Ozone-induced airway epithelial cell death, the neurokinin-1 receptor pathway, and the postnatal developing lung

Am J Physiol Lung Cell Mol Physiol. 2014 Sep 15;307(6):L471-81. doi: 10.1152/ajplung.00324.2013. Epub 2014 Jul 25.

Abstract

Children are uniquely susceptible to ozone because airway and lung growth continue for an extensive period after birth. Early-life exposure of the rhesus monkey to repeated ozone cycles results in region-specific disrupted airway/lung growth, but the mediators and mechanisms are poorly understood. Substance P (SP), neurokinin-1 receptor (NK-1R); and nuclear receptor Nur77 (NR4A1) are signaling pathway components involved in ozone-induced cell death. We hypothesize that acute ozone (AO) exposure during postnatal airway development disrupts SP/NK-1R/Nur77 pathway expression and that these changes correlate with increased ozone-induced cell death. Our objectives were to 1) spatially define the normal development of the SP/NK-1R/Nur77 pathway in conducting airways; 2) compare how postnatal age modulates responses to AO exposure; and 3) determine how concomitant, episodic ozone exposure modifies age-specific acute responses. Male infant rhesus monkeys were assigned at age 1 mo to two age groups, 2 or 6 mo, and then to one of three exposure subgroups: filtered air (FA), FA+AO (AO: 8 h/day × 2 days), or episodic biweekly ozone exposure cycles (EAO: 8 h/day × 5 days/14-day cycle+AO). O3 = 0.5 ppm. We found that 1) ozone increases SP/NK-1R/Nur77 pathway expression in conducting airways, 2) an ozone exposure cycle (5 days/cycle) delivered early at age 2 mo resulted in an airway that was hypersensitive to AO exposure at the end of 2 mo, and 3) continued episodic exposure (11 cycles) resulted in an airway that was hyposensitive to AO exposure at 6 mo. These observations collectively associate with greater overall inflammation and epithelial cell death, particularly in early postnatal (2 mo), distal airways.

Keywords: NK-1R; bronchial epithelium; lung; neurokinin; substance P.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Death / drug effects
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Lung / growth & development
  • Lung / metabolism*
  • Lung / pathology
  • Macaca mulatta
  • Male
  • Nuclear Receptor Subfamily 4, Group A, Member 1 / metabolism
  • Oxidants, Photochemical / adverse effects*
  • Oxidants, Photochemical / pharmacology
  • Ozone / adverse effects*
  • Ozone / pharmacology
  • Receptors, Neurokinin-1 / metabolism*
  • Respiratory Mucosa / metabolism*
  • Respiratory Mucosa / pathology

Substances

  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • Oxidants, Photochemical
  • Receptors, Neurokinin-1
  • Ozone