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J. Biol. Chem., Vol. 283, Issue 24, 16612-16621, June 13, 2008

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Molecular Mechanism for Establishment of Signal-dependent Regulation in the PhoP/PhoQ System^*

Wei Kong, Natasha Weatherspoon, and Yixin Shi¹

From the Center for Infectious Diseases and Vaccinology at the Biodesign Institute and The School of Life Sciences, Arizona State University, Tempe, Arizona 85287-4501

In this report, we demonstrate that H-NS is essential for establishing the Mg²⁺-responsive transcriptional regulation of the PhoP regulon in Salmonella. Deletion of this regulatory gene abolished the transcriptional repression of PhoP-activated genes when bacteria were grown in high environmental Mg²⁺, thus stimulating expression of phoP and other PhoP regulon genes. In the absence of H-NS, transcriptional activation was PhoP-dependent for those genes only activated by PhoP, but was PhoP-independent for those genes activated by both PhoP and SlyA. The H-NS protein footprints the phoP promoter in a sequence located upstream of the PhoP box; mutation of this cis-acting factor abolished transcriptional repression of the phoP gene equivalent to the phenotype exhibited in the hns mutant. Further results showed that H-NS gel shifts other PhoP regulon promoters, indicating that a PhoP-activated gene would be transcriptionally repressed via direct H-NS binding and inhibition of its activator PhoP. Furthermore, H-NS footprints a newly identified SlyA box and the reverse PhoP box in the pagC promoter, suggesting that both SlyA and PhoP compete with this regulatory protein. Therefore, H-NS should pair with SlyA and PhoP to establish a forward regulatory loop to regulate expression of pagC, and perhaps other PhoP- and SlyA-dependent genes.

Received for publication, January 22, 2008 , and in revised form, April 16, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grant AI24533 (to W. K.). This work was also supported by start-up funds from Arizona State University (for Y. 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 To whom correspondence should be addressed: School of Life Sciences, AZ State University, PO Box 874501, Tempe, AZ, 85287-4501. Fax: 480-965-6899; E-mail: yixin.shi{at}asu.edu.

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