Distribution of TRPVs, P2X3, and Parvalbumin in the Human Nodose Ganglion

Sato, Daisuke; Sato, Tadasu; Urata, Yusuke; Okajima, Takayuki; Kawamura, Shota; Kurita, Manatsu; Takahashi, Kenta; Nanno, Masakazu; Watahiki, Asami; Kokubun, Souichi; Shimizu, Yoshinaka; Kasahara, Eriko; Shoji, Nobuyuki; Sasano, Takashi; Ichikawa, Hiroyuki

doi:10.1007/s10571-014-0062-9

Cited by 18 publications

(9 citation statements)

References 28 publications

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“…First, we only found P2X3 in a small population (18%) of IB4 fibers, thus it is possible that the afferent fibers containing P2X3 in our anatomical studies were not represented in the C-fiber populations studied in the prior electrophysiological studies. Previous studies have reported a similar proportion of nodose ganglion cells contain P2X3 in the rat (Wang et al , 2014), although much higher proportions have been reported in humans (Sato et al , 2014). The nodose ganglion is variably successful as a proxy for central terminals, since ion channels or receptors can be differentially trafficked to central and peripheral regions of the sensory neuron after synthesis in the ganglion.…”

Section: Discussionmentioning

confidence: 57%

Localization of TRPV1 and P2X3 in unmyelinated and myelinated vagal afferents in the rat

Hermes

Andresen

Aicher

2016

Journal of Chemical Neuroanatomy

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The vagus nerve is dominated by afferent fibers that convey sensory information from the viscera to the brain. Most vagal afferents are unmyelinated, slow-conducting C-fibers, while a smaller portion are myelinated, fast-conducting A-fibers. Vagal afferents terminate in the nucleus tractus solitarius (NTS) in the dorsal brainstem and regulate autonomic and respiratory reflexes, as well as ascending pathways throughout the brain. Vagal afferents form glutamatergic excitatory synapses with postsynaptic NTS neurons that are modulated by a variety of channels. The organization of vagal afferents with regard to fiber type and channels is not well understood. In the present study, we used tract tracing methods to identify distinct populations of vagal afferents to determine if key channels are selectively localized to specific groups of afferent fibers. Vagal afferents were labeled with isolectin B4 (IB4) or cholera toxin B (CTb) to detect unmyelinated and myelinated afferents, respectively. We find that TRPV1 channels are preferentially found in unmyelinated vagal afferents identified with IB4, with almost half of all IB4 fibers showing co-localization with TRPV1. These results agree with prior electrophysiological findings. In contrast, we found that the ATP-sensitive channel P2X3 is found in a subset of both myelinated and unmyelinated vagal afferent fibers. Specifically, 18% of IB4 and 23% of CTb afferents contained P2X3. The majority of CTb-ir vagal afferents contained neither channel. Since neither channel was found in all vagal afferents, there are likely further degrees of heterogeneity in the modulation of vagal afferent sensory input to the NTS beyond fiber type.

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Section: Discussionmentioning

confidence: 57%

Localization of TRPV1 and P2X3 in unmyelinated and myelinated vagal afferents in the rat

Hermes

Andresen

Aicher

2016

Journal of Chemical Neuroanatomy

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“…We have demonstrated expression of P2X3 and P2X2, and αβ-MeATP caused a [Ca 2+ ] i level increase in guinea pig nodose ganglion neurons, which is in agreement with previous studies. 23 , 39 αβ-MeATP was also able to depolarize guinea pig and human vagus nerves, and both the increase in calcium levels and the vagal depolarization evoked by αβ-MeATP were inhibited by the P2X1 and P2X3 inhibitor TNP-ATP and the P2X3 inhibitor AF-353. Both inhibitors were also shown to inhibit depolarization induced by TRPV4 ligands and hypo-osmotic solution in guinea pig and human vagus, confirming the hypothesis that TRPV4- and hypotonicity-mediated activation of vagal afferents is mediated by the release of ATP and activation of P2X3 receptors.…”

Section: Discussionmentioning

confidence: 97%

Transient receptor potential cation channel, subfamily V, member 4 and airway sensory afferent activation: Role of adenosine triphosphate

Bonvini

Birrell

Grace

et al. 2016

Journal of Allergy and Clinical Immunology

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BackgroundSensory nerves innervating the airways play an important role in regulating various cardiopulmonary functions, maintaining homeostasis under healthy conditions and contributing to pathophysiology in disease states. Hypo-osmotic solutions elicit sensory reflexes, including cough, and are a potent stimulus for airway narrowing in asthmatic patients, but the mechanisms involved are not known. Transient receptor potential cation channel, subfamily V, member 4 (TRPV4) is widely expressed in the respiratory tract, but its role as a peripheral nociceptor has not been explored.ObjectiveWe hypothesized that TRPV4 is expressed on airway afferents and is a key osmosensor initiating reflex events in the lung.MethodsWe used guinea pig primary cells, tissue bioassay, in vivo electrophysiology, and a guinea pig conscious cough model to investigate a role for TRPV4 in mediating sensory nerve activation in vagal afferents and the possible downstream signaling mechanisms. Human vagus nerve was used to confirm key observations in animal tissues.ResultsHere we show TRPV4-induced activation of guinea pig airway–specific primary nodose ganglion cells. TRPV4 ligands and hypo-osmotic solutions caused depolarization of murine, guinea pig, and human vagus and firing of Aδ-fibers (not C-fibers), which was inhibited by TRPV4 and P2X3 receptor antagonists. Both antagonists blocked TRPV4-induced cough.ConclusionThis study identifies the TRPV4-ATP-P2X3 interaction as a key osmosensing pathway involved in airway sensory nerve reflexes. The absence of TRPV4-ATP–mediated effects on C-fibers indicates a distinct neurobiology for this ion channel and implicates TRPV4 as a novel therapeutic target for neuronal hyperresponsiveness in the airways and symptoms, such as cough.

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“…The superior cervical ganglion (SCG), a large sympathetic ganglion of the neck, is an interesting example of the complicated anatomical relationships between the parasympathetic and sympathetic nervous systems. The SCG is well known to be in close proximity of the nodose ganglion (NG) in most mammals including humans (Appelgren, Hansson, & Schmiterloew, 1963; Chungcharoen, De Burgh Daly, & Schweitzer, 1952; Fioretto, de Abreu, Castro, Guidi, & Ribeiro, 2007; Jamieson, Smith, & Anson, 1952; Phillips, Randall, & Armour, 1986; Randall, Armour, Randall, & Smith, 1971; Sato et al, 2014). Connections between the SCG and other cervical nerve systems are established by numerous small nerve branches and filaments arising from the NG, vagus nerve, and cervical plexus (Fioretto et al, 2007; Janes et al, 1986; Mitsuoka, Kikutani, & Sato, 2017; Nourinezhad, Mazaheri, & Biglari, 2015; Rodrigues, 1930).…”

Section: Introductionmentioning

confidence: 99%

Characterization of a cell bridge variant connecting the nodose and superior cervical ganglia in the mouse: Prevalence, anatomical features, and practical implications

Bookout

Gautron

2020

J of Comparative Neurology

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While autonomic ganglia have been extensively studied in rats instead of mice, there is renewed interest in the anatomy of the mouse autonomic nervous system. This study examined the prevalence and anatomical features of a cell bridge linking two autonomic ganglia of the neck, namely, the nodose ganglion (NG) and the superior cervical ganglion (SCG) in a cohort of C57BL/6J mice. We identified a cell bridge between the NG and the cranial pole of the SCG. This cell bridge was tubular shaped with an average length and width of 700 and 240 μm, respectively. The cell bridge was frequently unilateral and significantly more prevalent in the ganglionic masses from males (38%) than females (21%). On each of its extremities, it contained a mixed of vagal afferents and postganglionic sympathetic neurons. The two populations of neurons abruptly replaced each other in the middle of the cell bridge. We examined the mRNA expression for selected autonomic markers in samples of the NG with or without cell bridge. Our results indicated that the cell bridge was enriched in both markers of postganglionic sympathetic and vagal afferents neurons. Lastly, using FluoroGold microinjection into the NG, we found that the existence of a cell bridge may occasionally lead to the inadvertent contamination of the SCG. In summary, this study describes the anatomy of a cell bridge variant consisting of the fusion of the mouse NG and SCG. The practical implications of our observations are discussed with respect to studies of the mouse vagal afferents, an area of research of increasing popularity.

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Distribution of TRPVs, P2X3, and Parvalbumin in the Human Nodose Ganglion

Cited by 18 publications

References 28 publications

Localization of TRPV1 and P2X3 in unmyelinated and myelinated vagal afferents in the rat

Localization of TRPV1 and P2X3 in unmyelinated and myelinated vagal afferents in the rat

Transient receptor potential cation channel, subfamily V, member 4 and airway sensory afferent activation: Role of adenosine triphosphate

Characterization of a cell bridge variant connecting the nodose and superior cervical ganglia in the mouse: Prevalence, anatomical features, and practical implications

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