Laminar-specific and developmental expression of aquaporin-4 in the mouse hippocampus

Neuroscience

Volumn 178, Issue , 2011, Pages 21-32

  Hsu, M S ^a   Seldin, M ^b   Lee, D J ^c   Seifert, G ^d   Steinhauser C ^d   Binder, D K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Aquaporin; Astrocyte; Glial cell; Potassium; Water

Indexed keywords

AQUAPORIN 4; GLIAL FIBRILLARY ACIDIC PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR4.1; PROTEIN S100B; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DENSITOMETRY; DENTATE GYRUS; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GLIA; HIPPOCAMPUS; HOMEOSTASIS; IMMUNOREACTIVITY; MALE; MOUSE; NERVE EXCITABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; THALAMUS INTRALAMINAR NUCLEUS;

ANIMALS; AQUAPORIN 4; ASTROCYTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; MALE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE GROWTH FACTORS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S100 PROTEINS;

EID: 79952005026     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.020     Document Type: Article

References (47)

1. Amiry-Moghaddam M., Ottersen O.P. The molecular basis of water transport in the brain. Nat Rev Neurosci 2003, 4:991-1001.
2. + clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci U S A 2003, 100:13615-13620.
3. Andrew R.D., Fagan M., Ballyk B.A., Rosen A.S. Seizure susceptibility and the osmotic state. Brain Res 1989, 498:175-180.
4. Badaut J., Ashwal S., Adami A., Tone B., Recker R., Spagnoli D., Ternon B., Obenaus A. Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 2011, Sep 29, [Epub ahead of print].
5. Ballanyi K., Grafe P., ten Bruggencate G. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol 1987, 382:159-174.
6. Bergles D.E., Jabs R., Steinhäuser C. Neuron-glia synapses in the brain. Brain Res Rev 2010, 63:130-137.
7. Binder D.K., Papadopoulos M.C., Haggie P.M., Verkman A.S. In vivo measurement of brain extracellular space diffusion by cortical surface photobleaching. J Neurosci 2004, 24:8049-8056.
8. Binder D.K., Yao X., Zador Z., Sick T.J., Verkman A.S., Manley G.T. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 2006, 53:631-636.
9. Connors N.C., Adams M.E., Froehner S.C., Kofuji P. The potassium channel Kir41 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J Biol Chem 2004, 279:28387-28392.
10. Diers-Fenger M., Kirchhoff F., Kettenmann H., Levine J.M., Trotter J. AN2/NG2 protein-expressing glial progenitor cells in the murine CNS: isolation, differentiation, and association with radial glia. Glia 2001, 34:213-228.
11. Frigeri A., Nicchia G.P., Nico B., Quondamatteo F., Herken R., Roncali L., Svelto M. Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J 2001, 15:90-98.
12. Hibino H., Fujita A., Iwai K., Yamada M., Kurachi Y. Differential assembly of inwardly rectifying K+ channel subunits, Kir41 and Kir51, in brain astrocytes. J Biol Chem 2004, 279:44065-44073.
13. Higashi K., Fujita A., Inanobe A., Tanemoto M., Doi K., Kubo T., Kurachi Y. An inwardly rectifying K(+) channel, Kir41, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 2001, 281:C922-C931.
14. Hinterkeuser S., Schröder W., Hager G., Seifert G., Blümcke I., Elger C.E., Schramm J., Steinhäuser C. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 2000, 12:2087-2096.
15. Hsu M.S., Lee D.J., Binder D.K. Potential role of the glial water channel aquaporin-4 in epilepsy. Neuron Glia Biol 2007, 3:287-297.
16. Jabs R., Pivneva T., Hüttmann K., Wyczynski A., Nolte C., Kettenmann H., Steinhäuser C. Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J Cell Sci 2005, 118:3791-3803.
17. Kim J.E., Ryu H.J., Yeo S.I., Seo C.H., Lee B.C., Choi I.G., Kim D.S., Kang T.C. Differential expressions of aquaporin subtypes in astroglia in the hippocampus of chronic epileptic rats. Neuroscience 2009, 163:781-789.
18. Kofuji P., Ceelen P., Zahs K.R., Surbeck L.W., Lester H.A., Newman E.A. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 2000, 20:5733-5740.
19. Kofuji P., Newman E.A. Potassium buffering in the central nervous system. Neuroscience 2004, 129:1045-1056.
20. Ma T., Yang B., Gillespie A., Carlson E.J., Epstein C.J., Verkman A.S. Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J Clin Invest 1997, 100:957-962.
21. Mangin J.M., Kunze A., Chittajallu R., Gallo V. Satellite NG2 progenitor cells share common glutamatergic inputs with associated interneurons in the mouse dentate gyrus. J Neurosci 2008, 28:7610-7623.
22. Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A.W., Chan P., Verkman A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 2000, 6:159-163.
23. Matthias K., Kirchhoff F., Seifert G., Hüttmann K., Matyash M., Kettenmann H., Steinhäuser C. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 2003, 23:1750-1758.
24. Matyash V., Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 2010, 63:2-10.
25. Nagelhus E.A., Mathiisen T.M., Ottersen O.P. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with Kir41. Neuroscience 2004, 129:905-913.
26. Nagelhus E.A., Veruki M.L., Torp R., Haug F.M., Laake J.H., Nielsen S., Agre P., Ottersen O.P. Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Muller cells and fibrous astrocytes. J Neurosci 1998, 18:2506-2519.
27. Neely J.D., Amiry-Moghaddam M., Ottersen O.P., Froehner S.C., Agre P., Adams M.E. Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc Natl Acad Sci U S A 2001, 98:14108-14113.
28. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M., Bourque C., Agre P., Ottersen O.P. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 1997, 17:171-180.
29. Niermann H., Amiry-Moghaddam M., Holthoff K., Witte O.W., Ottersen O.P. A novel role of vasopressin in the brain: modulation of activity-dependent water flux in the neocortex. J Neurosci 2001, 21:3045-3051.
30. Nolte C., Matyash M., Pivneva T., Schipke C.G., Ohlemeyer C., Hanisch U.K., Kirchhoff F., Kettenmann H. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 2001, 33:72-86.
31. Ogata K., Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 2002, 113:221-233.
32. Papadopoulos M.C., Manley G.T., Krishna S., Verkman A.S. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 2004, 18:1291-1293.
33. Ruiz-Ederra J., Zhang H., Verkman A.S. Evidence against functional interaction between aquaporin-4 water channels and Kir41 potassium channels in retinal Muller cells. J Biol Chem 2007, 282:21866-21872.
34. Schröder W., Seifert G., Hüttmann K., Hinterkeuser S., Steinhäuser C. AMPA receptor-mediated modulation of inward rectifier K+ channels in astrocytes of mouse hippocampus. Mol Cell Neurosci 2002, 19:447-458.
35. Schwartzkroin P.A., Baraban S.C., Hochman D.W. Osmolarity, ionic flux, and changes in brain excitability. Epilepsy Res 1998, 32:275-285.
36. Seifert G., Huttmann K., Binder D.K., Hartmann C., Wyczynski A., Neusch C., Steinhauser C. Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 2009, 29:7474-7488.
37. Sievers J., Hartmann D., Pehlemann F.W., Berry M. Development of astroglial cells in the proliferative matrices, the granule cell layer, and the hippocampal fissure of the hamster dentate gyrus. J Comp Neurol 1992, 320:1-32.
38. Traynelis S.F., Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 1988, 59:259-276.
39. Vajda Z., Pedersen M., Fuchtbauer E.M., Wertz K., Stodkilde-Jorgensen H., Sulyok E., Doczi T., Neely J.D., Agre P., Frokiaer J., Nielsen S. Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc Natl Acad Sci U S A 2002, 99:13131-13136.
40. Verkman A.S. More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 2005, 118:3225-3232.
41. Wallraff A., Köhling R., Heinemann U., Theis M., Willecke K., Steinhäuser C. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 2006, 26:5438-5447.
42. Wallraff A., Odermatt B., Willecke K., Steinhäuser C. Distinct types of astroglial cells in the hippocampus differ in gap junction coupling. Glia 2004, 48:36-43.
43. Wen H., Nagelhus E.A., Amiry-Moghaddam M., Agre P., Ottersen O.P., Nielsen S. Ontogeny of water transport in rat brain: postnatal expression of the aquaporin-4 water channel. Eur J Neurosci 1999, 11:935-945.
44. Yaari Y., Konnerth A., Heinemann U. Nonsynaptic epileptogenesis in the mammalian hippocampus in vitro. II. Role of extracellular potassium. J Neurophysiol 1986, 56:424-438.
45. Yao X., Hrabetova S., Nicholson C., Manley G.T. Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J Neurosci 2008, 28:5460-5464.
46. Zhang H., Verkman A.S. Aquaporin-4 independent Kir41 K+ channel function in brain glial cells. Mol Cell Neurosci 2008, 37:1-10.
47. Zhao T., Kraemer N., Oldekamp J., Cankaya M., Szabo N., Conrad S., Skutella T., Alvarez-Bolado G. Emx2 in the developing hippocampal fissure region. Eur J Neurosci 2006, 23:2895-2907.