Nitric oxide-related inhibition of carotid chemosensory nerve activity in the cat

Chugh, Deepak K.; Katayama, Masao; Mokashi, A.; Bebout, D. E.; Ray, Dilip Kumar; Lahiri, S.

doi:10.1016/0034-5687(94)90022-1

Cited by 70 publications

(49 citation statements)

References 6 publications

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“…In the CB, NO produced by the eNOS may inhibit chemosensory activity by increasing blood flow and O 2 delivery to glomus cells (8,28). The withdrawal of an inhibitory vascular tone mediated by NO is expected to increase basal chemosensory discharges and is compatible with an increased duration of the responses to bolus injections of excitatory stimuli, as we observed here after the inhibition of the eNOS.…”

Section: Discussionsupporting

confidence: 68%

“…In the nucleus tractus solitarii, NO plays a significant excitatory role in sustaining the ventilatory response to hypoxia (14,18,35). However, several lines of evidence indicate that NO produced within the carotid body (CB) is an inhibitory modulator of hypoxic chemoreception (2,8,20,25,34,38). The administration of the precursor L-arginine, NO donor molecules (8,22,38), and NO gas (20) to the cat CB perfused in vitro reduces the chemosensory response to hypoxia.…”

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confidence: 99%

“…However, several lines of evidence indicate that NO produced within the carotid body (CB) is an inhibitory modulator of hypoxic chemoreception (2,8,20,25,34,38). The administration of the precursor L-arginine, NO donor molecules (8,22,38), and NO gas (20) to the cat CB perfused in vitro reduces the chemosensory response to hypoxia. On the other hand, the inhibition of NOS increases the frequency of carotid chemosensory discharges (f x ) in the cat CB in situ and in vitro (19,38).…”

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confidence: 99%

“…33 for review). NO has been proposed to produce vasodilatation in the CB (5,8,28,38), retrograde inhibition of the glomus cell's excitability (39), inhibition of Ca 2ϩ channels in glomus cells (36), modulation of petrosal ganglion neuron's excitability (1), and inhibition of mitochondrial metabolism (22,28). At least three isoforms of NOS have been isolated (32): neuronal (nNOS), endothelial (eNOS), and inducible.…”

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confidence: 99%

“…In the rat, Western blots of CB homogenates showed a relative abundance of eNOS protein compared with nNOS (13). The NO produced by eNOS may regulate blood flow and subsequent changes in CB tissue PO 2 , whereas NO produced by nNOS in terminals of sensory C fibers and parasympathetic neurons may regulate glomus cell excitability and the vascular tone, respectively (8,28,34,38,39). The contribution of nNOS and eNOS isoforms to the production of NO in the CB has been assessed indirectly by testing the effect of the pharmacological and genetic suppression…”

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Inhibitory effects of NO on carotid body: contribution of neural and endothelial nitric oxide synthase isoforms

Valdés

Mosqueira

Rey

et al. 2003

American Journal of Physiology-Lung Cellular and Molecular Phys

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Valdé s, Viviana, Matías Mosqueira, Sergio Rey, Rodrigo Del Rio, and Rodrigo Iturriaga. Inhibitory effects of NO on carotid body: contribution of neural and endothelial nitric oxide synthase isoforms. Am J Physiol Lung Cell Mol Physiol 284: L57-L68, 2003. First published September 6, 2002 10.1152/ajplung.00494.2001.-We tested the hypothesis that nitric oxide (NO) produced within the carotid body is a tonic inhibitor of chemoreception and determined the contribution of neuronal and endothelial nitric oxide synthase (eNOS) isoforms to the inhibitory NO effect. Accordingly, we studied the effect of NO generated from S-nitroso-Nacetylpenicillamide (SNAP) and compared the effects of the nonselective inhibitor N -nitro-L-arginine methyl ester (L-NAME) and the selective nNOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole (TRIM) on chemosensory dose-response curves induced by nicotine and NaCN and responses to hypoxia (PO2 Ϸ 30 Torr). CBs excised from pentobarbitoneanesthetized cats were perfused in vitro with Tyrode at 38°C and pH 7.40, and chemosensory discharges were recorded from the carotid sinus nerve. SNAP (100 M) reduced the responses to nicotine and NaCN. L-NAME (1 mM) enhanced the responses to nicotine and NaCN by increasing their duration, but TRIM (100 M) only enhanced the responses to high doses of NaCN. The amplitude of the response to hypoxia was enhanced by L-NAME but not by TRIM. Our results suggest that both isoforms contribute to the NO action, but eNOS being the main source for NO in the cat CB and exerting a tonic effect upon chemoreceptor activity. chemoreceptor; nitric oxide THE VENTILATORY EFFECTS of nitric oxide (NO) and the role played by nitric oxide synthase (NOS) isoforms are complex (14,18,30). In the nucleus tractus solitarii, NO plays a significant excitatory role in sustaining the ventilatory response to hypoxia (14,18,35). However, several lines of evidence indicate that NO produced within the carotid body (CB) is an inhibitory modulator of hypoxic chemoreception (2,8,20,25,34,38). The administration of the precursor L-arginine, NO donor molecules (8,22,38), and NO gas (20) to the cat CB perfused in vitro reduces the chemosensory response to hypoxia. On the other hand, the inhibition of NOS increases the frequency of carotid chemosensory discharges (f x ) in the cat CB in situ and in vitro (19,38). However, little is known about the effects of NO on chemosensory responses induced by other excitatory stimuli, such as nicotine and NaCN. In a previous paper, we found that the NO donor sodium nitroprusside (SNP) reversibly reduced chemosensory responses induced by single doses of NaCN and nicotine in the superfused cat CB (2). In anesthetized cats, the NOS inhibitor N -nitro-L-arginine methyl ester (L-NAME) increased basal f x and enhanced responses to NaCN and dopamine (19). These results suggest that, besides the well-known inhibitory effect of NO on hypoxic chemoreception, NO may also modulate the responses to other stimuli.In the cat CB, NOS immunoreactivity and diaphorase activitie...

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Section: Discussionsupporting

confidence: 68%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Inhibitory effects of NO on carotid body: contribution of neural and endothelial nitric oxide synthase isoforms

Valdés

Mosqueira

Rey

et al. 2003

American Journal of Physiology-Lung Cellular and Molecular Phys

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Reduced number of intrinsic pulmonary nitrergic neurons in Fawn‐Hooded rats as compared to control rat strains

et al. 2003

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The Fawn-Hooded rat (FHR) strain reveals a congenital predisposition to primary (idiopathic) pulmonary hypertension (PPH), and can therefore be regarded as an animal model in which to study possible mechanisms underlying an inherited susceptibility to pulmonary hypertension. Pulmonary hypertension can be induced in FHRs after a short exposure to mild hypoxia, presumably because of an altered peripheral oxygen sensitivity. Given the presence of pulmonary nitrergic neurons in rat lungs, the observed link between airway hypoxia and the expression of pulmonary neuronal nitric oxide synthase (nNOS), and the fact that nNOS appears to be involved in peripheral chemoreceptor sensitivity, we examined the intrinsic pulmonary nitrergic innervation in the FHR. In the present study the number of intrapulmonary nitrergic nerve cell bodies, detected by NADPH diaphorase (NADPHd) histochemistry, was quantified in the FHR and three control rat strains. Compared to the control rat strains, the FHR lungs revealed a highly significantly lower number of intrinsic nitrergic neurons, while no apparent differences were found in the number of enteric nitrergic neurons in the esophagus. In conclusion, the possible links between neuronal NO, hypersensitivity to airway hypoxia, and the development of PPH clearly deserve further investigation. Anat Rec Part A 272A: 446 -453, 2003.

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Peripheral Chemoreceptors: Function and Plasticity of the Carotid Body

Kumar

Prabhakar

2012

Comprehensive Physiology

465

572

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The discovery of the sensory nature of the carotid body dates back to the beginning of the 20th century. Following these seminal discoveries, research into carotid body mechanisms moved forward progressively through the 20th century, with many descriptions of the ultrastructure of the organ and stimulus-response measurements at the level of the whole organ. The later part of 20th century witnessed the first descriptions of the cellular responses and electrophysiology of isolated and cultured type I and type II cells, and there now exist a number of testable hypotheses of chemotransduction. The goal of this article is to provide a comprehensive review of current concepts on sensory transduction and transmission of the hypoxic stimulus at the carotid body with an emphasis on integrating cellular mechanisms with the whole organ responses and highlighting the gaps or discrepancies in our knowledge. It is increasingly evident that in addition to hypoxia, the carotid body responds to a wide variety of blood-borne stimuli, including reduced glucose and immune-related cytokines and we therefore also consider the evidence for a polymodal function of the carotid body and its implications. It is clear that the sensory function of the carotid body exhibits considerable plasticity in response to the chronic perturbations in environmental O2 that is associated with many physiological and pathological conditions. The mechanisms and consequences of carotid body plasticity in health and disease are discussed in the final sections of this article.

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Nitric oxide-related inhibition of carotid chemosensory nerve activity in the cat

Cited by 70 publications

References 6 publications

Inhibitory effects of NO on carotid body: contribution of neural and endothelial nitric oxide synthase isoforms

Inhibitory effects of NO on carotid body: contribution of neural and endothelial nitric oxide synthase isoforms

Reduced number of intrinsic pulmonary nitrergic neurons in Fawn‐Hooded rats as compared to control rat strains

Peripheral Chemoreceptors: Function and Plasticity of the Carotid Body

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