CD8 T Cells Orchestrate PDC-XCR1 Dendritic Cell Spatial and Functional Cooperativity to Optimize Priming

Overview

Journal Immunity

Publisher Cell Press

Specialty Allergy & Immunology

Date 2017 Feb 14

PMID 28190711

Citations 172

Authors

Anna Brewitz

Sarah Eickhoff

Sabrina Dahling

Thomas Quast

Sammy Bedoui

Richard A Kroczek

Christian Kurts

Natalio Garbi

Winfried Barchet

Matteo Iannacone

Frederick Klauschen

Waldemar Kolanus

Tsuneyasu Kaisho

Marco Colonna

Ronald N Germain

Wolfgang Kastenmuller

Affiliations

Soon will be listed here.

Abstract

Adaptive cellular immunity is initiated by antigen-specific interactions between T lymphocytes and dendritic cells (DCs). Plasmacytoid DCs (pDCs) support antiviral immunity by linking innate and adaptive immune responses. Here we examined pDC spatiotemporal dynamics during viral infection to uncover when, where, and how they exert their functions. We found that pDCs accumulated at sites of CD8 T cell antigen-driven activation in a CCR5-dependent fashion. Furthermore, activated CD8 T cells orchestrated the local recruitment of lymph node-resident XCR1 chemokine receptor-expressing DCs via secretion of the XCL1 chemokine. Functionally, this CD8 T cell-mediated reorganization of the local DC network allowed for the interaction and cooperation of pDCs and XCR1 DCs, thereby optimizing XCR1 DC maturation and cross-presentation. These data support a model in which CD8 T cells upon activation create their own optimal priming microenvironment by recruiting additional DC subsets to the site of initial antigen recognition.

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References

Di Pucchio T, Chatterjee B, Smed-Sorensen A, Clayton S, Palazzo A, Montes M . Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat Immunol. 2008; 9(5):551-7. PMC: 2695657. DOI: 10.1038/ni.1602. View

Haeryfar S . The importance of being a pDC in antiviral immunity: the IFN mission versus Ag presentation?. Trends Immunol. 2005; 26(6):311-7. DOI: 10.1016/j.it.2005.04.002. View

Mouries J, Moron G, Schlecht G, Escriou N, Dadaglio G, Leclerc C . Plasmacytoid dendritic cells efficiently cross-prime naive T cells in vivo after TLR activation. Blood. 2008; 112(9):3713-22. PMC: 2572799. DOI: 10.1182/blood-2008-03-146290. View

Bachem A, Hartung E, Guttler S, Mora A, Zhou X, Hegemann A . Expression of XCR1 Characterizes the Batf3-Dependent Lineage of Dendritic Cells Capable of Antigen Cross-Presentation. Front Immunol. 2012; 3:214. PMC: 3399095. DOI: 10.3389/fimmu.2012.00214. View

Reizis B, Bunin A, Ghosh H, Lewis K, Sisirak V . Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol. 2011; 29:163-83. PMC: 4160806. DOI: 10.1146/annurev-immunol-031210-101345. View

Diacovo T, Blasius A, Mak T, Cella M, Colonna M . Adhesive mechanisms governing interferon-producing cell recruitment into lymph nodes. J Exp Med. 2005; 202(5):687-96. PMC: 2212867. DOI: 10.1084/jem.20051035. View

Yoneyama H, Matsuno K, Toda E, Nishiwaki T, Matsuo N, Nakano A . Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J Exp Med. 2005; 202(3):425-35. PMC: 2213078. DOI: 10.1084/jem.20041961. View

Swiecki M, Colonna M . The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol. 2015; 15(8):471-85. PMC: 4808588. DOI: 10.1038/nri3865. View

Salek-Ardakani S, Arens R, Flynn R, Sette A, Schoenberger S, Croft M . Preferential use of B7.2 and not B7.1 in priming of vaccinia virus-specific CD8 T cells. J Immunol. 2009; 182(5):2909-18. PMC: 2707928. DOI: 10.4049/jimmunol.0803545. View

10.

Mempel T, Henrickson S, von Andrian U . T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004; 427(6970):154-9. DOI: 10.1038/nature02238. View

11.

Veiga-Parga T, Sehrawat S, Rouse B . Role of regulatory T cells during virus infection. Immunol Rev. 2013; 255(1):182-96. PMC: 3748387. DOI: 10.1111/imr.12085. View

12.

Kamala T . Hock immunization: a humane alternative to mouse footpad injections. J Immunol Methods. 2007; 328(1-2):204-14. PMC: 2464360. DOI: 10.1016/j.jim.2007.08.004. View

13.

Reizis B, Colonna M, Trinchieri G, Barrat F, Gilliet M . Plasmacytoid dendritic cells: one-trick ponies or workhorses of the immune system?. Nat Rev Immunol. 2011; 11(8):558-65. PMC: 4157822. DOI: 10.1038/nri3027. View

14.

Sung J, Zhang H, Moseman E, Alvarez D, Iannacone M, Henrickson S . Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell. 2012; 150(6):1249-63. PMC: 3445043. DOI: 10.1016/j.cell.2012.08.015. View

15.

Jusforgues-Saklani H, Uhl M, Blachere N, Lemaitre F, Lantz O, Bousso P . Antigen persistence is required for dendritic cell licensing and CD8+ T cell cross-priming. J Immunol. 2008; 181(5):3067-76. DOI: 10.4049/jimmunol.181.5.3067. View

16.

Cervantes-Barragan L, Lewis K, Firner S, Thiel V, Hugues S, Reith W . Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc Natl Acad Sci U S A. 2012; 109(8):3012-7. PMC: 3286988. DOI: 10.1073/pnas.1117359109. View

17.

Hor J, Whitney P, Zaid A, Brooks A, Heath W, Mueller S . Spatiotemporally Distinct Interactions with Dendritic Cell Subsets Facilitates CD4+ and CD8+ T Cell Activation to Localized Viral Infection. Immunity. 2015; 43(3):554-65. DOI: 10.1016/j.immuni.2015.07.020. View

18.

Miller J, Brown B, Shay T, Gautier E, Jojic V, Cohain A . Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol. 2012; 13(9):888-99. PMC: 3985403. DOI: 10.1038/ni.2370. View

19.

Villadangos J, Young L . Antigen-presentation properties of plasmacytoid dendritic cells. Immunity. 2008; 29(3):352-61. DOI: 10.1016/j.immuni.2008.09.002. View

20.

Dorner B, Scheffold A, Rolph M, Huser M, Kaufmann S, Radbruch A . MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc Natl Acad Sci U S A. 2002; 99(9):6181-6. PMC: 122923. DOI: 10.1073/pnas.092141999. View