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Originally published as MBC in Press, 10.1091/mbc.E05-07-0626 on September 14, 2005

Vol. 16, Issue 11, 5356-5372, November 2005

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Functions of Adaptor Protein (AP)-3 and AP-1 in Tyrosinase Sorting from Endosomes to Melanosomes{boxd}

Alexander C. Theos * {dagger}, Danièle Tenza {ddagger}, José A. Martina §, Ilse Hurbain {ddagger}, Andrew A. Peden ||, Elena V. Sviderskaya ¶, Abigail Stewart *, Margaret S. Robinson *, Dorothy C. Bennett ¶, Daniel F. Cutler #, Juan S. Bonifacino §, Michael S. Marks {dagger}, and Graça Raposo {ddagger}

* Cambridge Institute for Medical Research, University of Cambridge, Wellcome Trust, Cambridge CB2 2XY, United Kingdom; {dagger} Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104; {ddagger} Institut Curie, Centre National de la Recherche Scientifique-Unité Mixte de Recherche 144, Paris 75248, France; § Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892; || Genentech, South San Francisco, CA 94080; Department of Basic Medical Sciences, St. George's Hospital Medical School, London SW17 ORE, United Kingdom; and # MRC Laboratory for Molecular Cell Biology, Cell Biology Unit, and Department of Biochemistry and Molecular Biology, University College London, London WC1E BT, United Kingdom

Submitted July 13, 2005; Revised August 29, 2005; Accepted September 1, 2005
Monitoring Editor: Sandra Schmid

Specialized cells exploit adaptor protein complexes for unique post-Golgi sorting events, providing a unique model system to specify adaptor function. Here, we show that AP-3 and AP-1 function independently in sorting of the melanocyte-specific protein tyrosinase from endosomes to the melanosome, a specialized lysosome-related organelle distinguishable from lysosomes. AP-3 and AP-1 localize in melanocytes primarily to clathrin-coated buds on tubular early endosomes near melanosomes. Both adaptors recognize the tyrosinase dileucine-based melanosome sorting signal, and tyrosinase largely colocalizes with each adaptor on endosomes. In AP-3-deficient melanocytes, tyrosinase accumulates inappropriately in vacuolar and multivesicular endosomes. Nevertheless, a substantial fraction still accumulates on melanosomes, concomitant with increased association with endosomal AP-1. Our data indicate that AP-3 and AP-1 function in partially redundant pathways to transfer tyrosinase from distinct endosomal subdomains to melanosomes and that the AP-3 pathway ensures that tyrosinase averts entrapment on internal membranes of forming multivesicular bodies.

This article was published online ahead of print in MBC in Press (http://www.molbiolcell.org/cgi/doi/10.1091/mbc.E05-07-0626) on September 14, 2005.

Abbreviations used: AP, adaptor protein; IEM, immunoelectron microscopy, ILV, intralumenal vesicle; LRO, lysosome-related organelle; MVB, multivesicular body; PAG, protein A-gold; PB, phosphate buffer; Tf, transferrin.

{boxd} The online version of this article contains supplemental material at MBC Online (http://www.molbiolcell.org).

Address correspondence to: Graça Raposo (g.raposo{at}curie.fr).




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