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Distribution of AMPA Glutamate Receptor GluR1 Subunit-immunoreactive Neurons and their Co-Localization with Calcium-binding Proteins and GABA in the Mouse Visual Cortex  

Kim, Tae-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University)
Ye, Eun-Ah (Department of Biology, College of Natural Sciences, Kyungpook National University)
Jeon, Chang-Jin (Department of Biology, College of Natural Sciences, Kyungpook National University)
Abstract
The neuronal localization of alpha-amino-3-hydroxyl-5-methyl-4-isoxazole propionic acid (AMPA) glutamate receptor (GluR) subunits is vital as they play key roles in the regulation of calcium permeability. We have examined the distribution of the calcium permeable AMPA glutamate receptor subunit GluR1 in the mouse visual cortex immunocytochemically. We compared this distribution to that of the calcium-binding proteins calbindin D28K, calretinin, and parvalbumin, and of GABA. The highest density of GluR1-immunoreactive (IR) neurons was found in layers II/III. Enucleation appeared to have no effect on the distribution of GluR1-IR neurons. The labeled neurons varied in morphology; the majority were round or oval and no pyramidal cells were labeled by the antibody. Two-color immunofluorescence revealed that 26.27%, 10.65%, and 40.31% of the GluR1-IR cells also contained, respectively, calbindin D28K, calretinin, and parvalbumin. 20.74% of the GluR1-IR neurons also expressed GABA. These results indicate that many neurons that express calcium-permeable GluR1 also express calcium binding proteins. They also demonstrate that one fifth of the GluR1-IR neurons in the mouse visual cortex are GABAergic interneurons.
Keywords
Calbindin D28K; Calretinin; GABA; GluR1; Localization; Parvalbumin; Visual Cortex;
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1 Andressen, C., Blumcke, I., and Celio, M. R. (1993) Calciumbinding proteins: selective markers of nerve cells. Cell Tissue Res. 271, 181−208   DOI   ScienceOn
2 Conti, F., Minelli, A., and Brecha, N. C. (1994) Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. J. Comp. Neurol. 350, 241−259   DOI   ScienceOn
3 Demeulemeester, H., Arckens, L., Vandesande, F., Orban, G. A., Heizmann, C. W., et al. (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp. Brain Res. 84, 538−544
4 Kharazia, V. N., Wenthold, R. J., and Weinberg, R. J. (1996) GluR1-immunopostive interneurons in rat neocortex. J. Comp. Neurol. 368, 399-412   DOI   ScienceOn
5 Kondo, M., Okabe, S., Sumino, R., and Okado, H. (2000) A high GluR1:GluR2 expression ratio is correlated with expression of $Ca^{2+}$-binding proteins in rat forebrain neurons. Eur. J. Neurosci. 12, 2812-2822   DOI   ScienceOn
6 Michaelis, E. K. (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54, 369− 415   DOI   ScienceOn
7 Park, H.-J., Hong, S.-K., Kong, J.-H., and Jeon, C.-J. (1999) Localization of calcium-binding protein parvalbumin-immunoreactive neurons in mouse and hamster visual cortex. Mol. Cells 9, 542-547
8 Pin, J. P. and Duvoisin, R. (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 1−26
9 Tamura, H., Hicks, T. P., Hata, Y., Tsumoto, T., and Yamatodani, A. (1990) Release of glutamate and aspartate from the visual cortex of the cat following activation of afferent pathways. Exp. Brain Res. 80, 447−455
10 Vickers, J. C., Huntley, G. W., Edwards, A. M., Moran, T., Rogers, S. W., et al. (1993) Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. J. Neurosci. 13, 2982−2992
11 Winsky, L., Isaacs, K. R., and Jacobowitz, D. M. (1996) Calretinin mRNA and immunoreactivity in the medullary reticular formation of the rat: colocalization with glutamate receptors. Brain Res. 741, 123−133   DOI
12 Wong-Riley, M. T. and Jacobs, P. (2002) AMPA glutamate receptor subunit 2 in normal and visually deprived macaque visual cortex. Vis. Neurosci. 19, 563-573
13 Du, J., Gray, N. A., Falke, C. A., Chen, W., Yuan, P., et al. (2004) Modulation of synaptic plasticity by antimanic agents: the role of AMPA glutamate receptor subunit 1 synaptic expression. J. Neurosci. 24, 6578−6589   DOI   ScienceOn
14 Park, H.-J., Kong, J.-H., Kang, Y.-S., Park, W.-M., Jeong, S.-A., et al. (2002) The distribution and morphology of calbindin D28K- and calretinin-immunoreactive neurons in the visual cortex of mouse. Mol. Cells 14, 143-149
15 Chard, P. S., Bleakman, D., Christakosm, S., Fullmer, C. S., and Miller, R. J. (1993) Calcium buffering properties of calbindin D28K and parvalbumin in rat sensory neurons. J. Physiol. 472, 341−357
16 Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., et al. (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262−2267   DOI   ScienceOn
17 Sheng, M. and Kim, M. J. (2002) Postsynaptic signaling and plasticity mechanisms. Science 298, 776−780   DOI
18 Van Damme, K., Massie, A., Vandesande, F., and Arckens, L. (2003) Distribution of the AMPA2 glutamate receptor subunit in adult cat visual cortex. Brain Res. 960, 1−8   DOI
19 Gutierrez-Ibarluzea, I., Mendizabal-Zubiaga, J. L., Reblet, C., and Bueno-Lopez, J. L. (1997) GABAergic neurons with AMPA GluR1 and GluR2/3 immunoreactivity in the rat striate cortex. Neuroreport 8, 2495-2499   DOI   ScienceOn
20 Nakanishi, S. (2005) Synaptic mechanisms of the cerebellar cortical network. Trends Neurosci. 28, 93−100   DOI   ScienceOn
21 He, Y., Hof, P. R., Janssen, W. G., Vissavajjhala, P., and Morrison, J. H. (2001) AMPA GluR2 subunit is differentially distributed on GABAergic neurons and pyramidal cells in the macaque monkey visual cortex. Brain Res. 921, 60−67
22 Ozawa, S., Kamiya, H., and Tsuzki, K. (1998) Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 54, 581−618   DOI   ScienceOn
23 Huettner, J. E. (2003) Kainate receptors and synaptic transmission. Prog. Neurobiol. 70, 387−407   DOI   ScienceOn
24 Song, I. and Huganir, R. L. (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25, 578−588   DOI   ScienceOn
25 Johnson, A. W., Bannerman, D. N., Rawlins, N. P., Sprengel, R., and Good, M. A. (2005) Impaired outcome-specific devaluation of instrumental responding in mice with a targeted deletion of the AMPA receptor glutamate receptor 1 subunit. J. Neurosci. 25, 2359−2365   DOI   ScienceOn
26 Meskenaite, V. (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J. Comp. Neurol. 379, 113-132   DOI   ScienceOn
27 Mayer, M. L. and Armstrong, N. (2004) Structure and function of glutamate receptor ion channels. Annu. Rev. Physiol. 66, 161−181   DOI   ScienceOn
28 Endo, T. and Isa, T. (2001) Functionally different AMPA-type glutamate receptors in morphologically identified neurons in rat superficial superior colliculus. Neuroscience 108, 129-141   DOI   ScienceOn
29 Carder, R. K. (1997) Immunocytochemical characterization of AMPA-selective glutamate receptor subunits: laminar and compartmental distribution in mascaque striate cortex. J. Neurosci. 17, 3352-3363
30 Carter, T. L., Rissman, R. A., Mishizen-Eberz, A. J., Wolfe, B. B., Hamilton, R. L., et al. (2004) Differential preservation of AMPA receptor subunits in the hippocampi of Alzheimer's disease patients according to Braak stage. Exp. Neurol. 187, 299−309   DOI   ScienceOn
31 Hollmann, M. and Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31−108   DOI   ScienceOn
32 Xu, L., Tanigawa, H., and Fujita, I. (2003) Distribution of alphaamino- 3-hydroxy-5-methyl-4-isoxazolepropionate-type glutamate receptor subunits (GluR2/3) along the ventral visual pathway in the monkey. J. Comp. Neurol. 456, 396−407   DOI   ScienceOn
33 Conti, F. and Weinberg, R. J. (1999) Shaping excitation at glutamatergic synapses. Trends Neurosci. 22, 451−458   DOI   ScienceOn
34 Vissavajjhala, P., Janssen, W. G., Hu, Y., Gazzaley, A. H., Moran, T., et al. (1996) Synaptic distribution of the AMPAGluR2 subunit and its colocalization with calcium-binding proteins in rat cerebral cortex: an immunohistochemical study using a GluR2-specific monoclonal antibody. Exp. Neurol. 142, 296-312   DOI   ScienceOn
35 Gonchar, Y. and Burkhalter, A. (1997) Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347−358   DOI   ScienceOn
36 Kondo, M., Sumino, R., and Okado, H. (1997) Combinations of AMPA receptor subunit expression in individual cortical neurons correlate with expression of specific calcium-binding proteins. J. Neurosci. 17, 1570-1581
37 Baimbridge, K. G., Celio, M. R., and Rogers, J. H. (1992) Calcium- binding proteins in the nervous system. Trends Neurosci. 15, 303-308   DOI   ScienceOn
38 Ryoo, S.-R., Ahn, C.-H., Lee, J.-Y., Kang, Y.-S., and Jeon, C.-J. (2003) Immunocytochemical localization of neurons containing the AMPA GluR2/3 subunit in the hamster visual cortex. Mol. Cells 16, 211−215
39 Gutierrez-Igarza, K., Fogarty, D. J., Perez-Cerda, F., Donate- Oliver, F., Albus, K., et al. (1996) Localization of AMPAselective glutamate receptor subunits in the adult cat visual cortex. Vis. Neurosci. 13, 61-72   DOI   ScienceOn
40 Munoz, A., Woods, T. M., and Jones, E. G. (1999) Laminar and cellular distribution of AMPA, Kainite, and NMDA receptor subunits in monkey sensory-motor cortex. J. Comp. Neurol. 407, 472-490   DOI   ScienceOn