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The Journal of Neuroscience, April 19, 2006, 26(16):4289-4297; doi:10.1523/JNEUROSCI.4178-05.2006

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Cellular/Molecular
Compartment-Dependent Colocalization of Kir3.2-Containing K⁺ Channels and GABA_B Receptors in Hippocampal Pyramidal Cells

Ákos Kulik,^1,2 Imre Vida,¹ Yugo Fukazawa,^2,5 Nicole Guetg,^1,3 Yu Kasugai,² Cheryl L. Marker,⁴ Franck Rigato,¹ Bernhard Bettler,³ Kevin Wickman,⁴ Michael Frotscher,¹ and Ryuichi Shigemoto^2,5,6

¹Institute of Anatomy and Cell Biology, Department of Neuroanatomy, University of Freiburg, 79104 Freiburg, Germany, ²Division of Cerebral Structure, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8787, Japan, ³Pharmazentrum, Department of Clinical–Biological Sciences, University of Basel, 4056 Basel, Switzerland, ⁴Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455, ⁵Department of Physiological Sciences, The Graduate University of Advanced Studies (Sokendai), Myodaiji, Okazaki 444-8787, Japan, and ⁶SORST Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan

Correspondence should be addressed to Ákos Kulik, Institute of Anatomy and Cell Biology, Department of Neuroanatomy, University of Freiburg, Albertstrasse 17, 79104 Freiburg, Germany. Email: Akos.Kulik{at}anat.uni-freiburg.de

G-protein-coupled inwardly rectifying K⁺ channels (Kir3 channels) coupled to metabotropic GABA_B receptors are essential for the control of neuronal excitation. To determine the distribution of Kir3 channels and their spatial relationship to GABA_B receptors on hippocampal pyramidal cells, we used a high-resolution immunocytochemical approach. Immunoreactivity for the Kir3.2 subunit was most abundant postsynaptically and localized to the extrasynaptic plasma membrane of dendritic shafts and spines of principal cells. Quantitative analysis of immunogold particles for Kir3.2 revealed an enrichment of the protein around putative glutamatergic synapses on dendritic spines, similar to that of GABA_B1. Consistent with this observation, a high degree of coclustering of Kir3.2 and GABA_B1 was revealed around excitatory synapses by the highly sensitive SDS-digested freeze–fracture replica immunolabeling. In contrast, in dendritic shafts receptors and channels were found to be mainly segregated. These results suggest that Kir3.2-containing K⁺ channels on dendritic spines preferentially mediate the effect of GABA, whereas channels on dendritic shafts are likely to be activated by other neurotransmitters as well. Thus, Kir3 channels, localized to different subcellular compartments of hippocampal principal cells, appear to be differentially involved in synaptic integration in pyramidal cell dendrites.

Key words: GABA_B1; Kir3; G-protein-coupled receptors; electron microscopy; immunocytochemistry; spillover

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Received Sept. 30, 2005; revised Feb. 27, 2006; accepted Feb. 27, 2006.

Correspondence should be addressed to Ákos Kulik, Institute of Anatomy and Cell Biology, Department of Neuroanatomy, University of Freiburg, Albertstrasse 17, 79104 Freiburg, Germany. Email: Akos.Kulik{at}anat.uni-freiburg.de

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