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The Journal of Neuroscience, May 13, 2009, 29(19):6266-6275; doi:10.1523/JNEUROSCI.5867-08.2009

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Behavioral/Systems/Cognitive
ZO-1 and the Spatial Organization of Gap Junctions and Glutamate Receptors in the Outer Plexiform Layer of the Mammalian Retina

Christian Puller,1 Luis Pérez de Sevilla Müller,2 Ulrike Janssen-Bienhold,2 and Silke Haverkamp1

1Department of Neuroanatomy, Max Planck Institute for Brain Research, D-60528 Frankfurt, Germany, and 2Department of Neurobiology, University of Oldenburg, D-26111 Oldenburg, Germany

Correspondence should be addressed to Silke Haverkamp, Max-Planck-Institut für Hirnforschung, Deutschordenstrasse 46, D-60528 Frankfurt/Main, Germany. Email: haverkamp{at}mpih-frankfurt.mpg.de

Information processing in the retina starts at the first synaptic layer, where photoreceptors and second-order neurons exhibit a complex architecture of glutamatergic and electrical synapses. To investigate the composition of this highly organized synaptic network, we determined the spatial relationship of zonula occludens-1 (ZO-1) with different connexins (Cx) and glutamate receptor (GluR) subunits in the outer plexiform layer (OPL) of rabbit, mouse, and monkey retinas. ZO-1 is well known as an intracellular component of tight and adherens junctions, but also interacts with various connexins at gap junctions. We found ZO-1 closely associated with Cx50 on dendrites of A-type horizontal cells in rabbit, and with Cx57 at dendro-dendritic gap junctions of mouse horizontal cells. The spatial arrangement of ZO-1 at the giant gap-junctional plaques in rabbit was particularly striking. ZO-1 formed a clear margin around the large Cx50 plaques instead of being colocalized with the connexin staining. Our finding suggests the involvement of ZO-1 in the composition of tight or adherens junctions around gap-junctional plaques instead of interacting with connexins directly. Furthermore, gap junctions were found to be clustered in close proximity to GluRs at the level of desmosome-like junctions, where horizontal cell dendrites converge before invaginating the cone pedicle. Based on this distinct spatial organization of gap junctions and GluRs, it is tempting to speculate that glutamate released from the photoreceptors may play a role in modulating the conductance of electrical synapses in the OPL.


Received Dec. 10, 2008; revised March 20, 2009; accepted April 12, 2009.

Correspondence should be addressed to Silke Haverkamp, Max-Planck-Institut für Hirnforschung, Deutschordenstrasse 46, D-60528 Frankfurt/Main, Germany. Email: haverkamp{at}mpih-frankfurt.mpg.de






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