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J. Biol. Chem., Vol. 278, Issue 7, 5343-5352, February 14, 2003
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From the We have previously demonstrated that
Toxoplasma gondii has a tyrosine-based sorting system,
which mediates protein targeting to the lysosome-like rhoptry secretory
organelle. We now show that rhoptry protein targeting is also dependent
on a dileucine motif and occurs from a post-Golgi endocytic organelle
to mature rhoptries in an adaptin-dependent fashion. The
T. gondii AP-1 adaptin complex is implicated in this
transport because the µ1 chain of T. gondii AP-1
(a) was localized to multivesicular endosomes and the
limiting and luminal membranes of the rhoptries; (b) bound to endocytic tyrosine motifs in rhoptry proteins, but not in proteins from dense granule secretory organelles; (c) when mutated
in predicted tyrosine-binding motifs, led to accumulation of the
rhoptry protein ROP2 in a post-Golgi multivesicular compartment; and
(d) when depleted via antisense mRNA, resulted in
accumulation of multivesicular endosomes and immature rhoptries. These
are the first results to implicate AP-1 in transport from a post-Golgi
compartment to a mature secretory organelle and substantially expand
the role for AP-1 in anterograde protein transport.
The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AY117037.
AP-1 in Toxoplasma gondii Mediates Biogenesis of the
Rhoptry Secretory Organelle from a Post-Golgi Compartment*
§,§,,
, and¶**
Section of Infectious Diseases, Department
of Internal Medicine, and the ¶ Department of Cell Biology, Yale
University School of Medicine, New Haven, Connecticut 06520-8022
*
This work was supported by National Research Service Awards
5T32AI07404 and 5F32AI10044 (to H. M. N.) and Grant RO1 AI30060 (to
K. A. J.) from the National Institutes of Health and by a scholar
award in molecular parasitology from the Burroughs Wellcome Fund (to
K. A. J.). Work performed at the Institute for Genomic Research and
Washington University was supported by National Institutes of Health
Grants AI05093 and 1R01AI045806-01A1, respectively.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Present address: Dept. of Medical Microbiology, University of
Cape Town Medical School, Observatory 7925, Cape Town, South Africa.
**
To whom correspondence should be addressed: Dept. of Internal
Medicine, Yale University School of Medicine, LCI 808, 333 Cedar St.,
New Haven, CT 06520-8022. Tel.: 203-785-2115; Fax: 203-785-3864; E-mail: keith.joiner@yale.edu.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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