Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming

Dieke van Dinther; Henrike Veninga; Salvador Iborra; Ellen G. F. Borg; Leoni Hoogterp; Katarzyna Olesek; Marieke R. Beijer; Sjoerd T. T. Schetters; Hakan Kalay; Juan J. Garcia-Vallejo; Kees L. Franken; Lamin B. Cham; Karl S. Lang; Yvette van Kooyk; David Sancho; Paul R. Crocker; Joke M. M. den Haan

doi:10.1016/j.celrep.2018.01.021

Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming

Dieke van Dinther, Henrike Veninga, Salvador Iborra, Ellen G. F. Borg, Leoni Hoogterp, Katarzyna Olesek, Marieke R. Beijer, Sjoerd T. T. Schetters, Hakan Kalay, Juan J. Garcia-Vallejo, Kees L. Franken, Lamin B. Cham, Karl S. Lang, Yvette van Kooyk, David Sancho, Paul R. Crocker, Joke M. M. den Haan (Lead / Corresponding author)

Cell Signalling and Immunology

Research output: Contribution to journal › Article › peer-review

93 Citations (Scopus)

253 Downloads (Pure)

Abstract

Splenic CD169+ macrophages are located in the marginal zone to efficiently capture blood-borne pathogens. Here, we investigate the requirements for the induction of CD8+ T cell responses by antigens (Ags) bound by CD169+ macrophages. Upon Ag targeting to CD169+ macrophages, we show that BATF3-dependent CD8α+ dendritic cells (DCs) are crucial for DNGR-1-mediated cross-priming of CD8+ T cell responses. In addition, we demonstrate that CD169, a sialic acid binding lectin involved in cell-cell contact, preferentially binds to CD8α+ DCs and that Ag transfer to CD8α+ DCs and subsequent T cell activation is dependent on the sialic acid-binding capacity of CD169. Finally, functional CD169 mediates optimal CD8+ T cell responses to modified vaccinia Ankara virus infection. Together, these data indicate that the collaboration of CD169+ macrophages and CD8α+ DCs for the initiation of effective CD8+ T cell responses is facilitated by binding of CD169 to sialic acid containing ligands on CD8α+ DCs.

Original language	English
Pages (from-to)	1484-1495
Number of pages	12
Journal	Cell Reports
Volume	22
Issue number	6
DOIs	https://doi.org/10.1016/j.celrep.2018.01.021
Publication status	Published - 6 Feb 2018

Keywords

Journal article
CD169
Siglec-1
Sialoadhesin
macrophage
dendritic cell
antigen
T cell response
cross-presentation
DNGR-1
vaccinia

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1016/j.celrep.2018.01.021Licence: CC BY-NC-ND

Final Published Version
©2018 The Authors. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Final published version, 3.69 MBLicence: CC BY-NC-ND

Cite this

van Dinther, D., Veninga, H., Iborra, S., Borg, E. G. F., Hoogterp, L., Olesek, K., Beijer, M. R., Schetters, S. T. T., Kalay, H., Garcia-Vallejo, J. J., Franken, K. L., Cham, L. B., Lang, K. S., van Kooyk, Y., Sancho, D., Crocker, P. R., & den Haan, J. M. M. (2018). Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming. Cell Reports, 22(6), 1484-1495. https://doi.org/10.1016/j.celrep.2018.01.021

@article{babafd8417f147f1a79562907f771805,

title = "Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming",

abstract = "Splenic CD169+ macrophages are located in the marginal zone to efficiently capture blood-borne pathogens. Here, we investigate the requirements for the induction of CD8+ T cell responses by antigens (Ags) bound by CD169+ macrophages. Upon Ag targeting to CD169+ macrophages, we show that BATF3-dependent CD8α+ dendritic cells (DCs) are crucial for DNGR-1-mediated cross-priming of CD8+ T cell responses. In addition, we demonstrate that CD169, a sialic acid binding lectin involved in cell-cell contact, preferentially binds to CD8α+ DCs and that Ag transfer to CD8α+ DCs and subsequent T cell activation is dependent on the sialic acid-binding capacity of CD169. Finally, functional CD169 mediates optimal CD8+ T cell responses to modified vaccinia Ankara virus infection. Together, these data indicate that the collaboration of CD169+ macrophages and CD8α+ DCs for the initiation of effective CD8+ T cell responses is facilitated by binding of CD169 to sialic acid containing ligands on CD8α+ DCs.",

keywords = "Journal article, CD169, Siglec-1, Sialoadhesin, macrophage, dendritic cell, antigen, T cell response, cross-presentation, DNGR-1, vaccinia",

author = "{van Dinther}, Dieke and Henrike Veninga and Salvador Iborra and Borg, {Ellen G. F.} and Leoni Hoogterp and Katarzyna Olesek and Beijer, {Marieke R.} and Schetters, {Sjoerd T. T.} and Hakan Kalay and Garcia-Vallejo, {Juan J.} and Franken, {Kees L.} and Cham, {Lamin B.} and Lang, {Karl S.} and {van Kooyk}, Yvette and David Sancho and Crocker, {Paul R.} and {den Haan}, {Joke M. M.}",

note = "Work in the D.S. laboratory is funded by the CNIC; grant SAF2016-79040-R from the Spanish Ministry of Economy, Industry and Competitiveness (MINECO), Agencia Estatal de Investigaci{\'o}n and FEDER (European fund for Regional Development); Foundation Acteria; and the European Commission (635122-PROCROP H2020) and the European Research Council (ERC-2016-Consolidator Grant 725091). This work was supported by grants from the Dutch Cancer Society (VU2009-4504 and VU2013-5940) and by VUmc CCA (2015-5-22 to J.M.M.d.H.). S.I. is funded by grant SAF2015-74561-JIN.",

year = "2018",

month = feb,

day = "6",

doi = "10.1016/j.celrep.2018.01.021",

language = "English",

volume = "22",

pages = "1484--1495",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Elsevier",

number = "6",

}

van Dinther, D, Veninga, H, Iborra, S, Borg, EGF, Hoogterp, L, Olesek, K, Beijer, MR, Schetters, STT, Kalay, H, Garcia-Vallejo, JJ, Franken, KL, Cham, LB, Lang, KS, van Kooyk, Y, Sancho, D, Crocker, PR & den Haan, JMM 2018, 'Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming', Cell Reports, vol. 22, no. 6, pp. 1484-1495. https://doi.org/10.1016/j.celrep.2018.01.021

TY - JOUR

T1 - Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming

AU - van Dinther, Dieke

AU - Veninga, Henrike

AU - Iborra, Salvador

AU - Borg, Ellen G. F.

AU - Hoogterp, Leoni

AU - Olesek, Katarzyna

AU - Beijer, Marieke R.

AU - Schetters, Sjoerd T. T.

AU - Kalay, Hakan

AU - Garcia-Vallejo, Juan J.

AU - Franken, Kees L.

AU - Cham, Lamin B.

AU - Lang, Karl S.

AU - van Kooyk, Yvette

AU - Sancho, David

AU - Crocker, Paul R.

AU - den Haan, Joke M. M.

N1 - Work in the D.S. laboratory is funded by the CNIC; grant SAF2016-79040-R from the Spanish Ministry of Economy, Industry and Competitiveness (MINECO), Agencia Estatal de Investigación and FEDER (European fund for Regional Development); Foundation Acteria; and the European Commission (635122-PROCROP H2020) and the European Research Council (ERC-2016-Consolidator Grant 725091). This work was supported by grants from the Dutch Cancer Society (VU2009-4504 and VU2013-5940) and by VUmc CCA (2015-5-22 to J.M.M.d.H.). S.I. is funded by grant SAF2015-74561-JIN.

PY - 2018/2/6

Y1 - 2018/2/6

N2 - Splenic CD169+ macrophages are located in the marginal zone to efficiently capture blood-borne pathogens. Here, we investigate the requirements for the induction of CD8+ T cell responses by antigens (Ags) bound by CD169+ macrophages. Upon Ag targeting to CD169+ macrophages, we show that BATF3-dependent CD8α+ dendritic cells (DCs) are crucial for DNGR-1-mediated cross-priming of CD8+ T cell responses. In addition, we demonstrate that CD169, a sialic acid binding lectin involved in cell-cell contact, preferentially binds to CD8α+ DCs and that Ag transfer to CD8α+ DCs and subsequent T cell activation is dependent on the sialic acid-binding capacity of CD169. Finally, functional CD169 mediates optimal CD8+ T cell responses to modified vaccinia Ankara virus infection. Together, these data indicate that the collaboration of CD169+ macrophages and CD8α+ DCs for the initiation of effective CD8+ T cell responses is facilitated by binding of CD169 to sialic acid containing ligands on CD8α+ DCs.

AB - Splenic CD169+ macrophages are located in the marginal zone to efficiently capture blood-borne pathogens. Here, we investigate the requirements for the induction of CD8+ T cell responses by antigens (Ags) bound by CD169+ macrophages. Upon Ag targeting to CD169+ macrophages, we show that BATF3-dependent CD8α+ dendritic cells (DCs) are crucial for DNGR-1-mediated cross-priming of CD8+ T cell responses. In addition, we demonstrate that CD169, a sialic acid binding lectin involved in cell-cell contact, preferentially binds to CD8α+ DCs and that Ag transfer to CD8α+ DCs and subsequent T cell activation is dependent on the sialic acid-binding capacity of CD169. Finally, functional CD169 mediates optimal CD8+ T cell responses to modified vaccinia Ankara virus infection. Together, these data indicate that the collaboration of CD169+ macrophages and CD8α+ DCs for the initiation of effective CD8+ T cell responses is facilitated by binding of CD169 to sialic acid containing ligands on CD8α+ DCs.

KW - Journal article

KW - CD169

KW - Siglec-1

KW - Sialoadhesin

KW - macrophage

KW - dendritic cell

KW - antigen

KW - T cell response

KW - cross-presentation

KW - DNGR-1

KW - vaccinia

U2 - 10.1016/j.celrep.2018.01.021

DO - 10.1016/j.celrep.2018.01.021

M3 - Article

C2 - 29425504

SN - 2211-1247

VL - 22

SP - 1484

EP - 1495

JO - Cell Reports

JF - Cell Reports

IS - 6

ER -

Functional CD169 on Macrophages Mediates Interaction with Dendritic Cells for CD8+ T Cell Cross-Priming

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

Fingerprint

Cite this