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J. Biol. Chem., Vol. 278, Issue 27, 24837-24848, July 4, 2003

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An Ancestral Secretory Apparatus in the Protozoan Parasite Giardia intestinalis^*,

Matthias Marti **, Attila Regös, Yajie Li , Elisabeth M. Schraner , Peter Wild , Norbert Müller ¶, Lea G. Knopf and Adrian B. Hehl ||

From the Institute of Parasitology, University of Zürich, CH-8057 Zürich, Switzerland, the Electron Microscopy Unit, Institutes of Veterinary Anatomy and Virology, University of Zürich, CH-8057 Zürich, Switzerland, and the ^¶Institute of Parasitology, University of Bern, CH-3012 Bern, Switzerland

The protozoan parasite Giardia intestinalis belongs to one of the earliest diverged eukaryotic lineages. This is also reflected in a simple intracellular organization, as Giardia lacks common subcellular compartments such as mitochondria, peroxisomes, and apparently also a Golgi apparatus. During encystation, developmentally regulated formation of large secretory compartments containing cyst wall material occurs. Despite the lack of any morphological similarities, these encystation-specific vesicles (ESVs) show several biochemical characteristics of maturing Golgi cisternae. Previous studies suggested that Golgi structure and function are induced only during encystation in Giardia, giving rise to the hypothesis that ESVs, as a Giardia Golgi equivalent, are generated de novo. Alternatively, ESV compartments could be built on the template structure of a cryptic Golgi in trophozoites in response to ER export of cyst wall material during encystation. We addressed this question by defining the molecular framework of the Giardia secretory apparatus using a comparative genomic approach. Analysis of the corresponding transcriptome during growth and encystation revealed surprisingly little stage-specific regulation. A panel of antibodies was generated against selected marker proteins to investigate the developmental dynamics of the endomembrane system. We show evidence that Giardia accommodates the export of large amounts of cyst wall material through re-organization of membrane compartment(s) in trophozoites with biochemical similarities to ESVs. This suggests that ESVs are selectively stabilized Golgi-like compartments in a unique and archetypical secretory system, which arise from a structural template in trophozoites rather than being generated de novo.

Received for publication, February 27, 2003 , and in revised form, April 23, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AF503489, AF503488, AF486294, AF486293, AY078979, AY078978, AY078976, AY078977, AF456417, AF456415, AF481768, AF481767, AF481766, AF481765, AF456416, and AY219652.

^* This work was supported in part by Swiss National Science Foundation Grants 31-58912.99 and 31-100270/1, the Novartis Foundation, and the "Stiftung für wissenschaftliche Forschung an der Universität Zürich." The costs of publication of this article were defrayed in part by the payment of page charges. This 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 tables.

^** Present address: Division of Infection and Immunity, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3050, Australia.

Supported by a training grant from the China Scholarship Council. Present address: Dept. of Parasitology, Harbin Medical University, 150086, Harbin, Peoples Republic of China.

^|| To whom correspondence should be addressed. Institute of Parasitology, University of Zürich, Winterthurerstrasse 266a, CH-8057 Zürich, Switzerland. Tel.: 41-1-635-8526; Fax: 41-1-635-8907; E-mail: ahehl{at}vetparas.unizh.ch.

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