RORγt-expressing dendritic cells are functionally versatile and evolutionarily conserved antigen-presenting cells
(2025) In Proceedings of the National Academy of Sciences of the United States of America 122(9).- Abstract
Conventional dendritic cells (cDCs) are potent antigen-presenting cells (APCs) that integrate signals from their environment allowing them to direct situation-adapted immunity. Thereby they harbor great potential for being targeted in vaccination, autoimmunity, and cancer. Here, we use fate mapping, functional analyses, and comparative cross-species transcriptomics to show that RORγt+ DCs are a conserved, functionally versatile, and transcriptionally distinct type of DCs. RORγt+ DCs entail various populations described in different contexts including Janus cells/RORγt-expressing extrathymic Aire-expressing cells (eTACs), subtypes of Thetis cells, RORγt+-DC (R-DC) like cells, cDC2C and ACY3+... (More)
Conventional dendritic cells (cDCs) are potent antigen-presenting cells (APCs) that integrate signals from their environment allowing them to direct situation-adapted immunity. Thereby they harbor great potential for being targeted in vaccination, autoimmunity, and cancer. Here, we use fate mapping, functional analyses, and comparative cross-species transcriptomics to show that RORγt+ DCs are a conserved, functionally versatile, and transcriptionally distinct type of DCs. RORγt+ DCs entail various populations described in different contexts including Janus cells/RORγt-expressing extrathymic Aire-expressing cells (eTACs), subtypes of Thetis cells, RORγt+-DC (R-DC) like cells, cDC2C and ACY3+ DCs. We show that in response to inflammatory triggers, RORγt+ DCs can migrate to lymph nodes and in the spleen can activate naïve CD4+ T cells. These findings expand the functional repertoire of RORγt+ DCs beyond the known role of eTACs and Thetis cells in inducing T cell tolerance to self-antigens and intestinal microbes in mice. We further show that RORγt+ DCs with proinflammatory features accumulate in autoimmune neuroinflammation in mice and men. Thus, our work establishes RORγt+ DCs as immune sentinel cells that exhibit a broad functional spectrum ranging from inducing peripheral T cell tolerance to T cell activation depending on signals they integrate from their environment.
(Less)
- author
- organization
-
- Division of Molecular Medicine and Gene Therapy
- WCMM-Wallenberg Centre for Molecular Medicine
- Cell Reprogramming in Hematopoiesis and Immunity (research group)
- StemTherapy: National Initiative on Stem Cells for Regenerative Therapy
- LUCC: Lund University Cancer Centre
- Department of Experimental Medical Science
- Virus Recognition (research group)
- publishing date
- 2025-03
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- AIRE, antigen presenting cells, dendritic cells, innate lymphocytes, RORγt
- in
- Proceedings of the National Academy of Sciences of the United States of America
- volume
- 122
- issue
- 9
- article number
- e2417308122
- publisher
- National Academy of Sciences
- external identifiers
-
- pmid:39993193
- scopus:85219601765
- ISSN
- 0027-8424
- DOI
- 10.1073/pnas.2417308122
- language
- English
- LU publication?
- yes
- id
- 6b31a785-6da6-4894-8e74-f63a01887473
- date added to LUP
- 2025-06-23 11:13:58
- date last changed
- 2025-07-21 12:30:13
@article{6b31a785-6da6-4894-8e74-f63a01887473, abstract = {{<p>Conventional dendritic cells (cDCs) are potent antigen-presenting cells (APCs) that integrate signals from their environment allowing them to direct situation-adapted immunity. Thereby they harbor great potential for being targeted in vaccination, autoimmunity, and cancer. Here, we use fate mapping, functional analyses, and comparative cross-species transcriptomics to show that RORγt<sup>+</sup> DCs are a conserved, functionally versatile, and transcriptionally distinct type of DCs. RORγt<sup>+</sup> DCs entail various populations described in different contexts including Janus cells/RORγt-expressing extrathymic Aire-expressing cells (eTACs), subtypes of Thetis cells, RORγt<sup>+</sup>-DC (R-DC) like cells, cDC2C and ACY3<sup>+</sup> DCs. We show that in response to inflammatory triggers, RORγt<sup>+</sup> DCs can migrate to lymph nodes and in the spleen can activate naïve CD4<sup>+</sup> T cells. These findings expand the functional repertoire of RORγt<sup>+</sup> DCs beyond the known role of eTACs and Thetis cells in inducing T cell tolerance to self-antigens and intestinal microbes in mice. We further show that RORγt<sup>+</sup> DCs with proinflammatory features accumulate in autoimmune neuroinflammation in mice and men. Thus, our work establishes RORγt<sup>+</sup> DCs as immune sentinel cells that exhibit a broad functional spectrum ranging from inducing peripheral T cell tolerance to T cell activation depending on signals they integrate from their environment.</p>}}, author = {{Narasimhan, Hamsa and Richter, Maria L. and Shakiba, Ramin and Papaioannou, Nikos E. and Stehle, Christina and Rengarajan, Kaushikk Ravi and Ulmert, Isabel and Kendirli, Arek and de la Rosa, Clara and Kuo, Pin Yu and Altman, Abigail and Münch, Philipp and Mahboubi, Saba and Küntzel, Vanessa and Sayed, Amina and Stange, Eva Lena and Pes, Jonas and Antonova, Alina Ulezko and Pereira, Carlos Filipe and Klein, Ludger and Dudziak, Diana and Colonna, Marco and Torow, Natalia and Hornef, Mathias W. and Clausen, Björn E. and Kerschensteiner, Martin and Lahl, Katharina and Romagnani, Chiara and Colomé-Tatché, Maria and Schraml, Barbara U.}}, issn = {{0027-8424}}, keywords = {{AIRE; antigen presenting cells; dendritic cells; innate lymphocytes; RORγt}}, language = {{eng}}, number = {{9}}, publisher = {{National Academy of Sciences}}, series = {{Proceedings of the National Academy of Sciences of the United States of America}}, title = {{RORγt-expressing dendritic cells are functionally versatile and evolutionarily conserved antigen-presenting cells}}, url = {{http://dx.doi.org/10.1073/pnas.2417308122}}, doi = {{10.1073/pnas.2417308122}}, volume = {{122}}, year = {{2025}}, }