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J. Biol. Chem., Vol. 280, Issue 46, 38583-38591, November 18, 2005

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A Novel Galectin-like Domain from Toxoplasma gondii Micronemal Protein 1 Assists the Folding, Assembly, and Transport of a Cell Adhesion Complex^*

Savvas Saouros1, Bryn Edwards-Jones1, Matthias Reiss¶, Kovilen Sawmynaden, Ernesto Cota, Peter Simpson, Timothy J. Dowse, Ursula Jäkle||, Stephanie Ramboarina, Tara Shivarattan, Stephen Matthews2, and Dominique Soldati-Favre, An International Scholar of the Howard Hughes Medical Institute**3

From the Department of Biological Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom, the Centre for Structural Biology, Imperial College London, South Kensington, London SW7 2AZ, United Kingdom, the ^**Department of Microbiology and Genetics, Faculty of Medicine, University of Geneva CMU, 1 rue Michel-Servet, 1211 Geneva 4, Switzerland, the ^||Zentrum fur Molekulare Biologie Heidelberg, INF 282, 69120 Heidelberg, Germany, and the ^¶Department of Molecular Virology, University Heidelberg, INF 345, 69120 Heidelberg, Germany

Immediately prior to invasion Toxoplasma gondii tachyzoites release a large number of micronemal proteins (TgMICs) that participate in host cell attachment and penetration. The TgMIC4-MIC1-MIC6 complex was the first to be identified in T. gondii and has been recently shown to be critical in invasion. This study establishes that the N-terminal thrombospondin type I repeat-like domains (TSR1-like) from TgMIC1 function as an independent adhesin as well as promoting association with TgMIC4. Using the newly solved three-dimensional structure of the C-terminal domain of TgMIC1 we have identified a novel Galectin-like fold that does not possess carbohydrate binding properties and redefines the architecture of TgMIC1. Instead, the TgMIC1 Galectin-like domain interacts and stabilizes TgMIC6, which provides the basis for a highly specific quality control mechanism for successful exit from the early secretory compartments and for subsequent trafficking of the complex to the micronemes.

Received for publication, August 31, 2005 , and in revised form, September 12, 2005.

The atomic coordinates and structure factors (code 2bvb) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

^* This work was supported by The Wellcome Trust (Research Leave Award (to S. M.) and Programme Grant (to D. S.)), The Medical Research Council (Project Grant (to S. M.)), and The Deutsche Forschungsgemeinshaft (DFG Grant SO 366/1-3 (to D. S.)). 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.

¹ These authors contributed equally to this work.

² To whom correspondence may be addressed. E-mail: s.j.matthews{at}imperial.ac.uk. ³ To whom correspondence may be addressed. E-mail: dominique.soldati-favre{at}medecine.unige.ch.

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