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Network of Dendritic Cells Within the Muscular Layer of the Mouse Intestine

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Network of Dendritic Cells Within the Muscular Layer of the Mouse Intestine Network of dendritic cells within the muscular layer of the mouse intestine Adriana Flores-Langarica*†, Selene Meza-Perez*, Juana Calderon-Amador*, Teresa Estrada-Garcia‡, Gordon MacPherson§, Serge Lebecque¶, Sem Saelandʈ, Ralph M. Steinman†**, and Leopoldo Flores-Romoʈ**†† *Department of Immunology, Escuela Nacional de Ciencias Biolo´gicas del Instituto Polite´cnico Nacional, Prolongacio´n de Carpio y Plan de Ayala, Casco de Santo Toma´s, 11340, Mexico; Departments of ††Cell Biology and ‡Molecular Biomedicine, Centro de Investigacio´n y de Estudios Avanzados Avenida Instituto Polite´cnico Nacional #2508, Zacatenco, 07360, Mexico; §Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford OX1 3RE, United Kingdom; ¶Centre Hopitalier Lyon Sud, Service de Pneumologie Ba៮timent 5F, 165 Chemin du Grand-Revoyet, 69495 Pierre-Be´nite Cedex, France; ʈInstitut National de la Sante´et de la Recherche Me´dicale, U 503, Institut Fe´de´ ratif de Recherche 128, 21 Avenue Tony Garnier, 69365 Lyon Cedex 07, France; and †Laboratory of Cellular Physiology and Immunology, The Rockefeller University, 1230 York Avenue, New York, NY 10021 Contributed by Ralph M. Steinman, November 8, 2005 Dendritic cells (DCs) are located at body surfaces such as the skin, located in secondary lymphoid organs (spleen, lymph nodes, and respiratory and genital tracts, and intestine. To further analyze Peyer’s patches). In their immature stage, DCs express many intestinal DCs, we adapted an epidermal sheet separation tech- receptors for antigen uptake as well as environmental sensing, nique and obtained two intestinal layers, facing the lumen and e.g., Toll-like receptors, whereas in the more mature state, DCs serosa. Unexpectedly, immunolabeling of the layer toward the express high levels of activation (CD25) (15) and costimulatory serosa revealed a regular, dense, planar network of cells with (CD40 and CD86) molecules important for T cell responses (14). prominent dendritic morphology within the external muscular In the intestine, DCs in the lamina propria and Peyer’s patches layer and with increasing frequency along the length of the are known to be arranged in a three-dimensional network close intestine. Direct examination of the serosal-disposed layers to the luminal epithelium (16, 17). Here, we applied to the showed a significant fraction of the DCs to express DEC-205͞ intestine a technique used to separate the epidermis and dermis CD205, CD11c, Langerin͞CD207, Fc␥ receptor͞CD16͞32, CD14, and of the skin. We were able to separate the intestinal layers in a low levels of activation markers, CD25, CD80, CD86, and CD95. By suitable manner for immunohistochemical analysis. Unexpect- more sensitive FACS analyses, cells from this layer contained two edly, we observed a strongly MHC-IIϩ population with clear CD11c؉ populations of CD45؉ CD205؉, CD19؊ leukocytes, MHC II؉ dendritic morphology in the layer toward the serosa, which also -and MHC II؊. When ovalbumin conjugated to an anti-DEC-205 expressed CD45, confirming their hematopoietic origin. Pheno antibody was injected into mice, the conjugate targeted to these typically, these cells expressed DC markers such as DEC-205͞ DCs, which upon isolation were able to stimulate ovalbumin- CD205, Langerin͞CD207, and CD11c, as well as molecules such ؉ ؉ specific, CD4 and CD8 T cell antigen receptor-transgenic T cells. as CD16͞32 and CD14, which suggest an immature state. In vivo, these DCs responded to two microbial stimuli, systemic LPS Interestingly, this subset can process antigens from the circula- and oral live bacteria, by up-regulating CD80, CD86, DEC-205, and tion and clearly mature in vivo after stimulation with both IMMUNOLOGY Langerin within 12 h. This network of DCs thus represents a systemic LPS and live oral bacteria. We suggest that this mus- previously unrecognized antigen-presenting cell system in the cularis-associated network represents a previously unrecognized intestine. element of the DC system in the intestine. DEC-205 ͉ mucosal immunology ͉ antigen presentation Materials and Methods Mice. Specific pathogen-free, adult (6–8 weeks) BALB͞c and he human gastrointestinal tract has a luminal surface that is C57BL͞6 (B6) mice were provided by the Centro de Investiga- T400 m2 in area (1) and is in constant contact with antigens cio´n y de Estudios Avanzados animal facilities. For the ovalbu- derived from food, commensal bacteria, parasites, and other min (OVA)-specific T cell responses and T cell antigen receptor microbial sources. In the intestine, antigens are sampled by at (TCR), transgenic OT-I and OT-II mice were purchased from least two mechanisms: by the M cells in the Peyer’s patches (2) Jackson ImmunoResearch. Intestines from the transgenic and directly by dendritic cells (DCs) in the lamina propria (3, 4). CD11c-EYFPhigh mice (18) were kindly provided by M. C. Lamina propria DCs also sample dying epithelial cells and Nussenzweig (Howard Hughes Medical Institute, The Rock- transport these self constituents to the mesenteric lymph node efeller University, New York). (5). DCs within the intestine also comprise different subsets that in turn can respond to local microbial ligands, cytokines, and Reagents. EDTA was purchased from J.T. Baker. The following presumably other stimuli, thereby turning the subsequent im- monoclonal antibodies (mAb) were from BD Pharmingen: anti- mune response from tolerance to different forms of immunity CD4, anti-CD8, anti-CD19, anti-CD16͞32, anti-CD14, anti-CD25, (6, 7). anti-CD80, anti-CD86, biotinylated anti-CD11c, anti-CD31, anti- DCs are potent and specialized antigen-presenting cells (8) CD95, and FITC-conjugated anti-I-A͞I-E. Hybridoma supernatant and important modulators of immune responses (9). They anti-MHC-II (NIMR-4) was kindly provided by L. Santos- provide a link between innate and adaptive immunity (3, 10). Argumedo (Centro de Investigacio´n y de Estudios Avanzados del DCs are known to exist in two broad stages of maturation or Instituto Polite´cnico Nacional, Casco de Santo Toma´s, Mexico). differentiation. The immature stage is able to capture antigens Monoclonal antibody to mouse Langerin was produced and puri- by several mechanisms such as macropinocytosis, phagocytosis, and receptor-mediated uptake, especially through lectin recep- tors such as Langerin͞CD207 (11) and DEC-205͞CD205 (12). Conflict of interest statement: No conflicts declared. Typically, these immature cells are located in nonlymphoid Freely available online through the PNAS open access option. organs such as skin, trachea, intestine, vagina, etc., sites that are Abbreviations: DC, dendritic cell; OVA, ovalbumin; TCR, T cell antigen receptor. normally in contact with environmental antigens (13, 14). In **To whom correspondence may be addressed. E-mail: [email protected] or contrast, the mature stage is characterized by a high capacity for lefl[email protected]. T cell stimulation and differentiation, and these cells are often © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0504253102 PNAS ͉ December 27, 2005 ͉ vol. 102 ͉ no. 52 ͉ 19039–19044 Downloaded by guest on September 26, 2021 fied as described (19). DEC-205 antibody was produced by the conjugated to allophycocyanin in a second step. Appropriate NLDC-145 hybridoma. Enterotoxigenic Escherichia coli were cul- isotype controls were included in all experiments. Cells were tured in tripticase soy broth medium, washed three times in sterile analyzed by using a FACSCalibur cytometer and FLOJO software. saline solution, and adjusted to be inoculated orally in a 50-␮l volume. LPS from Salmonella minnesota was purchased from Targeting DEC-205؉ Cells in Vivo. C57BL͞6 (B6) mice were injected Sigma–Aldrich (catalog no. L6261) and reconstituted in sterile s.c. into each of the four paws with the DEC-205 mAb (NLDC- nonpyrogenic PBS. 145) and an Ig isotype control (both at 10 ␮g) diluted in sterile endotoxin-free PBS. Eighteen hours after injection, the intestine EDTA Treatment for Intestinal Layer Separation. After dissection, was removed and processed to obtain the intestinal layers. The portions of the intestine were placed in cold PBS to wash their layers were fixed as previously described and labeled with a contents and to eliminate the mesentery. The intestine was cut FITC-conjugated anti-MHC-II Ab and a phycoerythrin- into 3-cm portions, which were then opened lengthwise and conjugated anti-rat Ab to detect the DEC-205 Ab. separated according to the different anatomical regions (duo- denum, jejunum, ileum, and large intestine). The tissues were In Vivo OVA Targeting by DEC-205 and T Cell Proliferation Assay. B6 then incubated with 0.5 M EDTA at 37°C for 30 min for the small mice were injected i.p. with anti-DEC-OVA conjugate (10 ␮g) intestine and for 45 min for the large intestine. After EDTA prepared as described (20). Eighteen hours later, single cell incubation, the intestinal portions were washed in PBS and suspensions from the intestinal layer and the mesenteric node (as placed with the lumen side down. Layers were then carefully positive control) were obtained as described in Cell Suspension separated by traction by using fine forceps and scalpel. Two Preparation and FACS Analysis. From the node (dissociated for layers were thus obtained: an external one (toward lumen) and 25 min), CD11cϩ cells were purified by magnetic enrichment by an internal one (toward serosa). Finally, the intestinal layers using CD11c beads (Miltenyi Biotec, Auburn, CA), and CD11cϪ were placed in PBS and stretched out gently in preparation for cells were also collected as negative controls. CD11cϩ and fixation procedures. CD11cϪ lymph node cells and cell suspensions from the intes- tinal layer were cocultured in a 1:9 ratio (DC:T cell) of 105 TCR Semithin Sections. Tissue samples of the complete intestine and transgenic OT-I CD8ϩ or OT-II CD4ϩ T cells (enriched by also the two layers obtained after EDTA treatment were fixed negative selection with anti-MHC II and anti-T cell mAbs and in 2.5% glutaraldehyde for 1 h and postfixed with 1% osmium Dynabeads) in 96-well round-bottom plates, for 88 h.
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