Expression of mechanogated two-pore domain potassium channels in mouse lungs: special reference to mechanosensory airway receptors |
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Authors: | Robrecht Lembrechts Isabel Pintelon Kathy Schnorbusch Jean-Pierre Timmermans Dirk Adriaensen Inge Brouns |
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Institution: | (1) Department of Veterinary Sciences, Laboratory of Cell Biology and Histology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium; |
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Abstract: | Afferent activities arising from sensory nerve terminals located in lungs and airways are carried almost exclusively by fibres
travelling through the vagus nerve. Based on electrophysiological investigations, intrapulmonary airway-related vagal afferent
receptors have been classified into three main subtypes, two of which are myelinated and mechanosensitive, i.e., rapidly and
slowly adapting receptors. To allow for a full functional identification of the distinct populations of airway receptors,
morphological and neurochemical characteristics still need to be determined. Nerve terminals visualised using markers for
myelinated vagal afferents seem to be almost uniquely associated with two morphologically well-formed airway receptor end
organs, smooth muscle-associated airway receptors (SMARs) and neuroepithelial bodies (NEBs), localised in airway smooth muscle
and epithelium, respectively. Due to the lack of a selective marker for SMARs in mice, no further neurochemical coding is
available today. NEBs are extensively innervated diffusely spread groups of neuroendocrine cells in the airway epithelium,
and are known to receive at least two separate populations of myelinated vagal afferent nerve terminals. So far, however,
no evidence has been reported for the expression of channels that may underlie direct sensing and transduction of mechanical
stimuli by the receptor terminals in NEBs and SMARs. This study focused on the expression of mechanogated two-pore domain
K+ (K2P) channels, TREK-1 and TRAAK, in mouse airways and more particular in the NEB micro-environment and in SMARs by multiple immunostaining.
TREK-1 could be detected on smooth muscle cells surrounding intrapulmonary airways and blood vessels, while TRAAK was expressed
on myelinated vagal afferents terminating both in SMARs and in the NEB micro-environment. Co-stainings with known markers
for subpopulations of myelinated vagal afferents and general neuronal markers revealed that all identified SMARs exhibit TRAAK
immunoreactivity, and that at least three subpopulations exist in mouse airways. Also, the intraepithelial terminals of both
subpopulations of NEB-associated myelinated vagal sensory nerve fibres were shown to express TRAAK. In conclusion, the present
study finally characterised an intrinsically mechanosensitive ion channel, the K2P channel TRAAK, on the terminals of identified myelinated vagal nodose airway afferents, organised as SMARs and as components
of the innervation of NEBs. These data support the hypothesis that both SMARs and NEBs harbour the morphological counterparts
of electrophysiologically identified myelinated vagal airway mechanoreceptors. TRAAK appears to be strongly involved in regulating
airway mechanosensing since it was found to be expressed on the terminals of all subpopulations of potential vagal mechanosensors. |
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