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The Journal of Neuroscience, November 15, 2000, 20(22):8331-8343

Molecular and Functional Diversity of Neural Connexins in the Retina

R. Dermietzel¹, M. Kremer¹, G. Paputsoglu¹, A. Stang¹, I. M. Skerrett³, D. Gomès⁴, M. Srinivas⁵, U. Janssen-Bienhold², R. Weiler², B. J Nicholson³, R. Bruzzone⁴, and D. C. Spray⁵

¹ Department of Neuroanatomy and Molecular Brain Research, Ruhr Universität Bochum, DE-45801 Bochum, Germany, ² Universität Oldenburg, Department of Biology, Carl von Ossietzky Universität, DE-2611 Oldenburg Germany, ³ Department of Biological Sciences, State University of New York Buffalo, Buffalo, New York 14260, ⁴ Institut Pasteur, Unité de Neurovirologie et Régénération du Système Nerveux, F-75724 Paris Cedex 15, France, and ⁵ Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461

Electrical synapses (gap junctions) in neuronal circuits have become a major focus in the study of network properties such as synchronization and oscillation (Galarreta and Hestrin, 1999; Gibson et al., 1999). Despite the recent progress made in unraveling the contribution of gap junctions to network behavior, little is known about the molecular composition of the junctional constituents. By cloning gap junction proteins [connexins (Cxs)] from zebrafish retina and through functional expression, we demonstrate that the retina possesses a high degree of connexin diversity, which may account for differential functional properties of electrical synapses. Three new Cxs, designated as zebrafish Cx27.5 (zfCx27.5), zfCx44.1, and zfCx55.5, and the carp ortholog of mammalian Cx43 were cloned. By in situ hybridization and in situ RT-PCR, we demonstrate that the four fish connexin mRNAs show differential localization in the retina. Transient functional expression in paired Xenopus oocytes and in the neuroblastoma N2A cell line indicate an extreme range of electrophysiological properties of these connexins in terms of voltage dependence and unitary conductance. For instance, the new zfCx44.1 exhibited high sensitivity to voltage-induced closure with currents decaying rapidly for transjunctional potentials >10 mV, whereas zfCx55.5 channels showed an opposite voltage dependence in response to voltage steps of either polarity. Moreover, although zfCx44.1 channels showed unitary conductance as high as any previously reported for junctional channels (nearly 300 pS), zfCx55.5 and zfCx27.5 exhibited much lower unitary conductances (<60 pS).

Key words: electrical synapses; gap junctions; retina; cloning; zebrafish connexins; functional diversity

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20228331-13$05.00/0

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