Transmission to Interneurons Is via Slow Excitatory Synaptic Potentials Mediated by P2Y1 Receptors during Descending Inhibition in Guinea-Pig Ileum

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Thornton, Peter D J ^a,b   Gwynne, Rachel M ^a   McMillan, Darren J ^a,c   Bornstein, Joel C ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b JOHNSON AND JOHNSON   (United States)

^c OLYMPIC PARK SPORTS MEDICINE CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; GRANISETRON; HEXAMETHONIUM; METABOTROPIC RECEPTOR; NICOTINIC RECEPTOR; NITRIC OXIDE SYNTHASE; PURINERGIC P2 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SEROTONIN 3 RECEPTOR; ADENOSINE DIPHOSPHATE; N(6)-METHYL-2'-DEOXYADENOSINE 3',5'-DIPHOSPHATE; NICOTINIC RECEPTOR BLOCKING AGENT; PURINERGIC P2Y RECEPTOR ANTAGONIST; PYRIDOXAL 5 PHOSPHATE; PYRIDOXAL PHOSPHATE-6-AZOPHENYL-2',4'-DISULFONIC ACID; SEROTONIN 3 ANTAGONIST;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GUINEA PIG; ILEUM; IMMUNOREACTIVITY; IN VITRO STUDY; INTERNEURON; INTRACELLULAR RECORDING; MOUSE; MYENTERIC PLEXUS; NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; RECEPTOR BLOCKING; SYNAPTIC TRANSMISSION; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; INNERVATION; MALE; METABOLISM; PHYSIOLOGY; REFLEX; SYNAPSE; SYNAPTIC POTENTIAL;

ADENOSINE DIPHOSPHATE; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GUINEA PIGS; ILEUM; INTERNEURONS; MALE; NICOTINIC ANTAGONISTS; PURINERGIC P2Y RECEPTOR ANTAGONISTS; PYRIDOXAL PHOSPHATE; RECEPTORS, NICOTINIC; RECEPTORS, PURINERGIC P2Y1; RECEPTORS, SEROTONIN, 5-HT3; REFLEX; SEROTONIN 5-HT3 RECEPTOR ANTAGONISTS; SYNAPSES; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

EID: 84873598978     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040840     Document Type: Article

References (44)

1. Bayliss WM, Starling EH, (1899) The movements and innervation of the small intestine. J Physiol (Lond) 24: 99-143.
2. Furness JB (2006) The Enteric Nervous System. Oxford, UK: Blackwell Publishing Ltd.
3. Tonini M, Vicini R, Cervio E, De Ponti F, De Giorgio R, et al. (2005) 5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. Gastroenterology 129: 1557-1566.
4. Spencer N, Walsh M, Smith TK, (1999) Does the guinea-pig ileum obey the 'law of the intestine'? J Physiol (Lond) 517: 889-898.
5. Smith TK, Bornstein JC, Furness JB, (1991) Interactions between reflexes evoked by distension and mucosal stimulation: electrophysiological studies of guinea-pig ileum. J Auton Nerv Syst 34: 69-76.
6. Gwynne RM, Bornstein JC, (2007) Local inhibitory reflexes excited by mucosal application of nutrient amino acids in guinea-pig jejunum. Am J Physiol Gastrointest Liver Physiol 292: G1660-G1670.
7. Grider JR, Foxx-Orenstein AE, Jin J-G, (1998) 5-Hydroxytryptamine4 receptor agonists initiate the peristaltic reflex in human, rat, and guinea pig intestine. Gastroenterology 115: 370-380.
8. Gwynne RM, Bornstein JC, (2007) Synaptic transmission at functionally identified synapses in the enteric nervous system: roles for both ionotropic and metabotropic receptors. Curr Neuropharmacol 5: 1-17.
9. Johnson PJ, Yuan SY, Bornstein JC, Furness JB, (1996) Analysis of contributions of acetylcholine and tachykinins to neuro-neuronal transmission in motility reflexes in the guinea-pig ileum. Br J Pharmacol 118: 973-983.
10. Johnson PJ, Bornstein JC, Burcher E, (1998) Roles of neuronal NK1 and NK3 receptors in synaptic transmission during motility reflexes in the guinea-pig ileum. Br J Pharmacol 124: 1375-1384.
11. Bian X-C, Bertrand PP, Bornstein JC, (2000) Descending inhibitory reflexes involve P2X receptor-mediated transmission from interneurons to motor neurons in guinea-pig ileum. J Physiol (Lond) 528: 551-560.
12. Thornton PDJ, Bornstein JC, (2002) Slow excitatory synaptic potentials evoked by distension in myenteric descending interneurons of guinea-pig ileum. J Physiol (Lond) 539: 589-602.
13. 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.
14. Katayama Y, Morita K, (1989) Adenosine 5′-triphosphate modulates membrane potassium conductance in guinea-pig myenteric neurones. J Physiol (Lond) 408: 1-18.
15. Alex G, Kunze WAA, Furness JB, Clerc N, (2001) Comparison of the effects of neurokinin-3 receptor blockade on two forms of slow synaptic transmission in myenteric AH neurons. Neuroscience 104: 263-269.
16. Johnson PJ, Bornstein JC, (2004) Neurokinin-1 and -3 receptor blockade inhibits slow excitatory synaptic transmission in myenteric neurons and reveals slow inhibitory input. Neuroscience 126: 137-147.
17. Monro RL, Bornstein JC, Bertrand PP, (2005) Slow excitatory post-synaptic potentials in myenteric AH neurons of the guinea-pig ileum are reduced by the 5-hydroxytryptamine7 receptor antagonist SB 269970. Neuroscience 134: 975-986.
18. Brookes SJH, Steele PA, Costa M, (1991) Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine. Neuroscience 42: 863-878.
19. Monro RL, Bertrand PP, Bornstein JC, (2002) ATP and 5-HT are the principal neurotransmitters in the descending excitatory reflex pathway of the guinea-pig ileum. Neurogastro Mot 14: 255-264.
20. Spencer NJ, Smith CB, Smith TK, (2001) Role of muscle tone in peristalsis in guinea-pig small intestine. J Physiol (Lond) 530: 295-306.
21. Bertrand PP, (2006) Real-time measurement of serotonin release and motility in guinea pig ileum. J Physiol (Lond) 577: 689-704.
22. Kunze WAA, Furness JB, Bertrand PP, Bornstein JC, (1998) Intracellular recording from myenteric neurons of the guinea-pig ileum that respond to stretch. J Physiol (Lond) 506: 827-842.
23. Johnson PJ, Shum OR, Thornton PDJ, Bornstein JC, (1999) Evidence that inhibitory motor neurons of the guinea-pig small intestine exhibit fast excitatory synaptic potentials mediated via P2X receptors. Neurosci Lett 266: 169-172.
24. LePard KJ, Messori E, Galligan JJ, (1997) Purinergic fast excitatory postsynaptic potentials in myenteric neurons of guinea pig: distribution and pharmacology. Gastroenterology 113: 1522-1534.
25. Spencer NJ, Walsh M, Smith TK, (2000) Purinergic and cholinergic neuro-neuronal transmission underlying reflexes activated by mucosal stimulation in the isolated guinea-pig ileum. J Physiol (Lond) 522: 321-331.
26. Bornstein JC, Costa M, Furness JB, Lang RJ, (1986) Electrophysiological analysis of projections of enteric inhibitory motor neurones in the guinea-pig small intestine. J Physiol (Lond) 370: 61-74.
27. Gallego D, Vanden Berghe P, Farré R, Tack J, Jiménez M, (2008) P2Y1 receptors mediate inhibitory neuromuscular transmission and enteric neuronal activation in small intestine. Neurogastro Mot 20: 159-168.
28. Gallego D, Hernández P, Clavé P, Jiménez M, (2006) P2Y1 receptors mediate inhibitory purinergic neuromuscular transmission in the human colon. Am J Physiol Gastrointestand Liver Physiol 291: G584-G594.
29. Ralevic V, Burnstock G, (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492.
30. Hwang SJ, Durnin L, Dwyer L, Rhee P-L, Ward SM, et al. (2011) β-Nicotinamide adenine dinucleotide is an enteric inhibitory neurotransmitter in human and nonhuman primate colons. Gastroenterology 140: 608-617.
31. Mutafova-Yambolieva V, Hwang SJ, Hao X, Chen H, Zhu MX, et al. (2007) β-Nicotinamide adenine dinucleotide is an inhibitory neurotransmitter in visceral smooth muscle. Proc Natl Acad Sci U S A 104: 16359-16364.
32. Hu H-Z, Gao N, Zhu MX, Liu S, Ren J, et al. (2003) Slow excitatory synaptic transmission mediated by P2Y1 receptors in the guinea-pig enteric nervous system. J Physiol (Lond) 550: 493-504.
33. Monro RL, Bertrand PP, Bornstein JC, (2004) ATP participates in three excitatory post-synaptic potentials in the submucous plexus of the guinea pig ileum. J Physiol (Lond) 556: 571-584.
34. Foong JPP, Bornstein JC (2009) mGluR1 receptors contribute to non-purinergic slow excitatory transmission to submucosal VIP neurons of guinea-pig ileum. Front Neurosci: doi: 10.3389/neuro.3321.3001.2009.
35. Gallego D, Gil V, Aleu J, Aulí M, Clavé P, et al. (2008) Purinergic and nitrergic junction potential in the human colon. Am J Physiol Gastrointest Liver Physiol 295: G522-G533.
36. Alex G, Clerc N, Kunze WAA, Furness JB, (2002) Responses of myenteric S neurones to low frequency stimulation of their synaptic inputs. Neuroscience 110: 361-373.
37. Neunlist M, Dobreva G, Schemann M, (1999) Characteristics of mucosally projecting myenteric neurones in the guinea-pig proximal colon. J Physiol (Lond) 517: 533-546.
38. Bowser DN, Khakh BS, (2004) ATP Excites Interneurons and Astrocytes to Increase Synaptic Inhibition in Neuronal Networks. J Neurosci 24: 8606-8620.
39. Santello M, Bezzi P, Volterra A, (2011) TNFα controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69: 988-1001.
40. Aoyama T, Koga S, Nakatsuka T, Fujita T, Goto M, et al. (2010) Excitation of rat spinal ventral horn neurons by purinergic P2X and P2Y receptor activation. Brain Res 1340: 10-17.
41. Riedel G, Wetzel W, Reymann KG, (1996) Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 20: 761-789.
42. Pin J-P, (1998) The two faces of glutamate. Nature 394: 19-21.
43. Fiorillo CD, Williams JT, (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394: 78-82.
44. Gwynne RM, Bornstein JC, (2007) Mechanisms underlying nutrient induced segmentation in isolated guinea-pig small intestine. Am J Physiol Gastrointest Liver Physiol 292: G1162-G1172.