Prenatal nicotinic exposure augments cardiorespiratory responses to activation of bronchopulmonary C-fibers

Am J Physiol Lung Cell Mol Physiol. 2015 May 1;308(9):L922-30. doi: 10.1152/ajplung.00241.2014. Epub 2015 Mar 6.

Abstract

Rat pups prenatally exposed to nicotine (PNE) present apneic (lethal ventilatory arrest) responses during severe hypoxia. To clarify whether these responses are of central origin, we tested PNE effects on ventilation and diaphragm electromyography (EMGdi) during hypoxia in conscious rat pups. PNE produced apnea (lethal ventilatory arrest) identical to EMGdi silencing during hypoxia, indicating a central origin of this apneic response. We further asked whether PNE would sensitize bronchopulmonary C-fibers (PCFs), a key player in generating central apnea, with increase of the density and transient receptor potential cation channel subfamily V member 1 (TRPV1) expression of C-fibers/neurons in the nodose/jugular (N/J) ganglia and neurotrophic factors in the airways and lungs. We compared 1) ventilatory and pulmonary C-neural responses to right atrial bolus injection of capsaicin (CAP, 0.5 μg/kg), 2) bronchial substance P-immunoreactive (SP-IR) fiber density, 3) gene and protein expressions of TRPV1 in the ganglia, and 4) nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) protein in bronchoalveolar lavage fluid (BALF) and TrkA and TrkB genes in the ganglia between control and PNE pups. PNE markedly strengthened the PCF-mediated apneic response to CAP via increasing pulmonary C-neural sensitivity. PNE also enhanced bronchial SP-IR fiber density and N/J ganglia neural TRPV1 expression associated with increased gene expression of TrkA in the N/G ganglia and decreased NGF and BDNF in BALF. Our results suggest that PNE enhances PCF sensitivity likely through increasing PCF density and TRPV1 expression via upregulation of neural TrkA and downregulation of pulmonary BDNF, which may contribute to the PNE-promoted central apnea (lethal ventilatory arrest) during hypoxia.

Keywords: cardiorespiratory failure; central apnea; maternal cigarette smoking; sudden infant death syndrome; vagal afferents.

Publication types

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

MeSH terms

  • Animals
  • Apnea / chemically induced*
  • Brain-Derived Neurotrophic Factor / biosynthesis
  • Brain-Derived Neurotrophic Factor / genetics
  • Bronchoalveolar Lavage Fluid / chemistry
  • Capsaicin / pharmacology
  • Diaphragm / physiopathology
  • Electromyography
  • Female
  • Ganglia / cytology
  • Ganglia / metabolism
  • Humans
  • Hypoxia
  • Infant, Newborn
  • Male
  • Methacholine Chloride / pharmacology
  • Nerve Fibers, Unmyelinated / drug effects
  • Nerve Fibers, Unmyelinated / metabolism
  • Nerve Growth Factor / biosynthesis
  • Nerve Growth Factor / genetics
  • Nicotine / pharmacology*
  • Nodose Ganglion / metabolism
  • Pregnancy
  • Prenatal Exposure Delayed Effects*
  • Random Allocation
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, trkA / genetics
  • Receptor, trkB / genetics
  • Recombinant Proteins
  • Sensory System Agents / pharmacology
  • Smoking / adverse effects*
  • Substance P / immunology
  • Sudden Infant Death / etiology*
  • TRPV Cation Channels / biosynthesis
  • TRPV Cation Channels / genetics

Substances

  • Brain-Derived Neurotrophic Factor
  • Recombinant Proteins
  • Sensory System Agents
  • TRPV Cation Channels
  • Trpv1 protein, rat
  • tyrosine receptor kinase A Ig2
  • Methacholine Chloride
  • Substance P
  • Nicotine
  • Nerve Growth Factor
  • Receptor, trkA
  • Receptor, trkB
  • Capsaicin