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J. Biol. Chem., Vol. 279, Issue 48, 49804-49815, November 26, 2004

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Expression and Secretion of Salmonella Pathogenicity Island-2 Virulence Genes in Response to Acidification Exhibit Differential Requirements of a Functional Type III Secretion Apparatus and SsaL^*

Brian K. Coombes, Nat F. Brown, Yanet Valdez, John H. Brumell¶, and B. Brett Finlay||**

From the Michael Smith Laboratories and the Departments of ^||Biochemistry and Molecular Biology, ^**Microbiology, and Immunology, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada

Salmonella pathogenicity island (SPI)-2 is pivotal to the intracellular survival of Salmonella and for virulence in mammals. SPI-2 encodes virulence factors (called effectors) that are translocated into the host cell, a type III secretion apparatus and a two-component regulatory system that regulates intracellular expression of SPI-2. Salmonella SPI-2 secretion activity appears to be induced in response to acidification of the vacuole in which it replicates. Here we show that the expression of the SPI-2 proteins, SseB and SseD (filament and pore forming components of the secretion apparatus, respectively) in response to acidification requires an intact secretion system and SsaL, a Salmonella homologue of SepL, a regulator required for type III-dependent secretion of translocators but not effectors in attaching and effacing gastrointestinal pathogens. We show that the expression of SPI-2-encoded effectors is acid-regulated but can be uncoupled from the expression of filament and translocon components, thus showing a differential requirement of SsaL for expression. The secretion and translocation of SPI-2-encoded effectors requires SsaL, but SsaL is dispensable for the secretion of SPI-2 effectors encoded in other pathogenicity loci, suggesting a secretion regulation function for SsaL. Further, we demonstrate that the differential expression of adjacent genes within the sseA operon (sseD and sseE) occurs at the transcriptional level. These data indicate that a Salmonella SPI-2 activation state is achieved by an acidregulated response that requires SsaL. These data also suggest the existence of a previously unrecognized regulatory element within SPI-2 for the "effector operon" region downstream of sseD that might demarcate the expression of translocators and effectors.

Received for publication, April 19, 2004 , and in revised form, August 25, 2004.

^* This work was supported in part by grants (to B. B. F.) from the Canadian Institutes of Health Research (CIHR) and the Howard Hughes Medical Institute (HHMI). 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.

Recipient of a CIHR postdoctoral fellowship and a Michael Smith Foundation for Health Research fellowship.

^¶ Recipient of a CIHR New Investigator Award. Current address: Infection, Immunity, Injury and Repair Program, Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.

A CIHR Distinguished Investigator, an HHMI International Research Scholar, and the University of British Columbia Peter Wall Distinguished Professor. To whom correspondence should be addressed: Biotechnology Laboratory, 237-6174 University Boulevard, University of British Columbia, Vancouver, British Columbia, Canada, V6T 1Z3. Tel.: 604-822-2210; Fax: 604-822-9830; E-mail: bfinlay{at}interchange.ubc.ca.

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