The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>

Previously, we demonstrated that the nasal administration of <i>Dolosigranulum pigrum</i> 040417 differentially modulated the respiratory innate immune response triggered by the activation of Toll-like receptor 2 in infant mice. In this work, we aimed to evaluate the beneficial effects o...

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Main Authors: Fernanda Raya Tonetti, Mikado Tomokiyo, Ramiro Ortiz Moyano, Sandra Quilodrán-Vega, Hikari Yamamuro, Paulraj Kanmani, Vyacheslav Melnikov, Shoichiro Kurata, Haruki Kitazawa, Julio Villena
Format: Article
Language:English
Published: MDPI AG 2021-06-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/6/1324
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author Fernanda Raya Tonetti
Mikado Tomokiyo
Ramiro Ortiz Moyano
Sandra Quilodrán-Vega
Hikari Yamamuro
Paulraj Kanmani
Vyacheslav Melnikov
Shoichiro Kurata
Haruki Kitazawa
Julio Villena
author_facet Fernanda Raya Tonetti
Mikado Tomokiyo
Ramiro Ortiz Moyano
Sandra Quilodrán-Vega
Hikari Yamamuro
Paulraj Kanmani
Vyacheslav Melnikov
Shoichiro Kurata
Haruki Kitazawa
Julio Villena
author_sort Fernanda Raya Tonetti
collection DOAJ
description Previously, we demonstrated that the nasal administration of <i>Dolosigranulum pigrum</i> 040417 differentially modulated the respiratory innate immune response triggered by the activation of Toll-like receptor 2 in infant mice. In this work, we aimed to evaluate the beneficial effects of <i>D. pigrum</i> 040417 in the context of <i>Streptococcus pneumoniae</i> infection and characterize the role of alveolar macrophages (AMs) in the immunomodulatory properties of this respiratory commensal bacterium. The nasal administration of <i>D. pigrum</i> 040417 to infant mice significantly increased their resistance to pneumococcal infection, differentially modulated respiratory cytokines production, and reduced lung injuries. These effects were associated to the ability of the 040417 strain to modulate AMs function. Depletion of AMs significantly reduced the capacity of the 040417 strain to improve both the reduction of pathogen loads and the protection against lung tissue damage. We also demonstrated that the immunomodulatory properties of <i>D. pigrum</i> are strain-specific, as <i>D. pigrum</i> 030918 was not able to modulate respiratory immunity or to increase the resistance of mice to an <i>S. pneumoniae</i> infection. These findings enhanced our knowledge regarding the immunological mechanisms involved in modulation of respiratory immunity induced by beneficial respiratory commensal bacteria and suggested that particular strains could be used as next-generation probiotics.
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spelling doaj.art-4f8d0e51c74b4d17b754748dd41a2b372023-11-22T00:38:03ZengMDPI AGMicroorganisms2076-26072021-06-0196132410.3390/microorganisms9061324The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>Fernanda Raya Tonetti0Mikado Tomokiyo1Ramiro Ortiz Moyano2Sandra Quilodrán-Vega3Hikari Yamamuro4Paulraj Kanmani5Vyacheslav Melnikov6Shoichiro Kurata7Haruki Kitazawa8Julio Villena9Laboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucumán 4000, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 980-8572, JapanLaboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucumán 4000, ArgentinaLaboratory of Food Microbiology, Faculty of Veterinary Sciences, University of Concepción, Chillán 3780000, ChileFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 980-8572, JapanFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 980-8572, JapanGabrichevsky Research Institute for Epidemiology and Microbiology, 125212 Moscow, RussiaLaboratory of Molecular Genetics, Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, JapanFood and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai 980-8572, JapanLaboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucumán 4000, ArgentinaPreviously, we demonstrated that the nasal administration of <i>Dolosigranulum pigrum</i> 040417 differentially modulated the respiratory innate immune response triggered by the activation of Toll-like receptor 2 in infant mice. In this work, we aimed to evaluate the beneficial effects of <i>D. pigrum</i> 040417 in the context of <i>Streptococcus pneumoniae</i> infection and characterize the role of alveolar macrophages (AMs) in the immunomodulatory properties of this respiratory commensal bacterium. The nasal administration of <i>D. pigrum</i> 040417 to infant mice significantly increased their resistance to pneumococcal infection, differentially modulated respiratory cytokines production, and reduced lung injuries. These effects were associated to the ability of the 040417 strain to modulate AMs function. Depletion of AMs significantly reduced the capacity of the 040417 strain to improve both the reduction of pathogen loads and the protection against lung tissue damage. We also demonstrated that the immunomodulatory properties of <i>D. pigrum</i> are strain-specific, as <i>D. pigrum</i> 030918 was not able to modulate respiratory immunity or to increase the resistance of mice to an <i>S. pneumoniae</i> infection. These findings enhanced our knowledge regarding the immunological mechanisms involved in modulation of respiratory immunity induced by beneficial respiratory commensal bacteria and suggested that particular strains could be used as next-generation probiotics.https://www.mdpi.com/2076-2607/9/6/1324respiratory commensal bacteriaupper respiratory tractnext-generation probiotics<i>Dolosigranulum pigrum</i><i>Streptococcus pneumoniae</i>alveolar macrophages
spellingShingle Fernanda Raya Tonetti
Mikado Tomokiyo
Ramiro Ortiz Moyano
Sandra Quilodrán-Vega
Hikari Yamamuro
Paulraj Kanmani
Vyacheslav Melnikov
Shoichiro Kurata
Haruki Kitazawa
Julio Villena
The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
Microorganisms
respiratory commensal bacteria
upper respiratory tract
next-generation probiotics
<i>Dolosigranulum pigrum</i>
<i>Streptococcus pneumoniae</i>
alveolar macrophages
title The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
title_full The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
title_fullStr The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
title_full_unstemmed The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
title_short The Respiratory Commensal Bacterium <i>Dolosigranulum pigrum</i> 040417 Improves the Innate Immune Response to <i>Streptococcus pneumoniae</i>
title_sort respiratory commensal bacterium i dolosigranulum pigrum i 040417 improves the innate immune response to i streptococcus pneumoniae i
topic respiratory commensal bacteria
upper respiratory tract
next-generation probiotics
<i>Dolosigranulum pigrum</i>
<i>Streptococcus pneumoniae</i>
alveolar macrophages
url https://www.mdpi.com/2076-2607/9/6/1324
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