Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat

Zhao, Huan; Sprunger, Leslie K.; Simasko, Steven M.

doi:10.1152/ajpgi.00396.2009

Cited by 68 publications

(64 citation statements)

References 56 publications

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“…TRPA1 is crucial for the induction and propagation of the aberrant immune response in stress, and it is expressed in primary sensory neurons and in primary afferents neurons innervating the stomach [39, 40]. Previous results have shown that the gastric mucosa and submucosa are richly innervated by primary afferent neurons [41].…”

Section: Discussionmentioning

confidence: 99%

Transient Receptor Potential Ankyrin 1 and Substance P Mediate the Development of Gastric Mucosal Lesions in a Water Immersion Restraint Stress Rat Model

Jia

Xie

et al. 2018

Digestion

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Background: Activation of substance P (SP) contributes to the development and maintenance of gastric lesions, but the mechanisms underlying the release of SP and SP-mediated damage to the gastric mucosa remain unknown. Transient receptor potential ankyrin 1 (TRPA1) is expressed in SP-positive neurons in the dorsal root ganglion (DRG) and stomach of rats. We hypothesized that water immersion restraint stress (WIRS) may activate and sensitize TRPA1 in DRG neurons, subsequently inducing the release of SP from DRG and stomach cells, causing the development of acute gastric mucosal lesions (AGML). Methods: Changes in TRPA1 and SP expression in T8–11 DRG sensory neurons and the stomach in an AGML rat model were determined by reverse transcription polymerase chain reaction, western blotting and immunohistochemistry. The SP levels of serum and gastric mucosa were measured by using an enzyme-linked immunosorbent assay (ELISA). Gastric lesions were evaluated by histopathological changes. The TRPA1 antagonist HC-030031 and TRPA1 agonists allyl isothiocyanate were used to verify effect of TRPA1 and SP on AGML. Results: SP and TRPA1 in the DRG and stomach were upregulated, and the serum and gastric mucosa levels of SP were increased after WIRS, which are closely associated with AGML. The release of SP was suppressed and AGML were alleviated following a selective TRPA1 antagonist HC-030031. TRPA1 agonists AITC increased release of SP and led to moderate gastric lesions. We confirmed that WIRS induced the release of SP in the DRG, stomach, serum and gastric mucosa, and in a TRPA1-dependent manner. Conclusions: Upregulated SP and TRPA1 in the DRG and stomach and increased serum and gastric mucosa SP levels may contribute to stress-induced AGML. TRPA1 is a potential drug target to reduce stress-induced AGML development in patients with acute critical illnesses. This study may contribute to the discovery of drugs for AGML treatment.

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Section: Discussionmentioning

confidence: 99%

Transient Receptor Potential Ankyrin 1 and Substance P Mediate the Development of Gastric Mucosal Lesions in a Water Immersion Restraint Stress Rat Model

Jia

Xie

et al. 2018

Digestion

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“…TRAAK carries background K ? currents that are critical for the excitability of neurons and are broadly expressed in the nervous system, including vagal afferents (Zhao et al 2010). Mechanical stimuli, such as membrane stretch, shear stress or cell swelling, have been reported to open TRAAK channels (Maingret et al 1999;Kim 2003;Bayliss and Barret 2008).…”

Section: Discussionmentioning

confidence: 99%

“…Recently, it has been shown that vagal sensory neuronal cell bodies can express the mechanogated K 2P ion channels TREK-1 and TRAAK (Zhao et al 2010), while cell bodies located in vagal nodose ganglia give rise to the nerve terminals of SMARs and NEBs (for review see Adriaensen et al 2006;Brouns et al 2009a). At least subsets of the nerve endings of the vagal airway mechanoreceptors that have been characterised electrophysiologically may be located between NEB cells or ramify as SMARs.…”

Section: Introductionmentioning

confidence: 99%

Expression of mechanogated two-pore domain potassium channels in mouse lungs: special reference to mechanosensory airway receptors

Lembrechts

Pintelon

Schnorbusch

et al. 2011

Histochem Cell Biol

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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(+) (K(2P)) 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 K(2P) 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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“…Systemic treatment with capsaicin (n ϭ 8) was used to destroy small unmyelinated primary afferent neurons, including those in the vagi, as described previously (30,38,47). Briefly, a series of three capsaicin doses (25,50, and 50 mg/kg) was injected intraperitoneally over a 36-h period. Controls (n ϭ 8) were injected intraperitoneally with the vehicle solution under the same conditions as capsaicin, and according to an identical schedule.…”

Section: Surgeries and Capsaicin Treatmentmentioning

confidence: 99%

“…Rats were deeply anesthetized with isoflurane and decapitated, and the brains were immediately removed and frozen on dry ice. Hindbrain and hypothalamus were dissected using the method described by Zhao et al (50). A 7-mm coronal section of hypothalamic area was made from the optic chiasm to the mammillary bodies.…”

Section: Food Intake Following Intraperitoneal Cck-8 Injectionmentioning

confidence: 99%

Circulating GLP-1 and CCK-8 reduce food intake by capsaicin-insensitive, nonvagal mechanisms

Zhang

Ritter

2012

American Journal of Physiology-Regulatory, Integrative and Comp

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Zhang J, Ritter RC. Circulating GLP-1 and CCK-8 reduce food intake by capsaicin-insensitive, nonvagal mechanisms. Am J Physiol Regul Integr Comp Physiol 302: R264 -R273, 2012. First published October 26, 2011 doi:10.1152/ajpregu.00114.2011.-Previous reports suggest that glucagon-like peptide (GLP-1), a peptide secreted from the distal small intestine, is an endocrine satiation signal. Nevertheless, there are conflicting reports regarding the site where circulating GLP-1 acts to reduce food intake. To test the hypothesis that vagal afferents are necessary for reduction of food intake by circulating GLP-1, we measured intake of 15% sucrose during intravenous GLP-1 infusion in intact, vagotomized, and capsaicin-treated rats. We also measured sucrose intake during intravenous infusion of cholecystokinin, a peptide known to reduce food intake via abdominal vagal afferents. We found that reduction of intake by GLP-1 was not diminished by capsaicin treatment or vagotomy. In fact, reduction of sucrose intake by our highest GLP-1 dose was enhanced in vagotomized and capsaicin-treated rats. Intravenous GLP-1 induced comparable increases of hindbrain c-Fos immunoreactivity in intact, capsaicin-treated, and vagotomized rats. Plasma concentrations of active GLP-1 in capsaicin-treated rats did not differ from those of controls during the intravenous infusions. Finally, capsaicin treatment was not associated with altered GLP-1R mRNA in the brain, but nodose ganglia GLP-1R mRNA was significantly reduced in capsaicin-treated rats. Although reduction of food intake by intraperitoneal cholecystokinin was abolished in vagotomized and capsaicin-treated rats, reduction of intake by intravenous cholecystokinin was only partially attenuated. These results indicate that vagal or capsaicin-sensitive neurons are not necessary for reduction of food intake by circulating (endocrine) GLP-1, or cholecystokinin. Vagal participation in satiation by these peptides may be limited to paracrine effects exerted near the sites of their secretion.

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Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat

Cited by 68 publications

References 56 publications

Transient Receptor Potential Ankyrin 1 and Substance P Mediate the Development of Gastric Mucosal Lesions in a Water Immersion Restraint Stress Rat Model

Transient Receptor Potential Ankyrin 1 and Substance P Mediate the Development of Gastric Mucosal Lesions in a Water Immersion Restraint Stress Rat Model

Expression of mechanogated two-pore domain potassium channels in mouse lungs: special reference to mechanosensory airway receptors

Circulating GLP-1 and CCK-8 reduce food intake by capsaicin-insensitive, nonvagal mechanisms

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