ATP- and ACh-induced responses in isolated cat petrosal ganglion neurons

Alcayaga, C; Varas, Rodrigo; Valdés, Viviana; Cerpa, Verónica; Arroyo, Jorge G.; Iturriaga, Rodrigo; Alcayaga, Julio

doi:10.1016/j.brainres.2006.11.012

Cited by 16 publications

(7 citation statements)

References 32 publications

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“…In concert with these results, systemic blockade of both nicotinic and purinergic P2X receptors inhibited ventilation in newborn rats (Niane et al, 2012 ). Additional evidence supporting ACh as an important CB excitatory neurotransmitter was obtained in the following studies: (i) functional nicotinic AChR were present on >65% of isolated rat petrosal neurons (Zhong and Nurse, 1997 ) and in the majority of petrosal neurons that were functionally connected to the cat CB (Varas et al, 2003 ; Iturriaga and Alcayaga, 2004 ); (ii) in the isolated rat and cat CB-sinus nerve preparations in vitro nicotinic AChR blockers inhibited the hypoxia-induced chemosensory discharge (Iturriaga and Alcayaga, 2004 ; He et al, 2005 ; Zapata, 2007 ; Niane et al, 2009 ); and (iii) consistent with a postsynaptic role for ACh, α7 nAChR immunoreactivity has been localized to nerve endings surrounding type I clusters in rat and cat CB in situ (Shirahata et al, 2007 ; Niane et al, 2009 ), and there is electrophysiological evidence consistent with the presence of functional α7 nAChR in cat petrosal neurons (Alcayaga et al, 2007 ).…”

Section: Synaptic Transmission Between Chemoreceptor Type I Cells Andmentioning

confidence: 77%

Sensory Processing and Integration at the Carotid Body Tripartite Synapse: Neurotransmitter Functions and Effects of Chronic Hypoxia

2018

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Maintenance of homeostasis in the respiratory and cardiovascular systems depends on reflexes that are initiated at specialized peripheral chemoreceptors that sense changes in the chemical composition of arterial blood. In mammals, the bilaterally-paired carotid bodies (CBs) are the main peripheral chemoreceptor organs that are richly vascularized and are strategically located at the carotid bifurcation. The CBs contribute to the maintenance of O2, CO2/H+, and glucose homeostasis and have attracted much clinical interest because hyperactivity in these organs is associated with several pathophysiological conditions including sleep apnea, obstructive lung disease, heart failure, hypertension, and diabetes. In response to a decrease in O2 availability (hypoxia) and elevated CO2/H+ (acid hypercapnia), CB receptor type I (glomus) cells depolarize and release neurotransmitters that stimulate apposed chemoafferent nerve fibers. The central projections of those fibers in turn activate cardiorespiratory centers in the brainstem, leading to an increase in ventilation and sympathetic drive that helps restore blood PO2 and protect vital organs, e.g., the brain. Significant progress has been made in understanding how neurochemicals released from type I cells such as ATP, adenosine, dopamine, 5-HT, ACh, and angiotensin II help shape the CB afferent discharge during both normal and pathophysiological conditions. However, type I cells typically occur in clusters and in addition to their sensory innervation are ensheathed by the processes of neighboring glial-like, sustentacular type II cells. This morphological arrangement is reminiscent of a “tripartite synapse” and emerging evidence suggests that paracrine stimulation of type II cells by a variety of CB neurochemicals may trigger the release of “gliotransmitters” such as ATP via pannexin-1 channels. Further, recent data suggest novel mechanisms by which dopamine, acting via D2 receptors (D2R), may inhibit action potential firing at petrosal nerve endings. This review will update current ideas concerning the presynaptic and postsynaptic mechanisms that underlie chemosensory processing in the CB. Paracrine signaling pathways will be highlighted, and particularly those that allow the glial-like type II cells to participate in the integrated sensory response during exposures to chemostimuli, including acute and chronic hypoxia.

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Section: Synaptic Transmission Between Chemoreceptor Type I Cells Andmentioning

confidence: 77%

Sensory Processing and Integration at the Carotid Body Tripartite Synapse: Neurotransmitter Functions and Effects of Chronic Hypoxia

2018

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“…In addition, it is reported that neurotransmitters were involved in H 2 S-induced sensory excitation of carotid bodies. Acetylcholine (ACh) and adenosine triphosphate (ATP) are two excitatory neurotransmitters in the carotid bodies of both cats and rats [ 27 , 65 , 66 ]. Inhibition of purinergic receptors using pyridoxal phosphate-6-azophenyl-2′,4′-disulfonic acid, or application of hexamethonium, a blocker of nicotinic cholinergic receptors, prevented NaHS-evoked sensory excitation of the mouse carotid body [ 27 ].…”

Section: H 2 S and Hypoxic Sensing In The Cmentioning

confidence: 99%

Interaction of Hydrogen Sulfide with Oxygen Sensing under Hypoxia

Teng

Zhang

et al. 2015

Oxidative Medicine and Cellular Longevity

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Based on the discovery of endogenous H2S production, many in depth studies show this gasotransmitter with a variety of physiological and pathological functions. Three enzymes, cystathionine β-synthase (CBS), cystathionine γ-lyase (CSE), and 3-mercaptopyruvate sulfurtransferase (MST), are involved in enzymatic production of H2S. Emerging evidence has elucidated an important protective role of H2S in hypoxic conditions in many mammalian systems. However, the mechanisms by which H2S senses and responses to hypoxia are largely elusive. Hypoxia-inducible factors (HIFs) function as key regulators of oxygen sensing, activating target genes expression under hypoxia. Recent studies have shown that exogenous H2S regulates HIF action in different patterns. The activation of carotid bodies is a sensitive and prompt response to hypoxia, rapidly enhancing general O2 supply. H2S has been identified as an excitatory mediator of hypoxic sensing in the carotid bodies. This paper presents a brief review of the roles of these two pathways which contribute to hypoxic sensing of H2S.

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“…In cultured PG neurons ACh and nicotine induces depolarization (Zhong and Nurse, 1997 ; Varas et al, 2000 ) which is blocked by nAChR antagonists (Zhong and Nurse, 1997 ; Shirahata et al, 2000 ; Varas et al, 2006 ; Alcayaga et al, 2007 ). Agonist and antagonist sensibility indicate the presence of both α7 and α4β 4 (Shirahata et al, 2000 ; Varas et al, 2006 ) or α4β 2 nAChRs (Shirahata et al, 2000 ), in concordance with immunohistochemical evidence (Shirahata et al, 1998 , 2000 ).…”

Section: Petrosal Ganglion Neurons Projecting Through the Carotid Sinmentioning

confidence: 99%

Section: Petrosal Ganglion Neurons Projecting Through the Carotid Sinmentioning

confidence: 99%

“…Whole cell recordings of cultured cat PG neurons show that ATP induces a dose dependent depolarization that increased the discharge frequency and a sustained inward current at a holding potential near the resting Vm (−60 mV) (Alcayaga et al, 2007 ). These responses are mimicked by α,β-methylene ATP and blocked by suramin, suggesting the involvement of P2X2,3 receptors in the generation of these responses (Alcayaga et al, 2007 ). In an in vitro preparation containing NPJc neurons and CB cells obtained from Sprague-Dawley rats, that respond as a reconstituted arterial chemoreceptor (Zhong et al, 1997 ), hypoxia- and hypercapnia-induced responses recorded from PG neurons are partially blocked by reduced extracellular Ca 2+ /Mg 2+ ratio and suramin, a nucleotide receptor blocker.…”

Section: Petrosal Ganglion Neurons Projecting Through the Carotid Sinmentioning

confidence: 99%

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Petrosal ganglion: a more complex role than originally imagined

2014

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The petrosal ganglion (PG) is a peripheral sensory ganglion, composed of pseudomonopolar sensory neurons that innervate the posterior third of the tongue and the carotid sinus and body. According to their electrical properties PG neurons can be ascribed to one of two categories: (i) neurons with action potentials presenting an inflection (hump) on its repolarizing phase and (ii) neurons with fast and brisk action potentials. Although there is some correlation between the electrophysiological properties and the sensory modality of the neurons in some species, no general pattern can be easily recognized. On the other hand, petrosal neurons projecting to the carotid body are activated by several transmitters, with acetylcholine and ATP being the most conspicuous in most species. Petrosal neurons are completely surrounded by a multi-cellular sheet of glial (satellite) cells that prevents the formation of chemical or electrical synapses between neurons. Thus, PG neurons are regarded as mere wires that communicate the periphery (i.e., carotid body) and the central nervous system. However, it has been shown that in other sensory ganglia satellite glial cells and their neighboring neurons can interact, partly by the release of chemical neuro-glio transmitters. This intercellular communication can potentially modulate the excitatory status of sensory neurons and thus the afferent discharge. In this mini review, we will briefly summarize the general properties of PG neurons and the current knowledge about the glial-neuron communication in sensory neurons and how this phenomenon could be important in the chemical sensory processing generated in the carotid body.

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ATP- and ACh-induced responses in isolated cat petrosal ganglion neurons

Cited by 16 publications

References 32 publications

Sensory Processing and Integration at the Carotid Body Tripartite Synapse: Neurotransmitter Functions and Effects of Chronic Hypoxia

Sensory Processing and Integration at the Carotid Body Tripartite Synapse: Neurotransmitter Functions and Effects of Chronic Hypoxia

Interaction of Hydrogen Sulfide with Oxygen Sensing under Hypoxia

Petrosal ganglion: a more complex role than originally imagined

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