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 ISI 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 ISI Web of Science (166) Citing Articles via Google Scholar Google Scholar Articles by Washburn, M. S. Articles by Dingledine, R. Search for Related Content PubMed PubMed Citation Articles by Washburn, M. S. Articles by Dingledine, R.

 Previous Article  |  Next Article 

Volume 17, Number 24, Issue of December 15, 1997 pp. 9393-9406

Differential Dependence on GluR2 Expression of Three Characteristic Features of AMPA Receptors

Received June 3, 1997; revised Sept. 22, 1997; accepted Sept. 24, 1997.

Mark S. Washburn, Markus Numberger, Sunan Zhang, and Raymond Dingledine

Department of Pharmacology, Emory University School of Medicine, Atlanta, Georgia 30322

The GluR2 subunit controls three key features of ion flux through the AMPA subtype of glutamate receptorscalcium permeability, inward rectification, and channel block by external polyamines, but whether each of these features is equally sensitive to GluR2 abundance is unknown. The relations among these properties were compared in native AMPA receptors expressed by acutely isolated hippocampal interneurons and in recombinant receptors expressed by Xenopus oocytes. The shape of current-voltage (I-V) relations between 100 and +50 mV for either recombinant or native AMPA receptors was well described by a Woodhull block model in which the affinity for internal polyamine varied over a 1000-fold range in different cells. In oocytes injected with mixtures of GluR2:non-GluR2 mRNA, the relative abundance of GluR2 required to reduce the log of internal blocker affinity by 50% was two- to fourfold higher than that needed to half-maximally reduce divalent permeability or channel block by external polyamines. Likewise, in interneurons the affinity of externally applied argiotoxin for its blocking site was a steep function of internal blocker affinity. These results indicate that the number of GluR2 subunits in AMPA receptors is variable in both oocytes and interneurons. More GluR2 subunits in an AMPA receptor are required to maximally reduce internal blocker affinity than to abolish calcium permeability or external polyamine channel block. Accordingly, single-cell RT-PCR showed that approximately one-half of the physiologically characterized interneurons exhibiting inwardly rectifying AMPA receptors expressed detectable levels of edited GluR2. The physiological effects of a moderate change in GluR2 relative abundance, such as occurs after ischemia or seizures or after chronic exposure to morphine, thus will be dependent on the ambient GluR2 level in a cell-specific manner.

Key words: AMPA receptor; glutamate receptor; spider toxin; hippocampal interneuron; GluR2 subunit; RT-PCR; kainate; patch clamp; stratum radiatum; inward rectification; polyamine; spermine; calcium permeability; CA3; argiotoxin; Woodhull

This article has been cited by other articles:

				H. Xu, L.-J. Wu, H. Wang, X. Zhang, K. I. Vadakkan, S. S. Kim, H. W. Steenland, and M. Zhuo Presynaptic and Postsynaptic Amplifications of Neuropathic Pain in the Anterior Cingulate Cortex J. Neurosci., July 16, 2008; 28(29): 7445 - 7453. [Abstract] [Full Text] [PDF]

				J. Kim, S. Lee, K. Park, I. Hong, B. Song, G. Son, H. Park, W. R. Kim, E. Park, H. K. Choe, et al. Amygdala depotentiation and fear extinction PNAS, December 26, 2007; 104(52): 20955 - 20960. [Abstract] [Full Text] [PDF]

				Y. Xia, S. Nawy, and R. C. Carroll Activity-Dependent Synaptic Plasticity in Retinal Ganglion Cells J. Neurosci., November 7, 2007; 27(45): 12221 - 12229. [Abstract] [Full Text] [PDF]

				L. Pan and K. S. Broadie Drosophila Fragile X Mental Retardation Protein and Metabotropic Glutamate Receptor A Convergently Regulate the Synaptic Ratio of Ionotropic Glutamate Receptor Subclasses J. Neurosci., November 7, 2007; 27(45): 12378 - 12389. [Abstract] [Full Text] [PDF]

				M. T.-W. Ho, K. A. Pelkey, L. Topolnik, R. S. Petralia, K. Takamiya, J. Xia, R. L. Huganir, J.-C. Lacaille, and C. J. McBain Developmental Expression of Ca2+-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber CA3 Pyramid Synapses J. Neurosci., October 24, 2007; 27(43): 11651 - 11662. [Abstract] [Full Text] [PDF]

				L. Sun and S. June Liu Activation of extrasynaptic NMDA receptors induces a PKC-dependent switch in AMPA receptor subtypes in mouse cerebellar stellate cells J. Physiol., September 1, 2007; 583(2): 537 - 553. [Abstract] [Full Text] [PDF]

				J. Song, G. Shen, L. J. Greenfield Jr., and E. I. Tietz Benzodiazepine Withdrawal-Induced Glutamatergic Plasticity Involves Up-Regulation of GluR1-Containing {alpha}-Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptors in Hippocampal CA1 Neurons J. Pharmacol. Exp. Ther., August 1, 2007; 322(2): 569 - 581. [Abstract] [Full Text] [PDF]

				J. S. Diamond A light switch controlling Ca2+-permeable AMPA receptors in the retina J. Physiol., July 1, 2007; 582(1): 3 - 3. [Full Text] [PDF]

				I. K. Osswald, A. Galan, and D. Bowie Light triggers expression of philanthotoxin-insensitive Ca2+-permeable AMPA receptors in the developing rat retina J. Physiol., July 1, 2007; 582(1): 95 - 111. [Abstract] [Full Text] [PDF]

				J. Shin, F. Shen, and J. Huguenard PKC and polyamine modulation of GluR2-deficient AMPA receptors in immature neocortical pyramidal neurons of the rat J. Physiol., June 1, 2007; 581(2): 679 - 691. [Abstract] [Full Text] [PDF]

				K. P. Lamsa, J. H. Heeroma, P. Somogyi, D. A. Rusakov, and D. M. Kullmann Anti-Hebbian Long-Term Potentiation in the Hippocampal Feedback Inhibitory Circuit Science, March 2, 2007; 315(5816): 1262 - 1266. [Abstract] [Full Text] [PDF]

				W. Deng, R. L. Neve, P. A. Rosenberg, J. J. Volpe, and F. E. Jensen {alpha}-Amino-3-hydroxy-5-methyl-4-isoxazole Propionate Receptor Subunit Composition and cAMP-response Element-binding Protein Regulate Oligodendrocyte Excitotoxicity J. Biol. Chem., November 24, 2006; 281(47): 36004 - 36011. [Abstract] [Full Text] [PDF]

				J. Wu, Q. Liu, K. Yu, J. Hu, Y.-P. Kuo, M. Segerberg, P. A. St John, and R. J. Lukas Roles of nicotinic acetylcholine receptor {beta} subunits in function of human {alpha}4-containing nicotinic receptors J. Physiol., October 1, 2006; 576(1): 103 - 118. [Abstract] [Full Text] [PDF]

				B. Balland, P. Lachamp, C. Strube, J.-P. Kessler, and F. Tell Glutamatergic synapses in the rat nucleus tractus solitarii develop by direct insertion of calcium-impermeable AMPA receptors and without activation of NMDA receptors J. Physiol., July 1, 2006; 574(1): 245 - 261. [Abstract] [Full Text] [PDF]

				L. J. Blakemore, M. Resasco, M. A. Mercado, and P. Q. Trombley Evidence for Ca2+-permeable AMPA receptors in the olfactory bulb Am J Physiol Cell Physiol, March 1, 2006; 290(3): C925 - C935. [Abstract] [Full Text] [PDF]

				J. Shin, F. Shen, and J. R. Huguenard Polyamines Modulate AMPA Receptor-Dependent Synaptic Responses in Immature Layer V Pyramidal Neurons J Neurophysiol, May 1, 2005; 93(5): 2634 - 2643. [Abstract] [Full Text] [PDF]

				D. Stellwagen, E. C. Beattie, J. Y. Seo, and R. C. Malenka Differential Regulation of AMPA Receptor and GABA Receptor Trafficking by Tumor Necrosis Factor-{alpha} J. Neurosci., March 23, 2005; 25(12): 3219 - 3228. [Abstract] [Full Text] [PDF]

				H. Li, A. E. Bandrowski, and D. A. Prince Cortical Injury Affects Short-Term Plasticity of Evoked Excitatory Synaptic Currents J Neurophysiol, January 1, 2005; 93(1): 146 - 156. [Abstract] [Full Text] [PDF]

				F. Laezza and R. Dingledine Voltage-Controlled Plasticity at GluR2-Deficient Synapses Onto Hippocampal Interneurons J Neurophysiol, December 1, 2004; 92(6): 3575 - 3581. [Abstract] [Full Text] [PDF]

				R. Aronoff, J. E. Mellem, A. V. Maricq, R. Sprengel, and P. H. Seeburg Neuronal Toxicity in Caenorhabditis elegans from an Editing Site Mutant in Glutamate Receptor Channels J. Neurosci., September 15, 2004; 24(37): 8135 - 8140. [Abstract] [Full Text] [PDF]

				A. Terashima, L. Cotton, K. K. Dev, G. Meyer, S. Zaman, F. Duprat, J. M. Henley, G. L. Collingridge, and J. T. R. Isaac Regulation of Synaptic Strength and AMPA Receptor Subunit Composition by PICK1 J. Neurosci., June 9, 2004; 24(23): 5381 - 5390. [Abstract] [Full Text] [PDF]

				J. R. Brorson, D. Li, and T. Suzuki Selective Expression of Heteromeric AMPA Receptors Driven by Flip-Flop Differences J. Neurosci., April 7, 2004; 24(14): 3461 - 3470. [Abstract] [Full Text] [PDF]

				S. J. Myers, Y. Huang, T. Genetta, and R. Dingledine Inhibition of Glutamate Receptor 2 Translation by a Polymorphic Repeat Sequence in the 5'-Untranslated Leaders J. Neurosci., April 7, 2004; 24(14): 3489 - 3499. [Abstract] [Full Text] [PDF]

				S. B. Marrus, S. L. Portman, M. J. Allen, K. G. Moffat, and A. DiAntonio Differential Localization of Glutamate Receptor Subunits at the Drosophila Neuromuscular Junction J. Neurosci., February 11, 2004; 24(6): 1406 - 1415. [Abstract] [Full Text] [PDF]

				I. Joshi, S. Shokralla, P. Titis, and L.-Y. Wang The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse J. Neurosci., January 7, 2004; 24(1): 183 - 196. [Abstract] [Full Text] [PDF]

				J. E. Huettner Spine-Tingling Excitement from Glutamate Receptors Sci. Signal., November 25, 2003; 2003(210): pe53 - pe53. [Abstract] [Full Text] [PDF]

				F. Ogoshi and J. H. Weiss Heterogeneity of Ca2+-Permeable AMPA/Kainate Channel Expression in Hippocampal Pyramidal Neurons: Fluorescence Imaging and Immunocytochemical Assessment J. Neurosci., November 19, 2003; 23(33): 10521 - 10530. [Abstract] [Full Text] [PDF]

				P. SAH, E. S. L. FABER, M. LOPEZ DE ARMENTIA, and J. POWER The Amygdaloid Complex: Anatomy and Physiology Physiol Rev, July 1, 2003; 83(3): 803 - 834. [Abstract] [Full Text] [PDF]

				J. A. Campagna, K. W. Miller, and S. A. Forman Mechanisms of Actions of Inhaled Anesthetics N. Engl. J. Med., May 22, 2003; 348(21): 2110 - 2124. [Full Text] [PDF]

				P. SAH and M. L. DE ARMENTIA Excitatory Synaptic Transmission in the Lateral and Central Amygdala Ann. N.Y. Acad. Sci., April 1, 2003; 985(1): 67 - 77. [Abstract] [Full Text] [PDF]

				S. Michel, J. Itri, and C. S. Colwell Excitatory Mechanisms in the Suprachiasmatic Nucleus: The Role of AMPA/KA Glutamate Receptors J Neurophysiol, August 1, 2002; 88(2): 817 - 828. [Abstract] [Full Text] [PDF]

				C. Schmauss and J. R. Howe RNA Editing of Neurotransmitter Receptors in the Mammalian Brain Sci. Signal., May 21, 2002; 2002(133): pe26 - pe26. [Abstract] [Full Text] [PDF]

				S. S. Kumar, A. Bacci, V. Kharazia, and J. R. Huguenard A Developmental Switch of AMPA Receptor Subunits in Neocortical Pyramidal Neurons J. Neurosci., April 15, 2002; 22(8): 3005 - 3015. [Abstract] [Full Text] [PDF]

				C. Sommer and M. Kiessling Ischemia and Ischemic Tolerance Induction Differentially Regulate Protein Expression of GluR1, GluR2, and AMPA Receptor Binding Protein in the Gerbil Hippocampus: GluR2 (GluR-B) Reduction Does Not Predict Neuronal Death Stroke, April 1, 2002; 33(4): 1093 - 1100. [Abstract] [Full Text] [PDF]

				S. S. Kumar and J. R. Huguenard Properties of Excitatory Synaptic Connections Mediated by the Corpus Callosum in the Developing Rat Neocortex J Neurophysiol, December 1, 2001; 86(6): 2973 - 2985. [Abstract] [Full Text] [PDF]

				Y. Perez, F. Morin, and J.-C. Lacaille A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons PNAS, July 5, 2001; (2001) 161493498. [Abstract] [Full Text] [PDF]

				C. J. Lee, H. Kong, M. C. Manzini, C. Albuquerque, M. V. Chao, and A. B. MacDermott Kainate Receptors Expressed by a Subpopulation of Developing Nociceptors Rapidly Switch from High to Low Ca2+ Permeability J. Neurosci., July 1, 2001; 21(13): 4572 - 4581. [Abstract] [Full Text] [PDF]

				J. N. Armstrong and B. A. MacVicar Theta-Frequency Facilitation of AMPA Receptor-Mediated Synaptic Currents in the Principal Cells of the Medial Septum J Neurophysiol, April 1, 2001; 85(4): 1709 - 1718. [Abstract] [Full Text] [PDF]

				T. Opitz, S. Y. Grooms, M. V. L. Bennett, and R. S. Zukin Remodeling of alpha -amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia PNAS, November 21, 2000; 97(24): 13360 - 13365. [Abstract] [Full Text] [PDF]

				M. J. Thomas, R. C. Malenka, and A. Bonci Modulation of Long-Term Depression by Dopamine in the Mesolimbic System J. Neurosci., August 1, 2000; 20(15): 5581 - 5586. [Abstract] [Full Text] [PDF]

				J. J. Lawrence and L. O. Trussell Long-Term Specification of AMPA Receptor Properties after Synapse Formation J. Neurosci., July 1, 2000; 20(13): 4864 - 4870. [Abstract] [Full Text] [PDF]

				T. C. Smith, L.-Y. Wang, and J. R. Howe Heterogeneous Conductance Levels of Native AMPA Receptors J. Neurosci., March 15, 2000; 20(6): 2073 - 2085. [Abstract] [Full Text] [PDF]

				A. P. Haghighi and E. Cooper A Molecular Link between Inward Rectification and Calcium Permeability of Neuronal Nicotinic Acetylcholine alpha 3beta 4 and alpha 4beta 2 Receptors J. Neurosci., January 15, 2000; 20(2): 529 - 541. [Abstract] [Full Text] [PDF]

				T. G. Banke, D. Bowie, H.-K. Lee, R. L. Huganir, A. Schousboe, and S. F. Traynelis Control of GluR1 AMPA Receptor Function by cAMP-Dependent Protein Kinase J. Neurosci., January 1, 2000; 20(1): 89 - 102. [Abstract] [Full Text] [PDF]

				W. Vandenberghe, W. Robberecht, and J. R. Brorson AMPA Receptor Calcium Permeability, GluR2 Expression, and Selective Motoneuron Vulnerability J. Neurosci., January 1, 2000; 20(1): 123 - 132. [Abstract] [Full Text] [PDF]

				M. Noda, H. Nakanishi, J. Nabekura, and N. Akaike AMPA-Kainate Subtypes of Glutamate Receptor in Rat Cerebral Microglia J. Neurosci., January 1, 2000; 20(1): 251 - 258. [Abstract] [Full Text] [PDF]

				J. R. Brorson, Z. Zhang, and W. Vandenberghe Ca2+ Permeation of AMPA Receptors in Cerebellar Neurons Expressing Glu Receptor 2 J. Neurosci., November 1, 1999; 19(21): 9149 - 9159. [Abstract] [Full Text] [PDF]

				K. Oguro, N. Oguro, T. Kojima, S. Y. Grooms, A. Calderone, X. Zheng, M. V. L. Bennett, and R. S. Zukin Knockdown of AMPA Receptor GluR2 Expression Causes Delayed Neurodegeneration and Increases Damage by Sublethal Ischemia in Hippocampal CA1 and CA3 Neurons J. Neurosci., November 1, 1999; 19(21): 9218 - 9227. [Abstract] [Full Text] [PDF]

				C. Cui and M. L. Mayer Heteromeric Kainate Receptors Formed by the Coassembly of GluR5, GluR6, and GluR7 J. Neurosci., October 1, 1999; 19(19): 8281 - 8291. [Abstract] [Full Text] [PDF]

				J. R. Howe REVIEW {blacksquare} : How Glutamate Receptors Are Built Neuroscientist, September 1, 1999; 5(5): 311 - 323. [Abstract] [PDF]

				F. Laezza, J. J. Doherty, and R. Dingledine Long-Term Depression in Hippocampal Interneurons: Joint Requirement for Pre- and Postsynaptic Events Science, August 27, 1999; 285(5432): 1411 - 1414. [Abstract] [Full Text]

				A. DiAntonio, S. A. Petersen, M. Heckmann, and C. S. Goodman Glutamate Receptor Expression Regulates Quantal Size and Quantal Content at the Drosophila Neuromuscular Junction J. Neurosci., April 15, 1999; 19(8): 3023 - 3032. [Abstract] [Full Text] [PDF]

				H. S. Engelman, T. B. Allen, and A. B. MacDermott The Distribution of Neurons Expressing Calcium-Permeable AMPA Receptors in the Superficial Laminae of the Spinal Cord Dorsal Horn J. Neurosci., March 15, 1999; 19(6): 2081 - 2089. [Abstract] [Full Text] [PDF]

				R. Dingledine, K. Borges, D. Bowie, and S. F. Traynelis The Glutamate Receptor Ion Channels Pharmacol. Rev., March 1, 1999; 51(1): 7 - 62. [Abstract] [Full Text] [PDF]

				M. G. Weisskopf and J. E. LeDoux Distinct Populations of NMDA Receptors at Subcortical and Cortical Inputs to Principal Cells of the Lateral Amygdala J Neurophysiol, February 1, 1999; 81(2): 930 - 934. [Abstract] [Full Text] [PDF]

				R. Zwart and H. P. M. Vijverberg Four Pharmacologically Distinct Subtypes of alpha 4beta 2 Nicotinic Acetylcholine Receptor Expressed in Xenopus laevis Oocytes Mol. Pharmacol., December 1, 1998; 54(6): 1124 - 1131. [Abstract] [Full Text]

				S. J. Myers, J. Peters, Y. Huang, M. B. Comer, F. Barthel, and R. Dingledine Transcriptional Regulation of the GluR2 Gene: Neural-Specific Expression, Multiple Promoters, and Regulatory Elements J. Neurosci., September 1, 1998; 18(17): 6723 - 6739. [Abstract] [Full Text] [PDF]

				S. Y. Grooms, T. Opitz, M. V. L. Bennett, and R. S. Zukin Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death PNAS, March 28, 2000; 97(7): 3631 - 3636. [Abstract] [Full Text] [PDF]

				Y. Perez, F. Morin, and J.-C. Lacaille A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons PNAS, July 31, 2001; 98(16): 9401 - 9406. [Abstract] [Full Text] [PDF]