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J. Biol. Chem., Vol. 283, Issue 51, 35996-36010, December 19, 2008

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Characterization of SNAREs Determines the Absence of a Typical Golgi Apparatus in the Ancient Eukaryote Giardia lamblia^*

Eliana V. Elias, Rodrigo Quiroga, Natalia Gottig, Hideki Nakanishi, Theodore E. Nash^¶, Aaron Neiman, and Hugo D. Lujan¹

From the Laboratory of Biochemistry and Molecular Biology, School of Medicine, Catholic University of Cordoba/National Council for Science and Technology, Cordoba CP X5004ASK, Argentina, the Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, New York 11794, and the ^¶Laboratory of Parasitic Diseases, National Institutes of Health, NIAID, Bethesda, Maryland 20892

Giardia is a eukaryotic protozoal parasite with unusual characteristics, such as the absence of a morphologically evident Golgi apparatus. Although both constitutive and regulated pathways for protein secretion are evident in Giardia, little is known about the mechanisms involved in vesicular docking and fusion. In higher eukaryotes, soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) of the vesicle-associated membrane protein and syntaxin families play essential roles in these processes. In this work we identified and characterized genes for 17 SNAREs in Giardia to define the minimal set of subcellular organelles present during growth and encystation, in particular the presence or not of a Golgi apparatus. Expression and localization of all Giardia SNAREs demonstrate their presence in distinct subcellular compartments, which may represent the extent of the endomembrane system in eukaryotes. Remarkably, Giardia SNAREs, homologous to Golgi SNAREs from other organisms, do not allow the detection of a typical Golgi apparatus in either proliferating or differentiating trophozoites. However, some features of the Golgi, such as the packaging and sorting function, seem to be performed by the endoplasmic reticulum and/or the nuclear envelope. Moreover, depletion of individual genes demonstrated that several SNAREs are essential for viability, whereas others are dispensable. Thus, Giardia requires a smaller number of SNAREs compared with other eukaryotes to accomplish all of the vesicle trafficking events that are critical for the growth and differentiation of this important human pathogen.

Received for publication, August 22, 2008 , and in revised form, October 15, 2008.

^* This work was supported, in whole or in part, by the National Institutes of Health NIAID Intramural Research Program. This work was also supported by the Agencia Nacional para la Promoción de la Ciencia y la Tecnología (FONCYT), the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), the Howard Hughes Medical Institute (HHMI), and the Universidad Catolica de Córdoba. 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 supplemental Figs. S1-S10 and Tables S1-S5.

¹ An International Research Scholar of the HHMI and a member of the Scientist's Career of CONICET. To whom correspondence should be addressed: Laboratorio de Bioquimica y Biologia Molecular, Facultad de Medicina, Universidad Catolica de Cordoba, Jacinto Rios 571, CP X5004ASK, Cordoba, Argentina. Tel.: 54-351-4860708. E-mail: hlujan{at}ucc.edu.ar.

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