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Citations to this article

Specialized role of migratory dendritic cells in peripheral tolerance induction
Juliana Idoyaga, … , Miriam Merad, Ralph M. Steinman
Juliana Idoyaga, … , Miriam Merad, Ralph M. Steinman
Published January 9, 2013
Citation Information: J Clin Invest. 2013;123(2):844-854. https://doi.org/10.1172/JCI65260.
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Research Article Immunology Article has an altmetric score of 12

Specialized role of migratory dendritic cells in peripheral tolerance induction

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Abstract

Harnessing DCs for immunotherapies in vivo requires the elucidation of the physiological role of distinct DC populations. Migratory DCs traffic from peripheral tissues to draining lymph nodes charged with tissue self antigens. We hypothesized that these DC populations have a specialized role in the maintenance of peripheral tolerance, specifically, to generate suppressive Foxp3+ Tregs. To examine the differential capacity of migratory DCs versus blood-derived lymphoid-resident DCs for Treg generation in vivo, we targeted a self antigen, myelin oligodendrocyte glycoprotein, using antibodies against cell surface receptors differentially expressed in these DC populations. Using this approach together with mouse models that lack specific DC populations, we found that migratory DCs have a superior ability to generate Tregs in vivo, which in turn drastically improve the outcome of experimental autoimmune encephalomyelitis. These results provide a rationale for the development of novel therapies targeting migratory DCs for the treatment of autoimmune diseases.

Authors

Juliana Idoyaga, Christopher Fiorese, Lori Zbytnuik, Ashira Lubkin, Jennifer Miller, Bernard Malissen, Daniel Mucida, Miriam Merad, Ralph M. Steinman

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The Importance of Dendritic Cells in Maintaining Immune Tolerance
C Audiger, MJ Rahman, TJ Yun, KV Tarbell, S Lesage
Journal of immunology (Baltimore, Md. : 1950) 2017
Trial Watch: Dendritic cell-based anticancer immunotherapy
AD Garg, MV Perez, M Schaaf, P Agostinis, L Zitvogel, G Kroemer, L Galluzzi
OncoImmunology 2017
Dendritic Cells As Inducers of Peripheral Tolerance
CA Iberg, A Jones, D Hawiger
Trends in Immunology 2017
High-Dimensional Phenotypic Mapping of Human Dendritic Cells Reveals Interindividual Variation and Tissue Specialization
M Alcántara-Hernández, R Leylek, LE Wagar, EG Engleman, T Keler, MP Marinkovich, MM Davis, GP Nolan, J Idoyaga
Immunity 2017
RelB+ Steady-State Migratory Dendritic Cells Control the Peripheral Pool of the Natural Foxp3+ Regulatory T Cells
A Döhler, T Schneider, I Eckert, E Ribechini, N Andreas, M Riemann, B Reizis, F Weih, MB Lutz
Frontiers in immunology 2017
Ontogeny and function of murine epidermal Langerhans cells
DH Kaplan
Nature Immunology 2017
Bioconjugate Strategies for the Induction of Antigen-Specific Tolerance in Autoimmune Diseases
C Yu, , M Li, M An, H Liu
Bioconjugate Chemistry 2017
Transcriptional determinants of tolerogenic and immunogenic states during dendritic cell maturation
BV Lugt, J Riddell, AA Khan, JA Hackney, J Lesch, J DeVoss, MT Weirauch, H Singh, I Mellman
The Journal of Cell Biology 2017
Induction of CD4 + Regulatory and Polarized Effector/helper T Cells by Dendritic Cells
MB Lutz
Immune Network 2016
Dendritic cell-based immunotherapy
RL Sabado, S Balan, N Bhardwaj
Cell Research 2016
Classical dendritic cells are required for dietary antigen–mediated induction of peripheral Treg cells and tolerance
D Esterházy, J Loschko, M London, V Jove, TY Oliveira, D Mucida
Nature Immunology 2016
Altered dendritic cell functions in autoimmune diseases: distinct and overlapping profiles
F Coutant, P Miossec
Nature Reviews Rheumatology 2016
Direct Delivery of Antigens to Dendritic Cells via Antibodies Specific for Endocytic Receptors as a Promising Strategy for Future Therapies
C Lehmann, L Heger, G Heidkamp, A Baranska, J Lühr, A Hoffmann, D Dudziak
Human vaccines 2016
Functions of Murine Dendritic Cells
V Durai, KM Murphy
Immunity 2016
CD103+ Kidney Dendritic Cells Protect against Crescentic GN by Maintaining IL-10-Producing Regulatory T Cells
BD Evers, DR Engel, AM Bohner, AP Tittel, TA Krause, C Heuser, N Garbi, W Kastenmuller, M Mack, G Tiegs, U Panzer, P Boor, I Ludwig-Portugall, C Kurts
Journal of the American Society of Nephrology : JASN 2016
Visualization of immediate immune responses to pioneer metastatic cells in the lung
MB Headley, A Bins, A Nip, EW Roberts, MR Looney, A Gerard, MF Krummel
Nature 2016
The Dendritic Cell Major Histocompatibility Complex II (MHC II) Peptidome Derives from a Variety of Processing Pathways and Includes Peptides with a Broad Spectrum of HLA-DM Sensitivity
CC Clement, A Becerra, L Yin, V Zolla, L Huang, S Merlin, A Follenzi, SA Shaffer, LJ Stern, L Santambrogio
The Journal of biological chemistry 2016
Antibody Targeting of “Steady-State” Dendritic Cells Induces Tolerance Mediated by Regulatory T Cells
K Mahnke, S Ring, AH Enk
Frontiers in immunology 2016
Depletion of Regulatory T Cells Induces High Numbers of Dendritic Cells and Unmasks a Subset of Anti-Tumour CD8+CD11c+ PD-1lo Effector T Cells
N Goudin, P Chappert, J Mégret, DA Gross, B Rocha, O Azogui, IR Cohen
PloS one 2016
Dendritic Cells Coordinate the Development and Homeostasis of Organ-Specific Regulatory T Cells
DS Leventhal, DC Gilmore, JM Berger, S Nishi, V Lee, S Malchow, DE Kline, J Kline, DJ Vander Griend, H Huang, ND Socci, PA Savage
Immunity 2016
The melting pot of the MHC II peptidome
LJ Stern, L Santambrogio
Current Opinion in Immunology 2016
Immune Tolerance for Autoimmune Disease and Cell Transplantation
X Luo, SD Miller, LD Shea
Annual Review of Biomedical Engineering 2016
Antigen Presenting Properties of a Myeloid Dendritic-Like Cell in Murine Spleen
Y Hey, HC ONeill, A Haziot
PloS one 2016
Metabolites: deciphering the molecular language between DCs and their environment
L Minarrieta, P Ghorbani, T Sparwasser, L Berod
Seminars in Immunopathology 2016
Neuroimmune interactions: dendritic cell modulation by the sympathetic nervous system
MC Takenaka, MG Guereschi, AS Basso
Seminars in Immunopathology 2016
A Key Role for Inhibins in Dendritic Cell Maturation and Function
R Olguín-Alor, M la Fuente-Granada, LC Bonifaz, L Antonio-Herrera, EA García-Zepeda, G Soldevila, S Kovats
PloS one 2016
Tolerogenic dendritic cells
MC Takenaka, FJ Quintana
Seminars in Immunopathology 2016
Immunomodulatory Functions of BTLA and HVEM Govern Induction of Extrathymic Regulatory T Cells and Tolerance by Dendritic Cells
A Jones, J Bourque, L Kuehm, A Opejin, RM Teague, C Gross, D Hawiger
Immunity 2016
Preparation of Single-cell Suspensions for Cytofluorimetric Analysis from Different Mouse Skin Regions
A Broggi, C Cigni, I Zanoni, F Granucci
Journal of visualized experiments : JoVE 2016
Self-Antigen Presentation by Keratinocytes in the Inflamed Adult Skin Modulates T Cell Auto-Reactivity
M Meister, A Tounsi, E Gaffal, T Bald, M Papatriantafyllou, J Ludwig, G Pougialis, F Bestvater, L Klotz, G Moldenhauer, T Tüting, GJ Hämmerling, B Arnold, T Oelert
Journal of Investigative Dermatology 2015
CD11c-mediated deletion of Flip promotes autoreactivity and inflammatory arthritis
QQ Huang, H Perlman, R Birkett, R Doyle, D Fang, GK Haines, W Robinson, S Datta, Z Huang, QZ Li, H Phee, RM Pope
Nature Communications 2015
DC-Based Immunotherapy Combined with Low-Dose Methotrexate Effective in the Treatment of Advanced CIA in Mice
JE Park, J Jang, JH Choi, M Kang, YJ Woo, YR Seong, CB Choi, HS Lee, SC Bae, YS Bae
Journal of Immunology Research 2015
Peripherally Induced Tolerance Depends on Peripheral Regulatory T Cells That Require Hopx To Inhibit Intrinsic IL-2 Expression
A Jones, A Opejin, JG Henderson, C Gross, R Jain, JA Epstein, RA Flavell, D Hawiger
Journal of immunology (Baltimore, Md. : 1950) 2015
Tailored immunity by skin antigen-presenting cells
C Levin, H Perrin, B Combadiere
Human Vaccines & Immunotherapeutics 2015
The Role of Dendritic Cell Subsets and Innate Immunity in the Pathogenesis of Type 1 Diabetes and Other Autoimmune Diseases
JD Price, KV Tarbell
Frontiers in immunology 2015
Emerging and Novel Functions of Complement Protein C1q
L Kouser, SP Madhukaran, A Shastri, A Saraon, J Ferluga, M Al-Mozaini, U Kishore
Frontiers in immunology 2015
TREML4 adds fuel to the TLR7 fire
MG Netea, FL van de Veerdonk
Nature Immunology 2015
Engineering immunity: Modulating dendritic cell subsets and lymph node response to direct immune-polarization and vaccine efficacy
J Leleux, A Atalis, K Roy
Journal of Controlled Release 2015
Duality at the gate: Skin dendritic cells as mediators of vaccine immunity and tolerance
CJ Nirschl, N Anandasabapathy
Human Vaccines & Immunotherapeutics 2015
Skin dendritic cells induce follicular helper T cells and protective humoral immune responses
C Yao, SM Zurawski, ES Jarrett, B Chicoine, J Crabtree, EJ Peterson, G Zurawski, DH Kaplan, BZ Igyártó
Journal of Allergy and Clinical Immunology 2015
Imaging regulatory T cell dynamics and CTLA4-mediated suppression of T cell priming
MP Matheu, S Othy, ML Greenberg, TX Dong, M Schuijs, K Deswarte, H Hammad, BN Lambrecht, I Parker, MD Cahalan
Nature Communications 2015
Impact of dietary components on NK and Treg cell function for cancer prevention: DIETARY COMPONENTS AND CANCER: IMPACT ON NK AND TREG FUNCTION
YS Kim, TJ Sayers, NH Colburn, JA Milner, HA Young
Molecular Carcinogenesis 2015
Biodegradable polymeric microsphere-based vaccines and their applications in infectious diseases
CY Lin, SJ Lin, YC Yang, DY Wang, HF Cheng, MK Yeh
Human Vaccines & Immunotherapeutics 2015
DCIR2 + cDC2 DCs and Zbtb32 Restore CD4 + T-Cell Tolerance and Inhibit Diabetes
JD Price, C Hotta-Iwamura, Y Zhao, NM Beauchamp, KV Tarbell
Diabetes 2015
CDKN1A regulates Langerhans cell survival and promotes Treg cell generation upon exposure to ionizing irradiation
JG Price, J Idoyaga, H Salmon, B Hogstad, CL Bigarella, S Ghaffari, M Leboeuf, M Merad
Nature Immunology 2015
Dissolving Microneedle Delivery of Nanoparticle-Encapsulated Antigen Elicits Efficient Cross-Priming and Th1 Immune Responses by Murine Langerhans Cells
M Zaric, O Lyubomska, C Poux, ML Hanna, MT McCrudden, B Malissen, RJ Ingram, UF Power, CJ Scott, RF Donnelly, A Kissenpfennig
Journal of Investigative Dermatology 2015
Advancing drug delivery systems for the treatment of multiple sclerosis
I Tabansky, MD Messina, C Bangeranye, J Goldstein, KM Blitz-Shabbir, S Machado, V Jeganathan, P Wright, S Najjar, Y Cao, W Sands, DB Keskin, JN Stern
Immunologic Research 2015
Mechanisms regulating skin immunity and inflammation
M Pasparakis, I Haase, FO Nestle
Nature Reviews Immunology 2014
Trial watch: Dendritic cell-based anticancer therapy
N Bloy, J Pol, F Aranda, A Eggermont, I Cremer, WH Fridman, J Fučíková, J Galon, E Tartour, R Spisek, MV Dhodapkar, L Zitvogel, G Kroemer, L Galluzzi
OncoImmunology 2014
Regulatory dendritic cells for immunotherapy in immunologic diseases
JR Gordon, Y Ma, L Churchman, SA Gordon, W Dawicki
Frontiers in immunology 2014
Antigen-Conjugated Human IgE Induces Antigen-Specific T Cell Tolerance in a Humanized Mouse Model
G Baravalle, AM Greer, TN Laflam, JS Shin
Journal of immunology (Baltimore, Md. : 1950) 2014
The origins and functions of dendritic cells and macrophages in the skin
B Malissen, S Tamoutounour, S Henri
Nature Reviews Immunology 2014
Dendritic cell-targeted vaccines — hope or hype?
W Kastenmüller, K Kastenmüller, C Kurts, RA Seder
Nature Reviews Immunology 2014
Murine Langerin+ dermal dendritic cells prime CD8+ T cells while Langerhans cells induce cross-tolerance
V Flacher, CH Tripp, DG Mairhofer, RM Steinman, P Stoitzner, J Idoyaga, N Romani
EMBO Molecular Medicine 2014
Dendritic Cell-Targeted Vaccines
L Cohn, LÃ Delamarre
Frontiers in immunology 2014
Helminth Infections Decrease Host Susceptibility to Immune-Mediated Diseases
JV Weinstock, DE Elliott
Journal of immunology (Baltimore, Md. : 1950) 2014
The nature of activatory and tolerogenic dendritic cell-derived signal 2
F Granucci, MB Lutz, I Zanoni
Frontiers in immunology 2014
Adaptation in the innate immune system and heterologous innate immunity
SF Martin
Cellular and Molecular Life Sciences 2014
Human skin dendritic cells can be targeted in situ by intradermal injection of antibodies against lectin receptors
P Stoitzner, S Schaffenrath, CH Tripp, D Reider, K Komenda, BD Frari, G Djedovic, S Ebner, N Romani
Experimental Dermatology 2014
Peripherally Induced Tregs – Role in Immune Homeostasis and Autoimmunity
M Yadav, S Stephan, JA Bluestone
Frontiers in immunology 2013
Dendritic Cells in the Periphery Control Antigen-Specific Natural and Induced Regulatory T Cells
S Yamazaki, A Morita
Frontiers in immunology 2013
Pathological consequence of misguided dendritic cell differentiation in histiocytic diseases
ML Berres, CE Allen, M Merad
Advances in immunology 2013
Trial watch
E Vacchelli, I Vitale, A Eggermont, WH Fridman, J Fučíková, I Cremer, J Galon, E Tartour, L Zitvogel, G Kroemer, L Galluzzi
OncoImmunology 2013
Human dendritic cell subsets in vaccination
K Palucka, J Banchereau
Current Opinion in Immunology 2013
Dendritic Cells: Cellular Mediators for Immunological Tolerance
CY Chung, D Ysebaert, ZN Berneman, N Cools
Clinical and Developmental Immunology 2013
New approaches to transcutaneous immunotherapy: targeting dendritic cells with novel allergen conjugates
R Weiss, S Scheiblhofer, Y Machado, J Thalhamer
Current Opinion in Allergy and Clinical Immunology 2013
Immunogenicity of subcutaneously administered therapeutic proteins--a mechanistic perspective
AM Fathallah, RB Bankert, SV Balu-Iyer
The AAPS Journal 2013
It's Time to Bring Dendritic Cell Therapy to Type 1 Diabetes
RJ Creusot, N Giannoukakis, M Trucco, MJ Clare-Salzler, CG Fathman
Diabetes 2013
Targeted antigen delivery to DEC-205⁺ dendritic cells for tolerogenic vaccination
C Petzold, S Schallenberg, JN Stern, K Kretschmer
The review of diabetic studies : RDS 2012
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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