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Articles

Elevated Iron Status Increases Bacterial Invasion and Survival and Alters Cytokine/Chemokine mRNA Expression in Caco-2 Human Intestinal Cells¹

Susan L. Foster^*,, Stephen H. Richardson and Mark L. Failla^*2

^* Department of Nutrition and Foodservice Systems, The University of North Carolina at Greensboro, Greensboro, North Carolina 27402 and Department of Microbiology and Immunology, Wake Forest University School of Medicine, Winston-Salem, North Carolina 27157

²To whom correspondence should be addressed at Department of Nutrition Human Nutrition and Food Management, The Ohio State University, 325 Campbell Hall, Columbus, OH 43210. E-mail: failla.3{at}osu.edu

Iron status affects both microbial growth and immune function. Mammalian iron homeostasis is maintained primarily by regulating the absorption of the micronutrient in the proximal small intestine. The iron concentration of the enterocyte can fluctuate widely in response to both dietary and whole body iron status, as well as in response to infections. The possibility that an enterocyte with an elevated iron concentration is more susceptible to invasion by enteric pathogens is not known. Therefore, we examined the impact of enterocyte iron status on the invasion and survival of an enteric pathogen, as well as on the levels of several cytokine and chemokine mRNAs by the host cell. The enterocyte-like Caco-2 human intestinal cell line and Salmonella enteritidis served as the models to examine the effect of iron on the host-parasite interaction. Iron status of Caco-2 cells was altered by incubation in serum-free medium supplemented with varying levels of iron. Elevated iron status of Caco-2 cells increased the efficiency of the invasion and the number of bacteria surviving in the intracellular environment. Caco-2 cells constitutively expressed transforming growth factor-ß1, interleukin-8, monocyte chemotactic protein-1, tumor necrosis factor- and interleukin-1ß, and infection with S. enteritidis increased the relative quantities of all cytokine/chemokine mRNAs except interleukin-1ß. Elevated iron status of Caco-2 cells decreased the levels of cytokine/chemokine mRNAs by 25–45% in uninfected cells. In contrast, bacterial infection was associated with a 21–95% increase in cytokine/chemokine mRNAs levels in Caco-2 cells with higher iron concentration compared with infected cells with lower iron concentration. These data support the hypothesis that elevated enterocyte iron status increases susceptibility to infection and exacerbates the mucosal inflammatory response initiated by microbial invasion by increasing cytokine/chemokine expression.

KEY WORDS: • iron • Caco-2 human intestinal cells • transforming growth factor-ß1 • cytokines • chemokines • infection

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