Cells lining the gastrointestinal tract serve as both a barrier to and a pathway for infectious agent entry. Dendritic cells (DCs) present in the lamina propria under the columnar villus epithelium of the small bowel extend processes across this epithelium and capture bacteria, but previous studies provided limited information on the nature of the stimuli, receptors, and signaling events involved in promoting this phenomenon. Here, we use immunohistochemical as well as dynamic explant and intravital two-photon imaging to investigate this issue. Analysis of CD11c–enhanced green fluorescent protein (EGFP) or major histocompatibility complex CII-EGFP mice revealed that the number of trans-epithelial DC extensions, many with an unusual “balloon” shape, varies along the length of the small bowel. High numbers of such extensions were found in the proximal jejunum, but only a few were present in the terminal ileum. The extensions in the terminal ileum markedly increased upon the introduction of invasive or noninvasive Salmonella organisms, and chimeric mouse studies revealed the key role of MyD88-dependent Toll-like receptor (TLR) signaling by nonhematopoietic (epithelial) elements in the DC extension response. Collectively, these findings support a model in which epithelial cell TLR signaling upon exposure to microbial stimuli induces active DC sampling of the gut lumen at sites distant from organized lymphoid tissues.
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25 December 2006
Article|
December 04 2006
Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement
Marcello Chieppa,
Marcello Chieppa
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
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Maria Rescigno,
Maria Rescigno
2Department of Experimental Oncology, European Institute of Oncology, 20141 Milan, Italy
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Alex Y.C. Huang,
Alex Y.C. Huang
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
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Ronald N. Germain
Ronald N. Germain
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
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Marcello Chieppa
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
Maria Rescigno
2Department of Experimental Oncology, European Institute of Oncology, 20141 Milan, Italy
Alex Y.C. Huang
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
Ronald N. Germain
1Lymphocyte Biology Section, Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892
CORRESPONDENCE Ronald N. Germain: [email protected]
Abbreviations used: BB, balloon body; EGFP, enhanced GFP; PAMP, pathogen-associated molecular pattern; PG, peptidoglycan; SNARF, carboxylic acid acetate succinimidyl ester; TLR, Toll-like receptor.
A.Y.C. Huang's present address is Division of Pediatric Hematology/Oncology, Rainbow Babies and Children's Hospital, Case Western Reserve University School of Medicine, Cleveland, OH 44106.
Received:
September 01 2006
Accepted:
November 06 2006
Online ISSN: 1540-9538
Print ISSN: 0022-1007
The Rockefeller University Press
2006
J Exp Med (2006) 203 (13): 2841–2852.
Article history
Received:
September 01 2006
Accepted:
November 06 2006
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Citation
Marcello Chieppa, Maria Rescigno, Alex Y.C. Huang, Ronald N. Germain; Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement . J Exp Med 25 December 2006; 203 (13): 2841–2852. doi: https://doi.org/10.1084/jem.20061884
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