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Cd1c-Related Dcs That Express Cd207/Langerin, but Are Distinguishable from Langerhans Cells, Are Consistently Present in Human Tonsils

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Cd1c-Related Dcs That Express Cd207/Langerin, but Are Distinguishable from Langerhans Cells, Are Consistently Present in Human Tonsils View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector ORIGINAL RESEARCH published: 25 May 2016 doi: 10.3389/fimmu.2016.00197 CD1c-Related DCs that Express CD207/Langerin, but Are Distinguishable from Langerhans Cells, Are Consistently Present in Human Tonsils Anne De Monte1,2,3, Charles-Vivien Olivieri1,2, Sébastien Vitale3, Sonanda Bailleux4, Laurent Castillo5, Valérie Giordanengo3, Janet L. Maryanski1,2, Elodie Segura6 and Alain Doglio1,2* 1Laboratory MICORALIS EA7354, Faculté de chirurgie dentaire, Université Nice-Sophia-Antipolis, Nice, France, 2Laboratory Unité de Thérapie Cellulaire et Génique (UTCG), Centre Hospitalier Universitaire de Nice, Hôpital Pasteur, Nice, France, 3Laboratory of Virology, Centre Hospitalier Universitaire de Nice, Hôpital l’Archet, Nice, France, 4Department of Pediatric Otorhinolaryngology, Hôpitaux pédiatriques de Nice CHU-Lenval, Nice, France, 5Department of Otorhinolaryngology, Institut Universitaire de la Face et du Cou, Nice, France, 6INSERM U932, Institut Curie, Paris, France Edited by: Giovanna Schiavoni, Istituto Superiore di Sanità, Italy Several subsets of dendritic cells (DCs) are present in the oropharyngeal tonsillar tissues Reviewed by: and are thought to behave as major actors in development and regulation of immunity Susan Kovats, by acting as a first line of recognition for airborne and alimentary antigens. We previously Oklahoma Medical Research Foundation, USA discovered in human adult tonsils infected with Epstein–Barr virus (EBV), a subset of DCs Edda Fiebiger, that expressed langerin/CD207, a lectin usually recognized as a hallmark of epidermal Harvard Medical School, USA Langerhans cells (LCs). In the present study, we analyzed the content of several child *Correspondence: Alain Doglio and adult tonsils in order to characterize in more detail the phenotype of these tonsillar [email protected] CD207-expressing DCs (tCD207 DCs) and to compare it with that of other human DC subsets. We showed that all the human tonsils studied (n = 12) contained significant Specialty section: proportions of tCD207 DCs among tonsillar cells expressing HLA-DR. Moreover, the This article was submitted to Antigen Presenting Cell Biology, presence of tCD207 DCs in tonsils from young children free of EBV infection indicated a section of the journal that these cells could be established early in the tonsil independently of EBV infection. Frontiers in Immunology We also showed that tCD207 DCs, that were found mainly located within the tonsillar Received: 15 March 2016 Accepted: 06 May 2016 lymphoid stroma, were distinguishable from LCs by the level of expression of CD1a Published: 25 May 2016 and EpCAM, and also from human inflammatory DCs by the lack of CD1a, CD206, and Citation: CD14 expression. Detailed analysis of cell surface DC markers showed that tCD207 De Monte A, Olivieri CV, Vitale S, DCs were unrelated to CD141+ DCs or macrophages, but defined a subtype of tonsillar Bailleux S, Castillo L, Giordanengo V, Maryanski JL, Segura E and Doglio A DCs closely related to myeloid resident CD1c DCs. Since it was established that blood (2016) CD1c-Related DCs that CD1c myeloid DCs exhibit plasticity and are capable of expressing CD207 notably in the Express CD207/Langerin, but Are + + Distinguishable from Langerhans presence of inflammatory cytokines, it is tempting to speculate that CD207 CD1c DCs Cells, Are Consistently Present in may play a specific immune role. Human Tonsils. Front. Immunol. 7:197. Keywords: tonsil, dendritic cells, antigen-presenting cells, langerin, CD207, Langerhans cells, inflammatory doi: 10.3389/fimmu.2016.00197 dendritic cells, CD1c myeloid dendritic cells Frontiers in Immunology | www.frontiersin.org 1 May 2016 | Volume 7 | Article 197 De Monte et al. CD207/Langerin Dendritic Cells in Tonsils INTRODUCTION (12). Langerin/CD207 typically characterizes Langerhans cells (LCs) that represent migratory DCs present in the epidermis The Waldeyer’s ring is a ring of lymphoid tissue that circles the and form a distinct cell lineage (14–16). Interestingly, Bigley pharynx at the entrance of the aerodigestive tract. This mucosa- and co-workers (17) have recently shown that CD207 was also associated lymphoid tissue notably contains the palatine tonsils expressed on human DCs isolated from dermis, lung, liver, tonsil, that form dense compact bodies of lymphoid tissue and the and lymphoid tissue. These CD207-expressing DCs were shown adenoids, tubar, and lingual tonsil. The Waldeyer’s ring grows to be distinguishable from conventional LCs by the expression throughout childhood until the age of 11 years before steadily level of CD1a, EpCAM, CD11b, CD11c, CD13, and CD33, and declining with age (1, 2). These oropharyngeal immune tissues were proposed to be closely related to the CD1c+ DCs. Moreover, are the first organs in the lymphatic system that analyze and transcriptomic analysis has also established that CD207 can be react to airborne and alimentary products with the basic func- expressed by human “inflammatory” DCs (infDCs), a population tion to produce antibodies to common environmental antigens. of monocyte-derived DCs with a distinct phenotype that is com- Dendritic cells (DCs) that colonize tonsils are thus thought to play monly encountered in inflamed tissues 18( , 19). In this report, a pivotal role in controlling development of immunity since these we set out to further characterize the tCD207 DCs we previously professional antigen-presenting cells (APCs) have the capacity to discovered in tonsils, and we found evidence of CD207 expres- induce a primary immune response in naïve T lymphocytes, and sion by CD1c+ myeloid DCs. to play a pivotal immune role in regulating innate and adaptive immune responses (3–5). Usually human blood DCs have been divided into two main MATERIALS AND METHODS groups: plasmacytoid DCs (pDCs) and “myeloid” or “classi- cal” DCs (cDCs). The cDCs can be further separated into two Human Specimen Collection subsets that are usually referred to as BDCA1/CD1c+ DCs and Palatine tonsils were collected from 10 healthy children (aged BDCA3/CD141+ DCs (6), which are also found in all lymphoid from 1 to 11 years old, average 4.5 years, and median 3 years) organs and represent resident DCs (5, 7–9). Although pDCs and undergoing routine tonsillectomy (Table 1). Seven children had cDCs subsets have been widely characterized in human tonsils surgery for tonsillar hypertrophy inducing obstructive sleep (3–5, 10, 11), additional tonsillar DC subsets have also been apnea syndrome and three for recurrent tonsillitis. In addition, identified (12, 13). We previously discovered in adult human tonsils from two healthy adults were also collected for recurrent tonsil a new type of human DC expressing the type II trans- tonsillitis. Tonsils were directly obtained at the operating room membrane C-type lectin receptor langerin (CD207) (12). These of the pediatric and adult otorhinolaryngology departments of tonsillar CD207-expressing DCs (tCD207 DCs) abundantly Nice hospitals and processed extemporaneously for cell dissocia- infiltrated Epstein–Barr virus (EBV)-infected areas in tonsil tion. This study was carried out with approval from the national and were also commonly encountered in EBV-infected tumors ethical committee, “Comité de Protection des Personnes” depart- (i.e., nasopharyngeal carcinoma and Hodgkin’s lymphoma) ment “Sud-Méditerranée V,” with written informed consent from TABLE 1 | Characteristics of the study population. Patienta Age Gender Tonsillectomy tCD207 CD1c CD141/Clec9A pDCsb Macrophagesb EBV statusc indication DCsb DCsb DCsb Child 1 1 M Tonsillar hypertrophy 1.7 7.1 3.0 84.5 2.3 Negative Child 2 3 M Tonsillar hypertrophy 1.3 5.9 5.2 75.4 3.3 Positive Child 3 3 M Tonsillar hypertrophy 1.5 2.8 2.5 70.7 13.3 Negative Child 4 3 M Tonsillar hypertrophy 4.0 8.0 8.8 79.6 2.7 Negative Child 5 3 F Recurrent tonsillitis 5.6 13.1 6.0 58.8 6.5 Positive Child 6 4 M Tonsillar hypertrophy 0.6 3.2 2.6 88.6 1.2 Positive Child 7 4 M Recurrent tonsillitis 1.5 4.3 2.4 85.9 0.8 Positive Child 8 4 M Tonsillar hypertrophy 3.7 8.3 5.8 58.5 2.8 Positive Child 9 9 F Recurrent tonsillitis 4.7 12.0 2.8 63.2 5.8 Positive Child 10 11 F Tonsillar hypertrophy 7.5 10.7 0.8 78.1 1.5 Positive Mean (SD) in child’s group 3.2 (2.2) 7.5 (3.6) 4.0 (2.4) 74.3 (11.1) 4.0 (3.7) N/A Adult 11 49 M Recurrent tonsillitis 6.9 18.7 2.0 57.6 7.5 Positive Adult 12 52 M Recurrent tonsillitis 7.8 18.1 4.9 55.8 2.3 Positive Mean (SD) in adult’s group 7.3 (0.6) 18.4 (0.4) 3.4 (2.0) 56.7 (1.3) 4.9 (3.7) N/A aData are provided per subject. bFlow cytometric data are presented as % of LinnegHLA-DR+ cells gated as shown in Figure 1. Each DC population was defined as follows: tCD207 DCs are HLA-DR+ CD207+; CD1c DCs are HLA-DR+ CD11c+ CD1c+; CD141/Clec9A DCs are HLA-DR+ CD11c+ CD141+ Clec9A+; pDCs are HLA-DR+ CD304+; and macrophages are HLA-DR+ CD11c+ CD14+. cEBV status was defined for each child by EBV serology interpretation and for adults by EBV DNA detection. N/A, non-applicable. Frontiers in Immunology | www.frontiersin.org 2 May 2016 | Volume 7 | Article 197 De Monte et al. CD207/Langerin Dendritic Cells in Tonsils all donors or parental donors for children. All subjects gave sections of formalin-fixed paraffin-embedded tissues were written informed consent in accordance with the Declaration of deparaffinized, rehydrated, and stained with hematoxylin and Helsinki. eosin (H&E). Tissue sections were treated for heat-induced epitope retrieval using a pre-heated solution EDTA pH 9 at 97°C, and then non-specific staining was blocked with peroxidase- Tonsillar Cell Isolation and Flow blocking reagent (EnVision™ FLEX Peroxidase-Blocking Cytometric Analysis Reagent, Dako) and incubated with CD207 mouse monoclonal Release of mononuclear cells from tonsil stroma was performed antibody (Bio SB) diluted 1:50 in antibody diluent (EnVision™ as previously described (3).
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