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Vol. 12, Issue 2, 367-381, February 2001
Department of Biochemistry, Weill Graduate School of Medical
Sciences of Cornell University, New York, New York 10021
Insulin-regulated aminopeptidase (IRAP), a
transmembrane aminopeptidase, is dynamically retained
within the endosomal compartment of fibroblasts. The characteristics of
this dynamic retention are rapid internalization from the plasma
membrane and slow recycling back to the cell surface. These specialized
trafficking kinetics result in <15% of IRAP on the cell surface at
steady state, compared with 35% of the transferrin receptor, another
transmembrane protein that traffics between endosomes and the cell
surface. Here we demonstrate that a 29-amino acid region of IRAP's
cytoplasmic domain (residues 56-84) is necessary and sufficient to
promote trafficking characteristic of IRAP. A di-leucine sequence and a
cluster of acidic amino acids within this region are essential elements
of the motif that slows IRAP recycling. Rapid internalization requires
any two of three distinct motifs: M15,16,
DED64-66, and LL76,77. The DED and LL
sequences are part of the motif that regulates recycling, demonstrating
that this motif is bifunctional. In this study we used horseradish
peroxidase quenching of fluorescence to demonstrate that IRAP is
dynamically retained within the transferrin receptor-containing general
endosomal recycling compartment. Therefore, our data demonstrate that
motifs similar to those that determine targeting among distinct
membrane compartments can also regulate the rate of transport of
proteins from endosomal compartments. We propose a model for dynamic
retention in which IRAP is transported from the general endosomal
recycling compartment in specialized, slowly budding recycling vesicles
that are distinct from those that mediate rapid recycling back to the
surface (e.g., transferrin receptor-containing transport vesicles). It
is likely that the dynamic retention of IRAP is an example of a general
mechanism for regulating the distribution of proteins between the
surface and interior of cells.
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