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The Journal of Neuroscience, June 25, 2008, 28(26):6616-6626; doi:10.1523/JNEUROSCI.5597-07.2008

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Cellular/Molecular
Functional Remodeling of Gap Junction-Mediated Electrical Communication between Adrenal Chromaffin Cells in Stressed Rats

Claude Colomer,^1,2,3,4 Luis A. Olivos Ore,^1,2,3,4,5 Nathalie Coutry,^1,2,3,4 Marie-Noëlle Mathieu,^1,2,3,4 Sébastien Arthaud,⁶ Pierre Fontanaud,^1,2,3,4 Irena Iankova,⁷ Françoise Macari,^1,2,3,4 Erwan Thouënnon,⁶ Laurent Yon,⁶ Youssef Anouar,⁶ and Nathalie C. Guérineau^1,2,3,4

¹Institute of Functional Genomics, ²Centre National de la Recherche Scientifique UMR5203, ³Inserm U661, and ⁴University of Montpellier (IFR3), 34094 Montpellier, France, ⁵Department of Toxicology and Pharmacology, Complutense University of Madrid, 28040 Madrid, Spain, ⁶Inserm U413, University of Rouen, 76821 Mont-Saint-Aignan, France, and ⁷Inserm U896, 34298 Montpellier, France

Correspondence should be addressed to Dr. Nathalie C. Guérineau, Department of Endocrinology, Institute of Functional Genomics, 141 rue de la Cardonille, 34094 Montpellier CEDEX 05, France. Email: nathalie.guerineau{at}igf.cnrs.fr

An increase in circulating catecholamine levels represents one of the mechanisms whereby organisms cope with stress. In the periphery, catecholamines mainly originate from the sympathoadrenal system. As we reported, in addition to the central control through cholinergic innervation, a local gap junction-delineated route between adrenal chromaffin cells contributes to catecholamine exocytosis. Here, we investigated whether this intercellular communication is modified when the hormonal demand is increased as observed during cold stress. Our results show that in cold exposed rats, gap-junctional communication undergoes a functional plasticity, as evidenced by an increased number of dye-coupled cells. Of a physiological interest is that this upregulation of gap-junctional coupling results in the appearance of a robust electrical coupling between chromaffin cells that allows the transmission of action potentials between coupled cells. This enhancement of gap-junctional communication parallels an increase in expression levels of connexin36 (Cx36) and connexin43 (Cx43) proteins. Both transcriptional and posttranslational mechanisms are involved because Cx36 transcripts are increased in stressed rats and the expression of the scaffolding protein zonula occludens-1, known to interact with both Cx36 and Cx43, is also upregulated. Consistent with an upregulated coupling extent in stressed rats, the cytosolic Ca²⁺ concentration rises triggered in a single cell by an iontophoretic application of nicotine occur simultaneously in several neighboring cells. These results describe for the first time a functional plasticity of junctional coupling between adult chromaffin cells that should be crucial for adaptation to stress or sensitization to subsequent stressors.

Key words: gap-junctional communication; connexins; nicotinic stimulation; cold exposure; dual patch clamp; rat acute adrenal slices

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Received Dec. 18, 2007; revised April 18, 2008; accepted May 15, 2008.

Correspondence should be addressed to Dr. Nathalie C. Guérineau, Department of Endocrinology, Institute of Functional Genomics, 141 rue de la Cardonille, 34094 Montpellier CEDEX 05, France. Email: nathalie.guerineau{at}igf.cnrs.fr

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