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Cellular and Subcellular Evidence for Neuronal Interaction between the Chemokine Stromal Cell-Derived Factor-1/CXCL 12 and Vasopressin: Regulation in the Hypothalamo-Neurohypophysial System of the Brattleboro Rats

Institut National de la Santé et de la Recherche Médicale Unité 732 (C.C., P.M., P.K., S.M.P., W.R.), Université Pierre et Marie Curie, Hôpital Saint-Antoine, 75571 Paris Cedex 12, France; Equipe Accueil EA3453 (B.F., A.B.), Université Henri Poincaré, 54000 Nancy, France; and Centre National de la Recherche Scientifique Unité Mixte de Recherche 7101 (D.R., A.C.), Université Pierre et Marie Curie, 75252 Paris Cedex 05, France

Address all correspondence and requests for reprints to: Dr. William Rostène, Les Chimiokines et Leurs Récepteurs: Fonctions Cérébrales et Neuroendocriniennes, Institut National de la Santé et de la Recherche Médicale Unité 732-UPMC, Hôpital Saint-Antoine, 184 rue du Faubourg Saint-Antoine, 75571 Paris Cedex 12, France. E-mail: rostene{at}st-antoine.inserm.fr.

We previously described a colocalization between arginine vasopressin (AVP) and the chemokine stromal cell-derived factor-1 (SDF-1) in the magnocellular neurons of both the hypothalamic supraoptic and paraventricular nucleus as well as the posterior pituitary. SDF-1 physiologically affects the electrophysiological properties of AVP neurons and consequently AVP release. In the present study, we confirm by confocal and electron microscopy that AVP and SDF-1 have a similar cellular distribution inside the neuronal cell and can be found in dense core vesicles in the nerve terminals in the posterior pituitary. Because the Brattleboro rats represent a good model of AVP deficiency, we tested in these animals the fate of SDF-1 and its receptor CXCR4. We identified by immunohistochemistry that both SDF-1 and CXCR4 immunoreactivity were strongly decreased in Brattleboro rats and were strictly correlated with the expression of AVP protein in supraoptic nucleus, paraventricular nucleus, and the posterior pituitary. We observed by real-time PCR an increase in SDF-1 mRNA in both heterozygous and homozygous rats. The effect on the SDF-1/CXCR4 system was not linked to peripheral modifications of kidney water balance because it could not be restored by chronic infusion of deamino-8D-ariginine-vasopressin, an AVP V2-receptor agonist. These original data further suggest that SDF-1 may play an essential role in the regulation of water balance.