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J. Biol. Chem., Vol. 277, Issue 10, 8474-8481, March 8, 2002
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From the Giardia is an intestinal
parasite that belongs to the earliest diverging branch of the
eukaryotic lineage of descent. Giardia undergoes adaptation
for survival outside the host's intestine by differentiating into
infective cysts. Encystation involves the synthesis and transport of
cyst wall constituents to the plasma membrane for release and
extracellular organization. Nevertheless, little is known about the
molecular events related to cyst wall biogenesis in
Giardia. Among the components of the cyst wall there are
two proteins that we have previously identified and characterized: CWP1
(26 kDa) and CWP2 (39 kDa). Expression of these proteins is
coordinately induced, and both concentrated within encystation-specific secretory vesicles before their extracellular polymerization. Although highly similar to each other at the amino terminus, CWP2 includes a COOH-terminal 121-amino acid extension. Here, we show that
this extension, rich in basic residues, is cleaved from CWP2 before
cyst wall formation by an intracellular cysteine proteinase activity, which is induced during encystation like CWPs. Specific inhibitors prevent release of cyst wall materials, abolishing cyst wall
formation. We also report the purification, cloning, and
characterization of the encystation-specific cysteine proteinase responsible for the proteolytic processing of CWP2, which is homologue to lysosomal cathepsin C. Encystation-specific cysteine proteinase ESCP
possesses unique characteristics compared with cathepsins from higher
eukaryotes, such as a transmembrane domain and a short cytoplasmic
tail. These features make this enzyme the most divergent cathepsin C
identified to date and provide new insights regarding cyst wall
formation in Giardia.
The Activity of a Developmentally Regulated Cysteine Proteinase
Is Required for Cyst Wall Formation in the Primitive Eukaryote
Giardia lamblia*,
§,¶,,
,, and
Catedra de Bioquimica y Biologia Molecular,
Facultad de Ciencias Medicas, Universidad Nacional de Cordoba, CP5000
Argentina, the Unidad de Biologia Parasitaria, Facultad de
Ciencias, Montevideo, CP11600 Uruguay, and the ** Laboratory
of Parasitic Diseases, NIAID, National Institutes of Health,
Bethesda, Maryland 20892
*
This work was supported in part by the Agencia Nacional para
la Promocion de la Ciencia y la Tecnologia (ANPCYT), Fundacion Antorchas, Universidad Nacional de Cordoba, and the Consejo Nacional de
Investigaciones Cientificas y Tecnicas (CONICET).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.
The on-line version of this article (available at
http://www.jbc.org) contains Figs. 1S-3S.
§
Recipient of a fellowship from Consejo Provincial de Ciencia y
Tecnica de Cordoba.
¶
Recipient of a fellowship from CONICET.
Member of the Scientist Career of CONICET and an
International Research Scholar of the Howard Hughes Medical Institute.
To whom correspondence should be addressed: Catedra de Bioquimica y
Biologia Molecular, Facultad de Ciencias Medicas, Universidad Nacional
de Cordoba, Pabellon Argentina 2do piso, Ciudad
Universitaria. CP 5000. Cordoba, Argentina. Tel./Fax: 54-351-433-3024;
E-mail: hlujan@biomed.uncor.edu.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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