A novel IL-17-dependent mechanism of cross protection

Respiratory infection with mycoplasma protects against a secondary listeria infection

Amy N. Sieve, Karen D. Meeks, Sheetal Bodhankar, Suheung Lee, Jay K. Kolls, Jerry W. Simecka, Rance E. Berg

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Immune responses to pathogens occur within the context of current and previous infections. Cross protection refers to the phenomena where infection with a particular pathogen provides enhanced resistance to a subsequent unrelated pathogen in an antigen-independent manner. Proposed mechanisms of antigen-independent cross protection have involved the secretion of IFN-γ, which activates macrophages, thus providing enhanced innate immunity against the secondary viral or bacterial pathogen. Here we provide evidence that a primary infection with the chronic respiratory pathogen, Mycoplasma pulmonis, provides a novel form of cross protection against a secondary infection with Listeria monocytogenes that is not mediated by IFN-γ, but instead relies upon IL-17 and mobilization of neutrophils. Mice infected with M. pulmonis have enhanced clearance of L. monocytogenes from the spleen and liver, which is associated with increased numbers of Gr-1+CD11b+ cells and higher levels of IL-17. This enhanced clearance of L. monocytogenes was absent in mice depleted of Gr-1+ cells or in mice deficient in the IL-17 receptor. Additionally, both the IL-17 receptor and neutrophils were essential for optimal clearance of M. pulmonis. Tbus, a natural component of the immune response directed against M. pulmonis was able to enhance clearance of L. monocytogene.

Original languageEnglish (US)
Pages (from-to)426-438
Number of pages13
JournalEuropean Journal of Immunology
Volume39
Issue number2
DOIs
StatePublished - 2009
Externally publishedYes

Fingerprint

Mycoplasma pulmonis
Cross Protection
Listeriosis
Interleukin-17
Mycoplasma
Coinfection
Respiratory Tract Infections
Interleukin-17 Receptors
Listeria monocytogenes
Neutrophils
Infection
Antigens
Innate Immunity
Spleen
Macrophages
Liver

Keywords

  • Bacterial infection
  • Cytokine
  • Cytokine receptor
  • Neutrophil

ASJC Scopus subject areas

  • Immunology
  • Immunology and Allergy

Cite this

A novel IL-17-dependent mechanism of cross protection : Respiratory infection with mycoplasma protects against a secondary listeria infection. / Sieve, Amy N.; Meeks, Karen D.; Bodhankar, Sheetal; Lee, Suheung; Kolls, Jay K.; Simecka, Jerry W.; Berg, Rance E.

In: European Journal of Immunology, Vol. 39, No. 2, 2009, p. 426-438.

Research output: Contribution to journalArticle

Sieve, Amy N. ; Meeks, Karen D. ; Bodhankar, Sheetal ; Lee, Suheung ; Kolls, Jay K. ; Simecka, Jerry W. ; Berg, Rance E. / A novel IL-17-dependent mechanism of cross protection : Respiratory infection with mycoplasma protects against a secondary listeria infection. In: European Journal of Immunology. 2009 ; Vol. 39, No. 2. pp. 426-438.
@article{62360c28ee5d4e1a8300fe7470912dc1,
title = "A novel IL-17-dependent mechanism of cross protection: Respiratory infection with mycoplasma protects against a secondary listeria infection",
abstract = "Immune responses to pathogens occur within the context of current and previous infections. Cross protection refers to the phenomena where infection with a particular pathogen provides enhanced resistance to a subsequent unrelated pathogen in an antigen-independent manner. Proposed mechanisms of antigen-independent cross protection have involved the secretion of IFN-γ, which activates macrophages, thus providing enhanced innate immunity against the secondary viral or bacterial pathogen. Here we provide evidence that a primary infection with the chronic respiratory pathogen, Mycoplasma pulmonis, provides a novel form of cross protection against a secondary infection with Listeria monocytogenes that is not mediated by IFN-γ, but instead relies upon IL-17 and mobilization of neutrophils. Mice infected with M. pulmonis have enhanced clearance of L. monocytogenes from the spleen and liver, which is associated with increased numbers of Gr-1+CD11b+ cells and higher levels of IL-17. This enhanced clearance of L. monocytogenes was absent in mice depleted of Gr-1+ cells or in mice deficient in the IL-17 receptor. Additionally, both the IL-17 receptor and neutrophils were essential for optimal clearance of M. pulmonis. Tbus, a natural component of the immune response directed against M. pulmonis was able to enhance clearance of L. monocytogene.",
keywords = "Bacterial infection, Cytokine, Cytokine receptor, Neutrophil",
author = "Sieve, {Amy N.} and Meeks, {Karen D.} and Sheetal Bodhankar and Suheung Lee and Kolls, {Jay K.} and Simecka, {Jerry W.} and Berg, {Rance E.}",
year = "2009",
doi = "10.1002/eji.200838726",
language = "English (US)",
volume = "39",
pages = "426--438",
journal = "European Journal of Immunology",
issn = "0014-2980",
publisher = "Wiley-VCH Verlag",
number = "2",

}

TY - JOUR

T1 - A novel IL-17-dependent mechanism of cross protection

T2 - Respiratory infection with mycoplasma protects against a secondary listeria infection

AU - Sieve, Amy N.

AU - Meeks, Karen D.

AU - Bodhankar, Sheetal

AU - Lee, Suheung

AU - Kolls, Jay K.

AU - Simecka, Jerry W.

AU - Berg, Rance E.

PY - 2009

Y1 - 2009

N2 - Immune responses to pathogens occur within the context of current and previous infections. Cross protection refers to the phenomena where infection with a particular pathogen provides enhanced resistance to a subsequent unrelated pathogen in an antigen-independent manner. Proposed mechanisms of antigen-independent cross protection have involved the secretion of IFN-γ, which activates macrophages, thus providing enhanced innate immunity against the secondary viral or bacterial pathogen. Here we provide evidence that a primary infection with the chronic respiratory pathogen, Mycoplasma pulmonis, provides a novel form of cross protection against a secondary infection with Listeria monocytogenes that is not mediated by IFN-γ, but instead relies upon IL-17 and mobilization of neutrophils. Mice infected with M. pulmonis have enhanced clearance of L. monocytogenes from the spleen and liver, which is associated with increased numbers of Gr-1+CD11b+ cells and higher levels of IL-17. This enhanced clearance of L. monocytogenes was absent in mice depleted of Gr-1+ cells or in mice deficient in the IL-17 receptor. Additionally, both the IL-17 receptor and neutrophils were essential for optimal clearance of M. pulmonis. Tbus, a natural component of the immune response directed against M. pulmonis was able to enhance clearance of L. monocytogene.

AB - Immune responses to pathogens occur within the context of current and previous infections. Cross protection refers to the phenomena where infection with a particular pathogen provides enhanced resistance to a subsequent unrelated pathogen in an antigen-independent manner. Proposed mechanisms of antigen-independent cross protection have involved the secretion of IFN-γ, which activates macrophages, thus providing enhanced innate immunity against the secondary viral or bacterial pathogen. Here we provide evidence that a primary infection with the chronic respiratory pathogen, Mycoplasma pulmonis, provides a novel form of cross protection against a secondary infection with Listeria monocytogenes that is not mediated by IFN-γ, but instead relies upon IL-17 and mobilization of neutrophils. Mice infected with M. pulmonis have enhanced clearance of L. monocytogenes from the spleen and liver, which is associated with increased numbers of Gr-1+CD11b+ cells and higher levels of IL-17. This enhanced clearance of L. monocytogenes was absent in mice depleted of Gr-1+ cells or in mice deficient in the IL-17 receptor. Additionally, both the IL-17 receptor and neutrophils were essential for optimal clearance of M. pulmonis. Tbus, a natural component of the immune response directed against M. pulmonis was able to enhance clearance of L. monocytogene.

KW - Bacterial infection

KW - Cytokine

KW - Cytokine receptor

KW - Neutrophil

UR - http://www.scopus.com/inward/record.url?scp=60749095713&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=60749095713&partnerID=8YFLogxK

U2 - 10.1002/eji.200838726

DO - 10.1002/eji.200838726

M3 - Article

VL - 39

SP - 426

EP - 438

JO - European Journal of Immunology

JF - European Journal of Immunology

SN - 0014-2980

IS - 2

ER -