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J. Biol. Chem., Vol. 276, Issue 36, 33773-33781, September 7, 2001

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Activation of the Luteinizing Hormone/Choriogonadotropin Hormone Receptor Promotes ADP Ribosylation Factor 6 Activation in Porcine Ovarian Follicular Membranes^*

Lisa M. Salvador, Sutapa Mukherjee, Richard A. Kahn^§, Marilyn L. G. Lamm^¶, Asgerally T. Fazleabas, Evelyn T. Maizels, Marie-France Bader^**, Heidi Hamm^§§, Mark M. Rasenick, James E. Casanova^¶¶, and Mary Hunzicker-Dunn

From the Departments of  Cell and Molecular Biology and ^§§ Molecular Pharmacology and Biological Chemistry and the Neuroscience Institute, Northwestern University Medical School, Chicago, Illinois 60611, the ^§ Department of Biochemistry, Emory University School of Medicine, Atlanta, Georgia 30322, ^** INSERM, U-338 Biologie de la Communication Cellulaire, 5 rue Blaise Pascal, Strasbourg 67084 Cedex, France, the  Departments of Physiology & Biophysics and Psychiatry and the  Department of Obstetrics and Gynecology, University of Illinois College of Medicine, Chicago, Illinois 60612, and the ^¶¶ Department of Cell Biology, University of Virginia Health Sciences Center, Charlottesville, Virginia 22908

Previously we demonstrated in a cell-free ovarian follicular plasma membrane model that agonist-dependent desensitization of the luteinizing hormone/choriogonadotropin receptor (LH/CG R) is GTP-dependent, mimicked by the addition of ADP-ribosylation factor (ARF) nucleotide binding site opener, which acts as a guanine nucleotide exchange factor for ARFs 1 and 6, and selectively inhibited by synthetic N-terminal ARF6 peptides. We therefore sought direct evidence that activation of the LH/CG R promotes activation of ARF1 and/or ARF6. Using a classic ARF activation assay, the cholera toxin-catalyzed ADP-ribosylation of G_s, results show that LH/CG R activation stimulates an ARF protein by a brefeldin A-independent mechanism. Synthetic N-terminal inhibitory ARF6 but not ARF1 peptide blocks LH/CG R-stimulated ARF activity. LH/CG R activation also promotes the binding of a photoaffinity GTP analog to a protein that migrates on one- and two-dimensional polyacrylamide gel electrophoresis with ARF6. These results suggest that ARF6 is the predominant ARF activated by the LH/CG R. To activate ARF6, the LH/CG R does not appear to signal through the C-terminal regions of G_i or G_q or through the second or third intracellular loops or the N terminus of the cytoplasmic tail of the LH/CG R. Although exogenous recombinant ARNO promotes only a small increase in ARF6 activation in the presence of activated LH/CG R, hCG-stimulated ARF6 activation is reduced to basal levels by catalytically inactive ARF nucleotide binding-site opener. These results provide direct evidence that LH/CG R activation leads to the activation of membrane-delimited ARF6.

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