QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (164) Citing Articles via Google Scholar Google Scholar Articles by Matthias, K. Articles by Steinhäuser, C. Search for Related Content PubMed PubMed Citation Articles by Matthias, K. Articles by Steinhäuser, C. Pubmed/NCBI databases Substance via MeSH

 Previous Article  |  Next Article 

The Journal of Neuroscience, March 1, 2003, 23(5):1750

Segregated Expression of AMPA-Type Glutamate Receptors and Glutamate Transporters Defines Distinct Astrocyte Populations in the Mouse Hippocampus

Katja Matthias¹, Frank Kirchhoff², Gerald Seifert¹, Kerstin Hüttmann¹, Marina Matyash³, Helmut Kettenmann³, and Christian Steinhäuser¹

¹ Experimental Neurobiology, Department of Neurosurgery, University of Bonn, 53105 Bonn, Germany, ² Max Planck Institute for Experimental Medicine, 37075 Göttingen, Germany, and ³ Max Delbrück Center for Molecular Medicine, Cellular Neurosciences, 13092 Berlin, Germany

Recent data have suggested the existence of direct signaling pathways between glial cells and neurons. Here we report the coexistence of distinct types of cells expressing astrocyte-specific markers within the hippocampus that display diverse morphological, molecular, and functional profiles. Usage of transgenic mice with GFAP promoter-controlled enhanced green fluorescent protein (EGFP) expression allowed the identification of astroglial cells after fresh isolation or in brain slices. Combining patch-clamp recordings and single-cell reverse transcription-PCR, we distinguished two morphologically distinct types of EGFP-positive cells, one expressing glutamate transporters and the other expressing ionotropic glutamate receptors. None of the EGFP-positive cells coexpressed glutamate receptors and transporters. Subpopulations of glutamate receptor-bearing EGFP-positive cells expressed AN2, the mouse homolog of the rat NG2 proteoglycan or transcripts for excitatory amino acid carrier 1, a neuronal glutamate transporter. Our data demonstrate the presence of distinct, independent populations of cells with astroglial properties in the developing hippocampus that can differently modulate neuronal signaling pathways. The observed heterogeneity of cells with GFAP promoter-regulated EGFP expression and S100/GFAP immunoreactivity challenges the hitherto accepted definition of astrocytes.

Key words: glial cells; astrocytes; astron; AMPA receptors; glutamate transporters; patch clamp; hippocampus; GFAP promoter-controlled EGFP expression; transgenic mouse; NG2; S100b

---

Copyright © 2003 Society for Neuroscience  0270-6474/03/2351750-09$05.00/0

This article has been cited by other articles:

				A. Kunze, M. R. Congreso, C. Hartmann, A. Wallraff-Beck, K. Huttmann, P. Bedner, R. Requardt, G. Seifert, C. Redecker, K. Willecke, et al. Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus PNAS, July 7, 2009; 106(27): 11336 - 11341. [Abstract] [Full Text] [PDF]

				G. Seifert, K. Huttmann, D. K. Binder, C. Hartmann, A. Wyczynski, C. Neusch, and C. Steinhauser Analysis of Astroglial K+ Channel Expression in the Developing Hippocampus Reveals a Predominant Role of the Kir4.1 Subunit J. Neurosci., June 10, 2009; 29(23): 7474 - 7488. [Abstract] [Full Text] [PDF]

				J. Silbereis, E. Cheng, Y. M. Ganat, L. R. Ment, and F. M. Vaccarino Precursors with Glial Fibrillary Acidic Protein Promoter Activity Transiently Generate GABA Interneurons in the Postnatal Cerebellum Stem Cells, May 1, 2009; 27(5): 1152 - 1163. [Abstract] [Full Text] [PDF]

				J. Doherty, M. A. Logan, O. E. Tasdemir, and M. R. Freeman Ensheathing Glia Function as Phagocytes in the Adult Drosophila Brain J. Neurosci., April 15, 2009; 29(15): 4768 - 4781. [Abstract] [Full Text] [PDF]

				N. Rouach, A. Koulakoff, V. Abudara, K. Willecke, and C. Giaume Astroglial Metabolic Networks Sustain Hippocampal Synaptic Transmission Science, December 5, 2008; 322(5907): 1551 - 1555. [Abstract] [Full Text] [PDF]

				L. Dimou, C. Simon, F. Kirchhoff, H. Takebayashi, and M. Gotz Progeny of Olig2-Expressing Progenitors in the Gray and White Matter of the Adult Mouse Cerebral Cortex J. Neurosci., October 8, 2008; 28(41): 10434 - 10442. [Abstract] [Full Text] [PDF]

				U. Lalo, Y. Pankratov, S. P. Wichert, M. J. Rossner, R. A. North, F. Kirchhoff, and A. Verkhratsky P2X1 and P2X5 Subunits Form the Functional P2X Receptor in Mouse Cortical Astrocytes J. Neurosci., May 21, 2008; 28(21): 5473 - 5480. [Abstract] [Full Text] [PDF]

				V. Houades, A. Koulakoff, P. Ezan, I. Seif, and C. Giaume Gap Junction-Mediated Astrocytic Networks in the Mouse Barrel Cortex J. Neurosci., May 14, 2008; 28(20): 5207 - 5217. [Abstract] [Full Text] [PDF]

				A. Buffo, I. Rite, P. Tripathi, A. Lepier, D. Colak, A.-P. Horn, T. Mori, and M. Gotz Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain PNAS, March 4, 2008; 105(9): 3581 - 3586. [Abstract] [Full Text] [PDF]

				N. Kessaris, N. Pringle, and W. D Richardson Specification of CNS glia from neural stem cells in the embryonic neuroepithelium Phil Trans R Soc B, January 12, 2008; 363(1489): 71 - 85. [Abstract] [Full Text] [PDF]

				K. K. Murai and D. J. Van Meyel Neuron Glial Communication at Synapses: Insights From Vertebrates and Invertebrates Neuroscientist, December 1, 2007; 13(6): 657 - 666. [Abstract] [PDF]

				R. Kleene, G. Loers, J. Langer, Y. Frobert, F. Buck, and M. Schachner Prion Protein Regulates Glutamate-Dependent Lactate Transport of Astrocytes J. Neurosci., November 7, 2007; 27(45): 12331 - 12340. [Abstract] [Full Text] [PDF]

				B. Djukic, K. B. Casper, B. D. Philpot, L.-S. Chin, and K. D. McCarthy Conditional Knock-Out of Kir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation J. Neurosci., October 17, 2007; 27(42): 11354 - 11365. [Abstract] [Full Text] [PDF]

				J. Xu, H. Peng, N. Kang, Z. Zhao, J. H-C. Lin, P. K. Stanton, and J. Kang Glutamate-induced Exocytosis of Glutamate from Astrocytes J. Biol. Chem., August 17, 2007; 282(33): 24185 - 24197. [Abstract] [Full Text] [PDF]

				I. R. Winship, N. Plaa, and T. H. Murphy Rapid Astrocyte Calcium Signals Correlate with Neuronal Activity and Onset of the Hemodynamic Response In Vivo J. Neurosci., June 6, 2007; 27(23): 6268 - 6272. [Abstract] [Full Text] [PDF]

				M. D'Ascenzo, T. Fellin, M. Terunuma, R. Revilla-Sanchez, D. F. Meaney, Y. P. Auberson, S. J. Moss, and P. G. Haydon mGluR5 stimulates gliotransmission in the nucleus accumbens PNAS, February 6, 2007; 104(6): 1995 - 2000. [Abstract] [Full Text] [PDF]

				J. Oertel, C. Villmann, H. Kettenmann, F. Kirchhoff, and C.-M. Becker A Novel Glycine Receptor beta Subunit Splice Variant Predicts an Unorthodox Transmembrane Topology: ASSEMBLY INTO HETEROMERIC RECEPTOR COMPLEXES J. Biol. Chem., February 2, 2007; 282(5): 2798 - 2807. [Abstract] [Full Text] [PDF]

				A. Nishiyama Polydendrocytes: NG2 Cells with Many Roles in Development and Repair of the CNS Neuroscientist, February 1, 2007; 13(1): 62 - 76. [Abstract] [PDF]

				Y.-B. Lu, K. Franze, G. Seifert, C. Steinhauser, F. Kirchhoff, H. Wolburg, J. Guck, P. Janmey, E.-Q. Wei, J. Kas, et al. Viscoelastic properties of individual glial cells and neurons in the CNS PNAS, November 21, 2006; 103(47): 17759 - 17764. [Abstract] [Full Text] [PDF]

				G. P. Schools, M. Zhou, and H. K. Kimelberg Development of Gap Junctions in Hippocampal Astrocytes: Evidence That Whole Cell Electrophysiological Phenotype Is an Intrinsic Property of the Individual Cell J Neurophysiol, September 1, 2006; 96(3): 1383 - 1392. [Abstract] [Full Text] [PDF]

				P. G. Haydon and G. Carmignoto Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev, July 1, 2006; 86(3): 1009 - 1031. [Abstract] [Full Text] [PDF]

				X. Sun, A. Y. Shih, H. C. Johannssen, H. Erb, P. Li, and T. H. Murphy Two-photon Imaging of Glutathione Levels in Intact Brain Indicates Enhanced Redox Buffering in Developing Neurons and Cells at the Cerebrospinal Fluid and Blood-Brain Interface J. Biol. Chem., June 23, 2006; 281(25): 17420 - 17431. [Abstract] [Full Text] [PDF]

				A. Wallraff, R. Kohling, U. Heinemann, M. Theis, K. Willecke, and C. Steinhauser The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci., May 17, 2006; 26(20): 5438 - 5447. [Abstract] [Full Text] [PDF]

				R. Zur Nieden and J. W. Deitmer The Role of Metabotropic Glutamate Receptors for the Generation of Calcium Oscillations in Rat Hippocampal Astrocytes In Situ Cereb Cortex, May 1, 2006; 16(5): 676 - 687. [Abstract] [Full Text] [PDF]

				U. Lalo, Y. Pankratov, F. Kirchhoff, R. A. North, and A. Verkhratsky NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J. Neurosci., March 8, 2006; 26(10): 2673 - 2683. [Abstract] [Full Text] [PDF]

				C. Neusch, N. Papadopoulos, M. Muller, I. Maletzki, S. M. Winter, J. Hirrlinger, M. Handschuh, M. Bahr, D. W. Richter, F. Kirchhoff, et al. Lack of the Kir4.1 Channel Subunit Abolishes K+ Buffering Properties of Astrocytes in the Ventral Respiratory Group: Impact on Extracellular K+ Regulation J Neurophysiol, March 1, 2006; 95(3): 1843 - 1852. [Abstract] [Full Text] [PDF]

				T. Fellin, T. Pozzan, and G. Carmignoto Purinergic Receptors Mediate Two Distinct Glutamate Release Pathways in Hippocampal Astrocytes J. Biol. Chem., February 17, 2006; 281(7): 4274 - 4284. [Abstract] [Full Text] [PDF]

				B. Haas, C. G. Schipke, O. Peters, G. Sohl, K. Willecke, and H. Kettenmann Activity-dependent ATP-waves in the Mouse Neocortex are Independent from Astrocytic Calcium Waves Cereb Cortex, February 1, 2006; 16(2): 237 - 246. [Abstract] [Full Text] [PDF]

				A. Lomniczi, A. Cornea, M. E. Costa, and S. R. Ojeda Hypothalamic Tumor Necrosis Factor-{alpha} Converting Enzyme Mediates Excitatory Amino Acid-Dependent Neuron-to-Glia Signaling in the Neuroendocrine Brain J. Neurosci., January 4, 2006; 26(1): 51 - 62. [Abstract] [Full Text] [PDF]

				M. Zhou, G. P. Schools, and H. K. Kimelberg Development of GLAST(+) Astrocytes and NG2(+) Glia in Rat Hippocampus CA1: Mature Astrocytes Are Electrophysiologically Passive J Neurophysiol, January 1, 2006; 95(1): 134 - 143. [Abstract] [Full Text] [PDF]

				F. E. Jensen Role of Glutamate Receptors in Periventricular Leukomalacia J Child Neurol, December 1, 2005; 20(12): 950 - 959. [Abstract] [PDF]

				R. Jabs, T. Pivneva, K. Huttmann, A. Wyczynski, C. Nolte, H. Kettenmann, and C. Steinhauser Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity J. Cell Sci., August 15, 2005; 118(16): 3791 - 3803. [Abstract] [Full Text] [PDF]

				L. K. Bekar, M. E. Loewen, K. Cao, X. Sun, J. Leis, R. Wang, G. W. Forsyth, and W. Walz Complex Expression and Localization of Inactivating Kv Channels in Cultured Hippocampal Astrocytes J Neurophysiol, March 1, 2005; 93(3): 1699 - 1709. [Abstract] [Full Text] [PDF]

				K. Wosik, F. Ruffini, G. Almazan, A. Olivier, J. Nalbantoglu, and J. P. Antel Resistance of human adult oligodendrocytes to AMPA/kainate receptor-mediated glutamate injury Brain, December 1, 2004; 127(12): 2636 - 2648. [Abstract] [Full Text] [PDF]

				R Chittajallu, A Aguirre, and V Gallo NG2-positive cells in the mouse white and grey matter display distinct physiological properties J. Physiol., November 15, 2004; 561(1): 109 - 122. [Abstract] [Full Text] [PDF]

				T. Fellin and G. Carmignoto Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit J. Physiol., August 15, 2004; 559(1): 3 - 15. [Abstract] [Full Text] [PDF]

				G. Seifert, K. Huttmann, J. Schramm, and C. Steinhauser Enhanced Relative Expression of Glutamate Receptor 1 Flip AMPA Receptor Subunits in Hippocampal Astrocytes of Epilepsy Patients with Ammon's Horn Sclerosis J. Neurosci., February 25, 2004; 24(8): 1996 - 2003. [Abstract] [Full Text] [PDF]

				D. Grass, P. G. Pawlowski, J. Hirrlinger, N. Papadopoulos, D. W. Richter, F. Kirchhoff, and S. Hulsmann Diversity of Functional Astroglial Properties in the Respiratory Network J. Neurosci., February 11, 2004; 24(6): 1358 - 1365. [Abstract] [Full Text] [PDF]

				B. Scheffler, T. Schmandt, W. Schroder, B. Steinfarz, L. Husseini, J. Wellmer, G. Seifert, K. Karram, H. Beck, I. Blumcke, et al. Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures Development, November 15, 2003; 130(22): 5533 - 5541. [Abstract] [Full Text] [PDF]

				S. Fukuda, F. Kato, Y. Tozuka, M. Yamaguchi, Y. Miyamoto, and T. Hisatsune Two Distinct Subpopulations of Nestin-Positive Cells in Adult Mouse Dentate Gyrus J. Neurosci., October 15, 2003; 23(28): 9357 - 9366. [Abstract] [Full Text] [PDF]

				A. Loaiza, O. H. Porras, and L. F. Barros Glutamate Triggers Rapid Glucose Transport Stimulation in Astrocytes as Evidenced by Real-Time Confocal Microscopy J. Neurosci., August 13, 2003; 23(19): 7337 - 7342. [Abstract] [Full Text] [PDF]

				B. Odermatt, K. Wellershaus, A. Wallraff, G. Seifert, J. Degen, C. Euwens, B. Fuss, H. Bussow, K. Schilling, C. Steinhauser, et al. Connexin 47 (Cx47)-Deficient Mice with Enhanced Green Fluorescent Protein Reporter Gene Reveal Predominant Oligodendrocytic Expression of Cx47 and Display Vacuolized Myelin in the CNS J. Neurosci., June 1, 2003; 23(11): 4549 - 4559. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help