Purinergic neuromuscular transmission in the gastrointestinal tract; Functional basis for future clinical and pharmacological studies

British Journal of Pharmacology

Volumn 171, Issue 19, 2014, Pages 4360-4375

  Jiménez, Marcel ^a,b   Clavé, Pere ^b,c   Accarino, Anna ^d   Gallego, Diana ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d HOSPITAL DE MATARÓ   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; 4 (2 IODO 6 METHYLAMINO 9H PURIN 9 YL) 2 PHOSPHONOOXYBICYCLO[3.1.0]HEXANE 1 METHANOL; 4 [2 CHLORO 6 (METHYLAMINO) 9H PURIN 9 YL] 2 (PHOSPHONOOXY)BICYCLO[3.1.0]HEXANE 1 METHANOL DIHYDROGEN PHOSPHATE ESTER; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APAMIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NITRIC OXIDE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PURINE; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; SEROTONIN 4 RECEPTOR; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL 3; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; PURINERGIC P2Y RECEPTOR ANTAGONIST;

ELECTRICAL FIELD STIMULATION; ELECTROSTIMULATION; ESOPHAGUS; FAST INHIBITORY JUNCTION POTENTIAL; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; HUMAN; INHIBITORY NEURAL TONE; INHIBITORY NEUROMUSCULAR JUNCTION; INTERCALATION THEORY; INTESTINE INNERVATION; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; LOWER ESOPHAGUS SPHINCTER; MECHANICAL RELAXATION; MOLECULAR DYNAMICS; MUSCLE RELAXATION; NERVOUS SYSTEM PARAMETERS; NERVOUS SYSTEM POTENTIAL; NEUROMUSCULAR BLOCKING; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PURINERGIC NEUROMUSCULAR TRANSMISSION; REVIEW; SENSITIVITY ANALYSIS; SLOW INHIBITORY JUNCTION POTENTIAL; SMOOTH MUSCLE FIBER; THEORY; TRANSLATIONAL RESEARCH; ANIMAL; PHYSIOLOGY; SMOOTH MUSCLE; SYNAPTIC TRANSMISSION;

ADENOSINE TRIPHOSPHATE; ANIMALS; APAMIN; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; HUMANS; MUSCLE, SMOOTH; NITRIC OXIDE; PURINERGIC P2Y RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2Y1; SYNAPTIC TRANSMISSION;

EID: 84927772112     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12802     Document Type: Review

References (109)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1562.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ligand-gated ion channels. Br J Pharmacol 170: 1582-1603.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: Ion channels. Br J Pharmacol 170: 1607-1640.
4. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013d). The Concise Guide to PHARMACOLOGY 2013/14: Catalytic receptors. Br J Pharmacol 170: 1676-1703.
5. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013e). The Concise Guide to PHARMACOLOGY 2013/14: Transporters. Br J Pharmacol 170: 1706-1796.
6. Acheson A, Rayment S, Eames T, Mundey M, Nisar P, Scholefield J, et al. (2009). Investigation of the role of adrenergic and non-nitrergic, non-adrenergic neurotransmission in the sheep isolated internal anal sphincter. Neurogastroenterol Motil 21: 335-345.
7. Alberti E, Mikkelsen HB, Wang X, Diaz M, Larsen JO, Huizinga JD, et al. (2007). Pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats. Am J Physiol Gastrointest Liver Physiol 292: G1499-G1510.
8. Auli M, Martinez E, Gallego D, Opazo A, Espin F, Marti-Gallostra M, et al. (2008). Effects of excitatory and inhibitory neurotransmission on motor patterns of human sigmoid colon in vitro. Br J Pharmacol 155: 1043-1055.
9. Bayguinov O, Hagen B, Bonev AD, Nelson MT, Sanders KM, (2000). Intracellular calcium events activated by ATP in murine colonic myocytes. Am J Physiol Cell Physiol 279: C126-C135.
10. 2+ concentration induced by P2-purinoceptor activation in isolated myocytes from the rat gastrointestinal tract. Br J Pharmacol 117: 775-780.
11. Boeckxstaens GE, Pelckmans PA, Herman AG, Van Maercke YM, (1993). Involvement of nitric oxide in the inhibitory innervation of the human isolated colon. Gastroenterology 104: 690-697.
12. Boeckxstaens GE, Mebis J, Janssens J, Geboes K, De Man JG, Herman AG, et al. (1994). Clinical relevance of nitric oxide in the gut. Lancet 344: 129.
13. Boyer JL, Romero-Avila T, Schachter JB, Harden TK, (1996). Identification of competitive antagonists of the P2Y1 receptor. Mol Pharmacol 50: 1323-1329.
14. Bult H, Boeckxstaens GE, Pelckmans PA, Jordaens FH, Van Maercke YM, Herman AG, (1990). Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature 345: 346-347.
15. Burns AJ, Lomax AE, Torihashi S, Sanders KM, Ward SM, (1996). Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci U S A 93: 12008-12013.
16. Burnstock G, (1976). Do some nerve cells release more than one transmitter? Neuroscience 1: 239-248.
17. Burnstock G, (2008). The journey to establish purinergic signalling in the gut. Neurogastroenterol Motil 20 (Suppl. 1): 8-19.
18. Burnstock G, Campbell G, Satchell D, Smythe A, (1970). Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br J Pharmacol 40: 668-688.
19. Burnstock G, Cocks T, Crowe R, (1978). Evidence for purinergic innervation of the anococcygeus muscle. Br J Pharmacol 64: 13-20.
20. Camaioni E, Boyer JL, Mohanram A, Harden TK, Jacobson KA, (1998). Deoxyadenosine bisphosphate derivatives as potent antagonists at P2Y1 receptors. J Med Chem 41: 183-190.
21. Cattaneo M, Lecchi A, Ohno M, Joshi BV, Besada P, Tchilibon S, et al. (2004). Antiaggregatory activity in human platelets of potent antagonists of the P2Y 1 receptor. Biochem Pharmacol 68: 1995-2002.
22. Cayabyab FS, Daniel EE, (1996). Role of sarcoplasmic reticulum in inhibitory junction potentials and hyperpolarizations by nitric oxide donors in opossum oesophagus. Br J Pharmacol 118: 2185-2191.
23. Chaudhury A, He XD, Goyal RK, (2012). Role of myosin Va in purinergic vesicular neurotransmission in the gut. Am J Physiol Gastrointest Liver Physiol 302: G598-G607.
24. Christinck F, Jury J, Cayabyab F, Daniel EE, (1991a). Nitric oxide may be the final mediator of nonadrenergic, noncholinergic inhibitory junction potentials in the gut. Can J Physiol Pharmacol 69: 1448-1458.
25. Christinck F, Jury J, Cayabyab F, Daniel EE, (1991b). Nitric oxide may be the final mediator of nonadrenergic, noncholinergic inhibitory junction potentials in the gut. Can J Physiol Pharmacol 69: 1448-1458.
26. 2+ signaling in myenteric neurons via P2 purinoceptors. Am J Physiol 272: G463-G473.
27. Cobine CA, Hennig GW, Kurahashi M, Sanders KM, Ward SM, Keef KD, (2011). Relationship between interstitial cells of Cajal, fibroblast-like cells and inhibitory motor nerves in the internal anal sphincter. Cell Tissue Res 344: 17-30.
28. Crist JR, He XD, Goyal RK, (1992). Both ATP and the peptide VIP are inhibitory neurotransmitters in guinea-pig ileum circular muscle. J Physiol 447: 119-131.
29. Daniel EE, Posey-Daniel V, (1984). Neuromuscular structures in opossum esophagus: role of interstitial cells of Cajal. Am J Physiol 246: G305-G315.
30. De Man JG, De Winter BY, Seerden TC, De Schepper HU, Herman AG, Pelckmans PA, (2003). Functional evidence that ATP or a related purine is an inhibitory NANC neurotransmitter in the mouse jejunum: study on the identity of P2X and P2Y purinoceptors involved. Br J Pharmacol 140: 1108-1116.
31. Durnin L, Hwang SJ, Ward SM, Sanders KM, Mutafova-Yambolieva VN, (2012). Adenosine 5-diphosphate-ribose is a neural regulator in primate and murine large intestine along with beta-NAD(+). J Physiol 590: 1921-1941.
32. Durnin L, Sanders KM, Mutafova-Yambolieva VN, (2013). Differential release of beta-NAD(+) and ATP upon activation of enteric motor neurons in primate and murine colons. Neurogastroenterol Motil 25: e194-e204.
33. Fang X, Hu HZ, Gao N, Liu S, Wang GD, Wang XY, et al. (2006). Neurogenic secretion mediated by the purinergic P2Y1 receptor in guinea-pig small intestine. Eur J Pharmacol 536: 113-122.
34. + channel, SK3, in fibroblast-like cells forming gap junctions with smooth muscle cells in the mouse small intestine. J Pharmacol Sci 92: 35-42.
35. Gallego D, Hernandez P, Clave P, Jimenez M, (2006). P2Y1 receptors mediate inhibitory purinergic neuromuscular transmission in the human colon. Am J Physiol Gastrointest Liver Physiol 291: G584-G594.
36. Gallego D, Gil V, Aleu J, Auli M, Clave P, Jimenez M, (2008a). Purinergic and nitrergic junction potential in the human colon. Am J Physiol Gastrointest Liver Physiol 295: G522-G533.
37. Gallego D, Vanden Berghe P, Farre R, Tack J, Jimenez M, (2008b). P2Y1 receptors mediate inhibitory neuromuscular transmission and enteric neuronal activation in small intestine. Neurogastroenterol Motil 20: 159-168.
38. Gallego D, Gil V, Aleu J, Martinez-Cutillas M, Clave P, Jimenez M, (2011). Pharmacological characterization of purinergic inhibitory neuromuscular transmission in the human colon. Neurogastroenterol Motil 23: 792-e338.
39. Gallego D, Gil V, Martinez-Cutillas M, Mane N, Martin MT, Jimenez M, (2012). Purinergic neuromuscular transmission is absent in the colon of P2Y(1) knocked out mice. J Physiol 590: 1943-1956.
40. Gallego D, Malagelada C, Accarino A, De Giorgio R, Malagelada JR, Azpiroz F, et al. (2014). Nitrergic and purinergic mechanisms evoke inhibitory neuromuscular transmission in the human small intestine. Neurogastroenterol Motil 26: 419-429.
41. Gao N, Hu HZ, Zhu MX, Fang X, Liu S, Gao C, et al. (2006). The P2Y purinergic receptor expressed by enteric neurones in guinea-pig intestine. Neurogastroenterol Motil 18: 316-323.
42. Gil V, Gallego D, Grasa L, Martin MT, Jimenez M, (2010). Purinergic and nitrergic neuromuscular transmission mediates spontaneous neuronal activity in the rat colon. Am J Physiol Gastrointest Liver Physiol 299: G158-G169.
43. Gil V, Gallego D, Moha Ou Maati H, Peyronnet R, Martinez-Cutillas M, Heurteaux C, et al. (2012). Relative contribution of SKCa and TREK1 channels in purinergic and nitrergic neuromuscular transmission in the rat colon. Am J Physiol Gastrointest Liver Physiol 303: G412-G423.
44. Gil V, Martinez-Cutillas M, Mane N, Martin MT, Jimenez M, Gallego D, (2013). P2Y(1) knockout mice lack purinergic neuromuscular transmission in the antrum and cecum. Neurogastroenterol Motil 25: e170-e182.
45. Gomes P, Chevalier J, Boesmans W, Roosen L, Van den Abbeel V, Neunlist M, et al. (2009). ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived from embryonic mice. Neurogastroenterol Motil 21: 870-e62.
46. Goyal RK, (2011). Evidence for beta-nicotinamide adenine dinucleotide as a purinergic, inhibitory neurotransmitter in doubt. Gastroenterology 141: e27-e28.
47. Goyal RK, He XD, (1998). Evidence for NO. redox form of nitric oxide as nitrergic inhibitory neurotransmitter in gut. Am J Physiol 275: G1185-G1192.
48. Goyal RK, Sullivan MP, Chaudhury A, (2013). Progress in understanding of inhibitory purinergic neuromuscular transmission in the gut. Neurogastroenterol Motil 25: 203-207.
49. Grasa L, Gil V, Gallego D, Martin MT, Jimenez M, (2009). P2Y(1) receptors mediate inhibitory neuromuscular transmission in the rat colon. Br J Pharmacol 158: 1641-1652.
50. Groneberg D, Konig P, Koesling D, Friebe A, (2011). Nitric oxide-sensitive guanylyl cyclase is dispensable for nitrergic signaling and gut motility in mouse intestinal smooth muscle. Gastroenterology 140: 1608-1617.
51. Groneberg D, Lies B, Konig P, Jager R, Seidler B, Klein S, et al. (2013). Cell-specific deletion of nitric oxide-sensitive guanylyl cyclase reveals a dual pathway for nitrergic neuromuscular transmission in the murine fundus. Gastroenterology 145: 188-196.
52. Gulbransen BD, Sharkey KA, (2009). Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136: 1349-1358.
53. Gwynne RM, Bornstein JC, (2009). Electrical stimulation of the mucosa evokes slow EPSPs mediated by NK1 tachykinin receptors and by P2Y1 purinoceptors in different myenteric neurons. Am J Physiol Gastrointest Liver Physiol 297: G179-G186.
54. Hardy AR, Conley PB, Luo J, Benovic JL, Poole AW, Mundell SJ, (2005). P2Y1 and P2Y12 receptors for ADP desensitize by distinct kinase-dependent mechanisms. Blood 105: 3552-3560.
55. He XD, Goyal RK, (1993). Nitric oxide involvement in the peptide VIP-associated inhibitory junction potential in the guinea-pig ileum. J Physiol 461: 485-499.
56. Hoyle CH, Knight GE, Burnstock G, (1990). Suramin antagonizes responses to P2-purinoceptor agonists and purinergic nerve stimulation in the guinea-pig urinary bladder and taenia coli. Br J Pharmacol 99: 617-621.
57. Hu HZ, Gao N, Zhu MX, Liu S, Ren J, Gao C, et al. (2003). Slow excitatory synaptic transmission mediated by P2Y1 receptors in the guinea-pig enteric nervous system. J Physiol 550: 493-504.
58. Hwang SJ, Durnin L, Dwyer L, Rhee PL, Ward SM, Koh SD, et al. (2011). β-Nicotinamide adenine dinucleotide is an enteric inhibitory neurotransmitter in human and nonhuman primate colons. Gastroenterology 140: 608-617.
59. Hwang SJ, Blair PJ, Durnin L, Mutafova-Yambolieva V, Sanders KM, Ward SM, (2012). P2Y1 purinoreceptors are fundamental to inhibitory motor control of murine colonic excitability and transit. J Physiol 590: 1957-1972.
60. Iino S, Nojyo Y, (2009). Immunohistochemical demonstration of c-Kit-negative fibroblast-like cells in murine gastrointestinal musculature. Arch Histol Cytol 72: 107-115.
61. Jury J, Boev KR, Daniel EE, (1996). Nitric oxide mediates outward potassium currents in opossum esophageal circular smooth muscle. Am J Physiol 270: G932-G938.
62. Kadowaki M, Yoneda S, Takaki M, (2003). Involvement of a purinergic pathway in the sympathetic regulation of motility in rat ileum. Auton Neurosci 104: 10-16.
63. Keef KD, Du C, Ward SM, McGregor B, Sanders KM, (1993). Enteric inhibitory neural regulation of human colonic circular muscle: role of nitric oxide. Gastroenterology 105: 1009-1016.
64. Keef KD, Saxton SN, McDowall RA, Kaminski RE, Duffy AM, Cobine CA, (2013). Functional role of vasoactive intestinal polypeptide in inhibitory motor innervation in the mouse internal anal sphincter. J Physiol 591: 1489-1506.
65. Kimball BC, Mulholland MW, (1996). Enteric glia exhibit P2U receptors that increase cytosolic calcium by a phospholipase C-dependent mechanism. J Neurochem 66: 604-612.
66. 2+ signaling in cultured myenteric neurons via a PLC-dependent mechanism. Am J Physiol 270: G587-G593.
67. King BF, (1994). Prejunctional autoinhibition of purinergic transmission in circular muscle of guinea-pig ileum; a mechanism distinct from P1-purinoceptor activation. J Auton Nerv Syst 48: 55-63.
68. King BF, (2012). Resolution and concordance in dissecting the compound inhibitory junction potential. J Physiol 590: 1777-1778.
69. Knowles CH, De Giorgio R, Kapur RP, Bruder E, Farrugia G, Geboes K, et al. (2010). The London Classification of gastrointestinal neuromuscular pathology: report on behalf of the Gastro 2009 International Working Group. Gut 59: 882-887.
70. Knowles CH, Veress B, Kapur RP, Wedel T, Farrugia G, Vanderwinden JM, et al. (2011). Quantitation of cellular components of the enteric nervous system in the normal human gastrointestinal tract-report on behalf of the Gastro 2009 International Working Group. Neurogastroenterol Motil 23: 115-124.
71. + channels activated by ATP in murine colonic smooth muscle. Am J Physiol 273: C2010-C2021.
72. Kong ID, Koh SD, Sanders KM, (2000). Purinergic activation of spontaneous transient outward currents in guinea pig taenia colonic myocytes. Am J Physiol Cell Physiol 278: C352-C362.
73. Kurahashi M, Zheng H, Dwyer L, Ward SM, Don Koh S, Sanders KM, (2011). A functional role for the 'fibroblast-like cells' in gastrointestinal smooth muscles. J Physiol 589: 697-710.
74. Kurahashi M, Nakano Y, Hennig GW, Ward SM, Sanders KM, (2012). Platelet-derived growth factor receptor alpha-positive cells in the tunica muscularis of human colon. J Cell Mol Med 16: 1397-1404.
75. Lecea B, Gallego D, Farre R, Opazo A, Auli M, Jimenez M, et al. (2011). Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus. Am J Physiol Gastrointest Liver Physiol 300: G782-G794.
76. Lecea B, Gallego D, Farre R, Clave P, (2012). Origin and modulation of circular smooth muscle layer contractions in the porcine esophagus. Neurogastroenterol Motil 24: 779-789, e355.
77. 2+ release in smooth muscle via P2Y1 receptors. J Cell Sci 125: 5151-5158.
78. Mañe N, Gil V, Martinez-Cutillas M, Martin MT, Gallego D, Jimenez M, (2014). Dynamics of inhibitory co-transmission, membrane potential and pacemaker activity determine neuromyogenic function in the rat colon. Pflugers Arch. doi: 10.1007/s00424-014-1500-8.
79. Martinez-Cutillas M, Gallego D, Gil V, Martin MT, Jimenez M, (2011). Pharmacological characterization of purinergic receptors in human colonic smooth muscle cells using calcium imaging. Neurogastroenterol Motil 23 (Suppl. 1): 50.
80. Matsuyama H, Unno T, El-Mahmoudy AM, Komori S, Kobayashi H, Thapaliya S, et al. (2002). Peptidergic and nitrergic inhibitory neurotransmissions in the hamster jejunum: regulation of vasoactive intestinal peptide release by nitric oxide. Neuroscience 110: 779-788.
81. McDonnell B, Hamilton R, Fong M, Ward SM, Keef KD, (2008). Functional evidence for purinergic inhibitory neuromuscular transmission in the mouse internal anal sphincter. Am J Physiol Gastrointest Liver Physiol 294: G1041-G1051.
82. Mearin F, Mourelle M, Guarner F, Salas A, Riveros-Moreno V, Moncada S, et al. (1993). Patients with achalasia lack nitric oxide synthase in the gastro-oesophageal junction. Eur J Clin Invest 23: 724-728.
83. Mutafova-Yambolieva VN, Hwang SJ, Hao X, Chen H, Zhu MX, Wood JD, et al. (2007). Beta-nicotinamide adenine dinucleotide is an inhibitory neurotransmitter in visceral smooth muscle. Proc Natl Acad Sci U S A 104: 16359-16364.
84. Olson L, Alund M, Norberg KA, (1976). Fluorescence-microscopical demonstration of a population of gastro-intestinal nerve fibres with a selective affinity for quinacrine. Cell Tissue Res 171: 407-423.
85. Opazo A, Lecea B, Gil V, Jimenez M, Clave P, Gallego D, (2011). Specific and complementary roles for nitric oxide and ATP in the inhibitory motor pathways to rat internal anal sphincter. Neurogastroenterol Motil 23: e11-e25.
86. 2+ concentration in rat ileal myocytes. Br J Pharmacol 118: 2213-2219.
87. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al. (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-1106.
88. Powell AK, Fida R, Bywater RA, (2001). Ongoing nicotinic and non-nicotinic inputs to inhibitory neurons in the mouse colon. Clin Exp Pharmacol Physiol 28: 792-798.
89. Roberts JA, Lukewich MK, Sharkey KA, Furness JB, Mawe GM, Lomax AE, (2012). The roles of purinergic signaling during gastrointestinal inflammation. Curr Opin Pharmacol 12: 659-666.
90. Roberts JA, Durnin L, Sharkey KA, Mutafova-Yambolieva VN, Mawe GM, (2013). Oxidative stress disrupts purinergic neuromuscular transmission in the inflamed colon. J Physiol 591: 3725-3737.
91. Rodriguez-Rodriguez R, Yarova P, Winter P, Dora KA, (2009). Desensitization of endothelial P2Y1 receptors by PKC-dependent mechanisms in pressurized rat small mesenteric arteries. Br J Pharmacol 158: 1609-1620.
92. Sanger GJ, Broad J, Kung V, Knowles CH, (2013). Translational neuropharmacology: the use of human isolated gastrointestinal tissues. Br J Pharmacol 168: 28-43.
93. Spencer NJ, Bywater RA, Holman ME, Taylor GS, (1998). Spontaneous and evoked inhibitory junction potentials in the circular muscle layer of mouse colon. J Auton Nerv Syst 69: 115-121.
94. Stark ME, Bauer AJ, Szurszewski JH, (1991). Effect of nitric oxide on circular muscle of the canine small intestine. J Physiol 444: 743-761.
95. Strong DS, Cornbrooks CF, Roberts JA, Hoffman JM, Sharkey KA, Mawe GM, (2010). Purinergic neuromuscular transmission is selectively attenuated in ulcerated regions of inflamed guinea pig distal colon. J Physiol 588: 847-859.
96. Suzuki H, Ward SM, Bayguinov YR, Edwards FR, Hirst GD, (2003). Involvement of intramuscular interstitial cells in nitrergic inhibition in the mouse gastric antrum. J Physiol 546: 751-763.
97. Undi S, Benko R, Wolf M, Illenyi L, Vereczkei A, Kelemen D, et al. (2009). The NANC relaxation of the human ileal longitudinal and circular muscles is inhibited by MRS 2179, a P2 purinoceptor antagonist. Life Sci 84: 871-875.
98. Van Crombruggen K, Van Nassauw L, Timmermans JP, Lefebvre RA, (2007). Inhibitory purinergic P2 receptor characterisation in rat distal colon. Neuropharmacology 53: 257-271.
99. + channel, in the gut musculature in health and disease. Cell Tissue Res 310: 349-358.
100. Vigne P, Pacaud P, Loirand G, Breittmayer JP, Frelin C, (1998). PPADS inhibits P2Y1 purinoceptors in rat brain capillary endothelial cells and in rat ileal myocytes by an indirect mechanism. Biochem Biophys Res Commun 244: 332-335.
101. + channels by purinergic agonists in smooth muscle cells of the mouse ileum. J Physiol 502 (Pt 3): 497-508.
102. Wang GD, Wang XY, Hu HZ, Liu S, Gao N, Fang X, et al. (2007). Inhibitory neuromuscular transmission mediated by the P2Y1 purinergic receptor in guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 292: G1483-G1489.
103. Ward SM, Sanders KM, (2001). Interstitial cells of Cajal: primary targets of enteric motor innervation. Anat Rec 262: 125-135.
104. Wunderlich JE, Needleman BJ, Chen Z, Yu JG, Wang Y, Grants I, et al. (2008). Dual purinergic synaptic transmission in the human enteric nervous system. Am J Physiol Gastrointest Liver Physiol 294: G554-G566.
105. Xue L, Farrugia G, Sarr MG, Szurszewski JH, (1999). ATP is a mediator of the fast inhibitory junction potential in human jejunal circular smooth muscle. Am J Physiol 276: G1373-G1379.
106. Xue L, Farrugia G, Szurszewski JH, (2000). Effect of exogenous ATP on canine jejunal smooth muscle. Am J Physiol Gastrointest Liver Physiol 278: G725-G733.
107. Zhang Y, Mashimo H, Paterson WG, (2008). Regional differences in nitrergic innervation of the smooth muscle of murine lower oesophageal sphincter. Br J Pharmacol 153: 517-527.
108. Zhang Y, Lomax AE, Paterson WG, (2010). P2Y1 receptors mediate apamin-sensitive and -insensitive inhibitory junction potentials in murine colonic circular smooth muscle. J Pharmacol Exp Ther 333: 602-611.
109. Zizzo MG, Mule F, Serio R, (2007). Inhibitory purinergic transmission in mouse caecum: role for P2Y1 receptors as prejunctional modulators of ATP release. Neuroscience 150: 658-664.