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The Journal of Neuroscience, July 25, 2007, 27(30):8101-8111; doi:10.1523/JNEUROSCI.1912-07.2007

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Development/Plasticity/Repair
Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

Eszter Szabadits,^1 * Csaba Cserép,^1 * Anikó Ludányi,¹ István Katona,¹ Javier Gracia-Llanes,² Tamás F. Freund,¹ and Gábor Nyíri¹

¹Department of Cellular and Network Neurobiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary, and ²Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Valencia, E-46100 Burjasot, Spain

Correspondence should be addressed to Dr. Gábor Nyíri, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u. 43. H-1083 Budapest, Hungary. Email: nyiri{at}koki.hu

Nitric oxide (NO) plays an important role in synaptic plasticity as a retrograde messenger at glutamatergic synapses. Here we describe that, in hippocampal pyramidal cells, neuronal nitric oxide synthase (nNOS) is also associated with the postsynaptic active zones of GABAergic symmetrical synapses terminating on their somata, dendrites, and axon initial segments in both mice and rats. The NO receptor nitric oxide-sensitive guanylyl cyclase (NOsGC) is present in the brain in two functional subunit compositions: ₁ß₁ and ₂ß₁. The ß₁ subunit is expressed in both pyramidal cells and interneurons in the hippocampus. Using immunohistochemistry and in situ hybridization methods, we describe that the ₁ subunit is detectable only in interneurons, which are always positive for ß₁ subunit as well; however, pyramidal cells are labeled only for ß₁ and ₂ subunits. With double-immunofluorescent staining, we also found that most cholecystokinin- and parvalbumin-positive and smaller proportion of the somatostatin- and nNOS-positive interneurons are ₁ subunit positive. We also found that the ₁ subunit is present in parvalbumin- and cholecystokinin-positive interneuron terminals that establish synapses on somata, dendrites, or axon initial segments. Our results demonstrate that NOsGC, composed of ₁ß₁ subunits, is selectively expressed in different types of interneurons and is present in their presynaptic GABAergic terminals, in which it may serve as a receptor for NO produced postsynaptically by nNOS in the very same synapse.

Key words: retrograde signaling; cGMP; GABAergic plasticity; interneuron; rat; mouse

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Received April 27, 2007; revised June 13, 2007; accepted June 14, 2007.

Correspondence should be addressed to Dr. Gábor Nyíri, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u. 43. H-1083 Budapest, Hungary. Email: nyiri{at}koki.hu

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