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Originally published In Press as doi:10.1074/jbc.M908347199 on March 16, 2000

J. Biol. Chem., Vol. 275, Issue 21, 15637-15644, May 26, 2000
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Identification of a Plasma Membrane-associated Guanine Nucleotide Exchange Factor for ARF6 in Chromaffin Cells
POSSIBLE ROLE IN THE REGULATED EXOCYTOTIC PATHWAY*

Anne-Sophie CaumontDagger , Nicolas Vitale, Marc Gensse, Marie-Christine Galas, James E. Casanova§, and Marie-France Bader

From the INSERM, U-338 Biologie de la Communication Cellulaire, 5 rue Blaise Pascal, 67084 Strasbourg Cedex, France and the § Combined Program in Pediatric Gastroenterology and Nutrition, Massachusetts General Hospital East, Charlestown, Massachusetts 02129

ADP-ribosylation factors (ARFs) constitute a family of structurally related proteins that forms a subset of the Ras superfamily of regulatory GTP-binding proteins. Like other GTPases, activation of ARFs is facilitated by specific guanine nucleotide exchange factors (GEFs). In chromaffin cells, ARF6 is associated with the membrane of secretory granules. Stimulation of intact cells or direct elevation of cytosolic calcium in permeabilized cells triggers the rapid translocation of ARF6 to the plasma membrane and the concomitant activation of phospholipase D (PLD) in the plasma membrane. Both calcium-evoked PLD activation and catecholamine secretion in permeabilized cells are strongly inhibited by a synthetic peptide corresponding to the N-terminal domain of ARF6, suggesting that the ARF6-dependent PLD activation near the exocytotic sites represents a key event in the exocytotic reaction in chromaffin cells. In the present study, we demonstrate the occurrence of a brefeldin A-insensitive ARF6-GEF activity in the plasma membrane and in the cytosol of chromaffin cells. Furthermore, reverse transcriptase-polymerase chain reaction and immunoreplica analysis indicate that ARNO, a member of the brefeldin A-insensitive ARF-GEF family, is expressed and predominantly localized in the cytosol and in the plasma membrane of chromaffin cells. Using permeabilized chromaffin cells, we found that the introduction of anti-ARNO antibodies into the cytosol inhibits, in a dose-dependent manner, both PLD activation and catecholamine secretion in calcium-stimulated cells. Furthermore, co-expression in PC12 cells of a catalytically inactive ARNO mutant with human growth hormone as a marker of secretory granules in transfected cells resulted in a 50% inhibition of growth hormone secretion evoked by depolarization with high K+. The possibility that the plasma membrane-associated ARNO participates in the exocytotic pathway by activating ARF6 and downstream PLD is discussed.

* This work was supported in part by Association de la Recherche sur le Cancer ARC Grant 9101.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.

Dagger Supported by a fellowship from La Ligue Nationale Contre le Cancer.

To whom correspondence should be addressed. Tel.: 33-3-88-45-67-13; Fax: 33-3-88-60-08-06; E-mail: bader@neurochem.u-strasbg.fr.

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