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J. Biol. Chem., Vol. 278, Issue 24, 21701-21708, June 13, 2003

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Mining the Giardia lamblia Genome for New Cyst Wall Proteins^*

Chin-Hung Sun  , J. Michael McCaffery ¶, David S. Reiner  and Frances D. Gillin  ||

From the Department of Pathology, University of California at San Diego, School of Medicine, San Diego, California 92103-8416, ^¶ Integrated Imaging Center, Department of Biology, The Johns Hopkins University, Baltimore, Maryland 21218

The Giardia lamblia cyst wall (CW), which is required for survival outside the host and infection, is a primitive extracellular matrix. Because of the importance of the CW, we queried the Giardia Genome Project Database with the coding sequences of the only two known CW proteins, which are cysteine-rich and contain leucine-rich repeats (LRRs). We identified five new LRR-containing proteins, of which only one (CWP3) is up-regulated during encystation and incorporated into the cyst wall. Sequence comparison with CWP1 and -2 revealed conservation within the LRRs and the 44-amino-acid N-flanking region, although CWP3 is more divergent. Interestingly, all 14 cysteine residues of CWP3 are positionally conserved with CWP1 and -2. During encystation, C-terminal epitope-tagged CWP3 was transported to the wall of water-resistant cysts via the novel regulated secretory pathway in encystation-secretory vesicles (ESVs). Deletion analysis revealed that the four LRRs are each essential to target CWP3 to the ESVs and cyst wall. In a deletion of the most C-terminal region, fewer ESVs were stained in encysting cells, and there was no staining in cysts. In contrast, deletion of the 44 amino acids between the signal sequence and the LRRs or the region just C-terminal to the LRRs only decreased the number of cells with CWP3 targeting to ESVs and cyst wall by 50%. Our studies indicate that virtually every portion of the CWP3 protein is needed for efficient targeting to the regulated secretory pathway and incorporation into the cyst wall. Further, these data demonstrate the power of genomics in combination with rigorous functional analyses to verify annotation.

Received for publication, February 26, 2003 , and in revised form, April 8, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY225413, AY225414, and AY225415.

^* This work was supported by Public Health Service Grants GM61896, AI51687, AI42488, and DK35108 from the National Institutes of Health. 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.

Present address: Dept. of Parasitology, College of Medicine, National Taiwan University, Taipei 110, Taiwan.

^|| To whom correspondence should be addressed: Dept. of Pathology, School of Medicine, University of California at San Diego, 214 Dickinson St., 8416, San Diego, CA 92013-8416. Tel.: 619-543-6146; Fax: 619-543-6614; E-mail: fgillin{at}ucsd.edu.

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