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Originally published In Press as doi:10.1074/jbc.M000511200 on April 20, 2000

J. Biol. Chem., Vol. 275, Issue 26, 19638-19644, June 30, 2000
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Nitric Oxide Inhibits the Tumor Necrosis Factor alpha -regulated Endocytosis of Human Dendritic Cells in a Cyclic GMP-dependent Way*

Clara PaolucciDagger §, Patrizia Rovere||, Céline De NadaiDagger §, Angelo A. Manfredi||, and Emilio ClementiDagger **Dagger Dagger

From the Dagger  Department of Neuroscience-DIBIT and || Laboratory of Tumour Immunology, Gene Therapy Programme, San Raffaele Scientific Institute, 20132 Milano, Italy, the § Consiglio Nazionale delle Ricerche Centre for Cellular and Molecular Pharmacology, 20129 Milano, Italy, and the ** Department of Pharmaco-Biology, University of Calabria, 87036 Rende, Italy

Tumor necrosis factor-alpha (TNFalpha )-induced maturation of dendritic cells (DC), with down-regulation of their endocytic ability, has been reported to be mediated by the accumulation of the lipid messenger ceramide. We have now studied the effects and mechanisms of action of NO on endocytosis, investigated with fluorescein isothiocyanate-labeled dextran using human monocyte-derived DC, both immature and after treatment with TNFalpha . Exposure of DC to NO, released by either bystander phagocytes or NO donors, reversed the inhibition of endocytosis induced by TNFalpha . The intracellular accumulation of ceramide induced by TNFalpha was also inhibited by NO. In addition, NO was found to exert an inhibitory effect downstream of the TNFalpha -triggered ceramide accumulation, because NO donors reversed the inhibition of endocytosis induced by the cell-permeant C2-ceramide. These effects of NO were mimicked by the membrane-permeant cyclic GMP analogue, 8-Br cyclic GMP, and prevented by inhibition of the soluble guanylyl cyclase. At variance with rodents, the inducible isoform of the NO synthase was expressed neither in immature human DC nor after cell treatment with TNFalpha , interferon-gamma , and lipopolysaccharide, suggesting that regulation of these cells depends on exogenous NO. NO, working through cyclic GMP, might therefore prolong the ability of human DC to internalize antigens at the site of inflammation and thus modulate the initial steps leading to antigen-specific immune responses.

* This work was supported by grants from the Italian Association for Cancer Research (to E. C. and A. M.), Consiglio Nazionale delle Ricerche, Target Project Biotechnology (to E. C.), Ministero dell'Università e della Ricerca Scientifica e Tecnologica, Cofinanziamento 99 (to E. C.), Schering-Plough Italia (to E. C.), and Istituto Superiore di Sanità, Progetto Tubercolosi and HIV (to A. M.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

These authors contributed equally to this work.

Dagger Dagger To whom correspondence should be addressed: DIBIT-Scientific Institute San Raffaele, Via Olgettina 58, 20132 Milano, Italy. Tel.: 39-02-2643-4814; Fax: 39-02-2643-4813; E-mail: clementi.emilio@hsr.it.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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