Potential roles of ATP and local neurons in the monitoring of blood O2 content by rat aortic bodies
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New FindingsWhat is the central question of this study?How do aortic bodies monitor blood O2 content? We investigated whether ATP, known to be released from red blood cells during hypoxia, could contribute via interactions with local neurons.What is the main finding and its importance?In dissociated aortic body cultures from the vagus and recurrent laryngeal nerves, some local neurons expressed functional P2X2/3 purinoceptors and were electrically coupled; there was also the potential for cholinergic neurotransmission. Large molecules, such as Evans Blue, had easy access to local neurons via the circulation. We hypothesize that sensing of low blood O2 content may involve ATP release from red blood cells, leading to stimulation of local ‘sensory’ aortic body neurons.Aortic bodies are arterial chemoreceptors presumed to monitor blood O2 content by unknown mechanisms, in contrast to their well‐studied carotid body counterparts, which monitor and /pH. We recently showed that rat aortic body chemoreceptors (type I cells), located at the left vagus–recurrent laryngeal nerve bifurcation, responded to and /pH in a manner similar to carotid body type I cells. These aortic bodies are uniquely associated with a group of local neurons, which are also sensitive to these stimuli. Here, we hypothesized that these local neurons may contribute to monitoring blood O2 content. During perforated patch recordings, ATP, known to be released from (carotid body) type I cells and red blood cells during hypoxia, induced inward currents and excited ∼45% of local neurons (EC50∼1 μm), mainly via heteromeric P2X2/3 purinoceptors. While ATP also induced a rise in intracellular [Ca2+] in a subpopulation of these neurons, almost all of them responded to nicotinic cholinergic agonists. During paired recordings, several juxtaposed neurons showed strong bidirectional electrical coupling, suggesting a local co‐ordination of electrical activity. Perfusion with Evans Blue dye resulted in labelling of aortic body paraganglia, suggesting they have ready access to circulatory factors, e.g. ATP released from red blood cells during hypoxia. When combined with confocal immunofluorescence, the dye‐labelled regions coincided with areas containing tyrosine hydroxylase‐positive type I cell clusters and P2X2‐positive nerve endings. We propose a working model whereby local neurons, red blood cells, ATP signalling and low blood flow contribute to the unique ability of the aortic body to monitor blood O2 content.
