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J. Biol. Chem., Vol. 282, Issue 38, 28074-28086, September 21, 2007

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Transcriptional Regulation of AQP-8, a Caenorhabditis elegans Aquaporin Exclusively Expressed in the Excretory System, by the POU Homeobox Transcription Factor CEH-6^*

Allan K. Mah¹, Kristin R. Armstrong, Derek S. Chew, Jeffrey S. Chu², Domena K. Tu, Robert C. Johnsen, Nansheng Chen³, Helen M. Chamberlin⁴, and David L. Baillie⁵

From the Department Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada and the Department of Molecular Genetics, Ohio State University, Columbus, Ohio 43210

Due to the ever changing environmental conditions in soil, regulation of osmotic homeostasis in the soil-dwelling nematode Caenorhabditis elegans is critical. AQP-8 is a C. elegans aquaporin that is expressed in the excretory cell, a renal equivalent tissue, where the protein participates in maintaining water balance. To better understand the regulation of AQP-8, we undertook a promoter analysis to identify the aqp-8 cis-regulatory elements. Using progressive 5' deletions of upstream sequence, we have mapped an essential regulatory region to roughly 300 bp upstream of the translational start site of aqp-8. Analysis of this region revealed a sequence corresponding to a known DNA functional element (octamer motif), which interacts with POU homeobox transcription factors. Phylogenetic footprinting showed that this site is perfectly conserved in four nematode species. The octamer site's function was further confirmed by deletion analyses, mutagenesis, functional studies, and electrophoretic mobility shift assays. Of the three POU homeobox proteins encoded in the C. elegans genome, CEH-6 is the only member that is expressed in the excretory cell. We show that expression of AQP-8 is regulated by CEH-6 by performing RNA interference experiments. CEH-6's mammalian ortholog, Brn1, is expressed both in the kidney and the central nervous system and binds to the same octamer consensus binding site to drive gene expression. These parallels in transcriptional control between Brn1 and CEH-6 suggest that C. elegans may well be an appropriate model for determining gene-regulatory networks in the developing vertebrate kidney.

Received for publication, April 19, 2007 , and in revised form, July 13, 2007.

^* 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 Tables S1-S3.

² Supported by a Weyerhauser-Molecular Biology and Biochemistry fellowship and a Hemingway Nelson Architects Graduate Scholarship.

³ Supported by a grant from NSERC Canada and a Faculty start-up fund provided by Simon Fraser University.

⁴ Supported by National Science Foundation Grant IOB-0516554.

⁵ A Canada Research Chair in Genomics and supported by grants from NSERC and the Canadian Institutes of Health Research.

¹ Supported by a Natural Sciences and Engineering Reserach Council of Canada doctoral scholarship. To whom correspondence should be addressed: Dept. of Molecular Biology and Biochemistry, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada. Tel.: 604-291-4597; Fax: 604-291-5583; E-mail: amaha{at}sfu.ca.

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