Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection

Paul R. Dunbar, Emily K. Cartwright, Alexander N. Wein, Tetsuo Tsukamoto, Zheng Rong Tiger Li, Nivedha Kumar, Ida E. Uddbäck, Sarah L. Hayward, Satoshi Ueha, Shiki Takamura, Jacob E. Kohlmeier

Research output: Contribution to journalArticle

Abstract

Lung resident memory CD8 T cells (TRM) are critical for protection against respiratory viruses, but the cellular interactions required for their development are poorly understood. Herein we describe the necessity of classical monocytes for the establishment of lung TRM following influenza infection. We find that, during the initial appearance of lung TRM, monocytes and dendritic cells are the most numerous influenza antigen-bearing APCs in the lung. Surprisingly, depletion of DCs after initial T cell priming did not impact lung TRM development or maintenance. In contrast, a monocyte deficient pulmonary environment in CCR2−/− mice results in significantly less lung TRM following influenza infection, despite no defect in the antiviral effector response or in the peripheral memory pool. Imaging shows direct interaction of antigen-specific T cells with antigen-bearing monocytes in the lung, and pulmonary classical monocytes from the lungs of influenza infected mice are sufficient to drive differentiation of T cells in vitro. These data describe a novel role for pulmonary monocytes in mediating lung TRM development through direct interaction with T cells in the lung.

Original languageEnglish
Pages (from-to)161-171
Number of pages11
JournalMucosal Immunology
Volume13
Issue number1
DOIs
Publication statusPublished - 1 Jan 2020

Fingerprint

Virus Diseases
Monocytes
T-Lymphocytes
Lung
Human Influenza
Antigens
Drive
Infection
Dendritic Cells
Antiviral Agents
Maintenance

Cite this

Dunbar, P. R., Cartwright, E. K., Wein, A. N., Tsukamoto, T., Tiger Li, Z. R., Kumar, N., ... Kohlmeier, J. E. (2020). Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection. Mucosal Immunology, 13(1), 161-171. https://doi.org/10.1038/s41385-019-0224-7
Dunbar, Paul R. ; Cartwright, Emily K. ; Wein, Alexander N. ; Tsukamoto, Tetsuo ; Tiger Li, Zheng Rong ; Kumar, Nivedha ; Uddbäck, Ida E. ; Hayward, Sarah L. ; Ueha, Satoshi ; Takamura, Shiki ; Kohlmeier, Jacob E. / Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection. In: Mucosal Immunology. 2020 ; Vol. 13, No. 1. pp. 161-171.
@article{5fe53c4c900847029f40da9313ba5b48,
title = "Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection",
abstract = "Lung resident memory CD8 T cells (TRM) are critical for protection against respiratory viruses, but the cellular interactions required for their development are poorly understood. Herein we describe the necessity of classical monocytes for the establishment of lung TRM following influenza infection. We find that, during the initial appearance of lung TRM, monocytes and dendritic cells are the most numerous influenza antigen-bearing APCs in the lung. Surprisingly, depletion of DCs after initial T cell priming did not impact lung TRM development or maintenance. In contrast, a monocyte deficient pulmonary environment in CCR2−/− mice results in significantly less lung TRM following influenza infection, despite no defect in the antiviral effector response or in the peripheral memory pool. Imaging shows direct interaction of antigen-specific T cells with antigen-bearing monocytes in the lung, and pulmonary classical monocytes from the lungs of influenza infected mice are sufficient to drive differentiation of T cells in vitro. These data describe a novel role for pulmonary monocytes in mediating lung TRM development through direct interaction with T cells in the lung.",
author = "Dunbar, {Paul R.} and Cartwright, {Emily K.} and Wein, {Alexander N.} and Tetsuo Tsukamoto and {Tiger Li}, {Zheng Rong} and Nivedha Kumar and Uddb{\"a}ck, {Ida E.} and Hayward, {Sarah L.} and Satoshi Ueha and Shiki Takamura and Kohlmeier, {Jacob E.}",
year = "2020",
month = "1",
day = "1",
doi = "10.1038/s41385-019-0224-7",
language = "English",
volume = "13",
pages = "161--171",
journal = "Mucosal Immunology",
issn = "1933-0219",
publisher = "Nature Publishing Group",
number = "1",

}

Dunbar, PR, Cartwright, EK, Wein, AN, Tsukamoto, T, Tiger Li, ZR, Kumar, N, Uddbäck, IE, Hayward, SL, Ueha, S, Takamura, S & Kohlmeier, JE 2020, 'Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection', Mucosal Immunology, vol. 13, no. 1, pp. 161-171. https://doi.org/10.1038/s41385-019-0224-7

Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection. / Dunbar, Paul R.; Cartwright, Emily K.; Wein, Alexander N.; Tsukamoto, Tetsuo; Tiger Li, Zheng Rong; Kumar, Nivedha; Uddbäck, Ida E.; Hayward, Sarah L.; Ueha, Satoshi; Takamura, Shiki; Kohlmeier, Jacob E.

In: Mucosal Immunology, Vol. 13, No. 1, 01.01.2020, p. 161-171.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Pulmonary monocytes interact with effector T cells in the lung tissue to drive TRM differentiation following viral infection

AU - Dunbar, Paul R.

AU - Cartwright, Emily K.

AU - Wein, Alexander N.

AU - Tsukamoto, Tetsuo

AU - Tiger Li, Zheng Rong

AU - Kumar, Nivedha

AU - Uddbäck, Ida E.

AU - Hayward, Sarah L.

AU - Ueha, Satoshi

AU - Takamura, Shiki

AU - Kohlmeier, Jacob E.

PY - 2020/1/1

Y1 - 2020/1/1

N2 - Lung resident memory CD8 T cells (TRM) are critical for protection against respiratory viruses, but the cellular interactions required for their development are poorly understood. Herein we describe the necessity of classical monocytes for the establishment of lung TRM following influenza infection. We find that, during the initial appearance of lung TRM, monocytes and dendritic cells are the most numerous influenza antigen-bearing APCs in the lung. Surprisingly, depletion of DCs after initial T cell priming did not impact lung TRM development or maintenance. In contrast, a monocyte deficient pulmonary environment in CCR2−/− mice results in significantly less lung TRM following influenza infection, despite no defect in the antiviral effector response or in the peripheral memory pool. Imaging shows direct interaction of antigen-specific T cells with antigen-bearing monocytes in the lung, and pulmonary classical monocytes from the lungs of influenza infected mice are sufficient to drive differentiation of T cells in vitro. These data describe a novel role for pulmonary monocytes in mediating lung TRM development through direct interaction with T cells in the lung.

AB - Lung resident memory CD8 T cells (TRM) are critical for protection against respiratory viruses, but the cellular interactions required for their development are poorly understood. Herein we describe the necessity of classical monocytes for the establishment of lung TRM following influenza infection. We find that, during the initial appearance of lung TRM, monocytes and dendritic cells are the most numerous influenza antigen-bearing APCs in the lung. Surprisingly, depletion of DCs after initial T cell priming did not impact lung TRM development or maintenance. In contrast, a monocyte deficient pulmonary environment in CCR2−/− mice results in significantly less lung TRM following influenza infection, despite no defect in the antiviral effector response or in the peripheral memory pool. Imaging shows direct interaction of antigen-specific T cells with antigen-bearing monocytes in the lung, and pulmonary classical monocytes from the lungs of influenza infected mice are sufficient to drive differentiation of T cells in vitro. These data describe a novel role for pulmonary monocytes in mediating lung TRM development through direct interaction with T cells in the lung.

UR - http://www.scopus.com/inward/record.url?scp=85075210494&partnerID=8YFLogxK

U2 - 10.1038/s41385-019-0224-7

DO - 10.1038/s41385-019-0224-7

M3 - Article

C2 - 31723250

AN - SCOPUS:85075210494

VL - 13

SP - 161

EP - 171

JO - Mucosal Immunology

JF - Mucosal Immunology

SN - 1933-0219

IS - 1

ER -