Perinatal maternal antibiotic exposure augments lung injury in offspring in experimental bronchopulmonary dysplasia

Am J Physiol Lung Cell Mol Physiol. 2020 Feb 1;318(2):L407-L418. doi: 10.1152/ajplung.00561.2018. Epub 2019 Oct 23.

Abstract

During the newborn period, intestinal commensal bacteria influence pulmonary mucosal immunology via the gut-lung axis. Epidemiological studies have linked perinatal antibiotic exposure in human newborns to an increased risk for bronchopulmonary dysplasia, but whether this effect is mediated by the gut-lung axis is unknown. To explore antibiotic disruption of the newborn gut-lung axis, we studied how perinatal maternal antibiotic exposure influenced lung injury in a hyperoxia-based mouse model of bronchopulmonary dysplasia. We report that disruption of intestinal commensal colonization during the perinatal period promotes a more severe bronchopulmonary dysplasia phenotype characterized by increased mortality and pulmonary fibrosis. Mechanistically, metagenomic shifts were associated with decreased IL-22 expression in bronchoalveolar lavage and were independent of hyperoxia-induced inflammasome activation. Collectively, these results demonstrate a previously unrecognized influence of the gut-lung axis during the development of neonatal lung injury, which could be leveraged to ameliorate the most severe and persistent pulmonary complication of preterm birth.

Keywords: gut-lung axis; interleukin-22; microbiome; mucosal immunology; pulmonary fibrosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Airway Resistance / drug effects
  • Animals
  • Animals, Newborn
  • Anti-Bacterial Agents / adverse effects*
  • Bronchoalveolar Lavage Fluid
  • Bronchopulmonary Dysplasia / complications*
  • Bronchopulmonary Dysplasia / physiopathology
  • Cytokines / metabolism
  • Female
  • Granulocytes / metabolism
  • Hyperoxia / complications
  • Hyperoxia / physiopathology
  • Inflammasomes / metabolism
  • Leukocyte Common Antigens / metabolism
  • Lung / pathology
  • Lung Injury / chemically induced*
  • Lung Injury / microbiology
  • Lung Injury / physiopathology
  • Maternal Exposure*
  • Mice, Inbred C57BL
  • Oxygen / metabolism
  • Phenotype
  • Pregnancy
  • Prenatal Exposure Delayed Effects / pathology*
  • Prenatal Exposure Delayed Effects / physiopathology
  • Pulmonary Fibrosis / complications
  • Pulmonary Fibrosis / microbiology
  • Survival Analysis
  • Vascular Remodeling / drug effects

Substances

  • Anti-Bacterial Agents
  • Cytokines
  • Inflammasomes
  • Leukocyte Common Antigens
  • Oxygen