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Infection and Immunity, May 2009, p. 1904-1916, Vol. 77, No. 5
0019-9567/09/$08.00+0     doi:10.1128/IAI.01341-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Contribution of Flagellin Pattern Recognition to Intestinal Inflammation during Salmonella enterica Serotype Typhimurium Infection{triangledown}

Sebastian E. Winter,1,4 Parameth Thiennimitr,1 Sean-Paul Nuccio,1 Takeshi Haneda,1 Maria G. Winter,1 R. Paul Wilson,1 Joseph M. Russell,1 Thomas Henry,2 Quynh T. Tran,3 Sara D. Lawhon,3 Gabriel Gomez,3 Charles L. Bevins,1 Holger Rüssmann,4,5 Denise M. Monack,2 L. Garry Adams,3 and Andreas J. Bäumler1*

Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Ave., Davis, California,1 Department of Microbiology and Immunology, School of Medicine, Stanford University, Stanford, California,2 Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas,3 Max von Pettenkofer-Institut für Hygiene und Medizinische Mikrobiologie, Ludwig-Maximilians-Universität München, Munich, Germany,4 HELIOS Klinikum Emil von Behring; Institut für Mikrobiologie, Immunologie und Laboratoriumsmedizin, Berlin, Germany5

Received 1 November 2008/ Returned for modification 11 December 2008/ Accepted 11 February 2009

Salmonella enterica serotype Typhimurium causes acute inflammatory diarrhea in humans. Flagella contribute to intestinal inflammation, but the mechanism remains unclear since most mutations abrogating pattern recognition of flagellin also prevent motility and reduce bacterial invasion. To determine the contribution of flagellin pattern recognition to the generation of innate immune responses, we compared in two animal models a nonmotile, but flagellin-expressing and -secreting serotype Typhimurium strain (flgK mutant) to a nonmotile, non-flagellin-expressing strain (flgK fliC fljB mutant). In vitro, caspase-1 can be activated by cytosolic delivery of flagellin, resulting in release of the interferon gamma inducing factor interleukin-18 (IL-18). Experiments with streptomycin-pretreated caspase-1-deficient mice suggested that induction of gamma interferon expression in the murine cecum early (12 h) after serotype Typhimurium infection was caspase-1 dependent but independent of flagellin pattern recognition. In addition, mRNA levels of the CXC chemokines macrophage inflammatory protein 2 and keratinocyte-derived chemokine were markedly increased early after serotype Typhimurium infection of streptomycin-pretreated wild-type mice regardless of flagellin expression. In contrast, in bovine ligated ileal loops, flagellin pattern recognition contributed to increased mRNA levels of macrophage inflammatory protein 3{alpha} and more fluid accumulation at 2 h after infection. Collectively, our data suggest that pattern recognition of flagellin contributes to early innate host responses in the bovine ileal mucosa but not in the murine cecal mucosa.

* Corresponding author. Mailing address: Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Ave., Davis, CA 95616-8645. Phone: (530) 754-7225. Fax: (530) 754-7240. E-mail: ajbaumler{at}ucdavis.edu

{triangledown} Published ahead of print on 23 February 2009.

Editor: J. N. Weiser

Infection and Immunity, May 2009, p. 1904-1916, Vol. 77, No. 5
0019-9567/09/$08.00+0     doi:10.1128/IAI.01341-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



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