Interleukin-22 Reduces Lung Inflammation during Influenza A Virus Infection and Protects against Secondary Bacterial Infection

Ivanov, Stoyan; Renneson, Joelle; Fontaine, Josette; Barthélémy, Adeline; Paget, Christophe; Fernandez, Elodie Macho; Blanc, Fany; Trez, Carl De; Maele, Laurye Van; Dumoutier, Laure; Huerre, M; Eberl, Gérard; Si‐Tahar, Mustapha; Gosset, Pierre; Renauld, Jean‐Christophe; Sirard, Jean‐Claude; Faveeuw, Christelle; Trottein, François

doi:10.1128/jvi.02943-12

Cited by 136 publications

(155 citation statements)

References 82 publications

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“…Secondary bacterial infections are a common phenomenon during an influenza pandemic because influenza-mediated immune suppression promotes pulmonary infection by bacteria (26). Interestingly, some bacterial infections, such as those caused by Propionibacterium acnes (27) and Bordetella pertussis (8), conversely confer resistance to a subsequent influenza infection.…”

Section: Discussionmentioning

confidence: 99%

Klebsiella pneumoniaeAlleviates Influenza-Induced Acute Lung Injury via Limiting NK Cell Expansion

Wang

Sun

et al. 2014

The Journal of Immunology

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A protective effect induced by bacterial preinfection upon a subsequent lethal influenza virus infection has been observed, but the underlying immune mechanisms have not yet been fully elucidated. In this study, we used a mouse model of Klebsiella pneumoniae preinfection to gain insight into how bacterial preinfection influences the subsequent lethal influenza virus infection. We found that K. pneumoniae preinfection significantly attenuated lung immune injury and decreased mortality during influenza virus infection, but K. pneumoniae–specific immunity was not involved in this cross-protection against influenza virus. K. pneumoniae preinfection limited NK cell expansion, which was involved in influenza-induced immune injury and death. Furthermore, K. pneumoniae preinfection could not control NK cell expansion and death during influenza virus infection in Rag1−/− mice, but adoptive transfer of T cells from wild-type mice was able to restore this protective effect. Our data suggest that the adaptive immune response activated by bacterial infection limits the excessive innate immune response induced by a subsequent influenza infection, ultimately protecting mice from death.

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Section: Discussionmentioning

confidence: 99%

Klebsiella pneumoniaeAlleviates Influenza-Induced Acute Lung Injury via Limiting NK Cell Expansion

Wang

Sun

et al. 2014

The Journal of Immunology

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“…Moreover, IL-22 promotes maintenance and repair of the epithelial barrier in the intestine and respiratory tract, thus limiting pathogen dissemination [2,3]. We and others have shown also that IL-22 is required for lung defence and repair after infection with influenza virus [23] or after co-infection with influenza and Streptococcus pneumoniae [4]. Hence IL-22 is critical for mucosal immunity against viral and bacterial infections.…”

Section: Discussionmentioning

confidence: 99%

“…8). 1) Cigarette smoke in the lungs contributes to neutrophil infiltration and degranulation, resulting in the release of active proteases; 2) Matrix components and soluble mediators are degraded, which generates products acting as pro-inflammatory stimuli in a feedback loop [10]; 3) CG and other neutrophil proteases degrade IL-22R and impair the downstream STAT3-dependent antimicrobial effectors; and 4) such protease-dependent disarming of the IL-22/IL-22R axis may facilitate the replication and spread of pathogens, especially bacteria [4] and consequently, may be detrimental in the setting of AE-COPD.…”

Section: Discussionmentioning

confidence: 99%

“…IL-22 is an unusual interleukin because it does not directly regulate the function of immune cells and instead targets cells at barriers that separate the body from its external environment, such as the respiratory epithelium. We and others previously demonstrated that IL-22 protects and regenerates respiratory epithelial cells upon infection with influenza virus and limits secondary bacterial infections [4]. COPD is also characterised by high numbers of leukocytes, such as neutrophils in the lungs [5,6].…”

Section: Introductionmentioning

confidence: 99%

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Neutrophil proteases alter the interleukin-22-receptor-dependent lung antimicrobial defence

et al. 2015

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Chronic obstructive pulmonary disease (COPD) is punctuated by episodes of infectiondriven acute exacerbations. Despite the life-threatening nature of these exacerbations, the underlying mechanisms remain unclear, although a high number of neutrophils in the lungs of COPD patients is known to correlate with poor prognosis. Interleukin (IL)-22 is a cytokine that plays a pivotal role in lung antimicrobial defence and tissue protection. We hypothesised that neutrophils secrete proteases that may have adverse effects in COPD, by altering the IL-22 receptor (IL-22R)-dependent signalling.Using in vitro and in vivo approaches as well as reverse transcriptase quantitative PCR, flow cytometry and/or Western blotting techniques, we first showed that pathogens such as the influenza virus promote IL-22R expression in human bronchial epithelial cells, whereas Pseudomonas aeruginosa, bacterial lipopolysaccharide or cigarette smoke do not. Most importantly, neutrophil proteases cleave IL-22R and impair IL-22-dependent immune signalling and expression of antimicrobial effectors such as β-defensin-2. This proteolysis resulted in the release of a soluble fragment of IL-22R, which was detectable both in cellular and animal models as well as in sputa from COPD patients with acute exacerbations.Hence, our study reveals an unsuspected regulation by the proteolytic action of neutrophil enzymes of IL-22-dependent lung host response. This process probably enhances pathogen replication, and ultimately COPD exacerbations. @ERSpublications Neutrophil proteases alter lung antimicrobial defence and may predispose to infection-triggered COPD exacerbations http://ow.ly/MHqEt

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“…We have shown that IL-22 from type 3 innate lymphoid cells (ILC3s) is protective against ConA-induced hepatitis (12). In the lung, IL-22 has been reported to reduce inflammation during influenza A virus infection (13) and to be protective against secondary bacterial infection (14). In addition, IL-22 has been shown to be essential for lung repair after influenza A infection (15).…”

Section: Introductionmentioning

confidence: 99%

Innate-like function of memory Th17 cells for enhancing endotoxin-induced acute lung inflammation through IL-22

Sakaguchi

Chikuma

Shichita

et al. 2015

International Immunology

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Interleukin-22 Reduces Lung Inflammation during Influenza A Virus Infection and Protects against Secondary Bacterial Infection

Cited by 136 publications

References 82 publications

Klebsiella pneumoniaeAlleviates Influenza-Induced Acute Lung Injury via Limiting NK Cell Expansion

Klebsiella pneumoniaeAlleviates Influenza-Induced Acute Lung Injury via Limiting NK Cell Expansion

Neutrophil proteases alter the interleukin-22-receptor-dependent lung antimicrobial defence

Innate-like function of memory Th17 cells for enhancing endotoxin-induced acute lung inflammation through IL-22

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