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Published in: Digestive Diseases and Sciences 2/2018

01-02-2018 | Original Article

Distinct Expression of Phenotypic Markers in Placodes- and Neural Crest-Derived Afferent Neurons Innervating the Rat Stomach

Authors: Alzbeta Trancikova, Eva Kovacova, Fei Ru, Kristian Varga, Mariana Brozmanova, Milos Tatar, Marian Kollarik

Published in: Digestive Diseases and Sciences | Issue 2/2018

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Abstract

Background

Visceral pain is initiated by activation of primary afferent neurons among which the capsaicin-sensitive (TRPV1-positive) neurons play an important role. The stomach is a common source of visceral pain. Similar to other organs, the stomach receives dual spinal and vagal afferent innervation. Developmentally, spinal dorsal root ganglia (DRG) and vagal jugular neurons originate from embryonic neural crest and vagal nodose neurons originate from placodes. In thoracic organs the neural crest- and placodes-derived TRPV1-positive neurons have distinct phenotypes differing in activation profile, neurotrophic regulation and reflex responses. It is unknown to whether such distinction exists in the stomach.

Aims

We hypothesized that gastric neural crest- and placodes-derived TRPV1-positive neurons express phenotypic markers indicative of placodes and neural crest phenotypes.

Methods

Gastric DRG and vagal neurons were retrogradely traced by DiI injected into the rat stomach wall. Single-cell RT-PCR was performed on traced gastric neurons.

Results

Retrograde tracing demonstrated that vagal gastric neurons locate exclusively into the nodose portion of the rat jugular/petrosal/nodose complex. Gastric DRG TRPV1-positive neurons preferentially expressed markers PPT-A, TrkA and GFRα3 typical for neural crest-derived TRPV1-positive visceral neurons. In contrast, gastric nodose TRPV1-positive neurons preferentially expressed markers P2X2 and TrkB typical for placodes-derived TRPV1-positive visceral neurons. Differential expression of neural crest and placodes markers was less pronounced in TRPV1-negative DRG and nodose populations.

Conclusions

There are phenotypic distinctions between the neural crest-derived DRG and placodes-derived vagal nodose TRPV1-positive neurons innervating the rat stomach that are similar to those described in thoracic organs.
Literature
3.
go back to reference Boeckxstaens G, Camilleri M, Sifrim D, et al. Fundamentals of neurogastroenterology: physiology/motility–sensation. Gastroenterology. 2016;150:1292–1304.CrossRef Boeckxstaens G, Camilleri M, Sifrim D, et al. Fundamentals of neurogastroenterology: physiology/motility–sensation. Gastroenterology. 2016;150:1292–1304.CrossRef
5.
go back to reference Clarke GD, Davison JS. Mucosal receptors in the gastric antrum and small intestine of the rat with afferent fibres in the cervical vagus. J Physiol. 1978;284:55–67.CrossRefPubMedPubMedCentral Clarke GD, Davison JS. Mucosal receptors in the gastric antrum and small intestine of the rat with afferent fibres in the cervical vagus. J Physiol. 1978;284:55–67.CrossRefPubMedPubMedCentral
6.
go back to reference Andrews PL, Grundy D, Scratcherd T. Vagal afferent discharge from mechanoreceptors in different regions of the ferret stomach. J Physiol. 1980;298:513–524.CrossRefPubMedPubMedCentral Andrews PL, Grundy D, Scratcherd T. Vagal afferent discharge from mechanoreceptors in different regions of the ferret stomach. J Physiol. 1980;298:513–524.CrossRefPubMedPubMedCentral
7.
go back to reference Sharkey KA, Williams RG, Dockray GJ. Sensory substance p innervation of the stomach and pancreas. Demonstration of capsaicin-sensitive sensory neurons in the rat by combined immunohistochemistry and retrograde tracing. Gastroenterology. 1984;87:914–921.PubMed Sharkey KA, Williams RG, Dockray GJ. Sensory substance p innervation of the stomach and pancreas. Demonstration of capsaicin-sensitive sensory neurons in the rat by combined immunohistochemistry and retrograde tracing. Gastroenterology. 1984;87:914–921.PubMed
8.
go back to reference Green T, Dockray GJ. Calcitonin gene-related peptide and substance p in afferents to the upper gastrointestinal tract in the rat. Neurosci Lett. 1987;76:151–156.CrossRefPubMed Green T, Dockray GJ. Calcitonin gene-related peptide and substance p in afferents to the upper gastrointestinal tract in the rat. Neurosci Lett. 1987;76:151–156.CrossRefPubMed
9.
go back to reference Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol. 1989;283:248–268.CrossRefPubMed Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol. 1989;283:248–268.CrossRefPubMed
10.
go back to reference Blackshaw LA, Grundy D. Effects of cholecystokinin (cck-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst. 1990;31:191–201.CrossRefPubMed Blackshaw LA, Grundy D. Effects of cholecystokinin (cck-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst. 1990;31:191–201.CrossRefPubMed
11.
go back to reference Berthoud HR, Powley TL. Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol. 1992;319:261–276.CrossRefPubMed Berthoud HR, Powley TL. Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol. 1992;319:261–276.CrossRefPubMed
12.
go back to reference Page AJ, Blackshaw LA. An in vitro study of the properties of vagal afferent fibres innervating the ferret oesophagus and stomach. J Physiol. 1998;512:907–916.CrossRefPubMedPubMedCentral Page AJ, Blackshaw LA. An in vitro study of the properties of vagal afferent fibres innervating the ferret oesophagus and stomach. J Physiol. 1998;512:907–916.CrossRefPubMedPubMedCentral
13.
go back to reference Zagorodnyuk VP, Chen BN, Brookes SJ. Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol. 2001;534:255–268.CrossRefPubMedPubMedCentral Zagorodnyuk VP, Chen BN, Brookes SJ. Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol. 2001;534:255–268.CrossRefPubMedPubMedCentral
14.
go back to reference Ozaki N, Gebhart GF. Characterization of mechanosensitive splanchnic nerve afferent fibers innervating the rat stomach. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1449–G1459.CrossRefPubMed Ozaki N, Gebhart GF. Characterization of mechanosensitive splanchnic nerve afferent fibers innervating the rat stomach. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1449–G1459.CrossRefPubMed
15.
go back to reference Lamb K, Kang YM, Gebhart GF, Bielefeldt K. Nerve growth factor and gastric hyperalgesia in the rat. Neurogastroenterol Motil. 2003;15:355–361.CrossRefPubMed Lamb K, Kang YM, Gebhart GF, Bielefeldt K. Nerve growth factor and gastric hyperalgesia in the rat. Neurogastroenterol Motil. 2003;15:355–361.CrossRefPubMed
16.
go back to reference Schicho R, Florian W, Liebmann I, Holzer P, Lippe IT. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci. 2004;19:1811–1818.CrossRefPubMed Schicho R, Florian W, Liebmann I, Holzer P, Lippe IT. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci. 2004;19:1811–1818.CrossRefPubMed
17.
go back to reference Bielefeldt K, Zhong F, Koerber HR, Davis BM. Phenotypic characterization of gastric sensory neurons in mice. Am J Physiol Gastrointest Liver Physiol. 2006;291:G987–G997.CrossRefPubMed Bielefeldt K, Zhong F, Koerber HR, Davis BM. Phenotypic characterization of gastric sensory neurons in mice. Am J Physiol Gastrointest Liver Physiol. 2006;291:G987–G997.CrossRefPubMed
18.
go back to reference Wultsch T, Painsipp E, Shahbazian A, et al. Deletion of the acid-sensing ion channel ASIC3 prevents gastritis-induced acid hyperresponsiveness of the stomach–brainstem axis. Pain. 2008;134:245–253.CrossRefPubMed Wultsch T, Painsipp E, Shahbazian A, et al. Deletion of the acid-sensing ion channel ASIC3 prevents gastritis-induced acid hyperresponsiveness of the stomach–brainstem axis. Pain. 2008;134:245–253.CrossRefPubMed
19.
go back to reference Sakurai J, Obata K, Ozaki N, et al. Activation of extracellular signal-regulated protein kinase in sensory neurons after noxious gastric distention and its involvement in acute visceral pain in rats. Gastroenterology. 2008;134:1094–1103.CrossRefPubMed Sakurai J, Obata K, Ozaki N, et al. Activation of extracellular signal-regulated protein kinase in sensory neurons after noxious gastric distention and its involvement in acute visceral pain in rats. Gastroenterology. 2008;134:1094–1103.CrossRefPubMed
20.
go back to reference Young RL, Cooper NJ, Blackshaw LA. Chemical coding and central projections of gastric vagal afferent neurons. Neurogastroenterol Motil. 2008;20:708–718.CrossRefPubMed Young RL, Cooper NJ, Blackshaw LA. Chemical coding and central projections of gastric vagal afferent neurons. Neurogastroenterol Motil. 2008;20:708–718.CrossRefPubMed
21.
go back to reference Kondo T, Obata K, Miyoshi K, et al. Transient receptor potential A1 mediates gastric distention-induced visceral pain in rats. Gut. 2009;58:1342–1352.CrossRefPubMed Kondo T, Obata K, Miyoshi K, et al. Transient receptor potential A1 mediates gastric distention-induced visceral pain in rats. Gut. 2009;58:1342–1352.CrossRefPubMed
22.
go back to reference Kentish SJ, O’Donnell TA, Isaacs NJ, et al. Gastric vagal afferent modulation by leptin is influenced by food intake status. J Physiol. 2013;591:1921–1934.CrossRefPubMed Kentish SJ, O’Donnell TA, Isaacs NJ, et al. Gastric vagal afferent modulation by leptin is influenced by food intake status. J Physiol. 2013;591:1921–1934.CrossRefPubMed
23.
go back to reference Spencer NJ, Kyloh M, Beckett EA, Brookes S, Hibberd T. Different types of spinal afferent nerve endings in stomach and esophagus identified by anterograde tracing from dorsal root ganglia. J Comp Neurol. 2016;524:3064–3083.CrossRefPubMed Spencer NJ, Kyloh M, Beckett EA, Brookes S, Hibberd T. Different types of spinal afferent nerve endings in stomach and esophagus identified by anterograde tracing from dorsal root ganglia. J Comp Neurol. 2016;524:3064–3083.CrossRefPubMed
24.
go back to reference Powley TL, Hudson CN, McAdams JL, Baronowsky EA, Phillips RJ. Vagal intramuscular arrays: the specialized mechanoreceptor arbors that innervate the smooth muscle layers of the stomach examined in the rat. J Comp Neurol. 2016;524:713–737.CrossRefPubMed Powley TL, Hudson CN, McAdams JL, Baronowsky EA, Phillips RJ. Vagal intramuscular arrays: the specialized mechanoreceptor arbors that innervate the smooth muscle layers of the stomach examined in the rat. J Comp Neurol. 2016;524:713–737.CrossRefPubMed
25.
go back to reference Sharrad DF, Hibberd TJ, Kyloh MA, Brookes SJ, Spencer NJ. Quantitative immunohistochemical co-localization of TRPV1 and CGRP in varicose axons of the murine oesophagus, stomach and colorectum. Neurosci Lett. 2015;599:164–171.CrossRefPubMed Sharrad DF, Hibberd TJ, Kyloh MA, Brookes SJ, Spencer NJ. Quantitative immunohistochemical co-localization of TRPV1 and CGRP in varicose axons of the murine oesophagus, stomach and colorectum. Neurosci Lett. 2015;599:164–171.CrossRefPubMed
26.
go back to reference Spencer NJ, Zagorodnyuk V, Brookes SJ, Hibberd T. Spinal afferent nerve endings in visceral organs: recent advances. Am J Physiol Gastrointest Liver Physiol. 2016;311:G1056–G1063.CrossRefPubMed Spencer NJ, Zagorodnyuk V, Brookes SJ, Hibberd T. Spinal afferent nerve endings in visceral organs: recent advances. Am J Physiol Gastrointest Liver Physiol. 2016;311:G1056–G1063.CrossRefPubMed
27.
go back to reference Baker CV, Bronner-Fraser M. Vertebrate cranial placodes I. Embryonic induction. Dev Biol. 2001;232:1–61.CrossRefPubMed Baker CV, Bronner-Fraser M. Vertebrate cranial placodes I. Embryonic induction. Dev Biol. 2001;232:1–61.CrossRefPubMed
28.
go back to reference Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, Kollarik M. Subtypes of vagal afferent c-fibres in guinea-pig lungs. J Physiol. 2004;556:905–917.CrossRefPubMedPubMedCentral Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, Kollarik M. Subtypes of vagal afferent c-fibres in guinea-pig lungs. J Physiol. 2004;556:905–917.CrossRefPubMedPubMedCentral
30.
go back to reference Nassenstein C, Taylor-Clark TE, Myers AC, et al. Phenotypic distinctions between neural crest and placodal derived vagal c-fibres in mouse lungs. J Physiol. 2010;588:4769–4783.CrossRefPubMedPubMedCentral Nassenstein C, Taylor-Clark TE, Myers AC, et al. Phenotypic distinctions between neural crest and placodal derived vagal c-fibres in mouse lungs. J Physiol. 2010;588:4769–4783.CrossRefPubMedPubMedCentral
31.
go back to reference Surdenikova L, Ru F, Nassenstein C, Tatar M, Kollarik M. The neural crest- and placodes-derived afferent innervation of the mouse esophagus. Neurogastroenterol Motil. 2012;24:e517–e525.CrossRefPubMed Surdenikova L, Ru F, Nassenstein C, Tatar M, Kollarik M. The neural crest- and placodes-derived afferent innervation of the mouse esophagus. Neurogastroenterol Motil. 2012;24:e517–e525.CrossRefPubMed
32.
go back to reference Kwong K, Kollarik M, Nassenstein C, Ru F, Undem BJ. P2X2 receptors differentiate placodal vs. neural crest c-fiber phenotypes innervating guinea pig lungs and esophagus. Am J Physiol Lung Cell Mol Physiol. 2008;295:L858–L865.CrossRefPubMedPubMedCentral Kwong K, Kollarik M, Nassenstein C, Ru F, Undem BJ. P2X2 receptors differentiate placodal vs. neural crest c-fiber phenotypes innervating guinea pig lungs and esophagus. Am J Physiol Lung Cell Mol Physiol. 2008;295:L858–L865.CrossRefPubMedPubMedCentral
33.
go back to reference Lamb K, Kang YM, Gebhart GF, Bielefeldt K. Gastric inflammation triggers hypersensitivity to acid in awake rats. Gastroenterology. 2003;125:1410–1418.CrossRefPubMed Lamb K, Kang YM, Gebhart GF, Bielefeldt K. Gastric inflammation triggers hypersensitivity to acid in awake rats. Gastroenterology. 2003;125:1410–1418.CrossRefPubMed
34.
go back to reference Liu Q, Tang Z, Surdenikova L, et al. Sensory neuron-specific gpcr mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009;139:1353–1365.CrossRefPubMedPubMedCentral Liu Q, Tang Z, Surdenikova L, et al. Sensory neuron-specific gpcr mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009;139:1353–1365.CrossRefPubMedPubMedCentral
35.
go back to reference Ru F, Surdenikova L, Brozmanova M, Kollarik M. Adenosine-induced activation of esophageal nociceptors. Am J Physiol Gastrointest Liver Physiol. 2011;300:G485–G493.CrossRefPubMed Ru F, Surdenikova L, Brozmanova M, Kollarik M. Adenosine-induced activation of esophageal nociceptors. Am J Physiol Gastrointest Liver Physiol. 2011;300:G485–G493.CrossRefPubMed
36.
go back to reference Rozen S, Skaletsky J. Primer3 on the www for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics methods and protocols: methods in molecular biology. Totowa: Humana Press; 2000:365–386. Rozen S, Skaletsky J. Primer3 on the www for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics methods and protocols: methods in molecular biology. Totowa: Humana Press; 2000:365–386.
37.
go back to reference Wank M, Neuhuber WL. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections. J Comp Neurol. 2001;435:41–59.CrossRefPubMed Wank M, Neuhuber WL. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections. J Comp Neurol. 2001;435:41–59.CrossRefPubMed
38.
go back to reference McGovern AE, Driessen AK, Simmons DG, et al. Distinct brainstem and forebrain circuits receiving tracheal sensory neuron inputs revealed using a novel conditional anterograde transsynaptic viral tracing system. J Neurosci. 2015;35:7041–7055.CrossRefPubMed McGovern AE, Driessen AK, Simmons DG, et al. Distinct brainstem and forebrain circuits receiving tracheal sensory neuron inputs revealed using a novel conditional anterograde transsynaptic viral tracing system. J Neurosci. 2015;35:7041–7055.CrossRefPubMed
39.
go back to reference Ayer-LeLievre CS, Seiger A. Development of substance p-immunoreactive neurons in cranial sensory ganglia of the rat. Int J Dev Neurosci. 1984;2:451–463.CrossRefPubMed Ayer-LeLievre CS, Seiger A. Development of substance p-immunoreactive neurons in cranial sensory ganglia of the rat. Int J Dev Neurosci. 1984;2:451–463.CrossRefPubMed
41.
go back to reference Green T, Dockray GJ. Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig. Neuroscience. 1988;25:181–193.CrossRefPubMed Green T, Dockray GJ. Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig. Neuroscience. 1988;25:181–193.CrossRefPubMed
43.
go back to reference Airaksinen MS, Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci. 2002;3:383–394.CrossRefPubMed Airaksinen MS, Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci. 2002;3:383–394.CrossRefPubMed
44.
go back to reference Paratcha G, Ledda F. Gdnf and gfralpha: a versatile molecular complex for developing neurons. Trends Neurosci. 2008;31:384–391.CrossRefPubMed Paratcha G, Ledda F. Gdnf and gfralpha: a versatile molecular complex for developing neurons. Trends Neurosci. 2008;31:384–391.CrossRefPubMed
45.
go back to reference Canning BJ, Mazzone SB, Meeker SN, Mori N, Reynolds SM, Undem BJ. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J Physiol. 2004;557:543–558.CrossRefPubMedPubMedCentral Canning BJ, Mazzone SB, Meeker SN, Mori N, Reynolds SM, Undem BJ. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J Physiol. 2004;557:543–558.CrossRefPubMedPubMedCentral
46.
go back to reference Ho CY, Gu Q, Lin YS, Lee LY. Sensitivity of vagal afferent endings to chemical irritants in the rat lung. Respir Physiol. 2001;127:113–124.CrossRefPubMed Ho CY, Gu Q, Lin YS, Lee LY. Sensitivity of vagal afferent endings to chemical irritants in the rat lung. Respir Physiol. 2001;127:113–124.CrossRefPubMed
47.
go back to reference Hong JL, Ho CY, Kwong K, Lee LY. Activation of pulmonary c fibres by adenosine in anaesthetized rats: role of adenosine A1 receptors. J Physiol. 1998;508:109–118.CrossRefPubMedPubMedCentral Hong JL, Ho CY, Kwong K, Lee LY. Activation of pulmonary c fibres by adenosine in anaesthetized rats: role of adenosine A1 receptors. J Physiol. 1998;508:109–118.CrossRefPubMedPubMedCentral
48.
go back to reference Dusenkova S, Ru F, Surdenikova L, et al. The expression profile of acid-sensing ion channel (ASIC) subunits ASIC1a, ASIC1b, ASIC2a, ASIC2b, and ASIC3 in the esophageal vagal afferent nerve subtypes. Am J Physiol Gastrointest Liver Physiol. 2014;307:G922–G930.CrossRefPubMedPubMedCentral Dusenkova S, Ru F, Surdenikova L, et al. The expression profile of acid-sensing ion channel (ASIC) subunits ASIC1a, ASIC1b, ASIC2a, ASIC2b, and ASIC3 in the esophageal vagal afferent nerve subtypes. Am J Physiol Gastrointest Liver Physiol. 2014;307:G922–G930.CrossRefPubMedPubMedCentral
49.
go back to reference Ru F, Banovcin P Jr, Kollarik M. Acid sensitivity of the spinal dorsal root ganglia c-fiber nociceptors innervating the guinea pig esophagus. Neurogastroenterol Motil. 2015;27:865–874.CrossRefPubMedPubMedCentral Ru F, Banovcin P Jr, Kollarik M. Acid sensitivity of the spinal dorsal root ganglia c-fiber nociceptors innervating the guinea pig esophagus. Neurogastroenterol Motil. 2015;27:865–874.CrossRefPubMedPubMedCentral
50.
go back to reference Grabauskas G, Zhou SY, Lu Y, Song I, Owyang C. Essential elements for glucosensing by gastric vagal afferents: immunocytochemistry and electrophysiology studies in the rat. Endocrinology. 2013;154:296–307.CrossRefPubMed Grabauskas G, Zhou SY, Lu Y, Song I, Owyang C. Essential elements for glucosensing by gastric vagal afferents: immunocytochemistry and electrophysiology studies in the rat. Endocrinology. 2013;154:296–307.CrossRefPubMed
51.
go back to reference Lee LY, Shuei Lin Y, Gu Q, Chung E, Ho CY. Functional morphology and physiological properties of bronchopulmonary c-fiber afferents. Anat Rec A Discov Mol Cell Evol Biol. 2003;270:17–24.CrossRefPubMed Lee LY, Shuei Lin Y, Gu Q, Chung E, Ho CY. Functional morphology and physiological properties of bronchopulmonary c-fiber afferents. Anat Rec A Discov Mol Cell Evol Biol. 2003;270:17–24.CrossRefPubMed
52.
go back to reference Berthoud HR, Lynn PA, Blackshaw LA. Vagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1371–R1381.CrossRefPubMed Berthoud HR, Lynn PA, Blackshaw LA. Vagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1371–R1381.CrossRefPubMed
53.
go back to reference Yu S, Ru F, Ouyang A, Kollarik M. 5-Hydroxytryptamine selectively activates the vagal nodose c-fibre subtype in the guinea-pig oesophagus. Neurogastroenterol Motil. 2008;20:1042–1050.CrossRefPubMed Yu S, Ru F, Ouyang A, Kollarik M. 5-Hydroxytryptamine selectively activates the vagal nodose c-fibre subtype in the guinea-pig oesophagus. Neurogastroenterol Motil. 2008;20:1042–1050.CrossRefPubMed
54.
go back to reference Blackshaw LA, Grundy D. Effects of 5-hydroxytryptamine (5-ht) on the discharge of vagal mechanoreceptors and motility in the upper gastrointestinal tract of the ferret. J Auton Nerv Syst. 1993;45:51–59.CrossRefPubMed Blackshaw LA, Grundy D. Effects of 5-hydroxytryptamine (5-ht) on the discharge of vagal mechanoreceptors and motility in the upper gastrointestinal tract of the ferret. J Auton Nerv Syst. 1993;45:51–59.CrossRefPubMed
55.
go back to reference Blackshaw LA, Grundy D. Effects of 5-hydroxytryptamine on discharge of vagal mucosal afferent fibres from the upper gastrointestinal tract of the ferret. J Auton Nerv Syst. 1993;45:41–50.CrossRefPubMed Blackshaw LA, Grundy D. Effects of 5-hydroxytryptamine on discharge of vagal mucosal afferent fibres from the upper gastrointestinal tract of the ferret. J Auton Nerv Syst. 1993;45:41–50.CrossRefPubMed
56.
go back to reference Dang K, Bielfeldt K, Lamb K, Gebhart GF. Gastric ulcers evoke hyperexcitability and enhance P2X receptor function in rat gastric sensory neurons. J Neurophysiol. 2005;93:3112–3119.CrossRefPubMed Dang K, Bielfeldt K, Lamb K, Gebhart GF. Gastric ulcers evoke hyperexcitability and enhance P2X receptor function in rat gastric sensory neurons. J Neurophysiol. 2005;93:3112–3119.CrossRefPubMed
57.
go back to reference Cockayne DA, Dunn PM, Zhong Y, et al. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol. 2005;567:621–639.CrossRefPubMedPubMedCentral Cockayne DA, Dunn PM, Zhong Y, et al. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol. 2005;567:621–639.CrossRefPubMedPubMedCentral
58.
go back to reference Bielefeldt K, Ozaki N, Gebhart GF. Role of nerve growth factor in modulation of gastric afferent neurons in the rat. Am J Physiol Gastrointest Liver Physiol. 2003;284:G499–G507.CrossRefPubMed Bielefeldt K, Ozaki N, Gebhart GF. Role of nerve growth factor in modulation of gastric afferent neurons in the rat. Am J Physiol Gastrointest Liver Physiol. 2003;284:G499–G507.CrossRefPubMed
59.
go back to reference Michael GJ, Priestley JV. Differential expression of the mrna for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci. 1999;19:1844–1854.PubMed Michael GJ, Priestley JV. Differential expression of the mrna for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci. 1999;19:1844–1854.PubMed
60.
go back to reference Kashiba H, Uchida Y, Senba E. Distribution and colocalization of NGF and GDNF family ligand receptor MRNAS in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res. 2003;110:52–62.CrossRefPubMed Kashiba H, Uchida Y, Senba E. Distribution and colocalization of NGF and GDNF family ligand receptor MRNAS in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res. 2003;110:52–62.CrossRefPubMed
61.
go back to reference Fasanella KE, Christianson JA, Chanthaphavong RS, Davis BM. Distribution and neurochemical identification of pancreatic afferents in the mouse. J Comp Neurol. 2008;509:42–52.CrossRefPubMedPubMedCentral Fasanella KE, Christianson JA, Chanthaphavong RS, Davis BM. Distribution and neurochemical identification of pancreatic afferents in the mouse. J Comp Neurol. 2008;509:42–52.CrossRefPubMedPubMedCentral
62.
go back to reference Berthoud HR, Patterson LM, Willing AE, Mueller K, Neuhuber WL. Capsaicin-resistant vagal afferent fibers in the rat gastrointestinal tract: anatomical identification and functional integrity. Brain Res. 1997;746:195–206.CrossRefPubMed Berthoud HR, Patterson LM, Willing AE, Mueller K, Neuhuber WL. Capsaicin-resistant vagal afferent fibers in the rat gastrointestinal tract: anatomical identification and functional integrity. Brain Res. 1997;746:195–206.CrossRefPubMed
63.
go back to reference Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M. Brain-derived neurotrophic factor immunoreactive vagal sensory neurons innervating the gastrointestinal tract of the rat. J Chem Neuroanat. 2014;61–62:83–87.CrossRefPubMed Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M. Brain-derived neurotrophic factor immunoreactive vagal sensory neurons innervating the gastrointestinal tract of the rat. J Chem Neuroanat. 2014;61–62:83–87.CrossRefPubMed
64.
go back to reference Khurana RK, Petras JM. Sensory innervation of the canine esophagus, stomach, and duodenum. Am J Anat. 1991;192:293–306.CrossRefPubMed Khurana RK, Petras JM. Sensory innervation of the canine esophagus, stomach, and duodenum. Am J Anat. 1991;192:293–306.CrossRefPubMed
65.
go back to reference Elfvin LG, Lindh B. A study of the extrinsic innervation of the guinea pig pylorus with the horseradish peroxidase tracing technique. J Comp Neurol. 1982;208:317–324.CrossRefPubMed Elfvin LG, Lindh B. A study of the extrinsic innervation of the guinea pig pylorus with the horseradish peroxidase tracing technique. J Comp Neurol. 1982;208:317–324.CrossRefPubMed
66.
go back to reference Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M. Projections of calcitonin gene-related peptide immunoreactive neurons in the vagal ganglia of the rat. J Chem Neuroanat. 2011;41:55–62.CrossRefPubMed Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M. Projections of calcitonin gene-related peptide immunoreactive neurons in the vagal ganglia of the rat. J Chem Neuroanat. 2011;41:55–62.CrossRefPubMed
67.
go back to reference Carobi C, Magni F. The afferent innervation of the liver: a horseradish peroxidase study in the rat. Neurosci Lett. 1981;23:269–274.CrossRefPubMed Carobi C, Magni F. The afferent innervation of the liver: a horseradish peroxidase study in the rat. Neurosci Lett. 1981;23:269–274.CrossRefPubMed
68.
go back to reference Luts A, Uddman R, Grunditz T, Sundler F. Peptide-containing neurons projecting to the vocal cords of the rat: retrograde tracing and immunocytochemistry. J Auton Nerv Syst. 1990;30:179–191.CrossRefPubMed Luts A, Uddman R, Grunditz T, Sundler F. Peptide-containing neurons projecting to the vocal cords of the rat: retrograde tracing and immunocytochemistry. J Auton Nerv Syst. 1990;30:179–191.CrossRefPubMed
69.
70.
go back to reference Springall DR, Cadieux A, Oliveira H, Su H, Royston D, Polak JM. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst. 1987;20:155–166.CrossRefPubMed Springall DR, Cadieux A, Oliveira H, Su H, Royston D, Polak JM. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst. 1987;20:155–166.CrossRefPubMed
71.
go back to reference Grunditz T, Hakanson R, Sundler F, Uddman R. Neuronal pathways to the rat thyroid revealed by retrograde tracing and immunocytochemistry. Neuroscience. 1988;24:321–335.CrossRefPubMed Grunditz T, Hakanson R, Sundler F, Uddman R. Neuronal pathways to the rat thyroid revealed by retrograde tracing and immunocytochemistry. Neuroscience. 1988;24:321–335.CrossRefPubMed
72.
go back to reference Brozmanova M, Ru F, Surdenikova L, Mazurova L, Taylor-Clark T, Kollarik M. Preferential activation of the vagal nodose nociceptive subtype by TRPA1 agonists in the guinea pig esophagus. Neurogastroenterol Motil. 2011;23:e437–e445.CrossRefPubMedPubMedCentral Brozmanova M, Ru F, Surdenikova L, Mazurova L, Taylor-Clark T, Kollarik M. Preferential activation of the vagal nodose nociceptive subtype by TRPA1 agonists in the guinea pig esophagus. Neurogastroenterol Motil. 2011;23:e437–e445.CrossRefPubMedPubMedCentral
73.
go back to reference Nassenstein C, Kwong K, Taylor-Clark T, et al. Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J Physiol. 2008;586:1595–1604.CrossRefPubMedPubMedCentral Nassenstein C, Kwong K, Taylor-Clark T, et al. Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J Physiol. 2008;586:1595–1604.CrossRefPubMedPubMedCentral
74.
go back to reference Kollarik M, Dinh QT, Fischer A, Undem BJ. Capsaicin-sensitive and -insensitive vagal bronchopulmonary c-fibres in the mouse. J Physiol. 2003;551:869–879.CrossRefPubMedPubMedCentral Kollarik M, Dinh QT, Fischer A, Undem BJ. Capsaicin-sensitive and -insensitive vagal bronchopulmonary c-fibres in the mouse. J Physiol. 2003;551:869–879.CrossRefPubMedPubMedCentral
75.
go back to reference Yu X, Hu Y, Ru F, Kollarik M, Undem BJ, Yu S. TRPM8 function and expression in vagal sensory neurons and afferent nerves innervating guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol. 2015;308:G489–G496.CrossRefPubMedPubMedCentral Yu X, Hu Y, Ru F, Kollarik M, Undem BJ, Yu S. TRPM8 function and expression in vagal sensory neurons and afferent nerves innervating guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol. 2015;308:G489–G496.CrossRefPubMedPubMedCentral
76.
go back to reference Chuaychoo B, Lee MG, Kollarik M, Pullmann R Jr, Undem BJ. Evidence for both adenosine A1 and A2A receptors activating single vagal sensory c-fibres in guinea pig lungs. J Physiol. 2006;575:481–490.CrossRefPubMedPubMedCentral Chuaychoo B, Lee MG, Kollarik M, Pullmann R Jr, Undem BJ. Evidence for both adenosine A1 and A2A receptors activating single vagal sensory c-fibres in guinea pig lungs. J Physiol. 2006;575:481–490.CrossRefPubMedPubMedCentral
77.
go back to reference Kwong K, Nassenstein C, de Garavilla L, Meeker S, Undem BJ. Thrombin and trypsin directly activate vagal c-fibres in mouse lung via protease-activated receptor-1. J Physiol. 2010;588:1171–1177.CrossRefPubMedPubMedCentral Kwong K, Nassenstein C, de Garavilla L, Meeker S, Undem BJ. Thrombin and trypsin directly activate vagal c-fibres in mouse lung via protease-activated receptor-1. J Physiol. 2010;588:1171–1177.CrossRefPubMedPubMedCentral
Metadata
Title
Distinct Expression of Phenotypic Markers in Placodes- and Neural Crest-Derived Afferent Neurons Innervating the Rat Stomach
Authors
Alzbeta Trancikova
Eva Kovacova
Fei Ru
Kristian Varga
Mariana Brozmanova
Milos Tatar
Marian Kollarik
Publication date
01-02-2018
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 2/2018
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-017-4883-5

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