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Journal of Bacteriology, August 2002, p. 4409-4419, Vol. 184, No. 16
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.16.4409-4419.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

MxiE Regulates Intracellular Expression of Factors Secreted by the Shigella flexneri 2a Type III Secretion System

Colleen D. Kane, Raymond Schuch,,{dagger} William A. Day, Jr,,{ddagger} and Anthony T. Maurelli*

Department of Microbiology and Immunology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814-4799

Received 21 March 2002/ Accepted 21 May 2002

The mxi-spa locus on the virulence plasmid of Shigella flexneri encodes components of the type III secretion system. mxiE, a gene within this locus, encodes a protein that is homologous to the AraC/XylS family of transcriptional regulators, but currently its role in pathogenesis remains undefined. We characterized the virulence phenotype of a nonpolar mxiE mutant and found that this mutant retained the ability to invade mammalian cells in tissue culture and secrete Ipas (type III effectors required for host cell invasion), although it was less efficient than wild-type Shigella at cell-to-cell spread. Despite its invasive properties in culture, the mxiE mutant was completely avirulent in an animal model. Potential targets for MxiE activation were identified by using promoter-green fluorescent protein fusions, and gene expression was examined under various growth conditions. Six MxiE-regulated genes were discovered: ospB, ospC1, ospE2, ospF, virA, and ipaH9.8. Notably, activation of these genes only occurred within the intracellular environment of the host and not during growth at 37°C in liquid culture. Interestingly, all of the MxiE-regulated proteins previously have been shown to be secreted through the type III secretion system and are putative virulence factors. Our findings suggest that some of these Osp proteins may be involved in postinvasion events related to virulence. Since bacterial pathogens adapt to multiple environments during the course of infecting a host, we propose that Shigella evolved a mechanism to take advantage of a unique intracellular cue, which is mediated through MxiE, to express proteins when the organism reaches the eukaryotic cytosol.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Rd., Bethesda, MD 20814-4799. Phone: (301) 295-3415. Fax: (301) 295-1545. E-mail: amaurelli{at}usuhs.mil.

{dagger} Present address: Laboratory of Bacterial Pathogenesis and Immunology, The Rockefeller University, New York, NY 10021.

{ddagger} Present address: Bacteriology Division, U.S. Army Medical Research Institute of Infectious Diseases, Ft. Detrick, MD 21702.

Journal of Bacteriology, August 2002, p. 4409-4419, Vol. 184, No. 16
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.16.4409-4419.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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