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Vol. 14, Issue 5, 1835-1851, May 2003

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The AP-1 Clathrin-adaptor Is Required for Lysosomal Enzymes Sorting and Biogenesis of the Contractile Vacuole Complex in Dictyostelium Cells

Yaya Lefkir ^*, Benoît de Chassey ^*, Annick Dubois ^*, Aleksandra Bogdanovic , Rebecca J. Brady , Olivier Destaing , Franz Bruckert , Theresa J. O'Halloran , Pierre Cosson ^¶, and François Letourneur ^* #

^* Institut de Biologie et Chimie des Protéines, UMR5086, CNRS/Université Lyon I, IFR 128 BioSciences Lyon-Gerland, 7, Passage du Vercors, 69367 Lyon cedex 07, France; Laboratoire de Biochimie et Biophysique des Systémes Intégrés, 38054 Grenoble Cedex 9, France; 241 Patterson Laboratories, Section of Molecular Cell and Developmental Biology, The University of Texas at Austin, Austin, Texas 78712; Laboratoire de Biologie Moléculaire et Cellulaire/UMR 5665 Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 07, France; and ^¶ Université de Genève, Centre Médical Universitaire, Département de Morphologie, CH-1211 Genève 4, Switzerland

Submitted October 2, 2002; Revised November 20, 2002; Accepted December 27, 2002
Monitoring Editor: Randy Schekman

Adaptor protein complexes (AP) are major components of the cytoplasmic coat found on clathrin-coated vesicles. Here, we report the molecular and functional characterization of Dictyostelium clathrin-associated AP-1 complex, which in mammalian cells, participates mainly in budding of clathrin-coated vesicles from the trans-Golgi network (TGN). The -adaptin AP-1 subunit was cloned and shown to belong to a Golgi-localized 300-kDa protein complex. Time-lapse analysis of cells expressing -adaptin tagged with the green-fluorescent protein demonstrates the dynamics of AP-1–coated structures leaving the Golgi apparatus and rarely moving toward the TGN. Targeted disruption of the AP-1 medium chain results in viable cells displaying a severe growth defect and a delayed developmental cycle compared with parental cells. Lysosomal enzymes are constitutively secreted as precursors, suggesting that protein transport between the TGN and lysosomes is defective. Although endocytic protein markers are correctly localized to endosomal compartments, morphological and ultrastructural studies reveal the absence of large endosomal vacuoles and an increased number of small vacuoles. In addition, the function of the contractile vacuole complex (CV), an osmoregulatory organelle is impaired and some CV components are not correctly targeted.

^# Corresponding author. E-mail address: f.letourneur{at}ibcp.fr.

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