujita, T. Nakada, K. Sakimura, and M. Nishizawa
Anti-aquaporin 4 antibody in selected Japanese multiple sclerosis patients with long spinal cord lesions
Multiple Sclerosis, August 1, 2007; 13(7): 850 - 855.
[Abstract] [PDF]
E. C. Johnson, L. Jia, W. O. Cepurna, T. A. Doser, and J. C. Morrison
Global Changes in Optic Nerve Head Gene Expression after Exposure to Elevated Intraocular Pressure in a Rat Glaucoma Model
Invest. Ophthalmol. Vis. Sci., July 1, 2007; 48(7): 3161 - 3177.
[Abstract] [Full Text] [PDF]
M. J. Cipolla
Cerebrovascular Function in Pregnancy and Eclampsia
Hypertension, July 1, 2007; 50(1): 14 - 24.
[Full Text] [PDF]
S. F. Roemer, J. E. Parisi, V. A. Lennon, E. E. Benarroch, H. Lassmann, W. Bruck, R. N. Mandler, B. G. Weinshenker, S. J. Pittock, D. M. Wingerchuk, et al.
Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis
Brain, May 1, 2007; 130(5): 1194 - 1205.
[Abstract] [Full Text] [PDF]
A. G. Euser and M. J. Cipolla
Cerebral Blood Flow Autoregulation and Edema Formation During Pregnancy in Anesthetized Rats
Hypertension, February 1, 2007; 49(2): 334 - 340.
[Abstract] [Full Text] [PDF]
K. I. Auguste, S. Jin, K. Uchida, D. Yan, G. T. Manley, M. C. Papadopoulos, and A. S. Verkman
Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury
FASEB J, January 1, 2007; 21(1): 108 - 116.
[Abstract] [Full Text] [PDF]
D. M. Menichella, M. Majdan, R. Awatramani, D. A. Goodenough, E. Sirkowski, S. S. Scherer, and D. L. Paul
Genetic and Physiological Evidence That Oligodendrocyte Gap Junctions Contribute to Spatial Buffering of Potassium Released during Neuronal Activity
J. Neurosci., October 25, 2006; 26(43): 10984 - 10991.
[Abstract] [Full Text] [PDF]
D. S. Frydenlund, A. Bhardwaj, T. Otsuka, M. N. Mylonakou, T. Yasumura, K. G. V. Davidson, E. Zeynalov, O. Skare, P. Laake, F.-M. Haug, et al.
Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice
PNAS, September 5, 2006; 103(36): 13532 - 13536.
[Abstract] [Full Text] [PDF]
S. J. Pittock, B. G. Weinshenker, C. F. Lucchinetti, D. M. Wingerchuk, J. R. Corboy, and V. A. Lennon
Neuromyelitis optica brain lesions localized at sites of high aquaporin 4 expression.
Arch Neurol, July 1, 2006; 63(7): 964 - 968.
[Abstract] [Full Text] [PDF]
D. M. Wingerchuk, V. A. Lennon, S. J. Pittock, C. F. Lucchinetti, and B. G. Weinshenker
Revised diagnostic criteria for neuromyelitis optica
Neurology, May 23, 2006; 66(10): 1485 - 1489.
[Abstract] [Full Text] [PDF]
M. Noda
The Subfornical Organ, a Specialized Sodium Channel, and the Sensing of Sodium Levels in the Brain
Neuroscientist, February 1, 2006; 12(1): 80 - 91.
[Abstract] [PDF]
L. A Lindsay and C. R Murphy
Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy
Reproduction, February 1, 2006; 131(2): 369 - 378.
[Abstract] [Full Text] [PDF]
S. Saadoun, M. C. Papadopoulos, H. Watanabe, D. Yan, G. T. Manley, and A. S. Verkman
Involvement of aquaporin-4 in astroglial cell migration and glial scar formation
J. Cell Sci., December 15, 2005; 118(24): 5691 - 5698.
[Abstract] [Full Text] [PDF]
A. Bosco, K. Cusato, G. P. Nicchia, A. Frigeri, and D. C. Spray
A Developmental Switch in the Expression of Aquaporin-4 and Kir4.1 from Horizontal to Muller Cells in Mouse Retina
Invest. Ophthalmol. Vis. Sci., October 1, 2005; 46(10): 3869 - 3875.
[Abstract] [Full Text] [PDF]
M. Amiry-Moghaddam, H. Lindland, S. Zelenin, B. A. Roberg, B. B. Gundersen, P. Petersen, E. Rinvik, I. A. Torgner, and O. P. Ottersen
Brain mitochondria contain aquaporin water channels: evidence for the expression of a short AQP9 isoform in the inner mitochondrial membrane
FASEB J, September 1, 2005; 19(11): 1459 - 1467.
[Abstract] [Full Text] [PDF]
M. C. Papadopoulos and A. S. Verkman
Aquaporin-4 Gene Disruption in Mice Reduces Brain Swelling and Mortality in Pneumococcal Meningitis
J. Biol. Chem., April 8, 2005; 280(14): 13906 - 13912.
[Abstract] [Full Text] [PDF]
W. Jalabi, N. Boehm, D. Grucker, and M. S. Ghandour
Recovery of Myelin after Induction of Oligodendrocyte Cell Death in Postnatal Brain
J. Neurosci., March 16, 2005; 25(11): 2885 - 2894.
[Abstract] [Full Text] [PDF]
A. M. Quick and M. J. Cipolla
Pregnancy-induced up-regulation of aquaporin-4 protein in brain and its role in eclampsia
FASEB J, February 1, 2005; 19(2): 170 - 175.
[Abstract] [Full Text] [PDF]
H. Hibino, A. Fujita, K. Iwai, M. Yamada, and Y. Kurachi
Differential Assembly of Inwardly Rectifying K+ Channel Subunits, Kir4.1 and Kir5.1, in Brain Astrocytes
J. Biol. Chem., October 15, 2004; 279(42): 44065 - 44073.
[Abstract] [Full Text] [PDF]
V. Gresz, T.-H. Kwon, H. Gong, P. Agre, M. C. Steward, L. S. King, and S. Nielsen
Immunolocalization of AQP-5 in rat parotid and submandibular salivary glands after stimulation or inhibition of secretion in vivo
Am J Physiol Gastrointest Liver Physiol, July 1, 2004; 287(1): G151 - G161.
[Abstract] [Full Text] [PDF]
R. M. Bachoo, R. S. Kim, K. L. Ligon, E. A. Maher, C. Brennan, N. Billings, S. Chan, C. Li, D. H. Rowitch, W. H. Wong, et al.
Molecular diversity of astrocytes with implications for neurological disorders
PNAS, June 1, 2004; 101(22): 8384 - 8389.
[Abstract] [Full Text] [PDF]
M. A. Knepper and S. Nielsen
Peter Agre, 2003 Nobel Prize Winner in Chemistry
J. Am. Soc. Nephrol., April 1, 2004; 15(4): 1093 - 1095.
[Abstract] [Full Text] [PDF]
C. R. A. Santos, M. D. Estevao, J. Fuentes, J. C. R. Cardoso, M. Fabra, A. L. Passos, F. J. Detmers, P. M. T. Deen, J. Cerda, and D. M. Power
Isolation of a novel aquaglyceroporin from a marine teleost (Sparus auratus): function and tissue distribution
J. Exp. Biol., March 1, 2004; 207(7): 1217 - 1227.
[Abstract] [Full Text] [PDF]
E. Solenov, H. Watanabe, G. T. Manley, and A. S. Verkman
Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method
Am J Physiol Cell Physiol, February 1, 2004; 286(2): C426 - C432.
[Abstract] [Full Text]
M.-M. Trinh-Trang-Tan, G. Geelen, L. Teillet, and B. Corman
Urea transporter expression in aging kidney and brain during dehydration
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2003; 285(6): R1355 - R1365.
[Abstract] [Full Text] [PDF]
C. S. Furman, D. A. Gorelick-Feldman, K. G. V. Davidson, T. Yasumura, J. D. Neely, P. Agre, and J. E. Rash
Aquaporin-4 square array assembly: Opposing actions of M1 and M23 isoforms
PNAS, November 11, 2003; 100(23): 13609 - 13614.
[Abstract] [Full Text] [PDF]
M. Amiry-Moghaddam, A. Williamson, M. Palomba, T. Eid, N. C. de Lanerolle, E. A. Nagelhus, M. E. Adams, S. C. Froehner, P. Agre, and O. P. Ottersen
Delayed K+ clearance associated with aquaporin-4 mislocalization: Phenotypic defects in brains of {alpha}-syntrophin-null mice
PNAS, November 11, 2003; 100(23): 13615 - 13620.
[Abstract] [Full Text] [PDF]
M. Simard, G. Arcuino, T. Takano, Q. S. Liu, and M. Nedergaard
Signaling at the Gliovascular Interface
J. Neurosci., October 8, 2003; 23(27): 9254 - 9262.
[Abstract] [Full Text] [PDF]
M. Amiry-Moghaddam, T. Otsuka, P. D. Hurn, R. J. Traystman, F.-M. Haug, S. C. Froehner, M. E. Adams, J. D. Neely, P. Agre, O. P. Ottersen, et al.
An alpha -syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain
PNAS, February 18, 2003; 100(4): 2106 - 2111.
[Abstract] [Full Text] [PDF]
Z. Vajda, M. Pedersen, E.-M. Fuchtbauer, K. Wertz, H. Stodkilde-Jorgensen, E. Sulyok, T. Doczi, J. D. Neely, P. Agre, J. Frokiar, et al.
Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice
PNAS, October 1, 2002; 99(20): 13131 - 13136.
[Abstract] [Full Text] [PDF]
M. Zelenina, S. Zelenin, A. A. Bondar, H. Brismar, and A. Aperia
Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine
Am J Physiol Renal Physiol, August 1, 2002; 283(2): F309 - F318.
[Abstract] [Full Text] [PDF]
S Saadoun, M C Papadopoulos, D C Davies, S Krishna, and B A Bell
Aquaporin-4 expression is increased in oedematous human brain tumours
J. Neurol. Neurosurg. Psychiatry, February 1, 2002; 72(2): 262 - 265.
[Abstract] [Full Text] [PDF]
S. Nielsen, J. Frokiar, D. Marples, T.-H. Kwon, P. Agre, and M. A. Knepper
Aquaporins in the Kidney: From Molecules to Medicine
Physiol Rev, January 1, 2002; 82(1): 205 - 244.
[Abstract] [Full Text] [PDF]
J. D. Neely, M. Amiry-Moghaddam, O. P. Ottersen, S. C. Froehner, P. Agre, and M. E. Adams
Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein
PNAS, November 20, 2001; 98(24): 14108 - 14113.
[Abstract] [Full Text] [PDF]
H. Niermann, M. Amiry-Moghaddam, K. Holthoff, O. W. Witte, and O. P. Ottersen
A Novel Role of Vasopressin in the Brain: Modulation of Activity-Dependent Water Flux in the Neocortex
J. Neurosci., May 1, 2001; 21(9): 3045 - 3051.
[Abstract] [Full Text] [PDF]
P. T. Hurley, C. J. Ferguson, T.-H. Kwon, M.-L. E. Andersen, A. G. Norman, M. C. Steward, S. Nielsen, and R. M. Case
Expression and immunolocalization of aquaporin water channels in rat exocrine pancreas
Am J Physiol Gastrointest Liver Physiol, April 1, 2001; 280(4): G701 - G709.
[Abstract] [Full Text] [PDF]
J. E. Rash, T. Yasumura, F. E. Dudek, and J. I. Nagy
Cell-Specific Expression of Connexins and Evidence of Restricted Gap Junctional Coupling between Glial Cells and between Neurons
J. Neurosci., March 15, 2001; 21(6): 1983 - 2000.
[Abstract] [Full Text] [PDF]
B Nico, A Frigeri, G. Nicchia, F Quondamatteo, R Herken, M Errede, D Ribatti, M Svelto, and L Roncali
Role of aquaporin-4 water channel in the development and integrity of the blood-brain barrier
J. Cell Sci., January 4, 2001; 114(7): 1297 - 1307.
[Abstract] [PDF]
A. FRIGERI, G. P. NICCHIA, B. NICO, F. QUONDAMATTEO, R. HERKEN, L. RONCALI, and M. SVELTO
Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice
FASEB J, January 1, 2001; 15(1): 90 - 98.
[Abstract] [Full Text] [PDF]
C. Riemer, I. Queck, D. Simon, R. Kurth, and M. Baier
Identification of Upregulated Genes in Scrapie-Infected Brain Tissue
J. Virol., November 1, 2000; 74(21): 10245 - 10248.
[Abstract] [Full Text]
H. Vorum, T.-H. Kwon, C. Fulton, B. Simonsen, I. Choi, W. Boron, A. B. Maunsbach, S. Nielsen, and C. Aalkjar
Immunolocalization of electroneutral Na-HCO3- cotransporter in rat kidney
Am J Physiol Renal Physiol, November 1, 2000; 279(5): F901 - F909.
[Abstract] [Full Text] [PDF]
E. Watanabe, A. Fujikawa, H. Matsunaga, Y. Yasoshima, N. Sako, T. Yamamoto, C. Saegusa, and M. Noda
Nav2/NaG Channel Is Involved in Control of Salt-Intake Behavior in the CNS
J. Neurosci., October 15, 2000; 20(20): 7743 - 7751.
[Abstract] [Full Text] [PDF]
K. S. Wang, A. R. Komar, T. Ma, F. Filiz, J. McLeroy, K. Hoda, A. S. Verkman, and J. A. Bastidas
Gastric acid secretion in aquaporin-4 knockout mice
Am J Physiol Gastrointest Liver Physiol, August 1, 2000; 279(2): G448 - G453.
[Abstract] [Full Text] [PDF]
C. V. BORLONGAN, M. YAMAMOTO, N. TAKEI, M. KUMAZAKI, C. UNGSUPARKORN, H. HIDA, P. R. SANBERG, and H. NISHINO
Glial cell survival is enhanced during melatonin-induced neuroprotection against cerebral ischemia
FASEB J, July 1, 2000; 14(10): 1307 - 1317.
[Abstract] [Full Text]
P. AGRE
Aquaporin Water Channels in Kidney
J. Am. Soc. Nephrol., April 1, 2000; 11(4): 764 - 777.
[Full Text] [PDF]
H. K. Kimelberg
{blacksquare} Review : Cell Volume in the CNS: Regulation and Implications for Nervous System Function and Pathology
Neuroscientist, February 1, 2000; 6(1): 14 - 25.
[Abstract] [PDF]
T.-H. Kwon, A. Pushkin, N. Abuladze, S. Nielsen, and I. Kurtz
Immunoelectron microscopic localization of NBC3 sodium-bicarbonate cotransporter in rat kidney
Am J Physiol Renal Physiol, February 1, 2000; 278(2): F327 - F336.
[Abstract] [Full Text] [PDF]
B. M. Christensen, M. Zelenina, A. Aperia, and S. Nielsen
Localization and regulation of PKA-phosphorylated AQP2 in response to V2-receptor agonist/antagonist treatment
Am J Physiol Renal Physiol, January 1, 2000; 278(1): F29 - F42.
[Abstract] [Full Text] [PDF]
M. Yasui, T.-H. Kwon, M. A. Knepper, S. Nielsen, and P. Agre
Aquaporin-6: An intracellular vesicle water channel protein in renal epithelia
PNAS, May 11, 1999; 96(10): 5808 - 5813.
[Abstract] [Full Text] [PDF]
D. Sarfaraz and C. L. Fraser
Effects of arginine vasopressin on cell volume regulation in brain astrocyte in culture
Am J Physiol Endocrinol Metab, March 1, 1999; 276(3): E596 - E601.
[Abstract] [Full Text] [PDF]
H. Funaki, T. Yamamoto, Y. Koyama, D. Kondo, E. Yaoita, K. Kawasaki, H. Kobayashi, S. Sawaguchi, H. Abe, and I. Kihara
Localization and expression of AQP5 in cornea, serous salivary glands, and pulmonary epithelial cells
Am J Physiol Cell Physiol, October 1,
