Novel mouse models based on intersectional genetics to identify and characterize plasmacytoid dendritic cells.
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
07
02
2022
accepted:
03
02
2023
medline:
3
4
2023
pubmed:
18
3
2023
entrez:
17
3
2023
Statut:
ppublish
Résumé
Plasmacytoid dendritic cells (pDCs) are the main source of type I interferon (IFN-I) during viral infections. Their other functions are debated, due to a lack of tools to identify and target them in vivo without affecting pDC-like cells and transitional DCs (tDCs), which harbor overlapping phenotypes and transcriptomes but a higher efficacy for T cell activation. In the present report, we present a reporter mouse, pDC-Tom, designed through intersectional genetics based on unique Siglech and Pacsin1 coexpression in pDCs. The pDC-Tom mice specifically tagged pDCs and, on breeding with Zbtb46
Identifiants
pubmed: 36928414
doi: 10.1038/s41590-023-01454-9
pii: 10.1038/s41590-023-01454-9
pmc: PMC10063451
doi:
Substances chimiques
Interferon Type I
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
714-728Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Tomasello, E., Pollet, E., Vu Manh, T. P., Uze, G. & Dalod, M. Harnessing mechanistic knowledge on beneficial versus deleterious IFN-I effects to design innovative immunotherapies targeting cytokine activity to specific cell types. Front. Immunol. 5, 526 (2014).
doi: 10.3389/fimmu.2014.00526
pubmed: 25400632
pmcid: 4214202
King, C. & Sprent, J. Dual nature of type I Interferons in SARS-CoV-2-induced inflammation. Trends Immunol. 42, 312–322 (2021).
doi: 10.1016/j.it.2021.02.003
pubmed: 33622601
pmcid: 7879020
Reizis, B. Plasmacytoid dendritic cells: development, regulation, and function. Immunity 50, 37–50 (2019).
doi: 10.1016/j.immuni.2018.12.027
pubmed: 30650380
pmcid: 6342491
Rodrigues, P. F. et al. Distinct progenitor lineages contribute to the heterogeneity of plasmacytoid dendritic cells. Nat. Immunol. 19, 711–722 (2018).
doi: 10.1038/s41590-018-0136-9
pubmed: 29925996
pmcid: 7614340
Dress, R. J. et al. Plasmacytoid dendritic cells develop from Ly6D
doi: 10.1038/s41590-019-0420-3
pubmed: 31213723
Leylek, R. et al. Integrated cross-species analysis identifies a conserved transitional dendritic cell population. Cell Rep. 29, 3736–3750.e3738 (2019).
doi: 10.1016/j.celrep.2019.11.042
pubmed: 31825848
pmcid: 6951814
Zucchini, N. et al. Individual plasmacytoid dendritic cells are major contributors to the production of multiple innate cytokines in an organ-specific manner during viral infection. Int. Immunol. 20, 45–56 (2008).
doi: 10.1093/intimm/dxm119
pubmed: 18000008
Anderson, D. A. 3rd & Murphy, K. M. Models of dendritic cell development correlate ontogeny with function. Adv. Immunol. 143, 99–119 (2019).
doi: 10.1016/bs.ai.2019.09.001
pubmed: 31607369
Dalod, M. & Scheu, S. Dendritic cell functions in vivo: a user’s guide to current and next- generation mutant mouse models. Eur. J. Immunol. 52, 1712–1749 (2022).
Swiecki, M. et al. Cell depletion in mice that express diphtheria toxin receptor under the control of SiglecH encompasses more than plasmacytoid dendritic cells. J. Immunol. 192, 4409–4416 (2014).
doi: 10.4049/jimmunol.1303135
pubmed: 24683186
Brewitz, A. et al. CD8
doi: 10.1016/j.immuni.2017.01.003
pubmed: 28190711
pmcid: 5362251
Puttur, F. et al. Absence of Siglec-H in MCMV infection elevates interferon alpha production but does not enhance viral clearance. PLoS Pathog. 9, e1003648 (2013).
doi: 10.1371/journal.ppat.1003648
pubmed: 24086137
pmcid: 3784486
Wohner, M. et al. Molecular functions of the transcription factors E2A and E2-2 in controlling germinal center B cell and plasma cell development. J. Exp. Med. 213, 1201–1221 (2016).
doi: 10.1084/jem.20152002
pubmed: 27261530
pmcid: 4925024
Swiecki, M., Gilfillan, S., Vermi, W., Wang, Y. & Colonna, M. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8
doi: 10.1016/j.immuni.2010.11.020
pubmed: 21130004
pmcid: 3588567
Stutte, S. et al. Type I interferon mediated induction of somatostatin leads to suppression of ghrelin and appetite thereby promoting viral immunity in mice. Brain Behav. Immun. 95, 429–443 (2021).
doi: 10.1016/j.bbi.2021.04.018
pubmed: 33895286
Luche, H., Weber, O., Nageswara Rao, T., Blum, C. & Fehling, H. J. Faithful activation of an extra-bright red fluorescent protein in ‘knock-in’ Cre-reporter mice ideally suited for lineage tracing studies. Eur. J. Immunol. 37, 43–53 (2007).
doi: 10.1002/eji.200636745
pubmed: 17171761
Schlitzer, A. et al. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 16, 718–728 (2015).
doi: 10.1038/ni.3200
pubmed: 26054720
Robbins, S. H. et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 9, R17 (2008).
doi: 10.1186/gb-2008-9-1-r17
pubmed: 18218067
pmcid: 2395256
Esashi, E., Bao, M., Wang, Y. H., Cao, W. & Liu, Y. J. PACSIN1 regulates the TLR7/9-mediated type I interferon response in plasmacytoid dendritic cells. Eur. J. Immunol. 42, 573–579 (2012).
doi: 10.1002/eji.201142045
pubmed: 22488361
pmcid: 3656478
Tomasello, E. et al. Molecular dissection of plasmacytoid dendritic cell activation in vivo during a viral infection. EMBO J. 37, e98836 (2018).
doi: 10.15252/embj.201798836
pubmed: 30131424
pmcid: 6166132
Bar-On, L. et al. CX3CR1+ CD8alpha+ dendritic cells are a steady-state population related to plasmacytoid dendritic cells. Proc. Natl Acad. Sci. USA 107, 14745–14750 (2010).
doi: 10.1073/pnas.1001562107
pubmed: 20679228
pmcid: 2930429
Naik, S. H. et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8, 1217–1226 (2007).
doi: 10.1038/ni1522
pubmed: 17922015
Onai, N. et al. Identification of clonogenic common Flt3
doi: 10.1038/ni1518
pubmed: 17922016
Fogg, D. K. et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311, 83–87 (2006).
doi: 10.1126/science.1117729
pubmed: 16322423
Auffray, C. et al. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206, 595–606 (2009).
doi: 10.1084/jem.20081385
pubmed: 19273628
pmcid: 2699130
Satpathy, A. T. et al. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209, 1135–1152 (2012).
doi: 10.1084/jem.20120030
pubmed: 22615127
pmcid: 3371733
Abbas, A. et al. The activation trajectory of plasmacytoid dendritic cells in vivo during a viral infection. Nat. Immunol. 21, 983–997 (2020).
doi: 10.1038/s41590-020-0731-4
pubmed: 32690951
pmcid: 7610367
Attaf, N. et al. FB5P-seq: FACS-based 5-prime end single-cell RNA-seq for integrative analysis of transcriptome and antigen receptor repertoire in B and T cells. Front. Immunol. 11, 216 (2020).
doi: 10.3389/fimmu.2020.00216
pubmed: 32194545
pmcid: 7062913
Lau, C. M. et al. Leukemia-associated activating mutation of Flt3 expands dendritic cells and alters T cell responses. J. Exp. Med. 213, 415–431 (2016).
doi: 10.1084/jem.20150642
pubmed: 26903243
pmcid: 4813676
Crozat, K. et al. Cutting edge: expression of XCR1 defines mouse lymphoid-tissue resident and migratory dendritic cells of the CD8alpha+ type. J. Immunol. 187, 4411–4415 (2011).
doi: 10.4049/jimmunol.1101717
pubmed: 21948982
Manh, T. P., Alexandre, Y., Baranek, T., Crozat, K. & Dalod, M. Plasmacytoid, conventional, and monocyte-derived dendritic cells undergo a profound and convergent genetic reprogramming during their maturation. Eur. J. Immunol. 43, 1706–1715 (2013).
doi: 10.1002/eji.201243106
pubmed: 23553052
Ardouin, L. et al. Broad and largely concordant molecular changes characterize tolerogenic and immunogenic dendritic cell maturation in thymus and periphery. Immunity 45, 305–318 (2016).
doi: 10.1016/j.immuni.2016.07.019
pubmed: 27533013
Maier, B. et al. A conserved dendritic-cell regulatory program limits antitumour immunity. Nature 580, 257–262 (2020).
doi: 10.1038/s41586-020-2134-y
pubmed: 32269339
pmcid: 7787191
Blasius, A. L., Cella, M., Maldonado, J., Takai, T. & Colonna, M. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107, 2474–2476 (2006).
doi: 10.1182/blood-2005-09-3746
pubmed: 16293595
pmcid: 1895736
Contractor, N., Louten, J., Kim, L., Biron, C. A. & Kelsall, B. L. Cutting edge: Peyer’s patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: possible role for IL-10, TGFbeta, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J. Immunol. 179, 2690–2694 (2007).
doi: 10.4049/jimmunol.179.5.2690
pubmed: 17709480
Wendland, M. et al. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc. Natl Acad. Sci. USA 104, 6347–6352 (2007).
doi: 10.1073/pnas.0609180104
pubmed: 17404233
pmcid: 1851094
Bonnardel, J. et al. Innate and adaptive immune functions of peyer’s patch monocyte-derived cells. Cell Rep. 11, 770–784 (2015).
doi: 10.1016/j.celrep.2015.03.067
pubmed: 25921539
Da Silva, C., Wagner, C., Bonnardel, J., Gorvel, J. P. & Lelouard, H. The Peyer’s patch mononuclear phagocyte system at steady state and during infection. Front. Immunol. 8, 1254 (2017).
doi: 10.3389/fimmu.2017.01254
pubmed: 29038658
pmcid: 5630697
Scheu, S., Dresing, P. & Locksley, R. M. Visualization of IFNbeta production by plasmacytoid versus conventional dendritic cells under specific stimulation conditions in vivo. Proc. Natl Acad. Sci. USA 105, 20416–20421 (2008).
doi: 10.1073/pnas.0808537105
pubmed: 19088190
pmcid: 2629269
Dalod, M. et al. Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195, 517–528 (2002).
doi: 10.1084/jem.20011672
pubmed: 11854364
pmcid: 2193614
Assil, S. et al. Plasmacytoid dendritic cells and infected cells form an interferogenic synapse required for antiviral responses. Cell Host Microbe 25, 730–745.e736 (2019).
doi: 10.1016/j.chom.2019.03.005
pubmed: 31003939
Megjugorac, N. J. et al. Image-based study of interferongenic interactions between plasmacytoid dendritic cells and HSV-infected monocyte-derived dendritic cells. Immunol. Invest. 36, 739–761 (2007).
doi: 10.1080/08820130701715845
pubmed: 18161527
Asselin-Paturel, C., Brizard, G., Pin, J. J., Briere, F. & Trinchieri, G. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171, 6466–6477 (2003).
doi: 10.4049/jimmunol.171.12.6466
pubmed: 14662846
Blasius, A. L. et al. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177, 3260–3265 (2006).
doi: 10.4049/jimmunol.177.5.3260
pubmed: 16920966
Alexandre, Y. O., Cocita, C. D., Ghilas, S. & Dalod, M. Deciphering the role of DC subsets in MCMV infection to better understand immune protection against viral infections. Front. Microbiol. 5, 378 (2014).
doi: 10.3389/fmicb.2014.00378
pubmed: 25120535
pmcid: 4114203
Ghilas, S. et al. Natural killer cells and dendritic epidermal gammadelta T cells orchestrate type 1 conventional DC spatiotemporal repositioning toward CD8
doi: 10.1016/j.isci.2021.103059
pubmed: 34568787
pmcid: 8449251
Feng, J. et al. Clonal lineage tracing reveals shared origin of conventional and plasmacytoid dendritic cells. Immunity 55, 405–422 e411 (2022).
doi: 10.1016/j.immuni.2022.01.016
pubmed: 35180378
pmcid: 9344860
Lancien, M. et al. Dendritic cells require TMEM176A/B ion channels for optimal MHC class II antigen presentation to naive CD4
doi: 10.4049/jimmunol.2000498
pubmed: 34233909
Segovia, M. et al. Autologous dendritic cells prolong allograft survival through Tmem176b-dependent antigen cross-presentation. Am. J. Transpl. 14, 1021–1031 (2014).
doi: 10.1111/ajt.12708
Segovia, M. et al. Targeting TMEM176B enhances antitumor immunity and augments the efficacy of immune checkpoint blockers by unleashing inflammasome activation. Cancer Cell 35, 767–781.e766 (2019).
doi: 10.1016/j.ccell.2019.04.003
pubmed: 31085177
pmcid: 6521897
Meskas, J., Yokosawa, D., Wang, S., Segat, G.C. & Brinkman, R.R. flowCut: An R package for automated removal of outlier events and flagging of files based on time versus fluorescence analysis. Cytometry A 103, 71–81 (2023).
doi: 10.1002/cyto.a.24670
pubmed: 35796000
Becht, E. et al. Dimensionality reduction for visualizing single-cell data using UMAP. Nat. Biotechnol. 37, 38–44 (2019).
Stassen, S. V. et al. PARC: ultrafast and accurate clustering of phenotypic data of millions of single cells. Bioinformatics 36, 2778–2786 (2020).
doi: 10.1093/bioinformatics/btaa042
pubmed: 31971583
pmcid: 7203756
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).
doi: 10.1038/nbt.4096
pubmed: 29608179
pmcid: 6700744
Ginhoux, F., Guilliams, M. & Merad, M. Expanding dendritic cell nomenclature in the single-cell era. Nat. Rev. Immunol. 22, 67–68 (2022).
doi: 10.1038/s41577-022-00675-7
pubmed: 35027741
See, P. et al. Mapping the human DC lineage through the integration of high-dimensional techniques. Science 356, eaag3009 (2017).
doi: 10.1126/science.aag3009
pubmed: 28473638
pmcid: 7611082
Levine, J. H. et al. Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis. Cell 162, 184–197 (2015).
doi: 10.1016/j.cell.2015.05.047
pubmed: 26095251
pmcid: 4508757
Spinelli, L., Carpentier, S., Montanana Sanchis, F., Dalod, M. & Vu Manh, T. P. BubbleGUM: automatic extraction of phenotype molecular signatures and comprehensive visualization of multiple Gene Set Enrichment Analyses. BMC Genomics 16, 814 (2015).
doi: 10.1186/s12864-015-2012-4
pubmed: 26481321
pmcid: 4617899