Tumor Necrosis Factor-mediated 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

Research output: Contribution to journalArticle

7 Citations (Scopus)
119 Downloads (Pure)

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 IFN-I production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nucleus of CD169(+) cells; this translocation was inhibited when paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and severe disease development. These findings indicate that TNF mediates the maintenance of CD169(+) cells and innate and adaptive immune activation during VSV infection.IMPORTANCE Over the last decade, strategically placed CD169(+) metallophilic macrophages in the marginal zone of the murine spleen and LN have been shown to play a very important role in host defense against viral pathogens. CD169(+) macrophages are shown to activate innate and adaptive immunity via "enforced virus replication" a controlled amplification of virus particles. However, factors regulating the CD169(+) macrophages remain to be studied. In this paper, we show that after Vesicular stomatitis virus infection, phagocytes produce tumor necrosis factor (TNF) which signals via TNFR1 and promote "enforced virus replication" in CD169(+) macrophages. Consequently, lack of TNF or TNFR1 resulted in defective immune activation and VSV clearance.

Original languageEnglish
Article numbere01637-17
Pages (from-to)1-18
Number of pages18
JournalJournal of Virology
Volume92
Issue number3
Early online date15 Nov 2017
DOIs
Publication statusPublished - Feb 2018

Fingerprint

Vesiculovirus
Vesicular Stomatitis
tumor necrosis factors
Virus Diseases
cell viability
Cell Survival
Tumor Necrosis Factor-alpha
Tumor Necrosis Factor Receptors
infection
macrophages
Virus Replication
virus replication
Macrophages
Adaptive Immunity
receptors
cells
Viruses
phagocytes
cell nucleus
Phagocytes

Keywords

  • TNF
  • MALT1
  • Innate immunity
  • Interferon
  • NF-κB
  • Interferons
  • Tumor necrosis factor
  • Adaptive Immunity
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein/genetics
  • Transcription Factor RelA/metabolism
  • Mice, Inbred C57BL
  • Vesiculovirus/physiology
  • Macrophages/immunology
  • Immunity, Innate
  • Tumor Necrosis Factor-alpha/immunology
  • Animals
  • Virus Replication
  • Vesicular Stomatitis/immunology
  • Interferon Type I/immunology
  • Mice
  • Receptors, Tumor Necrosis Factor, Type I/immunology
  • Sialic Acid Binding Ig-like Lectin 1

Cite this

Shinde, P. V., Xu, H. C., Maney, S. K., Kloetgen, A., Namineni, S., Zhuang, Y., ... Lang, P. A. (2018). Tumor Necrosis Factor-mediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection. Journal of Virology, 92(3), 1-18. [e01637-17]. https://doi.org/10.1128/JVI.01637-17
Shinde, Prashant V. ; Xu, Haifeng C. ; Maney, Sathish Kumar ; Kloetgen, Andreas ; Namineni, Sukumar ; Zhuang, Yuan ; Honke, Nadine ; Shaabani, Namir ; Bellora, Nicolas ; Doerrenberg, Mareike ; Trilling, Mirko ; Pozdeev, Vitaly I. ; van Rooijen, Nico ; Scheu, Stefanie ; Pfeffer, Klaus ; Crocker, Paul R. ; Tanaka, Masato ; Duggimpudi, Sujitha ; Knolle, Percy ; Heikenwalder, Mathias ; Ruland, Jürgen ; Mak, Tak W. ; Brenner, Dirk ; Pandyra, Aleksandra A. ; Hoell, Jessica I. ; Borkhardt, Arndt ; Häussinger, Dieter ; Lang, Karl S. ; Lang, Philipp A. / Tumor Necrosis Factor-mediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection. In: Journal of Virology. 2018 ; Vol. 92, No. 3. pp. 1-18.
@article{4322ba9a6ecf4ad5a17a870fd265a2ca,
title = "Tumor Necrosis Factor-mediated 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 IFN-I production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nucleus of CD169(+) cells; this translocation was inhibited when paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and severe disease development. These findings indicate that TNF mediates the maintenance of CD169(+) cells and innate and adaptive immune activation during VSV infection.IMPORTANCE Over the last decade, strategically placed CD169(+) metallophilic macrophages in the marginal zone of the murine spleen and LN have been shown to play a very important role in host defense against viral pathogens. CD169(+) macrophages are shown to activate innate and adaptive immunity via {"}enforced virus replication{"} a controlled amplification of virus particles. However, factors regulating the CD169(+) macrophages remain to be studied. In this paper, we show that after Vesicular stomatitis virus infection, phagocytes produce tumor necrosis factor (TNF) which signals via TNFR1 and promote {"}enforced virus replication{"} in CD169(+) macrophages. Consequently, lack of TNF or TNFR1 resulted in defective immune activation and VSV clearance.",
keywords = "TNF, MALT1, Innate immunity, Interferon, NF-κB, Interferons, Tumor necrosis factor, Adaptive Immunity, Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein/genetics, Transcription Factor RelA/metabolism, Mice, Inbred C57BL, Vesiculovirus/physiology, Macrophages/immunology, Immunity, Innate, Tumor Necrosis Factor-alpha/immunology, Animals, Virus Replication, Vesicular Stomatitis/immunology, Interferon Type I/immunology, Mice, Receptors, Tumor Necrosis Factor, Type I/immunology, Sialic Acid Binding Ig-like Lectin 1",
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 = "This study was supported by the Alexander von Humboldt Foundation (SKA2010), the German Research Council (SFB974,LA2558/3-1,LA2558/5-1,GRK1949 & TRR60), the J{\"u}rgen Manchot Graduate School MOIII, and the NIHtetramer facility. D.B. is funded by the ATTRACT Programme (A14/BM/7632103/DBRRIL) and a CORE grant (C15/BM/10355103) of the National Research Fund Luxembourg (FNR).",
year = "2018",
month = "2",
doi = "10.1128/JVI.01637-17",
language = "English",
volume = "92",
pages = "1--18",
journal = "Journal of Virology",
issn = "0022-538X",
publisher = "American Society for Microbiology",
number = "3",

}

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 Factor-mediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection', Journal of Virology, vol. 92, no. 3, e01637-17, pp. 1-18. https://doi.org/10.1128/JVI.01637-17

Tumor Necrosis Factor-mediated survival of CD169+ cells promotes immune activation during vesicular stomatitis virus infection. / Shinde, Prashant V.; Xu, Haifeng C.; Maney, Sathish Kumar; Kloetgen, Andreas; Namineni, Sukumar; Zhuang, Yuan; Honke, Nadine; Shaabani, Namir; Bellora, Nicolas; Doerrenberg, Mareike; Trilling, Mirko; Pozdeev, Vitaly I.; van Rooijen, Nico; Scheu, Stefanie; Pfeffer, Klaus; Crocker, Paul R.; Tanaka, Masato; Duggimpudi, Sujitha; Knolle, Percy; Heikenwalder, Mathias; Ruland, Jürgen; Mak, Tak W.; Brenner, Dirk; Pandyra, Aleksandra A.; Hoell, Jessica I.; Borkhardt, Arndt; Häussinger, Dieter; Lang, Karl S.; Lang, Philipp A. (Lead / Corresponding author).

In: Journal of Virology, Vol. 92, No. 3, e01637-17, 02.2018, p. 1-18.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Tumor Necrosis Factor-mediated 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 - This study was supported by the Alexander von Humboldt Foundation (SKA2010), the German Research Council (SFB974,LA2558/3-1,LA2558/5-1,GRK1949 & TRR60), the Jürgen Manchot Graduate School MOIII, and the NIHtetramer facility. D.B. is funded by the ATTRACT Programme (A14/BM/7632103/DBRRIL) and a CORE grant (C15/BM/10355103) of the National Research Fund Luxembourg (FNR).

PY - 2018/2

Y1 - 2018/2

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 IFN-I production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nucleus of CD169(+) cells; this translocation was inhibited when paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and severe disease development. These findings indicate that TNF mediates the maintenance of CD169(+) cells and innate and adaptive immune activation during VSV infection.IMPORTANCE Over the last decade, strategically placed CD169(+) metallophilic macrophages in the marginal zone of the murine spleen and LN have been shown to play a very important role in host defense against viral pathogens. CD169(+) macrophages are shown to activate innate and adaptive immunity via "enforced virus replication" a controlled amplification of virus particles. However, factors regulating the CD169(+) macrophages remain to be studied. In this paper, we show that after Vesicular stomatitis virus infection, phagocytes produce tumor necrosis factor (TNF) which signals via TNFR1 and promote "enforced virus replication" in CD169(+) macrophages. Consequently, lack of TNF or TNFR1 resulted in defective immune activation and VSV clearance.

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 IFN-I production during VSV infection, with a severe disease outcome. Specifically, TNF triggered RelA translocation into the nucleus of CD169(+) cells; this translocation was inhibited when paracaspase MALT-1 was absent. Consequently, MALT1 deficiency resulted in reduced VSV replication, defective innate immune activation, and severe disease development. These findings indicate that TNF mediates the maintenance of CD169(+) cells and innate and adaptive immune activation during VSV infection.IMPORTANCE Over the last decade, strategically placed CD169(+) metallophilic macrophages in the marginal zone of the murine spleen and LN have been shown to play a very important role in host defense against viral pathogens. CD169(+) macrophages are shown to activate innate and adaptive immunity via "enforced virus replication" a controlled amplification of virus particles. However, factors regulating the CD169(+) macrophages remain to be studied. In this paper, we show that after Vesicular stomatitis virus infection, phagocytes produce tumor necrosis factor (TNF) which signals via TNFR1 and promote "enforced virus replication" in CD169(+) macrophages. Consequently, lack of TNF or TNFR1 resulted in defective immune activation and VSV clearance.

KW - TNF

KW - MALT1

KW - Innate immunity

KW - Interferon

KW - NF-κB

KW - Interferons

KW - Tumor necrosis factor

KW - Adaptive Immunity

KW - Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein/genetics

KW - Transcription Factor RelA/metabolism

KW - Mice, Inbred C57BL

KW - Vesiculovirus/physiology

KW - Macrophages/immunology

KW - Immunity, Innate

KW - Tumor Necrosis Factor-alpha/immunology

KW - Animals

KW - Virus Replication

KW - Vesicular Stomatitis/immunology

KW - Interferon Type I/immunology

KW - Mice

KW - Receptors, Tumor Necrosis Factor, Type I/immunology

KW - Sialic Acid Binding Ig-like Lectin 1

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

U2 - 10.1128/JVI.01637-17

DO - 10.1128/JVI.01637-17

M3 - Article

C2 - 29142134

VL - 92

SP - 1

EP - 18

JO - Journal of Virology

JF - Journal of Virology

SN - 0022-538X

IS - 3

M1 - e01637-17

ER -