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Monocyte Recruitment, Activation, and Function in the Gut-Associated Lymphoid Tissue during Oral Salmonella Infection¹

Department of Microbiology and Immunology, Göteborg University, Göteborg, Sweden

Neutrophils, monocytes, and dendritic cells (DC) are phenotypically and functionally related phagocytes whose presence in infected tissues is critical to host survival. Their overlapping expression pattern of surface molecules, the differentiation capacity of monocytes, and the presence of monocyte subsets underscores the complexity of understanding the role of these cells during infection. In this study we use five- to seven-color flow cytometry to assess the phenotype and function of monocytes recruited to Peyer’s patches (PP) and mesenteric lymph nodes (MLN) after oral Salmonella infection of mice. The data show that CD68^highGr-1^int (intermediate) monocytes, along with CD68^intGr-1^high neutrophils, rapidly accumulate in PP and MLN. The monocytes have increased MHC-II and costimulatory molecule expression and, in contrast to neutrophils and DC, produce inducible NO synthase. Although neutrophils and monocytes from infected mice produce TNF- and IL-1 upon ex vivo culture, DC do not. In addition, although recruited monocytes internalize Salmonella in vitro and in vivo they did not induce the proliferation of OT-II CD4⁺ T cells after coincubation with Salmonella expressing OVA despite their ability to activate OT-II cells when pulsed with the OVA_323–339 peptide. We also show that recruited monocytes enter the PP of infected mice independently of the mucosal addressin cell adhesion molecule-1 (MAdCAM-1). Finally, recruited but not resident monocytes increase in the blood of orally infected mice, and MHC-II up-regulation, but not TNF- or iNOS production, occur already in the blood. These studies are the first to describe the accumulation and function of monocyte subsets in the blood and GALT during oral Salmonella infection.

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 This work was supported by grants from the Swedish Research Council (621-2004-1378) and the Swedish Foundation for Strategic Research Microbes and Man Program (A3 01:93/01/01) and was performed at the Mucosal Immunobiology and Vaccine Center funded by the Swedish Foundation for Strategic Research.

² Address correspondence and reprint requests to Dr. Mary Jo Wick, Department of Microbiology and Immunology, Box 435, Göteborg, Sweden. E-mail address: mary-jo.wick{at}immuno.gu.se

³ Abbreviations used in this paper: int, intermediate; 7-AAD, 7-aminoactinomycin D; CCD, cytochalasin D; DC, dendritic cells; eGFP, enhanced GFP; iNOS, inducible NO synthase; LB, Luria-Bertani; MAdCAM-1, mucosal addressin cell adhesion molecule-1; mono/mac, monocyte/macrophage; MLN, mesenteric lymph node; PP, Peyer’s patch.

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