Inflammatory Type 2 cDCs Acquire Features of cDC1s and Macrophages to Orchestrate Immunity to Respiratory Virus Infection
The phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antig...
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| Published in | Immunity (Cambridge, Mass.) Vol. 52; no. 6; pp. 1039 - 1056.e9 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
16.06.2020
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antigen-presenting cells (APCs). Using single-cell technologies in models of respiratory viral infection, we found that lung cDC2s acquired expression of the Fc receptor CD64 shared with MCs and of IRF8 shared with cDC1s. These inflammatory cDC2s (inf-cDC2s) were superior in inducing CD4+ T helper (Th) cell polarization while simultaneously presenting antigen to CD8+ T cells. When carefully separated from inf-cDC2s, MCs lacked APC function. Inf-cDC2s matured in response to cell-intrinsic Toll-like receptor and type 1 interferon receptor signaling, upregulated an IRF8-dependent maturation module, and acquired antigens via convalescent serum and Fc receptors. Because hybrid inf-cDC2s are easily confused with monocyte-derived cells, their existence could explain why APC functions have been attributed to MCs.
[Display omitted]
•Type I interferon drives differentiation of inf-cDC2s that closely resemble MCs•Inf-cDC2s prime CD4+ and CD8+ T cells, whereas MCs lack APC function•Inf-cDC2s internalize antibody-complexed antigen via Fc receptors•IRF8 controls maturation gene module in inf-cDC2s
The dichotomy between type 1 and 2 conventional DCs under steady-state conditions is well defined. Bosteels et al. demonstrate that, upon inflammation, cDC2s acquire a hybrid inf-cDC2 phenotype, sharing phenotype, gene expression, and function with cDC1s and monocyte-derived cells, to optimally boost CD4 and CD8 immunity via Fc receptors. |
|---|---|
| AbstractList | The phenotypic and functional dichotomy between IRF8
+
type 1 and IRF4
+
type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antigen-presenting cells (APCs). Using single-cell technologies in models of respiratory viral infection, we found that lung cDC2s acquired expression of the Fc receptor CD64 shared with MCs and of IRF8 shared with cDC1s. These inflammatory cDC2s (inf-cDC2s) were superior in inducing CD4
+
T helper (Th) cell polarization while simultaneously presenting antigen to CD8
+
T cells. When carefully separated from inf-cDC2s, MCs lacked APC function. Inf-cDC2s matured in response to cell-intrinsic Toll-like receptor and type 1 interferon receptor signaling, upregulated an IRF8-dependent maturation module, and acquired antigens via convalescent serum and Fc receptors. Because hybrid inf-cDC2s are easily confused with monocyte-derived cells, their existence could explain why APC functions have been attributed to MCs.
•
Type I interferon drives differentiation of inf-cDC2s that closely resemble MCs
•
Inf-cDC2s prime CD4
+
and CD8
+
T cells, whereas MCs lack APC function
•
Inf-cDC2s internalize antibody-complexed antigen via Fc receptors
•
IRF8 controls maturation gene module in inf-cDC2s
The dichotomy between type 1 and 2 conventional DCs under steady-state conditions is well defined. Bosteels et al. demonstrate that, upon inflammation, cDC2s acquire a hybrid inf-cDC2 phenotype, sharing phenotype, gene expression, and function with cDC1s and monocyte-derived cells, to optimally boost CD4 and CD8 immunity via Fc receptors. The phenotypic and functional dichotomy between IRF8 type 1 and IRF4 type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antigen-presenting cells (APCs). Using single-cell technologies in models of respiratory viral infection, we found that lung cDC2s acquired expression of the Fc receptor CD64 shared with MCs and of IRF8 shared with cDC1s. These inflammatory cDC2s (inf-cDC2s) were superior in inducing CD4 T helper (Th) cell polarization while simultaneously presenting antigen to CD8 T cells. When carefully separated from inf-cDC2s, MCs lacked APC function. Inf-cDC2s matured in response to cell-intrinsic Toll-like receptor and type 1 interferon receptor signaling, upregulated an IRF8-dependent maturation module, and acquired antigens via convalescent serum and Fc receptors. Because hybrid inf-cDC2s are easily confused with monocyte-derived cells, their existence could explain why APC functions have been attributed to MCs. The phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antigen-presenting cells (APCs). Using single-cell technologies in models of respiratory viral infection, we found that lung cDC2s acquired expression of the Fc receptor CD64 shared with MCs and of IRF8 shared with cDC1s. These inflammatory cDC2s (inf-cDC2s) were superior in inducing CD4+ T helper (Th) cell polarization while simultaneously presenting antigen to CD8+ T cells. When carefully separated from inf-cDC2s, MCs lacked APC function. Inf-cDC2s matured in response to cell-intrinsic Toll-like receptor and type 1 interferon receptor signaling, upregulated an IRF8-dependent maturation module, and acquired antigens via convalescent serum and Fc receptors. Because hybrid inf-cDC2s are easily confused with monocyte-derived cells, their existence could explain why APC functions have been attributed to MCs. [Display omitted] •Type I interferon drives differentiation of inf-cDC2s that closely resemble MCs•Inf-cDC2s prime CD4+ and CD8+ T cells, whereas MCs lack APC function•Inf-cDC2s internalize antibody-complexed antigen via Fc receptors•IRF8 controls maturation gene module in inf-cDC2s The dichotomy between type 1 and 2 conventional DCs under steady-state conditions is well defined. Bosteels et al. demonstrate that, upon inflammation, cDC2s acquire a hybrid inf-cDC2 phenotype, sharing phenotype, gene expression, and function with cDC1s and monocyte-derived cells, to optimally boost CD4 and CD8 immunity via Fc receptors. SummaryThe phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it is unknown how robust this dichotomy is under inflammatory conditions, when additionally monocyte-derived cells (MCs) become competent antigen-presenting cells (APCs). Using single-cell technologies in models of respiratory viral infection, we found that lung cDC2s acquired expression of the Fc receptor CD64 shared with MCs and of IRF8 shared with cDC1s. These inflammatory cDC2s (inf-cDC2s) were superior in inducing CD4+ T helper (Th) cell polarization while simultaneously presenting antigen to CD8+ T cells. When carefully separated from inf-cDC2s, MCs lacked APC function. Inf-cDC2s matured in response to cell-intrinsic Toll-like receptor and type 1 interferon receptor signaling, upregulated an IRF8-dependent maturation module, and acquired antigens via convalescent serum and Fc receptors. Because hybrid inf-cDC2s are easily confused with monocyte-derived cells, their existence could explain why APC functions have been attributed to MCs. |
| Author | Lesage, Manon Bosteels, Cedric Louagie, Els Bosteels, Victor Martens, Liesbet Neyt, Katrijn Williams, David L. Mayer, Johannes U. Sichien, Dorine Debeuf, Nincy Tang, Shiau-Choot Scott, Charlotte L. Ronchese, Franca Vanheerswynghels, Manon Vandamme, Niels Saeys, Yvan Hammad, Hamida Guilliams, Martin van Helden, Mary J. De Prijck, Sofie Lambrecht, Bart N. |
| Author_xml | – sequence: 1 givenname: Cedric surname: Bosteels fullname: Bosteels, Cedric organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 2 givenname: Katrijn surname: Neyt fullname: Neyt, Katrijn organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 3 givenname: Manon surname: Vanheerswynghels fullname: Vanheerswynghels, Manon organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 4 givenname: Mary J. surname: van Helden fullname: van Helden, Mary J. organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 5 givenname: Dorine surname: Sichien fullname: Sichien, Dorine organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 6 givenname: Nincy surname: Debeuf fullname: Debeuf, Nincy organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 7 givenname: Sofie surname: De Prijck fullname: De Prijck, Sofie organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 8 givenname: Victor surname: Bosteels fullname: Bosteels, Victor organization: Department of Internal Medicine and Pediatrics, Ghent University, Ghent 9000, Belgium – sequence: 9 givenname: Niels surname: Vandamme fullname: Vandamme, Niels organization: Data Mining and Modeling for Biomedicine Group, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 10 givenname: Liesbet surname: Martens fullname: Martens, Liesbet organization: Data Mining and Modeling for Biomedicine Group, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 11 givenname: Yvan surname: Saeys fullname: Saeys, Yvan organization: Data Mining and Modeling for Biomedicine Group, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 12 givenname: Els surname: Louagie fullname: Louagie, Els organization: Argenx BV, Ghent 9052, Belgium – sequence: 13 givenname: Manon surname: Lesage fullname: Lesage, Manon organization: Argenx BV, Ghent 9052, Belgium – sequence: 14 givenname: David L. surname: Williams fullname: Williams, David L. organization: Department of Surgery and Center of Excellence in Inflammation, Infectious Disease and Immunity, Quillen College of Medicine, East Tennessee State University, Johnson City, TN, USA – sequence: 15 givenname: Shiau-Choot surname: Tang fullname: Tang, Shiau-Choot organization: Malaghan Institute of Medical Research, Wellington 6012, New Zealand – sequence: 16 givenname: Johannes U. surname: Mayer fullname: Mayer, Johannes U. organization: Malaghan Institute of Medical Research, Wellington 6012, New Zealand – sequence: 17 givenname: Franca surname: Ronchese fullname: Ronchese, Franca organization: Malaghan Institute of Medical Research, Wellington 6012, New Zealand – sequence: 18 givenname: Charlotte L. surname: Scott fullname: Scott, Charlotte L. organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 19 givenname: Hamida surname: Hammad fullname: Hammad, Hamida organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 20 givenname: Martin surname: Guilliams fullname: Guilliams, Martin email: martin.guilliams@ugent.vib.be organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium – sequence: 21 givenname: Bart N. surname: Lambrecht fullname: Lambrecht, Bart N. email: bart.lambrecht@ugent.be organization: Laboratory of Immunoregulation and Mucosal Immunology, VIB-UGent Center for Inflammation Research, Ghent 9052, Belgium |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32392463$$D View this record in MEDLINE/PubMed |
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| Keywords | CD64 type 1 interferon transcription factor inf-cDC2 Fc receptor convalescent serum inflammation monocyte IRF8 virus dendritic cell |
| Language | English |
| License | Copyright © 2020 Elsevier Inc. All rights reserved. Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active. |
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| Snippet | The phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it... The phenotypic and functional dichotomy between IRF8 type 1 and IRF4 type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted; it... SummaryThe phenotypic and functional dichotomy between IRF8+ type 1 and IRF4+ type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well... The phenotypic and functional dichotomy between IRF8 + type 1 and IRF4 + type 2 conventional dendritic cells (cDC1s and cDC2s, respectively) is well accepted;... |
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| SubjectTerms | Antigen Presentation Antigen-presenting cells Antigens Biomarkers CD4 antigen CD64 CD8 antigen Cell culture Cell Plasticity - immunology Chemokines convalescent serum dendritic cell Dendritic cells Dendritic Cells - immunology Dendritic Cells - metabolism Disease Susceptibility Fc receptor Fc receptors Gene Expression Profiling Gene Expression Regulation Gene Regulatory Networks Immunity Immunophenotyping inf-cDC2 Infections Inflammation Interferon Interferon regulatory factor 4 Interferon Type I - metabolism IRF8 Kinases Lungs Lymphocytes Lymphocytes T Macrophages Macrophages - immunology Macrophages - metabolism monocyte Monocytes Monocytes - immunology Monocytes - metabolism Organ Specificity - immunology Population Receptors Receptors, Fc - metabolism Respirovirus Infections - etiology Respirovirus Infections - metabolism T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism Toll-like receptors transcription factor Transcription Factors type 1 interferon Viral infections virus Virus Diseases - genetics Virus Diseases - immunology Virus Diseases - metabolism Virus Diseases - virology Viruses |
| Title | Inflammatory Type 2 cDCs Acquire Features of cDC1s and Macrophages to Orchestrate Immunity to Respiratory Virus Infection |
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