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Journal of Bacteriology, November 2005, p. 7407-7416, Vol. 187, No. 21
0021-9193/05/$08.00+0     doi:10.1128/JB.187.21.7407-7416.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Resolvase-In Vivo Expression Technology Analysis of the Salmonella enterica Serovar Typhimurium PhoP and PmrA Regulons in BALB/c Mice{dagger}

Massimo Merighi,1,{ddagger} Craig D. Ellermeier,2,§ James M. Slauch,2 and John S. Gunn1*

Department of Molecular Virology, Immunology, and Medical Genetics, and Center for Microbial Interface Biology, College of Medicine and Public Health, Ohio State University, Columbus, Ohio 43210,1 Department of Microbiology and College of Medicine, University of Illinois, Urbana, Illinois 618012

Received 30 May 2005/ Accepted 24 August 2005

Salmonella enterica modulates resistance to antimicrobial peptides in part via covalent modifications of the lipopolysaccharide (LPS). The two-component systems PhoP/PhoQ and PmrA/PmrB are activated during infection and regulate several genes involved in LPS modifications by responding to signals such as pH, iron, magnesium, and antimicrobial peptides. A recombination-based in vivo expression technology approach was adopted to analyze the spatial-temporal patterns of in vivo expression of genes of the PhoP and PmrA regulons and to identify the in vivo signals modulating their transcription. In vitro, we showed PhoP- and/or PmrA-dependent induction of pmrH (LPS aminoarabinose modification operon) by acidic pH, low levels of magnesium, or high levels of Fe(III). Upregulation in cultured J774A.1 macrophages was shown for pmrH, pagP (LPS palmitate addition), and ssaB (pathogenicity island II secretion) but not for prgH (pathogenicity island I secretion). Increased levels of pmrH, phoP, and prgH transcription but not ssaB were observed in bacteria isolated from the lumen of the distal ileum. Bacteria isolated from spleens of orally inoculated mice showed no further induction of prgH but had the highest expression of pmrH, pagP, and ssaB. In vivo induction of pmrH was fully dependent on pmrA and phoP, and buffering stomach acidity, iron chelation, or low-iron diets did not affect the expression of pmrH in the intestinal lumen. The observation of pmrH and pagP expression in the intestine refutes the paradigm of PhoP/PhoQ and PmrA/PmrB in vivo expression as solely intracellularly induced and supports previous data demonstrating peroral virulence attenuation of pmrH mutants.

* Corresponding author. Mailing address: 270 TMRF, 420 W 12th Avenue, Columbus, OH 43210. Phone: (614) 292-6036. Fax: (614) 292-5495. E-mail: gunn.43{at}osu.edu.

{dagger} Supplemental material for this article is available at http://jb.asm.org/.

{ddagger} Present address: Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA 02115.

§ Present address: Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138.

Journal of Bacteriology, November 2005, p. 7407-7416, Vol. 187, No. 21
0021-9193/05/$08.00+0     doi:10.1128/JB.187.21.7407-7416.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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