Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice

Abstract Background Supplemental oxygen impairs lung development in newborn infants with respiratory distress. Lactobacillus johnsonii supplementation attenuates respiratory viral infection in mice and exhibits anti-inflammatory effects. This study investigated the protective effects of intranasal a...

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Main Authors: Chung-Ming Chen, Yu-Chen S. H. Yang, Hsiu-Chu Chou, Shan Lin
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Journal of Biomedical Science
Subjects:
Online Access:https://doi.org/10.1186/s12929-023-00958-8
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author Chung-Ming Chen
Yu-Chen S. H. Yang
Hsiu-Chu Chou
Shan Lin
author_facet Chung-Ming Chen
Yu-Chen S. H. Yang
Hsiu-Chu Chou
Shan Lin
author_sort Chung-Ming Chen
collection DOAJ
description Abstract Background Supplemental oxygen impairs lung development in newborn infants with respiratory distress. Lactobacillus johnsonii supplementation attenuates respiratory viral infection in mice and exhibits anti-inflammatory effects. This study investigated the protective effects of intranasal administration of L. johnsonii on lung development in hyperoxia-exposed neonatal mice. Methods Neonatal C57BL/6N mice were reared in either room air (RA) or hyperoxia condition (85% O2). From postnatal days 0 to 6, they were administered intranasal 10 μL L. johnsonii at a dose of 1 × 105 colony-forming units. Control mice received an equal volume of normal saline (NS). We evaluated the following four study groups: RA + NS, RA + probiotic, O2 + NS, and O2 + probiotic. On postnatal day 7, lung and intestinal microbiota were sampled from the left lung and lower gastrointestinal tract, respectively. The right lung of each mouse was harvested for Western blot, cytokine, and histology analyses. Results The O2 + NS group exhibited significantly lower body weight and vascular density and significantly higher mean linear intercept (MLI) and lung cytokine levels compared with the RA + NS and RA + probiotic groups. At the genus level of the gut microbiota, the O2 + NS group exhibited significantly higher Staphylococcus and Enterobacter abundance and significantly lower Lactobacillus abundance compared with the RA + NS and RA + probiotic groups. Intranasal L. johnsonii treatment increased the vascular density, decreased the MLI and cytokine levels, and restored the gut microbiota in hyperoxia-exposed neonatal mice. Conclusions Intranasal administration of L. johnsonii protects against hyperoxia-induced lung injury and modulates the gut microbiota.
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spelling doaj.art-ee97a516d5604f55ad4df7addee29f7a2023-08-06T11:21:35ZengBMCJournal of Biomedical Science1423-01272023-07-0130111310.1186/s12929-023-00958-8Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal miceChung-Ming Chen0Yu-Chen S. H. Yang1Hsiu-Chu Chou2Shan Lin3Department of Pediatrics, Taipei Medical University HospitalJoint Biobank, Office of Human Research, Taipei Medical UniversityDepartment of Anatomy and Cell Biology, School of Medicine, College of Medicine, Taipei Medical UniversityBiotech Research Institute, Grape King Bio Ltd.Abstract Background Supplemental oxygen impairs lung development in newborn infants with respiratory distress. Lactobacillus johnsonii supplementation attenuates respiratory viral infection in mice and exhibits anti-inflammatory effects. This study investigated the protective effects of intranasal administration of L. johnsonii on lung development in hyperoxia-exposed neonatal mice. Methods Neonatal C57BL/6N mice were reared in either room air (RA) or hyperoxia condition (85% O2). From postnatal days 0 to 6, they were administered intranasal 10 μL L. johnsonii at a dose of 1 × 105 colony-forming units. Control mice received an equal volume of normal saline (NS). We evaluated the following four study groups: RA + NS, RA + probiotic, O2 + NS, and O2 + probiotic. On postnatal day 7, lung and intestinal microbiota were sampled from the left lung and lower gastrointestinal tract, respectively. The right lung of each mouse was harvested for Western blot, cytokine, and histology analyses. Results The O2 + NS group exhibited significantly lower body weight and vascular density and significantly higher mean linear intercept (MLI) and lung cytokine levels compared with the RA + NS and RA + probiotic groups. At the genus level of the gut microbiota, the O2 + NS group exhibited significantly higher Staphylococcus and Enterobacter abundance and significantly lower Lactobacillus abundance compared with the RA + NS and RA + probiotic groups. Intranasal L. johnsonii treatment increased the vascular density, decreased the MLI and cytokine levels, and restored the gut microbiota in hyperoxia-exposed neonatal mice. Conclusions Intranasal administration of L. johnsonii protects against hyperoxia-induced lung injury and modulates the gut microbiota.https://doi.org/10.1186/s12929-023-00958-8ProbioticsHyperoxiaMean linear interceptVascular endothelial growth factorMicrobiota
spellingShingle Chung-Ming Chen
Yu-Chen S. H. Yang
Hsiu-Chu Chou
Shan Lin
Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
Journal of Biomedical Science
Probiotics
Hyperoxia
Mean linear intercept
Vascular endothelial growth factor
Microbiota
title Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
title_full Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
title_fullStr Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
title_full_unstemmed Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
title_short Intranasal administration of Lactobacillus johnsonii attenuates hyperoxia-induced lung injury by modulating gut microbiota in neonatal mice
title_sort intranasal administration of lactobacillus johnsonii attenuates hyperoxia induced lung injury by modulating gut microbiota in neonatal mice
topic Probiotics
Hyperoxia
Mean linear intercept
Vascular endothelial growth factor
Microbiota
url https://doi.org/10.1186/s12929-023-00958-8
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