Polarized distribution of AMPA, but not GABAA, receptors in radial glia-like cells of the adult dentate gyrus

GLIA

Volumn 61, Issue 7, 2013, Pages 1146-1154

  Renzel, Roland ^a   Sadek, Ahmed Ramadan ^b   Chang, Cin He ^a   Gray, William P ^b,c   Seifert, Gerald ^a   Steinhäuser, Christian ^a  

^a UNIVERSITY OF BONN   (Germany)

^b SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

^c CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Adult neurogenesis; AMPA receptor; Dentate gyrus; GABAA receptor; RG like cell

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA1; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA3; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CALCIUM; GLUTAMATE TRANSPORTER; IONOTROPIC RECEPTOR;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTICLE; ASTROCYTE; DENTATE GYRUS; GLIA CELL; HIPPOCAMPUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATIC CELL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BICUCULLINE; BIOPHYSICAL PROCESSES; DENTATE GYRUS; EXCITATORY AMINO ACID AGENTS; FATTY ACID-BINDING PROTEINS; GABA AGENTS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HUMANS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MUSCIMOL; NERVE TISSUE PROTEINS; NEUROGLIA; POTASSIUM CHANNEL BLOCKERS; RECEPTORS, AMPA; RECEPTORS, GABA-A; TETRAETHYLAMMONIUM;

EID: 84879606774     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22505     Document Type: Article

References (39)

1. Bai F, Bergeron M, Nelson DL. Chronic AMPA receptor potentiator (LY451646) treatment increases cell proliferation in adult rat hippocampus. Neuropharmacology 2003;44:1013-1021.
2. Chaudhry FA, Lehre KP, Campagne MV, Ottersen OP, Danbolt NC, Storm-Mathisen J. Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 1995;15:711-720.
3. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 2004;42:535-552.
4. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716.
5. Duveau V, Laustela S, Barth L, Gianolini F, Vogt KE, Keist R, Chandra D, Homanics GE, Rudolph U, Fritschy JM. Spatiotemporal specificity of GABAA receptor-mediated regulation of adult hippocampal neurogenesis. Eur J Neurosci 2011;34:362-373.
6. Eliasof S, Jahr CE. Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc Natl Acad Sci USA 1996;93:4153-4158.
7. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003;23:373-382.
8. Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 2003;23:9357-9366.
9. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006;439:589-593.
10. Ge S, Pradhan DA, Ming GL, Song H. GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 2007;30:1-8.
11. Hüttmann K, Sadgrove M, Wallraff A, Hinterkeuser S, Kirchhoff F, Steinhäuser C, Gray WP. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: Functional and immunocytochemical analysis. Eur J Neurosci 2003;18:2769-2778.
12. Jagasia R, Song H, Gage FH, Lie DC. New regulators in adult neurogenesis and their potential role for repair. Trends Mol Med 2006;12:400-405.
13. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447-452.
14. Kunze A, Congreso MR, Hartmann C, Wallraff-Beck A, Hüttmann K, Bedner P, Requardt R, Seifert G, Redecker C, Willecke K, Hofmann A, Pfeifer A, Theis M, Steinhäuser C. Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 2009;106:11336-11341.
15. Langer J, Rose CR. Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 2009;587:5859-5877.
16. Langer J, Stephan J, Theis M, Rose CR. Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ. Glia 2012;60:239-252.
17. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005;437:1370-1375.
18. Magistretti PJ, Chatton JY. Relationship between L-glutamate-regulated intracellular Na+ dynamics and ATP hydrolysis in astrocytes. J Neural Transm 2005;112:77-85.
19. 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.
20. Nacher J, Rosell DR, Alonso-Llosa G, McEwen BS. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 2001;13:512-520.
21. Nagelhus EA, Mathiisen TM, Ottersen OP. Aquaporin-4 in the central nervous system: Cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 2004;129:905-913.
22. Newman EA. Inward-rectifying potassium channels in retinal glial (Müller) cells. J Neurosci 1993;13:3333-3345.
23. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, 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.
24. Olsen RW, Sieghart W. International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: Classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol Rev 2008;60:243-260.
25. Pleasure SJ, Collins AE, Lowenstein DH. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J Neurosci 2000;20:6095-6105.
26. Price DL, Ludwig JW, Mi H, Schwarz TL, Ellisman MH. Distribution of rSlo Ca(2+)-activated K(+) channels in rat astrocyte perivascular endfeet. Brain Res 2002;956:183-193.
27. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 2007;27:6607-6619.
28. Reichenbach A, Derouiche A, Kirchhoff F. Morphology and dynamics of perisynaptic glia. Brain Res Rev 2010;63:11-25.
29. + channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 2009;29:7474-7488.
30. Seifert G, Weber M, Schramm J, Steinhäuser C. Changes in splice variant expression and subunit assembly of AMPA receptors during maturation of hippocampal astrocytes. Mol Cell Neurosci 2003;22:248-258.
31. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004;478:359-378.
32. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001;21:7153-7160.
33. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T. DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 1998;53:195-201.
34. Song H, Stevens C, Gage F. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002;417:39-44.
35. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D, Gu Y, Meletis K, Huang ZJ, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian KM, Ming GL, Song H. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 2012;489:150-154.
36. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005;47:803-815.
37. 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.
38. Wang LP, Kempermann G, Kettenmann H. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 2005;29:181-189.
39. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008;132:645-660.