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Classical Dendritic Cells Present Sublingual Antigen and Induce Foxp3 Þ Regulatory T Cells in Draining Lymph Nodes

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Classical Dendritic Cells Present Sublingual Antigen and Induce Foxp3 Þ Regulatory T Cells in Draining Lymph Nodes ARTICLES Oral CD103 À CD11b þ classical dendritic cells present sublingual antigen and induce Foxp3 þ regulatory T cells in draining lymph nodes Y Tanaka1,2, H Nagashima3, K Bando1,4,LLu1,5, A Ozaki1, Y Morita1, S Fukumoto2, N Ishii3 and S Sugawara1 Sublingual immunotherapy (SLIT) is a safe and efficient treatment for type 1 allergies; however, the underlying immunological mechanisms, particularly the phenotype of oral antigen-presenting cells (APCs) responsible for the induction of regulatory T (Treg) cells, remain unclear. We show here that the sublingual application of ovalbumin (OVA) induced antigen-specific Foxp3 þ Treg cells in draining submandibular lymph nodes (ManLNs). Oral APCs were classified into macrophages, classical dendritic cells (cDCs), and Langerhans cells by flow cytometry. A major subset of oral cDCs with the CD103 À CD11b þ phenotype showed retinoic acid (RA)-producing activity and converted naive CD4 þ T cells to Foxp3 þ Treg cells in a transforming growth factor-b- and RA-dependent manner in vitro. In the ManLNs, migratory CD103 À CD11b þ cDCs also showed RA-producing activity. After the sublingual application of fluorescent OVA, fluorescence was detected in oral macrophages in tissues, followed by migratory CD103 À CD11b þ cDCs in ManLNs and migratory CD103 À CD11b þ cDCs were the main APCs responsible for the induction of sublingual antigen- specific Treg cells. The transfer of OVA-SLIT-inducedTreg cells suppressed the OVA-induced hypersensitivity response. These results suggest that oral CD103 À CD11b þ cDCs transport sublingual antigens to draining ManLNs and induce antigen-specific Foxp3 þ Treg cells, and, thus, provide a rationale for developing cDC-based therapeutic approaches in SLIT. INTRODUCTION from the sublingual mucosa5 and interleukin (IL)-10-produ- Sublingual immunotherapy (SLIT) is an allergen-specific cing Treg cells in peripheral blood samples.6,7 Thus, a deeper treatment for type 1 allergies, such as allergic rhinitis, with understanding of the mechanisms underlying Treg-cell induc- an improved safety profile and long-lasting effects.1,2 SLIT tion by SLIT may contribute to the development of new operates by acting on the sublingual mucosa and increases therapeutic strategies. allergen tolerance, possibly with the redirection of allergen- The oral cavity is colonized by a large number of commensal specific CD4 þ T-cell responses from T-helper (Th) 2 to Th1 microbes and is constantly exposed to food antigens. However, and the generation of regulatory T (Treg) cells.1–3 Treg cells are acute allergic and inflammatory reactions occur relatively induced in the thymus and are also induced from naive CD4 þ rarely at the oral mucosa.1 SLIT takes advantage of the pro- T cells in the periphery, and the transcriptional factor Foxp3 is tolerogenic property of the oral mucosa for its beneficial effects required for the development and maintenance of the and good safety profile; however, the underlying immunolo- immunosuppressive functions of Treg cells.4 SLIT has been gical mechanisms currently remain unclear. The oral mucosa associated with increased numbers of Foxp3 þ cells in biopsies consists of two main layers, the stratified epithelium and 1Division of Oral Immunology, Department of Oral Biology, Tohoku University Graduate School of Dentistry, Sendai, Japan. 2Division of Pediatric Dentistry, Department of Oral Health and Development Sciences, Tohoku University Graduate School of Dentistry, Sendai, Japan. 3Department of Microbiology and Immunology, Tohoku University Graduate School of Medicine, Sendai, Japan. 4Division of Orthodontics and Dentofacial Orthopedics, Department of Oral Health and Development Sciences, Tohoku University Graduate School of Dentistry, Sendai, Japan and 5Division of Oral Diagnosis, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, Sendai, Japan. Correspondence: S Sugawara ([email protected]) Received 2 August 2015; accepted 7 April 2016; published online 11 May 2016. doi:10.1038/mi.2016.46 MucosalImmunology | VOLUME 10 NUMBER 1 | JANUARY 2017 79 ARTICLES þ a Vehicle or OVA APCs in the LP, (ii) a minor subset of CD207 (langerin) OT-II Analysis Langerhans cells (LCs) located in the epithelium, and (iii) B220 þ 120G8 þ plasmacytoid dendritic cells (pDCs) found in 012 5day the LP.9 Among these APCs, LCs and CD11b þ CD11c À Gate: macrophage (Mf)-like cells are considered to be critical for ManLN AurLN MesLN 9–11 + + CD45.2 CD4 0.29 0.00 0.86 capturing sublingual antigens. A previous study suggested that oral CD11b þ CD11c À Mf-like cells presented sublingual Vehicle antigens in draining lymph nodes (LNs) and promoted the differentiation of interferon-g-producing Th1 cells and Foxp3 þ Treg cells.11 However, the role of oral CD11c þ classical dendritic 8 3.8 0.64 0.75 cells (cDCs) in tolerance induction has not yet been examined. In contrast, the mechanisms that underlie systemic tolerance OVA to orally administered antigens, which is called ‘‘oral tolerance’’ Foxp3 and originates in the intestinal immune system, have been extensively investigated.12 In the LP of the intestines, most TCR V 2 major histocompatibility complex II (MHCII) þ CD11c þ 13,14 þ b c + dendritic cells (DCs) express CD103. These CD103 þ + DCs are migratory cDCs in the LP. Intestinal CD103 cDCs 5 1,200 Foxp3 + * produce the vitamin A metabolite retinoic acid (RA), and V 2 ** 1,000 of + 4 þ + Vehicle 800 Vehicle intestinal CD103 cDC-derived RA acts as a cofactor in the 3 V 2 + CD4 OVA 600 OVA transforming growth factor (TGF)-b-mediated conversion of + 2 400 naive CD4 þ T cells into Foxp3 þ Treg cells.15,16 Intestinal CD4 + %Foxp3 1 200 CD103 þ cDCs express high levels of aldh1a2, the gene 0 Total number of 0 15 CD45.2 encoding retinal dehydrogenase (RALDH) 2, which is a key CD45.2 enzyme in the metabolic conversion of retinal to RA. Another population in the intestinal LP was shown to be CX3CR1high tissue-resident Mfs.13 CD64, the high-affinity IgG receptor d + + Gate:CD45.2 CD4 FcgRI, was recently identified as a specific marker for Mfs, 0.14 0.00 0.10 0.03 0.10 0.00 0.10 0.00 including intestinal CX3CR1high cells.17,18 Vehicle We recently reported that sublingual antigens were trans- ported across sublingual ductal epithelial cells to oral APCs 0.00 0.00 0.00 0.03 around the duct in mice.19 Therefore, we herein attempted to 3.5 0.16 3.5 0.00 3.4 0.01 3.4 0.00 OVA accurately identify and characterize oral APCs and clarify their roles in SLIT on the basis of established evidence regarding the Foxp3 properties of intestinal DCs. The results obtained revealed the 4.1 0.00 0.14 0.03 previously unappreciated role of oral cDCs in Treg-cell IFN-γ IL-4 IL-10 IL-17A induction and provide a rationale for developing cDC-based Figure 1 Sublingual antigen induces antigen-specific Foxp3 þ Treg cells therapeutic approaches in SLIT. in ManLNs. Naive OT-II CD4 þ T cells (CD45.2 þ ) were adoptively transferred into CD45.1 þ congenic mice, and OVA or vehicle was administered sublingually on days 1 and 2. On day 5, the conversion of RESULTS Foxp3 þ Treg cells in ManLNs, AurLNs, and MesLNs was analyzed by flow Sublingual administration of soluble protein antigen cytometry. (a) Representative plots with numbers indicating the induces antigen-specific Foxp3 þ Treg cells in draining percentage of gated cells. (b, c) Percentage of CD45.2 þ CD4 þ Va2 þ OT-II T cells expressing Foxp3 (b) and total number of ManLNs CD45.2 þ CD4 þ Va2 þ Foxp3 þ OT-II T cells per mouse (c). Bars represent It currently remains unclear whether SLIT, in effect, induces the mean±s.d. (n ¼ 3). *Po0.05 and **Po0.01 as determined by the Foxp3 þ Treg cells in vivo. In order to examine this, ovalbumin Student’s t-test with Welch’s correction. (d) Intracellular cytokine staining þ þ of ManLN cells. Results are representative of three independent (OVA)-specific naive OT-II CD4 T cells (CD45.2 ) were þ experiments. AurLN, auricular lymph node; IFN, interferon; IL, interleukin; adoptively transferred into CD45.1 congenic mice, and the ManLN, submandibular lymph node; MesLN, mesenteric lymph node; OVA protein was sublingually administered to the recipients OVA, ovalbumin; Treg, regulatory T. on days 1 and 2. On day 5, the transferred OT-II T cells were detected in ManLNs, the draining LNs of the sublingual underlying lamina propria (LP), which are the equivalents of mucosa,20 and in non-draining auricular and mesenteric LNs the epidermis and dermis of the skin, respectively.8 In the (MesLNs), whereas the marked conversion of Foxp3 þ cells was sublingual mucosa, four subsets of antigen-presenting cells only detected in the draining ManLNs (Figure 1a). The (APCs) with distinct tissue distributions have been detected percentage of Foxp3 þ cells among the transferred OT-II using immunohistochemistry and flow cytometry: (i) a major CD4 þ T cells and total number of converted Foxp3 þ Treg cells subpopulation of CD11b þ CD11c À and CD11b þ CD11c þ per mouse were significantly increased in the ManLNs only 80 VOLUME 10 NUMBER 1 | JANUARY 2017 | www.nature.com/mi ARTICLES a c Trypsin-EDTA Collagenase + − + Trypsin-EDTA → Collagenase CD45+ APC MHCII CD64 CD11c Collagenase 69.0 28.0 15.2 15.4 LC 80 MHCII 70 CD11c CD207 cDC 59.5 84.1 84.1 ) 3 60 CD64 CD64 EpCAM CD11b 10 M × 50 b Collagenase 40 + – + + MHCII CD64 CD11c CD45 APC 30 77.0 23.8 0.53 0.61 LC Cell number ( 20 MHCII 10 CD11c CD207 * cDC 68.9 99.2 99.2 0 Mφ cDC LC CD64 CD64 M EpCAM CD11b Figure 2 Oral APC subsets.
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