Purinergic inhibitory regulation of esophageal smooth muscle is mediated by P2Y receptors and ATP-dependent potassium channels in rats.
ATP-dependent potassium channel
Esophagus
P2 receptor
Purine
Smooth muscle
Journal
The journal of physiological sciences : JPS
ISSN: 1880-6562
Titre abrégé: J Physiol Sci
Pays: Japan
ID NLM: 101262417
Informations de publication
Date de publication:
23 Apr 2024
23 Apr 2024
Historique:
received:
19
09
2023
accepted:
20
03
2024
medline:
24
4
2024
pubmed:
24
4
2024
entrez:
23
4
2024
Statut:
epublish
Résumé
Purines such as ATP are regulatory transmitters in motility of the gastrointestinal tract. The aims of this study were to propose functional roles of purinergic regulation of esophageal motility. An isolated segment of the rat esophagus was placed in an organ bath, and mechanical responses were recorded using a force transducer. Exogenous application of ATP (10-100 μM) evoked relaxation of the esophageal smooth muscle in a longitudinal direction under the condition of carbachol (1 μM) -induced precontraction. Pretreatment with a non-selective P2 receptor antagonist, suramin (500 μM), and a P2Y receptor antagonist, cibacron blue F3GA (200 μM), inhibited the ATP (100 μM) -induced relaxation, but a P2X receptor antagonist, pyridoxal phosphate-6-azophenyl-2,4-disulfonic acid (50 μM), did not affect it. A blocker of ATP-dependent potassium channels (K
Identifiants
pubmed: 38654149
doi: 10.1186/s12576-024-00916-5
pii: 10.1186/s12576-024-00916-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
26Subventions
Organisme : Grants-in-Aid for Scientific Research (KAKENHI)
ID : 23K05553
Organisme : Grants-in-Aid for Scientific Research (KAKENHI)
ID : 23H00360
Informations de copyright
© 2024. The Author(s).
Références
Neuhuber WL, Wörl J (2006) Enteric co-innervation of striated muscle in the esophagus: still enigmatic? Histochem Cell Biol 146:721–735
doi: 10.1007/s00418-016-1500-1
Shiina T, Shima T, Wörl J, Neuhuber WL, Shimizu Y (2010) The neural regulation of the mammalian esophageal motility and its implication for esophageal diseases. Pathophysiology 17:129–133
pubmed: 19497713
doi: 10.1016/j.pathophys.2009.03.008
Wörl J, Neuhuber WL (2005) Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol 123:117–130
pubmed: 15729553
doi: 10.1007/s00418-005-0764-7
Shiina T, Shima T, Masuda K, Hirayama H, Iwami M, Takewaki T, Kuramoto H, Shimizu Y (2010) Contractile properties of esophageal striated muscle: comparison with cardiac and skeletal muscles in rats. J Biomed Biotech 2010:459789
doi: 10.1155/2010/459789
Shiina T, Shimizu Y, Izumi N, Suzuki Y, Asano M, Atoji Y, Nikami H, Takewaki T (2005) A comparative histological study on the distribution of striated and smooth muscles and glands in the esophagus of wild birds and mammals. J Vet Med Sci 67:115–117
pubmed: 15699607
doi: 10.1292/jvms.67.115
Shiina T, Shima T, Hirayama H, Kuramoto H, Takewaki T, Shimizu Y (2010) Contractile responses induced by physalaemin, an analogue of substance P, in the rat esophagus. Eur J Pharmacol 628:202–206
pubmed: 19958761
doi: 10.1016/j.ejphar.2009.11.039
Shiina T, Naitou K, Nakamori H, Sakai H, Shimizu Y (2015) Regulation of longitudinal esophageal motility in the house musk shrew (Suncus murinus). Auton Neurosci 189:37–42
pubmed: 25694232
doi: 10.1016/j.autneu.2015.02.003
Shiina T, Naitou K, Nakamori H, Suzuki Y, Horii K, Sano Y, Shimaoka H, Shimizu Y (2016) Serotonin-induced contractile responses of esophageal smooth muscle in the house musk shrew (Suncus murinus). Neurogastroenterol Motil 28:1641–1648
pubmed: 27194102
doi: 10.1111/nmo.12863
Bieger D, Neuhuber WL (2006) Neural circuits and mediators regulating swallowing in the brainstem. GI Motility Onl. https://doi.org/10.1038/gimo74
doi: 10.1038/gimo74
Clouse RE, Diamant NE (2006) Motor Function of the Esophagus. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 4th edn. Elsevier Academic Press, Burlington, pp 913–926
doi: 10.1016/B978-012088394-3/50039-8
Boudaka A, Wörl J, Shiina T, Neuhuber WL, Kobayashi H, Shimizu Y, Takewaki T (2007) Involvement of TRPV1-dependent and -independent components in the regulation of vagally induced contractions in the mouse esophagus. Eur J Pharmacol 556:157–165
pubmed: 17156774
doi: 10.1016/j.ejphar.2006.11.005
Boudaka A, Wörl J, Shiina T, Shimizu Y, Takewaki T, Neuhuber WL (2009) Galanin modulates vagally induced contractions in the mouse esophagus. Neurogastroenterol Motil 21:180–188
pubmed: 19077146
doi: 10.1111/j.1365-2982.2008.01224.x
Izumi N, Matsuyama H, Ko M, Shimizu Y, Takewaki T (2003) Role of intrinsic nitrergic neurones on vagally mediated striated muscle contractions in the hamster oesophagus. J Physiol 551:287–294
pubmed: 12813149
pmcid: 2343159
doi: 10.1113/jphysiol.2003.044669
Shiina T, Shimizu Y, Boudaka A, Wörl J, Takewaki T (2006) Tachykinins are involved in local reflex modulation of vagally mediated striated muscle contractions in the rat esophagus via tachykinin NK1 receptors. Neuroscience 139:495–503
pubmed: 16458437
doi: 10.1016/j.neuroscience.2005.12.027
Shiina T, Shima T, Suzuki Y, Wörl J, Shimizu Y (2012) Neural regulation of esophageal striated muscle in the house musk shrew (Suncus murinus). Auton Neurosci 168:25–31
pubmed: 22285704
doi: 10.1016/j.autneu.2012.01.003
Burnstock G, Ralevic V (2013) Purinergic signaling and blood vessels in health and disease. Pharmacol Rev 66:102–192
pubmed: 24335194
doi: 10.1124/pr.113.008029
Burnstock G (2014) Purinergic signalling in the gastrointestinal tract and related organs in health and disease. Purinergic Signal 10:3–50
pubmed: 24307520
doi: 10.1007/s11302-013-9397-9
Furness JB (2006) The enteric nervous system. Blackwell Publishing, Malden
Hansen MB (2003) Neurohumoral control of gastrointestinal motility. Physiol Res 52:1–30
pubmed: 12625803
doi: 10.33549/physiolres.930255
Sanders KM (1998) G protein-coupled receptors in gastrointestinal physiology. IV. Neural regulation of gastrointestinal smooth muscle. Am J Physiol 275:G1-7
pubmed: 9655677
Burnstock G (1996) Development and perspectives of the purinoceptor concept. J Auton Pharmacol 16:295–302
pubmed: 9131402
doi: 10.1111/j.1474-8673.1996.tb00039.x
Burnstock G (1997) The past, present and future of purine nucleotides as signalling molecules. Neuropharmacology 36:1127–1139
pubmed: 9364468
doi: 10.1016/S0028-3908(97)00125-1
Jiménez M, Clavé P, Accarino A, Gallego D (2014) Purinergic neuromuscular transmission in the gastrointestinal tract; functional basis for future clinical and pharmacological studies. Br J Pharmacol 171:4360–4375
pubmed: 24910216
pmcid: 4209144
doi: 10.1111/bph.12802
Goyal RK, Sullivan MP, Chaudhury A (2013) Progress in understanding of inhibitory purinergic neuromuscular transmission in the gut. Neurogastroenterol Motil 25:203–207
pubmed: 23414428
pmcid: 8630810
doi: 10.1111/nmo.12090
Kestler C, Neuhuber WL, Raab M (2009) Distribution of P2X3 receptor immunoreactivity in myenteric ganglia of the mouse esophagus. Histochem Cell Biol 131:13–27
pubmed: 18810483
doi: 10.1007/s00418-008-0498-4
Wang ZJ, Neuhuber WL (2003) Intraganglionic laminar endings in the rat esophagus contain purinergic P2X2 and P2X3 receptor immunoreactivity. Anat Embryol (Berl) 207:363–371
pubmed: 14624359
doi: 10.1007/s00429-003-0351-4
Kwon TH, Jung H, Cho EJ, Jeong JH, Sohn UD (2015) The signaling mechanism of contraction induced by ATP and UTP in feline esophageal smooth muscle cells. Mol Cells 38:616–623
pubmed: 26013385
pmcid: 4507027
doi: 10.14348/molcells.2015.2357
Mihara H, Boudaka A, Sugiyama T, Moriyama Y, Tominaga M (2011) Transient receptor potential vanilloid 4 (TRPV4)-dependent calcium influx and ATP release in mouse oesophageal keratinocytes. J Physiol 589:3471–3482
pubmed: 21540339
pmcid: 3167111
doi: 10.1113/jphysiol.2011.207829
Bieger D, Triggle C (1985) Pharmacological properties of mechanical responses of the rat oesophageal muscularis mucosae to vagal and field stimulation. Br J Pharmacol 84:93–106
pubmed: 3156647
pmcid: 1987205
Storr M, Geisler F, Neuhuber WL, Schusdziarra V, Allescher HD (2000) Endomorphin-1 and -2, endogenous ligands for the mu-opioid receptor, inhibit striated and smooth muscle contraction in the rat oesophagus. Neurogastroenterol Motil 12:441–448
pubmed: 11012944
doi: 10.1046/j.1365-2982.2000.00220.x
Storr M, Geisler F, Neuhuber WL, Schusdziarra V, Allescher HD (2001) Characterization of vagal input to the rat esophageal muscle. Auton Neurosci 91:1–9
pubmed: 11515794
doi: 10.1016/S1566-0702(01)00290-9
Dunn PM, Blakeley AGH (1988) Suramin: a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br J Pharmacol 93:243–245
pubmed: 3359103
pmcid: 1853806
doi: 10.1111/j.1476-5381.1988.tb11427.x
Hourani SMO, Hall DA, Nieman CJ (1992) Effects of the P2-purinoceptor antagonist, suramin, on human platelet aggregation induced by adenosine 5’-diphosphate. Br J Pharmacol 105:453–457
pubmed: 1559134
pmcid: 1908649
doi: 10.1111/j.1476-5381.1992.tb14274.x
Uneyama H, Uneyama C, Ebihara S, Akaike N (1994) Suramin and reactive blue 2 are antagonists for a newly identified purinoceptor on rat megakaryocyte. Br J Pharmacol 111:245–249
pubmed: 7516802
pmcid: 1910005
doi: 10.1111/j.1476-5381.1994.tb14051.x
Burnstock G, Warland JJI (1987) P2-purinoceptors of two subtypes in the rabbit mesenteric artery: reactive blue 2 selectively inhibits responses mediated via the P2Y- but not P2X-purinoceptor. Br J Pharmacol 90:383–391
pubmed: 3828656
pmcid: 1916939
doi: 10.1111/j.1476-5381.1987.tb08968.x
Ziganshin AU, Hoyle CH, Bo X, Lambrecht G, Mutschler E, Bäumert HG, Burnstock G (1993) PPADS selectively antagonizes P2X-purinoceptor-mediated responses in the rabbit urinary bladder. Br J Pharmacol 110:1491–1495
pubmed: 8306091
pmcid: 2175839
doi: 10.1111/j.1476-5381.1993.tb13990.x
Ziganshin AU, Hoyle CH, Lambrecht G, Mutschler E, Bümert HG, Burnstock G (1994) Selective antagonism by PPADS at P2X-purinoceptors in rabbit isolated blood vessels. Br J Pharmacol 111:923–929
pubmed: 8019770
pmcid: 1910106
doi: 10.1111/j.1476-5381.1994.tb14827.x
Windscheif U, Ralevic V, Bäumert HG, Mutschler E, Lambrecht G, Burnstock G (1994) Vasoconstrictor and vasodilator responses to various agonists in the rat perfused mesenteric arterial bed: selective inhibition by PPADS of contractions mediated via P2X-purinoceptors. Br J Pharmacol 113:1015–1021
pubmed: 7858843
pmcid: 1510409
doi: 10.1111/j.1476-5381.1994.tb17094.x
Lambrecht G (1996) Design and pharmacology of selective P2-purinoceptor antagonists. J Auton Pharmacol 16:341–344
pubmed: 9131412
doi: 10.1111/j.1474-8673.1996.tb00049.x
von Kügelgen I, Wetter A (2000) Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch Pharmacol 362:310–323
doi: 10.1007/s002100000310
Carl A, Kenyon JL, Uemura D, Fusetani N, Sanders KM (1991) Regulation of Ca
pubmed: 1651653
doi: 10.1152/ajpcell.1991.261.2.C387
Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291–366
pubmed: 20086079
doi: 10.1152/physrev.00021.2009
Koh SD, Sanders KM, Carl A (1996) Regulation of smooth muscle delayed rectifier K
pubmed: 8765999
doi: 10.1007/s004240050151
Nelson MT, Quayle JM (1995) Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268:C799–C822
pubmed: 7733230
doi: 10.1152/ajpcell.1995.268.4.C799
Zhang L, Bonev AD, Mawe GM, Nelson MT (1994) Protein kinase A mediates activation of ATP-sensitive K
pubmed: 7943248
Dreisig K, Kornum BR (2016) A critical look at the function of the P2Y11 receptor. Purinergic Signal 12:427–437
pubmed: 27246167
pmcid: 5023629
doi: 10.1007/s11302-016-9514-7
Alkayed F, Kashimata M, Koyama N, Hayashi T, Tamura Y, Azuma Y (2012) P2Y11 purinoceptor mediates the ATP-enhanced chemotactic response of rat neutrophils. J Pharmacol Sci 120:288–295
pubmed: 23182888
doi: 10.1254/jphs.12173FP
Barragán-Iglesias P, Mendoza-Garcés L, Pineda-Farias JB, Solano-Olivares V, Rodríguez-Silverio J, Flores-Murrieta FJ, Granados-Soto V, Rocha-González HI (2015) Participation of peripheral P2Y1, P2Y6 and P2Y11 receptors in formalin-induced inflammatory pain in rats. Pharmacol Biochem Behav 128:23–32
pubmed: 25449358
doi: 10.1016/j.pbb.2014.11.001
Barragán-Iglesias P, Pineda-Farias JB, Cervantes-Durán C, Bravo-Hernández M, Rocha-González HI, Murbartián J, Granados-Soto V (2014) Role of spinal P2Y6 and P2Y11 receptors in neuropathic pain in rats: possible involvement of glial cells. Mol Pain 10:29
pubmed: 24886406
pmcid: 4039548
doi: 10.1186/1744-8069-10-29
Certal M, Vinhas A, Pinheiro AR, Ferreirinha F, Barros-Barbosa AR, Silva I, Costa MA, Correia-de-Sá P (2015) Calcium signaling and the novel anti-proliferative effect of the UTP-sensitive P2Y11 receptor in rat cardiac myofibroblasts. Cell Calcium 58:518–533
pubmed: 26324417
doi: 10.1016/j.ceca.2015.08.004
Dănilă MD, Privistirescu A, Duicu OM, Rațiu CD, Angoulvant D, Muntean DM, Sturza A (2017) The effect of purinergic signaling via the P2Y11 receptor on vascular function in a rat model of acute inflammation. Mol Cell Biochem 431:37–44
pubmed: 28213772
doi: 10.1007/s11010-017-2973-5
Djerada Z, Millart H (2013) Intracellular NAADP increase induced by extracellular NAADP via the P2Y11-like receptor. Biochem Biophys Res Commun 436:199–203
pubmed: 23726915
doi: 10.1016/j.bbrc.2013.04.110
Ohtomo K, Shatos MA, Vrouvlianis J, Li D, Hodges RR, Dartt DA (2011) Increase of intracellular Ca
pubmed: 22039237
pmcid: 3341118
doi: 10.1167/iovs.11-7809
Zhang PP, Zhang G, Zhou W, Weng SJ, Yang XL, Zhong YM (2016) Signaling mechanism for modulation by ATP of glycine receptors on rat retinal ganglion cells. Sci Rep 6:28938
pubmed: 27357477
pmcid: 4928062
doi: 10.1038/srep28938
Horii K, Suzuki Y, Shiina T, Saito S, Onouchi S, Horii Y, Shimaoka H, Shimizu Y (2019) ATP-dependent potassium channels contribute to motor regulation of esophageal striated muscle in rats. J Vet Med Sci 81:1266–1272
pubmed: 31292350
pmcid: 6785617
doi: 10.1292/jvms.19-0197
Horii K, Shiina T, Naitou K, Nakamori H, Sano Y, Shimizu Y (2016) Potassium channels contribute to motor regulation of esophageal striated muscle in rats. J Physiol Sci 66(Suppl 1):S-156
Otsuka Y, Bai X, Tanaka Y, Ihara E, Chinen T, Ogino H, Ogawa Y (2021) Involvement of interstitial cells of Cajal in nicotinic acetylcholine receptor-induced relaxation of the porcine lower esophageal sphincter. Eur J Pharmacol 910:174491
pubmed: 34506779
doi: 10.1016/j.ejphar.2021.174491
Shimbo T, Adachi T, Fujisawa S, Hongoh M, Ohba T, Ono K (2016) In vitro effect of nicorandil on the carbachol-induced contraction of the lower esophageal sphincter of the rat. J Pharmacol Sci 131:267–274
pubmed: 27562702
doi: 10.1016/j.jphs.2016.07.005
Furness JB (2008) The enteric nervous system: Normal functions and enteric neuropathies. Neurogastroenterol Motil 20(Suppl 1):32–38
pubmed: 18402640
doi: 10.1111/j.1365-2982.2008.01094.x
Kou W, Pandolfino JE, Kahrilas PJ, Patankar NA (2015) Simulation studies of circular muscle contraction, longitudinal muscle shortening, and their coordination in esophageal transport. Am J Physiol Gastrointest Liver Physiol 309:G238–G247
pubmed: 26113296
pmcid: 4537927
doi: 10.1152/ajpgi.00058.2015
Mittal RK (2013) Longitudinal muscle of the esophagus: its role in esophageal health and disease. Curr Opin Gastroenterol 29:421–430
pubmed: 23739655
Christensen J (1975) Pharmacology of the esophageal motor function. Annu Rev Pharmacol 15:243–258
pubmed: 238461
doi: 10.1146/annurev.pa.15.040175.001331