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Vol. 16, Issue 4, 1696-1710, April 2005

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MARCH-II Is a Syntaxin-6–binding Protein Involved in Endosomal Trafficking

Department of Biological Sciences, Tokyo Institute of Technology, Yokohama 226-8501, Japan

Submitted March 15, 2004; Revised January 6, 2005; Accepted January 21, 2005
Monitoring Editor: Jean Gruenberg

Membrane-associated RING-CH (MARCH) is a recently identified member of the mammalian E3 ubiquitin ligase family, some members of which down-regulate the expression of immune recognition molecules. Here, we have identified MARCH-II, which is ubiquitously expressed and localized to endosomal vesicles and the plasma membrane. Immunoprecipitation and in vitro binding studies established that MARCH-II directly associates with syntaxin 6. Overexpression of MARCH-II resulted in redistribution of syntaxin 6 as well as some syntaxin-6–interacting soluble N-ethylmaleimide–sensitive factor attachment protein receptors (SNAREs) into the MARCH-II–positive vesicles. In addition, the retrograde transport of TGN38 and a chimeric version of furin to trans-Golgi network (TGN) was perturbed—without affecting the endocytic degradative and biosynthetic secretory pathways—similar to effects caused by a syntaxin 6 mutant lacking the transmembrane domain. MARCH-II overexpression markedly reduced the cell surface expression of transferrin (Tf) receptor and Tf uptake and interfered with delivery of internalized Tf to perinuclear recycling endosomes. Depletion of MARCH-II by small interfering RNA perturbed the TGN localization of syntaxin 6 and TGN38/46. MARCH-II is thus likely a regulator of trafficking between the TGN and endosomes, which is a novel function for the MARCH family.

Abbreviations used: ER, endoplasmic reticulum; EGFR, epidermal growth factor receptor; MARCH, membrane-associated RING-CH; PHD, plant homeodomain; SEAP, secretory alkaline phosphatase; shRNA, short-hairpin RNA; siRNA, small interfering RNA; SNARE, soluble N-ethylmaleimide–sensitive factor attachment protein receptor; Tf, transferrin; TfR, Tf receptor; TGN, trans-Golgi network; TMR, tetramethylrhodamine; TRITC, tetramethyl rhodamine isothiocyanate.

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

Address correspondence to: Shigehisa Hirose (shirose{at}bio.titech.ac.jp).

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