Luminal Bacteria Recruit CD103+ Dendritic Cells into the Intestinal Epithelium to Sample Bacterial Antigens for Presentation
CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1+/gfp ×Cd11c-YFP mice to study thes...
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| Published in | Immunity (Cambridge, Mass.) Vol. 38; no. 3; pp. 581 - 595 |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
21.03.2013
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1+/gfp ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens.
► CD103+ DCs patrol the epithelium of the small intestine ► Salmonella infection recruits more DCs in a TLR and chemokine-dependent manner ► The DCs efficiently phagocytose salmonella using intraepithelial dendrites ► Soluble luminal antigens are sampled more efficiently by CX3CR1+ macrophages |
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| AbstractList | CD103+dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in liveCx3cr1+/gfpxCd11c-YFP mice to study these processes. At steady state, sparse CD103+DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge withSalmonellatriggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1+/gfp ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. ► CD103+ DCs patrol the epithelium of the small intestine ► Salmonella infection recruits more DCs in a TLR and chemokine-dependent manner ► The DCs efficiently phagocytose salmonella using intraepithelial dendrites ► Soluble luminal antigens are sampled more efficiently by CX3CR1+ macrophages CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1(+/gfp) ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens.CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1(+/gfp) ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1+/gfp Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1(+/gfp) ×Cd11c-YFP mice to study these processes. At steady state, sparse CD103+ DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103+ DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103+ DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103+ DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. CD103 + dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal bacteria or presenting bacterial antigens in mesentery lymph nodes. We used 2-photon microscopy in live Cx3cr1 +/gfp × Cd11c-YFP mice to study these processes. At steady state, sparse CD103 + DCs occupied the epithelium. They patrolled among enterocytes while extending dendrites toward the lumen, likely using tight-junction proteins to penetrate the epithelium. Challenge with Salmonella triggered chemokine- and toll-like receptor (TLR)-dependent recruitment of additional DCs from the lamina propria (LP). The DCs efficiently phagocytosed the bacteria using intraepithelial dendrites. Noninvasive bacteria were similarly sampled. In contrast, CD103 + DCs sampled soluble luminal antigen inefficiently. In mice harboring CD103 + DCs, antigen-specific CD8 T cells were subsequently activated in MLNs. Intestinal CD103 + DCs are therefore equipped with unique mechanisms to independently complete the processes of uptake, transportation, and presentation of bacterial antigens. |
| Author | Farache, Julia Koren, Idan Shakhar, Guy Kim, Ki-Wook Furtado, Glaucia C. Milo, Idan Zigmond, Ehud Lira, Sergio A. Gurevich, Irina |
| AuthorAffiliation | 2 Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029, USA 1 Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel |
| AuthorAffiliation_xml | – name: 2 Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029, USA – name: 1 Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel |
| Author_xml | – sequence: 1 givenname: Julia surname: Farache fullname: Farache, Julia organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 2 givenname: Idan surname: Koren fullname: Koren, Idan organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 3 givenname: Idan surname: Milo fullname: Milo, Idan organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 4 givenname: Irina surname: Gurevich fullname: Gurevich, Irina organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 5 givenname: Ki-Wook surname: Kim fullname: Kim, Ki-Wook organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 6 givenname: Ehud surname: Zigmond fullname: Zigmond, Ehud organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 7 givenname: Glaucia C. surname: Furtado fullname: Furtado, Glaucia C. organization: Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029, USA – sequence: 8 givenname: Sergio A. surname: Lira fullname: Lira, Sergio A. organization: Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029, USA – sequence: 9 givenname: Guy surname: Shakhar fullname: Shakhar, Guy email: shakhar@weizmann.ac.il organization: Department of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23395676$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Present address: Department of Microbial Pathogenesis, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, CT 06510, USA |
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| Snippet | CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal... CD103+ dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal... CD103+dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal... CD103 + dendritic cells (DCs) carry bacteria from the small intestine and can present antigens to T cells. Yet they have not been recorded sampling luminal... |
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| SubjectTerms | Animals Antigen Presentation - immunology Antigens, Bacterial - immunology Antigens, CD - immunology Antigens, CD - metabolism Bacteria Behavior Bone marrow CD11c Antigen - genetics CD11c Antigen - immunology CD11c Antigen - metabolism CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Cell Line, Tumor Cell Movement - immunology Cells, Cultured CX3C Chemokine Receptor 1 Dendritic Cells - immunology Dendritic Cells - metabolism Flow Cytometry Host-Pathogen Interactions - immunology Integrin alpha Chains - immunology Integrin alpha Chains - metabolism Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Intestinal Mucosa - microbiology Luminescent Proteins - genetics Luminescent Proteins - metabolism Lymphocyte Activation - immunology Mice Mice, Inbred C57BL Mice, Knockout Microscopy Microscopy, Fluorescence, Multiphoton Morphology Motility Mucous Membrane - immunology Mucous Membrane - metabolism Mucous Membrane - microbiology Receptors, Chemokine - genetics Receptors, Chemokine - immunology Receptors, Chemokine - metabolism Salmonella Salmonella typhi - immunology Salmonella typhi - physiology Salmonella typhimurium - immunology Salmonella typhimurium - physiology Toll-Like Receptors - immunology Toll-Like Receptors - metabolism |
| Title | Luminal Bacteria Recruit CD103+ Dendritic Cells into the Intestinal Epithelium to Sample Bacterial Antigens for Presentation |
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