Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon

Journal of Neuroscience

Volumn 30, Issue 19, 2010, Pages 6801-6809

  Gulbransen, Brian D ^a   Bains, Jaideep S ^a   Sharkey, Keith A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; NEUROTRANSMITTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DESCENDING COLON; GLIA; GUINEA PIG; INTESTINE INNERVATION; MALE; MYENTERIC PLEXUS; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SYMPATHETIC INNERVATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; COLON; GUINEA PIGS; MALE; MYENTERIC PLEXUS; NEURAL PATHWAYS; NEUROGLIA; NEURONS; NEURONS, AFFERENT; NEUROTRANSMITTER AGENTS; RECEPTORS, NICOTINIC; SYMPATHETIC NERVOUS SYSTEM; SYNAPTIC TRANSMISSION;

EID: 77952349469     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0603-10.2010     Document Type: Article

References (58)

1. Al-Humayyd M, White TD (1985) Adrenergic and possible nonadrenergic sources of adenosine 5′-triphosphate release from nerve varicosities isolated from ileal myenteric plexus. J Pharmacol Exp Ther 233:796-800. (Pubitemid 15024451)
2. 2+ elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450.
3. Bekar LK, He W, Nedergaard M (2008) Locus coeruleus alpha-adrenergic- mediated activation of cortical astrocytes in vivo. Cereb Cortex 18:2789-2795.
4. Blandizzi C, Fornai M, Colucci R, Baschiera F, Barbara G, De Giorgio R, De Ponti F, Breschi MC, Del Tacca M (2003) Altered prejunctional modulation of intestinal cholinergic and noradrenergic pathways by alpha2-adrenoceptors in the presence of experimental colitis. Br J Pharmacol 139:309-320. (Pubitemid 36760363)
5. Brierley SM, Carter R, Jones W 3rd, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA (2005) Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567:267-281. (Pubitemid 41167320)
6. Burnstock G (2009) Purinergic cotransmission. Exp Physiol 94:20-24.
7. Crowcroft PJ, Holman ME, Szurszewski JH (1971) Excitatory input from the distal colon to the inferior mesenteric ganglion in the guinea-pig. J Physiol 219:443-461.
8. Furness JB (2006) The enteric nervous system. Malden, MA: Blackwell.
9. Gabella G (1981) Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6:425-436.
10. Galligan JJ, Bertrand PP (1994) ATP mediates fast synaptic potentials in enteric neurons. J Neurosci 14:7563-7571.
11. Gershon MD, Sherman DL, Dreyfus CF (1980) Effects of indolic neurotoxins on enteric serotonergic neurons. J Comp Neurol 190:581-596.
12. Gershon MD, Sherman DL, Pintar JE (1990) Type-specific localization of monoamine oxidase in the enteric nervous system: relationship to 5-hydroxytryptamine, neuropeptides, and sympathetic nerves. J Comp Neurol 301:191-213.
13. Gomes P, Chevalier J, Boesmans W, Roosen L, van den Abbeel V, Neunlist M, Tack J, Vanden Berghe P (2009) ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived from embryonic mice. Neurogastroenterol Motil 21:870-e62.
14. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-749.
15. Gordon GR, Iremonger KJ, Kantevari S, Ellis-Davies GC, MacVicar BA, Bains JS (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64:391-403.
16. Gulbransen BD, Sharkey KA (2009) Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136:1349-1358.
17. Hanani M, Reichenbach A (1994) Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278:153-160. (Pubitemid 24281912)
18. Hirst GD, McKirdy HC (1974) Presynaptic inhibition at mammalian peripheral synapse? Nature 250:430-431.
19. Jacobson K, McHugh K, Collins SM (1997) The mechanism of altered neural function in a rat model of acute colitis. Gastroenterology 112:156-162. (Pubitemid 27008997)
20. Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206-2218. (Pubitemid 14248177)
21. 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. (Pubitemid 36143804)
22. Kettenmann H, Ransom B (2004) Neuroglia. New York: Oxford UP.
23. 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. (Pubitemid 26037315)
24. 2+ release in Bergmann glia cells in situ. J Neurosci 19:8401-8408.
25. LePard KJ, Galligan JJ (1999) Analysis of fast synaptic pathways in the myenteric plexus of guinea pig ileum. Am J Physiol 276:G529-G538.
26. Linden DR, Couvrette JM, Ciolino A, McQuoid C, Blaszyk H, Sharkey KA, Mawe GM (2005) Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 17:751-760. (Pubitemid 41400725)
27. Lomax AE, Zhang JY, Furness JB (2000) Origins of cholinergic inputs to the cell bodies of intestinofugal neurons in the guinea pig distal colon. J Comp Neurol 416:451-460.
28. Lomax AE, Sharkey KA, Furness JB (2010) The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol Motil 22:7-18.
29. Machaly M, Dalziel HH, Sneddon P (1988) Evidence for ATP as a cotransmitter in dog mesenteric artery. Eur J Pharmacol 147:83-91. (Pubitemid 18058728)
30. Maggi CA, Meli A, Santicioli P (1987) Four motor effects of capsaicin on guinea-pig distal colon. Br J Pharmacol 90:651-660. (Pubitemid 17105110)
31. Malin SA, Christianson JA, Bielefeldt K, Davis BM (2009) TPRV1 expression defines functionally distinct pelvic colon afferents. J Neurosci 29:743-752.
32. Messenger JP, Furness JB (1992) Distribution of enteric nerve cells that project to the coeliac ganglion of the guinea-pig. Cell Tissue Res 269:119-132.
33. 2+ current underlies the reduction in norepinephrine release during colitis. Am J Physiol Gastrointest Liver Physiol 296:G1077-G1084.
34. Nasser Y, Keenan CM, Ma AC, McCafferty DM, Sharkey KA (2007) Expression of a functional metabotropic glutamate receptor 5 on enteric glia is altered in states of inflammation. Glia 55:859-872. (Pubitemid 46787196)
35. Nurgali K, Furness JB, Stebbing MJ (2003) Analysis of purinergic and cholinergic fast synaptic transmission to identified myenteric neurons. Neuroscience 116:335-347. (Pubitemid 36139906)
36. Olsson C, Chen BN, Jones S, Chataway TK, Costa M, Brookes SJ (2006) Comparison of extrinsic efferent innervation of guinea pig distal colon and rectum. J Comp Neurol 496:787-801.
37. Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. Pflugers Arch 452:589-597. (Pubitemid 44015093)
38. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116. (Pubitemid 41434548)
39. Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192-2203. (Pubitemid 40322260)
40. Qayyum MA (1976) Fluorescence histochemical study of Aurbach's plexus of the ileum of 6-hydroxydopamine-treated guinea pig. Acta Anat (Basel) 96:497-512.
41. Robinson DR, McNaughton PA, Evans ML, Hicks GA (2004) Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16:113-124.
42. Schipke CG, Haas B, Kettenmann H (2008) Astrocytes discriminate and selectively respond to the activity of a subpopulation of neurons within the barrel cortex. Cereb Cortex 18:2450-2459.
43. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638-1643. (Pubitemid 351931254)
44. Serrano A, Haddjeri N, Lacaille JC, Robitaille R (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26:5370-5382. (Pubitemid 44318389)
45. Sharkey KA, Parr EJ, Keenan CM (1999) Immediate-early gene expression in the inferior mesenteric ganglion and colonic myenteric plexus of the guinea pig. J Neurosci 19:2755-2764.
46. Spencer N, McCarron SL, Smith TK (1999) Sympathetic inhibition of ascending and descending interneurones during the peristaltic reflex in the isolated guinea-pig distal colon. J Physiol 519:539-550. (Pubitemid 29430015)
47. Stebbing M, Johnson P, Vremec M, Bornstein J (2001) Role of alpha(2)-adrenoceptors in the sympathetic inhibition of motility reflexes of guine-apig ileum. J Physiol 534:465-478. (Pubitemid 32677741)
48. Stjärne L (1989) Basic mechanisms and local modulation of nerve impulse-induced secretion of neurotransmitters from individual sympathetic nerve varicosities. Rev Physiol Biochem Pharmacol 112:1-137.
49. Tack JF, Wood JD (1992) Actions of noradrenaline on myenteric neurons in the guinea pig gastric antrum. J Auton Nerv Syst 41:67-77. (Pubitemid 23000497)
50. Takahashi A, Camacho P, Lechleiter JD, Herman B (1999) Measurement of intracellular calcium. Physiol Rev 79:1089-1125.
51. Todorov LD, Mihaylova-Todorova ST, Bjur RA, Westfall DP (1999) Differential cotransmission in sympathetic nerves: role of frequency of stimulation and prejunctional autoreceptors. J Pharmacol Exp Ther 290:241-246.
52. Vanner S, Surprenant A (1996) Neural reflexes controlling intestinal microcirculation. Am J Physiol 271:G223-G230. (Pubitemid 26295129)
53. Venkova K, Krier J (1993) Stimulation of lumbar sympathetic nerves evokes contractions of cat colon circular muscle mediated by ATP and noradrenaline. Br J Pharmacol 110:1260-1270. (Pubitemid 24005270)
54. White TD (1982) Release of ATP from isolated myenteric varicosities by nicotinic agonists. Eur J Pharmacol 79:333-334.
55. White TD, Al-Humayyd M (1983) Acetylcholine releases ATP from varicosities isolated from guinea pig myenteric plexus. J Neurochem 40:1069-1075.
56. Wu LG, Saggau P (1994) Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12:1139-1148.
57. Yuyama N, Mizuno J, Tsuzuki H, Wada-Takahashi S, Takahashi O, Tamura K (2002) Effects of extrinsic autonomic inputs on expression of c-Fos immunoreactivity in myenteric neurons of the guinea pig distal colon. Brain Res 948:8-16. (Pubitemid 35283756)
58. Zhang W, Segura BJ, Lin TR, Hu Y, Mulholland MW (2003) Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia 42:252-262. (Pubitemid 36538338)