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J. Biol. Chem., Vol. 283, Issue 11, 6764-6772, March 14, 2008

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Control of Cellular Physiology by TM9 Proteins in Yeast and Dictyostelium^*

Romain Froquet, Nathalie Cherix, Raphael Birke, Mohammed Benghezal, Elisabetta Cameroni^¶, François Letourneur^||, Hans-Ulrich Mösch, Claudio De Virgilio^¶, and Pierre Cosson¹

From the Département de Physiologie et Métabolisme Cellulaire, Centre Médical Universitaire, Université de Genève, rue Michel Servet 1, CH-1211 Genève 4, Switzerland, Department of Genetics, Philipps University Marburg, Karl-von-Frisch-Strasse 8, D-35043 Marburg, Germany, the ^¶Department of Medicine, University of Fribourg, Division of Biochemistry, 1700 Fribourg, Switzerland, and the ^||Institut de Biologie et Chimie des Protéines, UMR 5086, CNRS, Université Lyon1, IFR128 BioSciences Lyon-Gerland, 7, Passage du Vercors, 69367 Lyon Cedex 07, France

TM9 proteins constitute a well defined family, characterized by the presence of a large variable extracellular domain and nine putative transmembrane domains. This family is highly conserved throughout evolution and comprises three members in Dictyostelium discoideum and Saccharomyces cerevisiae and four in humans and mice. In Dictyostelium, previous analysis demonstrated that TM9 proteins are implicated in cellular adhesion. In this study, we generated TM9 mutants in S. cerevisiae and analyzed their phenotype with particular attention to cellular adhesion. S. cerevisiae strains lacking any one of the three TM9 proteins were severely suppressed for adhesive growth and filamentous growth under conditions of nitrogen starvation. In these mutants, expression of the FLO11-lacZ reporter gene was strongly reduced, whereas expression of FRE(Ty1)-lacZ was not, suggesting that TM9 proteins are implicated at a late stage of nutrient-controlled signaling pathways. We also reexamined the phenotype of Dictyostelium TM9 mutant cells, focusing on nutrient-controlled cellular functions. Although the initiation of multicellular development and autophagy was unaltered in Dictyostelium TM9 mutants, nutrient-controlled secretion of lysosomal enzymes was dysregulated in these cells. These results suggest that in both yeast and amoebae, TM9 proteins participate in the control of specific cellular functions in response to changing nutrient conditions.

Received for publication, May 31, 2007 , and in revised form, December 21, 2007.

^* This work was supported by Fonds National Suisse de la Recherche Scientifique Grants 3100A0-108078 (to P. C.) and PP00A-106754/1 (to C. D. V.). This work was also supported in part by the 3R Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1–S3 and Table S1.

¹ To whom correspondence should be addressed. Tel.: 41-22-379-5293; Fax: 41-22-379-5338; E-mail: Pierre.Cosson{at}medecine.unige.ch.

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