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Cellular distribution and function of ion channels involved in transport processes in rat tracheal epithelium.

ABSTRACT: Transport of water and electrolytes in airway epithelia involves chloride-selective ion channels, which are controlled either by cytosolic Ca²⁺ or by cAMP The contributions of the two pathways to chloride transport differ among vertebrate species. Because rats are becoming more important as animal model for cystic fibrosis, we have examined how Ca²⁺- dependent and cAMP- dependent Cl^- secretion is organized in the rat tracheal epithelium. We examined the expression of the Ca²⁺-gated Cl^- channel anoctamin 1 (ANO1), the cystic fibrosis transmembrane conductance regulator (CFTR) Cl^- channel, the epithelial Na⁺ channel ENaC, and the water channel aquaporin 5 (AQP5) in rat tracheal epithelium. The contribution of ANO1 channels to nucleotide-stimulated Cl^- secretion was determined using the channel blocker Ani9 in short-circuit current recordings obtained from primary cultures of rat tracheal epithelial cells in Ussing chambers. We found that ANO1, CFTR and AQP5 proteins were expressed in nonciliated cells of the tracheal epithelium, whereas ENaC was expressed in ciliated cells. Among nonciliated cells, ANO1 occurred together with CFTR and Muc5b and, in addition, in a different cell type without CFTR and Muc5b. Bioelectrical studies with the ANO1-blocker Ani9 indicated that ANO1 mediated the secretory response to the nucleotide uridine-5'-triphosphate. Our data demonstrate that, in rat tracheal epithelium, Cl^- secretion and Na⁺ absorption are routed through different cell types, and that ANO1 channels form the molecular basis of Ca²⁺-dependent Cl^- secretion in this tissue. These characteristic features of Cl^--dependent secretion reveal similarities and distinct differences to secretory processes in human airways.

SUBMITTER: Hahn A

PROVIDER: S-EPMC5492199 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Cellular distribution and function of ion channels involved in transport processes in rat tracheal epithelium.

Hahn Anne A Faulhaber Johannes J Srisawang Lalita L Stortz Andreas A Salomon Johanna J JJ Mall Marcus A MA Frings Stephan S Möhrlen Frank F

Physiological reports 20170601 12

Transport of water and electrolytes in airway epithelia involves chloride-selective ion channels, which are controlled either by cytosolic Ca2+ or by cAMP The contributions of the two pathways to chloride transport differ among vertebrate species. Because rats are becoming more important as animal model for cystic fibrosis, we have examined how Ca2+- dependent and cAMP- dependent Cl- secretion is organized in the rat tracheal epithelium. We examined the expressio ...[more]

PMID: 28642338

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Project description:BACKGROUND:Genetic disruption of slc4a10, which encodes the sodium-dependent chloride/bicarbonate exchanger Ncbe, leads to a major decrease in Na+-dependent HCO3- import into choroid plexus epithelial cells in mice and to a marked reduction in brain intraventricular fluid volume. This suggests that Ncbe functionally is a key element in vectorial Na+ transport and thereby for cerebrospinal fluid secretion in the choroid plexus. However, slc4a10 disruption results in severe changes in expression of Na+,K+-ATPase complexes and other major transport proteins, indicating that profound cellular changes accompany the genetic manipulation. METHODS:A tandem mass tag labeling strategy was chosen for quantitative mass spectrometry. Alterations in the broader patterns of protein expression in the choroid plexus in response to genetic disruption of Ncbe was validated by semi-quantitative immunoblotting, immunohistochemistry and morphometry. RESULTS:The abundance of 601 proteins were found significantly altered in the choroid plexus from Ncbe ko mice relative to Ncbe wt. In addition to a variety of transport proteins, particularly large changes in the abundance of proteins involved in cellular energy metabolism were detected in the Ncbe ko mice. In general, the abundance of rate limiting glycolytic enzymes and several mitochondrial enzymes were reduced following slc4a10 disruption. Surprisingly, this was accompanied by increased ATP levels in choroid plexus cells, indicating that the reduction in capacity for energy metabolism was adaptive to high ATP rather than causal for a decreased capacity for ion and water transport. Ncbe-deficient cells also had a reduced cell area and decreased K+ content. CONCLUSION:Our findings suggest that the lack of effective Na+-entry into the epithelial cells of the choroid plexus leads to a profound change in the cellular phenotype, shifting from a high-rate secretory function towards a more dormant state; similar to what is observed during ageing or Alzheimer's disease.

Dataset Information

Cellular distribution and function of ion channels involved in transport processes in rat tracheal epithelium.

Publications

Cellular distribution and function of ion channels involved in transport processes in rat tracheal epithelium.

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