Tumor necrosis factormediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection

Prashant V. Shinde; Haifeng C. Xu; Sathish Kumar Maney; Andreas Kloetgen; Sukumar Namineni; Yuan Zhuang; Nadine Honke; Namir Shaabani; Nicolas Bellora; Mareike Doerrenberg; Mirko Trilling; Vitaly I. Pozdeev; Nico van Rooijen; Stefanie Scheu; Klaus Pfeffer; Paul R. Crocker; Masato Tanaka; Sujitha Duggimpudi; Percy Knolle; Mathias Heikenwalder; Jürgen Ruland; Tak W. Mak; Dirk Brenner; Aleksandra A. Pandyra; Jessica I. Hoell; Arndt Borkhardt; Dieter Häussinger; Karl S. Lang; Philipp A. Lang

doi:10.1128/JVI.01637-17

Tumor necrosis factormediated survival of CD169⁺ cells promotes immune activation during vesicular stomatitis virus infection

Prashant V. Shinde, Haifeng C. Xu, Sathish Kumar Maney, Andreas Kloetgen, Sukumar Namineni, Yuan Zhuang, Nadine Honke, Namir Shaabani, Nicolas Bellora, Mareike Doerrenberg, Mirko Trilling, Vitaly I. Pozdeev, Nico van Rooijen, Stefanie Scheu, Klaus Pfeffer, Paul R. Crocker, Masato Tanaka, Sujitha Duggimpudi, Percy Knolle, Mathias HeikenwalderJürgen Ruland, Tak W. Mak, Dirk Brenner, Aleksandra A. Pandyra, Jessica I. Hoell, Arndt Borkhardt, Dieter Häussinger, Karl S. Lang, Philipp A. Lang^*

^*Corresponding author for this work

Experimental and Molecular Immunology

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

14 Citations (Scopus)

Abstract

Innate immune activation is essential to mount an effective antiviral response and to prime adaptive immunity. Although a crucial role of CD169⁺ cells during vesicular stomatitis virus (VSV) infections is increasingly recognized, factors regulating CD169⁺ cells during viral infections remain unclear. Here, we show that tumor necrosis factor is produced by CD11b⁺ Ly6C⁺ Ly6G⁺ cells following infection with VSV. The absence of TNF or TNF receptor 1 (TNFR1) resulted in reduced numbers of CD169⁺ cells and in reduced type I interferon (IFN-I) production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nuclei of CD169⁺ cells; this translocation was inhibited when the paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and development of severe disease. These findings indicate that TNF mediates the maintenance of CD169⁺ cells and innate and adaptive immune activation during VSV infection.

Original language	English
Article number	e01637-17
Journal	Journal of Virology
Volume	92
Issue number	3
DOIs	https://doi.org/10.1128/JVI.01637-17
Publication status	Published - 1 Feb 2018

Keywords

Innate immunity
Interferon
Interferons
MALT1
NF-κB
TNF
Tumor necrosis factor

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10.1128/JVI.01637-17

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Shinde, P. V., Xu, H. C., Maney, S. K., Kloetgen, A., Namineni, S., Zhuang, Y., Honke, N., Shaabani, N., Bellora, N., Doerrenberg, M., Trilling, M., Pozdeev, V. I., van Rooijen, N., Scheu, S., Pfeffer, K., Crocker, P. R., Tanaka, M., Duggimpudi, S., Knolle, P., ... Lang, P. A. (2018). Tumor necrosis factormediated survival of CD169⁺ cells promotes immune activation during vesicular stomatitis virus infection. Journal of Virology, 92(3), Article e01637-17. https://doi.org/10.1128/JVI.01637-17

@article{1d6c6ba021b94a6abe1061eada9678ed,

title = "Tumor necrosis factormediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection",

abstract = "Innate immune activation is essential to mount an effective antiviral response and to prime adaptive immunity. Although a crucial role of CD169+ cells during vesicular stomatitis virus (VSV) infections is increasingly recognized, factors regulating CD169+ cells during viral infections remain unclear. Here, we show that tumor necrosis factor is produced by CD11b+ Ly6C+ Ly6G+ cells following infection with VSV. The absence of TNF or TNF receptor 1 (TNFR1) resulted in reduced numbers of CD169+ cells and in reduced type I interferon (IFN-I) production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nuclei of CD169+ cells; this translocation was inhibited when the paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and development of severe disease. These findings indicate that TNF mediates the maintenance of CD169+ cells and innate and adaptive immune activation during VSV infection.",

keywords = "Innate immunity, Interferon, Interferons, MALT1, NF-κB, TNF, Tumor necrosis factor",

author = "Shinde, {Prashant V.} and Xu, {Haifeng C.} and Maney, {Sathish Kumar} and Andreas Kloetgen and Sukumar Namineni and Yuan Zhuang and Nadine Honke and Namir Shaabani and Nicolas Bellora and Mareike Doerrenberg and Mirko Trilling and Pozdeev, {Vitaly I.} and {van Rooijen}, Nico and Stefanie Scheu and Klaus Pfeffer and Crocker, {Paul R.} and Masato Tanaka and Sujitha Duggimpudi and Percy Knolle and Mathias Heikenwalder and J{\"u}rgen Ruland and Mak, {Tak W.} and Dirk Brenner and Pandyra, {Aleksandra A.} and Hoell, {Jessica I.} and Arndt Borkhardt and Dieter H{\"a}ussinger and Lang, {Karl S.} and Lang, {Philipp A.}",

note = "Funding Information: This study was supported by the Alexander von Humboldt Foundation (SKA2010), the German Research Council (SFB974, LA2558/3-1, LA2558/5-1, GRK1949, and TRR60), J{\"u}rgen Manchot Graduate School MOI II, and the NIH tetramer facility. D.B. is funded by the ATTRACT Programme (A14/BM/7632103/DBRRIL) and a CORE grant (C15/BM/ 10355103) from the National Research Fund Luxembourg (FNR). J.R. is funded by the DFG (SFB 1054/B01) and the ERC (FP7; grant agreement no. 322865). Publisher Copyright: {\textcopyright} 2018 American Society for Microbiology.",

year = "2018",

month = feb,

day = "1",

doi = "10.1128/JVI.01637-17",

language = "English",

volume = "92",

journal = "Journal of Virology",

issn = "0022-538X",

publisher = "American Society for Microbiology",

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Shinde, PV, Xu, HC, Maney, SK, Kloetgen, A, Namineni, S, Zhuang, Y, Honke, N, Shaabani, N, Bellora, N, Doerrenberg, M, Trilling, M, Pozdeev, VI, van Rooijen, N, Scheu, S, Pfeffer, K, Crocker, PR, Tanaka, M, Duggimpudi, S, Knolle, P, Heikenwalder, M, Ruland, J, Mak, TW, Brenner, D, Pandyra, AA, Hoell, JI, Borkhardt, A, Häussinger, D, Lang, KS & Lang, PA 2018, 'Tumor necrosis factormediated survival of CD169⁺ cells promotes immune activation during vesicular stomatitis virus infection', Journal of Virology, vol. 92, no. 3, e01637-17. https://doi.org/10.1128/JVI.01637-17

TY - JOUR

T1 - Tumor necrosis factormediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection

AU - Shinde, Prashant V.

AU - Xu, Haifeng C.

AU - Maney, Sathish Kumar

AU - Kloetgen, Andreas

AU - Namineni, Sukumar

AU - Zhuang, Yuan

AU - Honke, Nadine

AU - Shaabani, Namir

AU - Bellora, Nicolas

AU - Doerrenberg, Mareike

AU - Trilling, Mirko

AU - Pozdeev, Vitaly I.

AU - van Rooijen, Nico

AU - Scheu, Stefanie

AU - Pfeffer, Klaus

AU - Crocker, Paul R.

AU - Tanaka, Masato

AU - Duggimpudi, Sujitha

AU - Knolle, Percy

AU - Heikenwalder, Mathias

AU - Ruland, Jürgen

AU - Mak, Tak W.

AU - Brenner, Dirk

AU - Pandyra, Aleksandra A.

AU - Hoell, Jessica I.

AU - Borkhardt, Arndt

AU - Häussinger, Dieter

AU - Lang, Karl S.

AU - Lang, Philipp A.

N1 - Funding Information: This study was supported by the Alexander von Humboldt Foundation (SKA2010), the German Research Council (SFB974, LA2558/3-1, LA2558/5-1, GRK1949, and TRR60), Jürgen Manchot Graduate School MOI II, and the NIH tetramer facility. D.B. is funded by the ATTRACT Programme (A14/BM/7632103/DBRRIL) and a CORE grant (C15/BM/ 10355103) from the National Research Fund Luxembourg (FNR). J.R. is funded by the DFG (SFB 1054/B01) and the ERC (FP7; grant agreement no. 322865). Publisher Copyright: © 2018 American Society for Microbiology.

PY - 2018/2/1

Y1 - 2018/2/1

N2 - Innate immune activation is essential to mount an effective antiviral response and to prime adaptive immunity. Although a crucial role of CD169+ cells during vesicular stomatitis virus (VSV) infections is increasingly recognized, factors regulating CD169+ cells during viral infections remain unclear. Here, we show that tumor necrosis factor is produced by CD11b+ Ly6C+ Ly6G+ cells following infection with VSV. The absence of TNF or TNF receptor 1 (TNFR1) resulted in reduced numbers of CD169+ cells and in reduced type I interferon (IFN-I) production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nuclei of CD169+ cells; this translocation was inhibited when the paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and development of severe disease. These findings indicate that TNF mediates the maintenance of CD169+ cells and innate and adaptive immune activation during VSV infection.

AB - Innate immune activation is essential to mount an effective antiviral response and to prime adaptive immunity. Although a crucial role of CD169+ cells during vesicular stomatitis virus (VSV) infections is increasingly recognized, factors regulating CD169+ cells during viral infections remain unclear. Here, we show that tumor necrosis factor is produced by CD11b+ Ly6C+ Ly6G+ cells following infection with VSV. The absence of TNF or TNF receptor 1 (TNFR1) resulted in reduced numbers of CD169+ cells and in reduced type I interferon (IFN-I) production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nuclei of CD169+ cells; this translocation was inhibited when the paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and development of severe disease. These findings indicate that TNF mediates the maintenance of CD169+ cells and innate and adaptive immune activation during VSV infection.

KW - Innate immunity

KW - Interferon

KW - Interferons

KW - MALT1

KW - NF-κB

KW - TNF

KW - Tumor necrosis factor

UR - http://www.scopus.com/inward/record.url?scp=85040672435&partnerID=8YFLogxK

UR - https://pubmed.ncbi.nlm.nih.gov/29142134

U2 - 10.1128/JVI.01637-17

DO - 10.1128/JVI.01637-17

M3 - Article

C2 - 29142134

AN - SCOPUS:85040672435

SN - 0022-538X

VL - 92

JO - Journal of Virology

JF - Journal of Virology

IS - 3

M1 - e01637-17

ER -

Tumor necrosis factormediated survival of CD169⁺ cells promotes immune activation during vesicular stomatitis virus infection

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Keywords

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