Purinergic signalling in the enteric nervous system (An overview of current perspectives)

Autonomic Neuroscience: Basic and Clinical

Volumn 191, Issue , 2015, Pages 141-147

  King, Brian F ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

ATP; ATP release; ENS; Neurotransmission; Nonadrenergic noncholinergic (NANC); P2X receptor; P2Y receptor

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM; CHOLINERGIC RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; ION CHANNEL; LIPID; MEMBRANE RECEPTOR; METABOTROPIC RECEPTOR; NEUROTRANSMITTER; NICOTINAMIDE ADENINE DINUCLEOTIDE; POTASSIUM; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC RECEPTOR; SODIUM;

AUTOREGULATION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHEMORECEPTOR; EXCITATORY POSTSYNAPTIC POTENTIAL; GASTROINTESTINAL TRACT; GENETIC TRANSCRIPTION; HUMAN; INTESTINE INNERVATION; INTRACELLULAR SIGNALING; MECHANORECEPTOR; MOTONEURON; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; METABOLISM;

ADENOSINE TRIPHOSPHATE; ANIMALS; ENTERIC NERVOUS SYSTEM; HUMANS; RECEPTORS, PURINERGIC;

EID: 84938750630     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2015.05.005     Document Type: Review

References (125)

1. Ase A.R., Bernier L.P., Blais D., Pankratov Y., Séguéla P. Modulation of heteromeric P2X1/5 receptors by phosphoinositides in astrocytes depends on the P2X1 subunit. J. Neurochem. 2010, 113:1676-1684.
2. Baqi Y., Atzler K., Köse M., Glänzel M., Müller C.E. High-affinity, non-nucleotide-derived competitive antagonists of platelet P2Y12 receptors. J. Med. Chem. 2009, 52:3784-3793.
3. Barajas-López C1., Huizinga J.D., Collins S.M., Gerzanich V., Espinosa-Luna R., Peres A.L. P2X purinoceptors of myenteric neurones from the guinea-pig ileum and their unusual pharmacological properties. Br. J. Pharmacol. 1996, 119:1541-1548.
4. Barajas-López C., Montaño L.M., Espinosa-Luna R. Inhibitory interactions between 5-HT3 and P2X channels in submucosal neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283(6):G1238-G1248.
5. Bayer S., Crenner F., Aunis D., Angel F. Effects of GABA on circular smooth muscle spontaneous activities of rat distal colon. Life Sci. 2002, 71:911-925.
6. Bernier L.P., Ase A.R., Chevallier S., Blais D., Zhao Q., Boué-Grabot E., Logothetis D., Séguéla P. Phosphoinositides regulate P2X4 ATP-gated channels through direct interactions. J. Neurosci. 2008, 28:12938-12945.
7. Bernier L.P., Ase A.R., Tong X., Hamel E., Blais D., Zhao Q., Logothetis D.E., Séguéla P. Direct modulation of P2X1 receptor-channels by the lipid phosphatidylinositol 4,5-bisphosphate. Mol. Pharmacol. 2008, 74:785-792.
8. Bertrand P.P. ATP and sensory transduction in the enteric nervous system. Neuroscientist 2003, 9:243-260.
9. Bertrand P.P., Bornstein J.C. ATP as a putative sensory mediator: activation of intrinsic sensory neurons of the myenteric plexus via P2X receptors. J. Neurosci. 2002, 22:4767-4775.
10. Bian X., Ren J., DeVries M., Schnegelsberg B., Cockayne D.A., Ford A.P., Galligan J.J. Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. Physiol 2003, 551:309-322.
11. Bo X., Alavi A., Xiang Z., Oglesby I., Ford A., Burnstock G. Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 1999, 10:1107-1111.
12. Boeckxstaens G.E., Pelckmans P.A., Bult H., De Man J.G., Herman A.G., van Maercke Y.M. Evidence for nitric oxide as mediator of non-adrenergic non-cholinergic relaxations induced by ATP and GABA in the canine gut. Br. J. Pharmacol. 1991, 102:434-438.
13. Brown S.G., King B.F., Kim Y.C., Jang S.Y., Burnstock G., Jacobson K.A. Activity of novel adenine nucleotide derivatives as agonists and antagonists at recombinant rat P2X receptors. Drug Dev. Res. 2000, 49(4):253-259.
14. Burnstock G. Neural nomenclature. Nature 1971, 229:282-283.
15. Burnstock G. The journey to establish purinergic signalling in the gut. Neurogastroenterol. Motil. 2008, 20(Suppl. 1):8-19.
16. Burnstock G. Purinergic signalling: its unpopular beginning, its acceptance and its exciting future. Bioessays 2012, 34:218-225.
17. Burnstock G. Purinergic signalling in the gastrointestinal tract and related organs in health and disease. Purinergic Signal 2014, 10:3-50.
18. Burnstock G., Kennedy C. Is there a basis for distinguishing two types of P2-purinoceptor?. Gen. Pharmacol. 1985, 16:433-440.
19. Burnstock G., Campbell G., Bennett M.R., Holman M.E. Inhibition of the smooth muscle of the taenia coli. Nature 1963, 200:581-582.
20. Burnstock G., Campbell G., Bennett M., Holman M.E. Innervation of the guinea-pig taenia coli: are there intrinsic inhibitory nerves which are distinct from sympathetic nerves?. Int. J. Neuropharmacol. 1964, 3:163-166.
21. Burnstock G., Campbell G., Rand M.J. The inhibitory innervation of the taenia of the guinea-pig caecum. J. Physiol. 1966, 182:504-526.
22. Burnstock G., Campbell G., Satchell D., Smythe A. Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br. J. Pharmacol. 1970, 40:668-688.
23. Burnstock G., Satchell D.G., Smythe A. A comparison of the excitatory and inhibitory effects of non-adrenergic, non-cholinergic nerve stimulation and exogenously applied ATP on a variety of smooth muscle preparations from different vertebrate species. Br. J. Pharmacol. 1972, 46:234-242.
24. Burnstock G., Fischer B., Hoyle C.H., Maillard M., Ziganshin A.U., Brizzolara A.L., von Isakovics A., Boyer J.L., Harden T.K., Jacobson K.A. Structure activity relationships for derivatives of adenosine-5'-triphosphate as agonists at P(2) purinoceptors: heterogeneity within P(2X) and P(2Y) subtypes. Drug Dev. Res. 1994, 31:206-219.
25. Burnstock G., Fredholm B.B., North R.A., Verkhratsky A. The birth and postnatal development of purinergic signalling. Acta Physiol. 2010, 199:93-147.
26. Castelucci P., Robbins H.L., Poole D.P., Furness J.B. The distribution of purine P2X2 receptors in the guinea-pig enteric nervous system. Histochem. Cell Biol. 2002, 2(117):415-422.
27. Chaudhury A., He X.D., Goyal R.K. Role of myosin Va in purinergic vesicular neurotransmission in the gut. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302:G598-G607.
28. Compan V., Ulmann L., Stelmashenko O., Chemin J., Chaumont S., Rassendren F. P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties. J. Neurosci. 2012, 32:4284-4296.
29. Clyne J.D., Brown T.C., Hume R.I. Expression level dependent changes in the properties of P2X2 receptors. Neuropharmacol. 2003, 44:403-412.
30. Cooke H.J., Wunderlich J., Christofi F.L. "The force be with you": ATP in gut mechanosensory transduction. News Physiol. Sci. 2003, 18:43-49.
31. De Man J.G., De Winter B.Y., Seerden T.C., De Schepper H.U., Herman A.G., Pelckmans P.A. 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. 2003, 140:1108-1116.
32. Decker D.A., Galligan J.J. Cross-inhibition between nicotinic acetylcholine receptors and P2X receptors in myenteric neurons and HEK-293 cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296:G1267-G1276.
33. Del Castillo J., Katz B. Production of membrane potential changes in the frog's heart by inhibitory nerve impulses. Nature 1955, 175:1035.
34. Devries M.P., Vessalo M., Galligan J.J. Deletion of P2X2 and P2X3 receptor subunits does not alter motility of the mouse colon. Front. Neurosci. 2010, 4:22. 10.3389/fnent.2010.00001.
35. Dickson E.J., Heredia D.J., Smith T.K. Critical role of 5-HT1A, 5-HT3, and 5-HT7 receptor subtypes in the initiation, generation, and propagation of the murine colonic migrating motor complex. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G144-G157.
36. +. J. Physiol. 2012, 590:1921-1941.
37. + and ATP upon activation of enteric motor neurons in primate and murine colons. Neurogastroenterol. Motil. 2013, 25:e194-e204.
38. Durnin L., Hwang S.J., Kurahashi M., Drumm B.T., Ward S.M., Sasse K.C., Sanders K.M., Mutafova-Yambolieva V.N. Uridine adenosine tetraphosphate is a novel neurogenic P2Y1 receptor activator in the gut. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:15821-15826.
39. Egan T.M., Khakh B.S. Contribution of calcium ions to P2X channel responses. J. Neurosci. 2004, 24:3413-3420.
40. Farrugia G., Szurszewski J.H. Carbon monoxide, hydrogen sulfide, and nitric oxide as signaling molecules in the gastrointestinal tract. Gastroenterology 2014, 147:303-313.
41. Felix R.A., Martin S., Pinion S., Crawford D.J. Development of a comprehensive set of P2 receptor pharmacological research compounds. Purinergic Signal 2012, 8(Suppl. 1):101-112.
42. Filtz T.M., Li Q., Boyer J.L., Nicholas R.A., Harden T.K. Expression of a cloned P2Y purinergic receptor that couples to phospholipase C. Mol. Pharmacol. 1994, 46:8-14.
43. Finger T.E., Danilova V., Barrows J., Bartel D.L., Vigers A.J., Stone L., Hellekant G., Kinnamon S.C. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310:1495-1499.
44. Fujiwara Y., Kubo Y. Regulation of the desensitization and ion selectivity of ATP-gated P2X2 channels by phosphoinositides. J. Physiol. 2006, 576:135-149.
45. Furness J.B., Costa M. The nervous release and the action of substances which affect intestinal muscle through neither adrenoreceptors nor cholinoreceptors. Phil. Trans. R. Soc. Lond. B Biol. Sci. 1973, 265:123-133.
46. Gallego D., Gil V., Martínez-Cutillas M., Mañé N., Martín M.T., Jiménez M. Purinergic neuromuscular transmission is absent in the colon of P2Y1 knocked out mice. J. Physiol. 2012, 590:1943-1956.
47. Galligan J.J., Bertrand P.P. ATP mediates fast synaptic potentials in enteric neurons. J. Neurosci. 1994, 14:7563-7571.
48. Galligan J.J., North R.A. Pharmacology and function of nicotinic acetylcholine and P2X receptors in the enteric nervous system. Neurogastroenterol. Motil. 2004, Suppl 1:64-70.
49. Gao N., Hu H.Z., Zhu M.X., Fang X., Liu S., Gao C., Wood J.D. The P2Y purinergic receptor expressed by enteric neurones in guinea-pig intestine. Neurogastroenterol. Motil. 2006, 18:316-323.
50. Giaroni C., Knight G.E., Ruan H.Z., Glass R., Bardini M., Lecchini S., Frigo G., Burnstock G. P2 receptors in the murine gastrointestinal tract. Neuropharmacology 2002, 43(8):1313-1323.
51. Gil V., Martínez-Cutillas M., Mañé N., Martín M.T., Jiménez M., Gallego D. P2Y1 knockout mice lack purinergic neuromuscular transmission in the antrum and cecum. Neurogastroenterol. Motil. 2013, 25:170-182.
52. Gillespie J.S. Spontaneous mechanical and electrical activity of stretched and unstretched intestinal smooth muscle cells and their response to sympathetic-nerve stimulation. J. Physiol. 1962, 162:54-75.
53. Gillespie J.S. The electrical and mechanical responses of intestinal smooth muscle cells to stimulation of their extrinsic parasympathetic nerves. J. Physiol. 1962, 162:76-92.
54. Gillespie J.S., MacKenna B.R. The inhibitory action of nicotine on the rabbit colon. J. Physiol. 1960, 152:191-205.
55. Goyal R.K. Evidence for β-nicotinamide adenine dinucleotide as a purinergic, inhibitory neurotransmitter in doubt. Gastroenterology 2011, 141:e27. (author reply e27-8.).
56. Goyal R.K., Sullivan M.P., Chaudhury A. Progress in understanding of inhibitory purinergic neuromuscular transmission in the gut. Neurogastroenterol. Motil. 2013, 25:203-207.
57. Grasa L., Gil V., Gallego D., Martín M.T., Jiménez M. P2Y1 receptors mediate inhibitory neuromuscular transmission in the rat colon. Br. J. Pharmacol. 2009, 158:1641-1652.
58. Gustafsson A.J., Muraro L., Dahlberg C., Migaud M., Chevallier O., Khanh H.N., Krishnan K., Li N., Islam M.S. ADP ribose is an endogenous ligand for the purinergic P2Y1 receptor. Mol. Cell. Endocrinol. 2011, 333:8-19.
59. Gwynne R.M., Bornstein J.C. 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. 2009, 297:G179-G186.
60. Hansen S.B. Lipid agonism: the PIP2 paradigm of ligand-gated ion channels. Biochim. Biophys. Acta 2015, 1851:620-628.
61. Hausmann R., Bodnar M., Woltersdorf R., Wang H., Fuchs M., Messemer N., Qin Y., Günther J., Riedel T., Grohmann M., Nieber K., Schmalzing G., Rubini P., Illes P. ATP binding site mutagenesis reveals different subunit stoichiometry of functional P2X2/3 and P2X2/6 receptors. J. Biol. Chem. 2012, 287:13930-13943.
62. Hellekant G., Schmolling J., Marambaud P., Rose-Hellekant T.A. 20150. CALHM1 deletion in mice affects glossopharyngeal taste responses, food intake, body weight, and life span. Chem. Senses 2015, (2015 Apr 8. pii: bjv009. [Epub ahead of print]).
63. Hoffmann K., Baqi Y., Morena M.S., Glänzel M., Müller C.E., von Kügelgen I. Interaction of new, very potent non-nucleotide antagonists with Arg256 of the human platelet P2Y12 receptor. J. Pharmacol. Exp. Ther. 2009, 331:648-655.
64. Hu H.Z., Gao N., Zhu M.X., Liu S., Ren J., Gao C., Xia Y., Wood J.D. Slow excitatory synaptic transmission mediated by P2Y1 receptors in the guinea-pig enteric nervous system. J. Physiol. 2003, 550:493-504.
65. Huang Y.A., Dando R., Roper S.D. Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J. Neurosci. 2009, 29:13909-13918.
66. Huang Y.A., Stone L.M., Pereira E., Yang R., Kinnamon J.C., Dvoryanchikov G., Chaudhari N., Finger T.E., Kinnamon S.C., Roper S.D. Knocking out P2X receptors reduces transmitter secretion in taste buds. J. Neurosci. 2011, 31:13654-136161.
67. Hwang S.J., Blair P.J., Durnin L., Mutafova-Yambolieva V., Sanders K.M., Ward S.M. P2Y1 purinoreceptors are fundamental to inhibitory motor control of murine colonic excitability and transit. J. Physiol. 2012, 590:1957-1972.
68. Jacobson K.A., Paoletta S., Katritch V., Wu B., Gao Z.G., Zhao Q., Stevens R.C., Kiselev E. Nucleotides acting at P2Y receptors: connecting structure and function. Mol. Pharmacol. 2015, (PMID:25837834 [Epub ahead of print]).
69. Janssens R., Communi D., Pirotton S., Samson M., Parmentier M., Boeynaems J.M. Cloning and tissue distribution of the human P2Y1 receptor. Biochem. Biophys. Res. Commun. 1996, 221:588-593.
70. Johnson P.J., Shum O.R., Thornton P.D., Bornstein J.C. Evidence that inhibitory motor neurons of the guinea-pig small intestine exhibit fast excitatory synaptic potentials mediated via P2X receptors. Neurosci. Lett. 1999, 266:169-172.
71. Karanjia R., García-Hernández L.M., Miranda-Morales M., Somani N., Espinosa-Luna R., Montaño L.M., Barajas-López C. Cross-inhibitory interactions between GABAA and P2X channels in myenteric neurones. Eur. J. Neurosci. 2006, 23:3259-3268.
72. Katayama Y., Morita K. Adenosine 5'-triphosphate modulates membrane potassium conductance in guinea-pig myenteric neurones. J. Physiol. 1989, 408:373-390.
73. Kato F., Shigetomi E. Direct modulation of evoked and spontaneous EPSCs by purinoceptors in the nucleus tractus solitarii of the rat. J. Physiol. 2001, 530:469-486.
74. Khakh B.S., Henderson G. ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol. Pharmacol. 1998, 54:373-378.
75. Khakh B.S., Gittermann D., Cockayne D.A., Jones A. ATP modulation of excitatory synapses onto interneurons. J. Neurosci. 2003, 23:7426-7437.
76. Kim M., Christofi F.L., Xue J., Robinson J.M., Cooke H.J. Mechanically evoked 5-hydroxytryptamine release is mediated by caveolin-associated cholesterol rich membrane domains. Neurogastroenterol. Motil. 2007, 19:309-317.
77. King B.F. Resolution and concordance in dissecting the compound inhibitory junction potential. J. Physiol. 2012, 590:1777-1778.
78. King B.F., Townsend-Nicholson A. Involvement of P2Y1 and P2Y11 purinoceptors in parasympathetic inhibition of colonic smooth muscle. J Pharmacol Exp Ther 2008, 324:1055-1063.
79. Kinnamon S.C., Finger T.E. A taste for ATP: neurotransmission in taste buds. Front. Cell. Neurosci. 2013, 7:264.
80. Lazarowski E.R. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal 2012, 8:359-373.
81. Léon C., Hechler B., Vial C., Leray C., Cazenave J.P., Gachet C. The P2Y1 receptor is an ADP receptor antagonized by ATP and expressed in platelets and megakaryoblastic cells. FEBS Lett. 1997, 403:26-30.
82. Liñán-Rico A., Wunderlich J.E., Enneking J.T., Tso D.R., Grants I., Williams K.C., Otey A., Michel K., Schemann M., Needleman 4, Harzman A., Christofi F.L. Neuropharmacology of purinergic receptors in human submucous plexus: involvement of P2X1, P2X2, P2X3 channels, P2Y and A3 metabotropic receptors in neurotransmission. Neuropharmacology 2015, 95:83-99.
83. Ma Z., Siebert A.P., Cheung K.H., Lee R.J., Johnson B., Cohen A.S., Vingtdeux V., Marambaud P., Foskett J.K. Calcium homeostasis modulator 1 (CALHM1) is the pore-forming subunit of an ion channel that mediates extracellular Ca2+ regulation of neuronal excitability. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1963-E1971.
84. Mamedova L.K., Joshi B.V., Gao Z.G., von Kügelgen I., Jacobson K.A. Diisothiocyanate derivatives as potent, insurmountable antagonists of P2Y6 nucleotide receptors. Biochem. Pharmacol. 2004, 67:1763-1770.
85. Matsuda N.M., Miller S.M. Non-adrenergic non-cholinergic inhibition of gastrointestinal smooth muscle and its intracellular mechanism(s). Fundam. Clin. Pharmacol. 2010, 24:261-268.
86. Mo G., Bernier L.P., Zhao Q., Chabot-Doré A.J., Ase A.R., Logothetis D., Cao C.Q., Séguéla P. Subtype-specific regulation of P2X3 and P2X2/3 receptors by phosphoinositides in peripheral nociceptors. Mol. Pain 2009, 5:47. 10.1186/1744-8069-5-47.
87. Monro R.L., Bertrand P.P., Bornstein J.C. ATP participates in three excitatory postsynaptic potentials in the submucous plexus of the guinea pig ileum. J. Physiol. 2004, 556:571-584.
88. Mutafova-Yambolieva V.N., Durnin L. The purinergic neurotransmitter revisited: a single substance or multiple players?. Pharmacol. Ther. 2014, 144:162-191.
89. Mutafova-Yambolieva V.N., Hwang S.J., Hao X., Chen H., Zhu M.X., Wood J.D., Ward S.M. Sanders KM (2007) Beta-nicotinamide adenine dinucleotide is an inhibitory neurotransmitter in visceral smooth muscle. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(41):16359-16364. (Oct. 9).
90. Nakatsuka T., Gu J.G. ATP P2X receptor-mediated enhancement of glutamate release and evoked EPSCs in dorsal horn neurons of the rat spinal cord. J. Neurosci. 2001, 21:6522-6531.
91. Neal K.B., Bornstein J.C. Mapping 5-HT inputs to enteric neurons of the guinea-pig small intestine. Neuroscience 2007, 145:556-567.
92. Nieto-Pescador M.G., Guerrero-Alba R., Valdez-Morales E., Espinosa-Luna R., Jiménez-Vargas N., Liñan-Rico Andrómeda A., Ramos-Lomas T.L., Díaz-Hernández Verónica V., Montaño L.M., Barajas-López C. P2X4 subunits are part of P2X native channels in murine myenteric neurons. Eur. J. Pharmacol. 2013, 709:93-102.
93. Ochoa-Cortes F., Liñán-Rico A., Jacobson K.A., Christofi F.L. Potential for developing purinergic drugs for gastrointestinal diseases. Inflamm. Bowel Dis. 2014, 20:1259-1287.
94. Palmer R.K., Boyer J.L., Schachter J.B., Nicholas R.A., Harden T.K. Agonist action of adenosine triphosphates at the human P2Y1 receptor. Mol. Pharmacol. 1998, 54:1118-1123.
95. 2+ channels. Eur. J. Pharmacol. 2014, 739:60-73.
96. Paton W.D., Vizi E.S., Zar M.A. The mechanism of acetylcholine release from parasympathetic nerves. J. Physiol. 1971, 215:819-848.
97. Poole D.P., Castelucci P., Robbins H.L., Chiocchetti R. Furness JB (2002) The distribution of P2X3 purine receptor subunits in the guinea pig enteric nervous system. Auton. Neurosci. 2002, 101:39-47.
98. Ren J., Bian X., DeVries M., Schnegelsberg B., Cockayne D.A., Ford A.P., Galligan J.J. P2X2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J. Physiol. 2003, 552:809-821.
99. Rong W., Keating C., Sun B., Dong L., Grundy D. Purinergic contribution to small intestinal afferent hypersensitivity in a murine model of postinfectious bowel disease. Neurogastroenterol. Motil. 2009, 21:665-671.
100. Roper S.D. Cell communication in taste buds. Cell. Mol. Life Sci. 2006, 63:1494-1500.
101. Roper S.D. Taste buds as peripheral chemosensory processors. Semin. Cell Dev. Biol. 2013, 24:71-79.
102. Ruan H.Z., Burnstock G. The distribution of P2X5 purinergic receptors in the enteric nervous system of mouse. Cell Tissue Res. 2005, 319:191-200.
103. Sawada K., Echigo N., Juge N., Miyaji T., Otsuka M., Omote H., Yamamoto A., Moriyama Y. Identification of a vesicular nucleotide transporter. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5683-5686.
104. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network. J. Neurosci. 2004, 24:3125-3135.
105. Simon J., Webb T.E., King B.F., Burnstock G., Barnard E.A. Characterisation of a recombinant P2Y purinoceptor. Eur. J. Pharmacol. 1995, 291:281-289.
106. Taruno A., Vingtdeux V., Ohmoto M., Ma Z., Dvoryanchikov G., Li A., Adrien L., Zhao H., Leung S., Abernethy M., Koppel J., Davies P., Civan M.M., Chaudhari N., Matsumoto I., Hellekant G., Tordoff M.G., Marambaud P., Foskett J.K. CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 2013, 495:223-226.
107. Thornton P.D., Gwynne R.M., McMillan D.J., Bornstein J.C. Transmission to interneurons is via slow excitatory synaptic potentials mediated by P2Y1 receptors during descending inhibition in guinea-pig ileum. PLoS One 2013, 8:e40840.
108. Tokuyama Y., Hara M., Jones E.M., Fan Z., Bell G.I. Cloning of rat and mouse P2Y purinoceptors. Biochem. Biophys. Res. Commun. 1995, 211(1):211-218.
109. Van Crombruggen K., Van Nassauw L., Timmermans J.P., Lefebvre R.A. Inhibitory purinergic P2 receptor characterization in rat distal colon. Neuropharmacology 2007, 53:257-271.
110. Van Geldre L.A., Lefebvre R.A. Interaction of NO and VIP in gastrointestinal smooth muscle relaxation. Curr. Pharm. Des. 2004, 10:2483-2497.
111. Vandenbeuch A., Larson E.D., Anderson C.B., Smith S.A., Ford A.P., Finger T.E., Kinnamon S.C. Postsynaptic P2X3-containing receptors in gustatory nerve fibres mediate responses to all taste qualities. J. Physiol. 2015, 593:1113-1125.
112. von Kügelgen I. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 2006, 110:415-432.
113. Wang G.D., Wang X.Y., Liu S., Xia Y., Zou F., Qu M., Needleman B.J., Mikami D.J., Wood J.D. Beta-nicotinamide adenine dinucleotide suppresses inhibitory musculomotor neurotransmission in guinea pig colon and human jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, (Epub ahead of print). 10.1152/ajpgi.00430.2014.
114. Webb T.E., Simon J., Krishek B.J., Bateson A.N., Smart T.G., King B.F., Burnstock G., Barnard E.A. Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Lett. 1993, 324:219-225.
115. White T.D., Leslie R.A. Depolarization-induced release of adenosine 5'-triphosphate from isolated varicosities derived from the myenteric plexus of the guinea pig small intestine. J. Neurosci. 1982, 2:206-215.
116. Xiang Z., Burnstock G. Distribution of P2Y2 receptors in the guinea pig enteric nervous system and its coexistence with P2X2 and P2X3 receptors, neuropeptide Y, nitric oxide synthase and calretinin. Histochem. Cell Biol. 2005, 124:379-390.
117. Xiang Z., Burnstock G. Distribution of P2Y6 and P2Y12 receptor: their colocalization with calbindin, calretinin and nitric oxide synthase in the guinea pig enteric nervous system. Histochem. Cell Biol. 2006, 125:327-336.
118. Yamboliev I.A., Smyth L.M., Durnin L., Dai Y., Mutafova-Yambolieva V.N. Storage and secretion of β-NAD, ATP and dopamine in NGF-differentiated rat pheochromocytoma PC12 cells. Eur. J. Neurosci. 2009, 30:756-768.
119. Yu Q., Zhao Z., Sun J., Guo W., Fu J., Burnstock G., He C., Xiang Z. Expression of P2X6 receptors in the enteric nervous system of the rat gastrointestinal tract. Histochem. Cell Biol. 2010, 133:177-188.
120. Zhang Y., Lomax A.E., Paterson W.G. P2Y1 receptors mediate apamin-sensitive and -insensitive inhibitory junction potentials in murine colonic circular smooth muscle. J. Pharmacol. Exp. Ther. 2010, 333:602-611.
121. Zhang J., Zhang K., Gao Z.G., Paoletta 2, Zhang D., Han G.W., Li T., Ma L., Zhang W., Müller C.E., Yang H., Jiang H., Cherezov V., Katritch V., Jacobson K.A., Stevens R.C., Wu B., Zhao Q. Agonist-bound structure of the human P2Y12 receptor. Nature 2014, 509:119-122.
122. Zhang D., Gao Z.G., Zhang K., Kiselev E., Crane S., Wang J., Paoletta S., Yi C., Ma L., Zhang W., Han G.W., Liu H., Cherezov V., Katritch V., Jiang H., Stevens R.C., Jacobson K.A., Zhao Q., Wu B. Two disparate ligand-binding sites in the human P2Y1 receptor. Nature 2015, 520:317-321.
123. Zhao Q., Yang M., Ting A.T., Logothetis D.E. PIP2 regulates the ionic current of P2X receptors and P2X7 receptor-mediated cell death. Channels 2007, 1:46-55.
124. Zhou X., Galligan J.J. P2X purinoceptors in cultured myenteric neurons of guinea-pig small intestine. J. Physiol. 1996, 496:719-729.
125. Zhou X., Galligan J.J. Synaptic activation and properties of 5-hydroxytryptamine(3) receptors in myenteric neurons of guinea pig intestine. J. Pharmacol. Exp. Ther. 1999, 290:803-810.