Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia

Koenraad F. Van Der Sluijs, Monique Nijhuis, Johannes H M Levels, Sandrine Florquin, Andrew L. Mellor, Henk M. Jansen, Tom Van Der Poll, René Lutter

Research output: Contribution to journalArticle

71 Citations (Scopus)

Abstract

Background. Airway infection with influenza virus induces local expression of the tryptophan-catabolizing enzyme indoleamine 2,3-dioxygenase (IDO), which has been shown to enhance inflammatory mediator responses in vitro. Because secondary pneumococcal infections occurring shortly after recovery from influenza are associated with enhanced inflammatory responses, we hypothesized that IDO activity contributes to the enhanced response to bacterial challenges in mice previously infected with influenza virus. Methods. On day 14 after influenza virus infection (with strain A/PR/8/34), C57B1/6 mice were intranasally inoculated with 1 × 104 colony-forming units of S. pneumoniae (serotype 3). Matrix-driven delivery pellets that contained 70 mg of the IDO inhibitor 1-methyl-DL-tryptophan (MeTrp) released over a period of 7 days were subcutaneously implanted 48 h before pneumococcal infection. Results. MeTrp treatment resulted in a 20-fold reduction in pneumococcal outgrowth 48 h after bacterial inoculation. Remarkably, pulmonary levels of interleukin-10 and tumor necrosis factor-α were significantly reduced in mice treated with MeTrp. Conclusions. Our data suggest that IDO expression during influenza virus infection alters the inflammatory response and facilitates the outgrowth of pneumococci during secondary bacterial pneumonia.

Original languageEnglish (US)
Pages (from-to)214-222
Number of pages9
JournalJournal of Infectious Diseases
Volume193
Issue number2
DOIs
StatePublished - Jan 15 2006

Fingerprint

Pneumococcal Pneumonia
Indoleamine-Pyrrole 2,3,-Dioxygenase
Orthomyxoviridae
Interleukin-10
Human Influenza
Pneumococcal Infections
Virus Diseases
Bacterial Pneumonia
Streptococcus pneumoniae
Coinfection
Tryptophan
Pneumonia
Stem Cells
Tumor Necrosis Factor-alpha
Lung
Enzymes
Infection
tryptophan methyl ester

ASJC Scopus subject areas

  • Immunology and Allergy
  • Infectious Diseases

Cite this

Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia. / Van Der Sluijs, Koenraad F.; Nijhuis, Monique; Levels, Johannes H M; Florquin, Sandrine; Mellor, Andrew L.; Jansen, Henk M.; Van Der Poll, Tom; Lutter, René.

In: Journal of Infectious Diseases, Vol. 193, No. 2, 15.01.2006, p. 214-222.

Research output: Contribution to journalArticle

Van Der Sluijs, KF, Nijhuis, M, Levels, JHM, Florquin, S, Mellor, AL, Jansen, HM, Van Der Poll, T & Lutter, R 2006, 'Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia', Journal of Infectious Diseases, vol. 193, no. 2, pp. 214-222. https://doi.org/10.1086/498911
Van Der Sluijs, Koenraad F. ; Nijhuis, Monique ; Levels, Johannes H M ; Florquin, Sandrine ; Mellor, Andrew L. ; Jansen, Henk M. ; Van Der Poll, Tom ; Lutter, René. / Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia. In: Journal of Infectious Diseases. 2006 ; Vol. 193, No. 2. pp. 214-222.
@article{eed528213d5f445bbe42dba609d7e29f,
title = "Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia",
abstract = "Background. Airway infection with influenza virus induces local expression of the tryptophan-catabolizing enzyme indoleamine 2,3-dioxygenase (IDO), which has been shown to enhance inflammatory mediator responses in vitro. Because secondary pneumococcal infections occurring shortly after recovery from influenza are associated with enhanced inflammatory responses, we hypothesized that IDO activity contributes to the enhanced response to bacterial challenges in mice previously infected with influenza virus. Methods. On day 14 after influenza virus infection (with strain A/PR/8/34), C57B1/6 mice were intranasally inoculated with 1 × 104 colony-forming units of S. pneumoniae (serotype 3). Matrix-driven delivery pellets that contained 70 mg of the IDO inhibitor 1-methyl-DL-tryptophan (MeTrp) released over a period of 7 days were subcutaneously implanted 48 h before pneumococcal infection. Results. MeTrp treatment resulted in a 20-fold reduction in pneumococcal outgrowth 48 h after bacterial inoculation. Remarkably, pulmonary levels of interleukin-10 and tumor necrosis factor-α were significantly reduced in mice treated with MeTrp. Conclusions. Our data suggest that IDO expression during influenza virus infection alters the inflammatory response and facilitates the outgrowth of pneumococci during secondary bacterial pneumonia.",
author = "{Van Der Sluijs}, {Koenraad F.} and Monique Nijhuis and Levels, {Johannes H M} and Sandrine Florquin and Mellor, {Andrew L.} and Jansen, {Henk M.} and {Van Der Poll}, Tom and Ren{\'e} Lutter",
year = "2006",
month = "1",
day = "15",
doi = "10.1086/498911",
language = "English (US)",
volume = "193",
pages = "214--222",
journal = "Journal of Infectious Diseases",
issn = "0022-1899",
publisher = "Oxford University Press",
number = "2",

}

TY - JOUR

T1 - Influenza-induced expression of indoleamine 2,3-dioxygenase enhances interleukin-10 production and bacterial outgrowth during secondary pneumococcal pneumonia

AU - Van Der Sluijs, Koenraad F.

AU - Nijhuis, Monique

AU - Levels, Johannes H M

AU - Florquin, Sandrine

AU - Mellor, Andrew L.

AU - Jansen, Henk M.

AU - Van Der Poll, Tom

AU - Lutter, René

PY - 2006/1/15

Y1 - 2006/1/15

N2 - Background. Airway infection with influenza virus induces local expression of the tryptophan-catabolizing enzyme indoleamine 2,3-dioxygenase (IDO), which has been shown to enhance inflammatory mediator responses in vitro. Because secondary pneumococcal infections occurring shortly after recovery from influenza are associated with enhanced inflammatory responses, we hypothesized that IDO activity contributes to the enhanced response to bacterial challenges in mice previously infected with influenza virus. Methods. On day 14 after influenza virus infection (with strain A/PR/8/34), C57B1/6 mice were intranasally inoculated with 1 × 104 colony-forming units of S. pneumoniae (serotype 3). Matrix-driven delivery pellets that contained 70 mg of the IDO inhibitor 1-methyl-DL-tryptophan (MeTrp) released over a period of 7 days were subcutaneously implanted 48 h before pneumococcal infection. Results. MeTrp treatment resulted in a 20-fold reduction in pneumococcal outgrowth 48 h after bacterial inoculation. Remarkably, pulmonary levels of interleukin-10 and tumor necrosis factor-α were significantly reduced in mice treated with MeTrp. Conclusions. Our data suggest that IDO expression during influenza virus infection alters the inflammatory response and facilitates the outgrowth of pneumococci during secondary bacterial pneumonia.

AB - Background. Airway infection with influenza virus induces local expression of the tryptophan-catabolizing enzyme indoleamine 2,3-dioxygenase (IDO), which has been shown to enhance inflammatory mediator responses in vitro. Because secondary pneumococcal infections occurring shortly after recovery from influenza are associated with enhanced inflammatory responses, we hypothesized that IDO activity contributes to the enhanced response to bacterial challenges in mice previously infected with influenza virus. Methods. On day 14 after influenza virus infection (with strain A/PR/8/34), C57B1/6 mice were intranasally inoculated with 1 × 104 colony-forming units of S. pneumoniae (serotype 3). Matrix-driven delivery pellets that contained 70 mg of the IDO inhibitor 1-methyl-DL-tryptophan (MeTrp) released over a period of 7 days were subcutaneously implanted 48 h before pneumococcal infection. Results. MeTrp treatment resulted in a 20-fold reduction in pneumococcal outgrowth 48 h after bacterial inoculation. Remarkably, pulmonary levels of interleukin-10 and tumor necrosis factor-α were significantly reduced in mice treated with MeTrp. Conclusions. Our data suggest that IDO expression during influenza virus infection alters the inflammatory response and facilitates the outgrowth of pneumococci during secondary bacterial pneumonia.

UR - http://www.scopus.com/inward/record.url?scp=30944440041&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=30944440041&partnerID=8YFLogxK

U2 - 10.1086/498911

DO - 10.1086/498911

M3 - Article

C2 - 16362885

AN - SCOPUS:30944440041

VL - 193

SP - 214

EP - 222

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

SN - 0022-1899

IS - 2

ER -