The Mincle-Activating Adjuvant TDB Induces MyD88-Dependent Th1 and Th17 Responses through IL-1R Signaling
Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We pr...
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| Published in | PloS one Vol. 8; no. 1; p. e53531 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
07.01.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0053531 |
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| Abstract | Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcRγ-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFNγ responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo. |
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| AbstractList | Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcRγ-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFNγ responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo. Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcR[gamma]-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFN[gamma] responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo. Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcRγ-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFNγ responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo . Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcRγ-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFNγ responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo.Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic analog of the mycobacterial cord factor trehalose-6,6-dimycolate (TDM), is a potent adjuvant inducing strong Th1 and Th17 immune responses. We previously identified the C-type lectin Mincle as receptor for these glycolipids that triggers the FcRγ-Syk-Card9 pathway for APC activation and adjuvanticity. Interestingly, in vivo data revealed that the adjuvant effect was not solely Mincle-dependent but also required MyD88. Therefore, we dissected which MyD88-dependent pathways are essential for successful immunization with a tuberculosis subunit vaccine. We show here that antigen-specific Th1/Th17 immune responses required IL-1 receptor-mediated signals independent of IL-18 and IL-33-signaling. ASC-deficient mice had impaired IL-17 but intact IFNγ responses, indicating partial independence of TDB adjuvanticity from inflammasome activation. Our data suggest that the glycolipid adjuvant TDB triggers Mincle-dependent IL-1 production to induce MyD88-dependent Th1/Th17 responses in vivo. |
| Audience | Academic |
| Author | Christensen, Dennis Wirtz, Stefan Agger, Else Marie Jozefowski, Katrin Wenzel, Jens Schleicher, Ulrike da Costa, Clarissa Prazeres Desel, Christiane Kirschning, Carsten Lang, Roland Russkamp, Norman Ritter, Manuel Werninghaus, Kerstin |
| AuthorAffiliation | 2 Institute of Medical Microbiology, Immunology and Hygiene, Technische Universität München, Munich, Germany 5 Institut für Medizinische Mikrobiologie, Essen, Germany 3 Statens Serum Institut, Department of Infectious Disease Immunology, Copenhagen, Denmark 1 Institute of Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen, Erlangen, Germany Institut de Pharmacologie et de Biologie Structurale, France 4 Medical Clinic 1, Gastroenterology, Pneumology and Endocrinology, University Hospital Erlangen, Erlangen, Germany |
| AuthorAffiliation_xml | – name: 2 Institute of Medical Microbiology, Immunology and Hygiene, Technische Universität München, Munich, Germany – name: Institut de Pharmacologie et de Biologie Structurale, France – name: 3 Statens Serum Institut, Department of Infectious Disease Immunology, Copenhagen, Denmark – name: 4 Medical Clinic 1, Gastroenterology, Pneumology and Endocrinology, University Hospital Erlangen, Erlangen, Germany – name: 1 Institute of Clinical Microbiology, Immunology and Hygiene, University Hospital Erlangen, Erlangen, Germany – name: 5 Institut für Medizinische Mikrobiologie, Essen, Germany |
| Author_xml | – sequence: 1 givenname: Christiane surname: Desel fullname: Desel, Christiane – sequence: 2 givenname: Kerstin surname: Werninghaus fullname: Werninghaus, Kerstin – sequence: 3 givenname: Manuel surname: Ritter fullname: Ritter, Manuel – sequence: 4 givenname: Katrin surname: Jozefowski fullname: Jozefowski, Katrin – sequence: 5 givenname: Jens surname: Wenzel fullname: Wenzel, Jens – sequence: 6 givenname: Norman surname: Russkamp fullname: Russkamp, Norman – sequence: 7 givenname: Ulrike surname: Schleicher fullname: Schleicher, Ulrike – sequence: 8 givenname: Dennis surname: Christensen fullname: Christensen, Dennis – sequence: 9 givenname: Stefan surname: Wirtz fullname: Wirtz, Stefan – sequence: 10 givenname: Carsten surname: Kirschning fullname: Kirschning, Carsten – sequence: 11 givenname: Else Marie surname: Agger fullname: Agger, Else Marie – sequence: 12 givenname: Clarissa Prazeres surname: da Costa fullname: da Costa, Clarissa Prazeres – sequence: 13 givenname: Roland surname: Lang fullname: Lang, Roland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23308247$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Desel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Desel et al 2013 Desel et al |
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| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: CD KW RL. Performed the experiments: CD KW MR KJ NR JW. Analyzed the data: CD KW RL JW. Contributed reagents/materials/analysis tools: US DC SW CK EMA CPdC. Wrote the paper: CD MR CPdC RL. Competing Interests: CAF01 is currently in clinical development at Statens Serum Institut and three clinical phase 1 studies have been conducted successfully. With regards to the intellectual property status on CAF01, the Statens Serum Institut has one issued patent (WO2006002642). None of the coauthors are registered as inventors on the patent and the full right has been transferred to Statens Serum Institut. EMA and/or DC are furthermore coinventors on patents on related technologies (WO2005004911A2, WO2009003474, WO2010054654, PCT/DK2012/000080) for all of which the full right has been transferred to Statens Serum Institut. This does not alter the authors’ adherence to the PLOS ONE policies on sharing data and materials. |
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| Snippet | Successful vaccination against intracellular pathogens requires the generation of cellular immune responses. Trehalose-6,6-dibehenate (TDB), the synthetic... |
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| SubjectTerms | Activation Adaptive Immunity Adjuvanticity Adjuvants, Immunologic - administration & dosage Adjuvants, Immunologic - chemistry Animals Antigen-presenting cells Antigens Antigens, Bacterial - chemistry Antigens, Bacterial - immunology Apoptosis Regulatory Proteins Biology CARD Signaling Adaptor Proteins Cord factor Cord Factors - chemistry Cord Factors - immunology Cytokines Cytoskeletal Proteins - deficiency Cytoskeletal Proteins - genetics Cytoskeletal Proteins - immunology Experiments Gene Expression Regulation Glycolipids Helper cells Hospitals Hygiene Immune response Immune response (cell-mediated) Immunization Immunoglobulins Immunology Infectious diseases Inflammasomes Interferon-gamma - genetics Interferon-gamma - immunology Interleukin 1 Interleukin 1 receptors Interleukin 17 Interleukin 18 Interleukin-17 - genetics Interleukin-17 - immunology Intracellular signalling Lectins Lectins, C-Type - deficiency Lectins, C-Type - genetics Lectins, C-Type - immunology Lymphocytes Lymphocytes T Medicine Membrane lipids Membrane Proteins - deficiency Membrane Proteins - genetics Membrane Proteins - immunology Mice Mice, Knockout Molecular Mimicry Mycobacterium tuberculosis MyD88 protein Myeloid Differentiation Factor 88 - genetics Myeloid Differentiation Factor 88 - immunology Neutrophils Plant lipids Receptors, Interleukin-1 - genetics Receptors, Interleukin-1 - immunology Signal Transduction Syk protein Th1 Cells - immunology Th17 Cells - immunology Trehalose Tuberculosis Tuberculosis - immunology Tuberculosis - prevention & control Tuberculosis vaccines Tuberculosis Vaccines - administration & dosage Tuberculosis Vaccines - chemistry Tuberculosis Vaccines - immunology Vaccination Vaccines Vaccines, Subunit γ-Interferon |
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| Title | The Mincle-Activating Adjuvant TDB Induces MyD88-Dependent Th1 and Th17 Responses through IL-1R Signaling |
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