Nitric oxide regulation of colonic epithelial ion transport: A novel role for enteric glia in the myenteric plexus

Journal of Physiology

Volumn 589, Issue 13, 2011, Pages 3333-3348

  Maceachern, Sarah J ^a   Patel, Bhavik A ^b   Mckay, Derek M ^a   Sharkey, Keith A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF BRIGHTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 PHENYL 4,4,5,5 TETRAMETHYLIMIDAZOLINE 1 OXYL 3 OXIDE; IMIDAZOLE DERIVATIVE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NICOTINIC RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

AMPEROMETRY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELLULAR DISTRIBUTION; CHOLINERGIC STIMULATION; COLON MUCOSA; CONTROLLED STUDY; ENZYME INHIBITION; GANGLION; GLIA; IMMUNOHISTOCHEMISTRY; ION TRANSPORT; MOUSE; MYENTERIC PLEXUS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; COLON; ENTERIC NERVOUS SYSTEM; FEMALE; INTESTINAL MUCOSA; ION TRANSPORT; MALE; MICE; MICE, KNOCKOUT; MYENTERIC PLEXUS; NEUROGLIA; NITRIC OXIDE;

EID: 79959697082     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.207902     Document Type: Article

References (56)

1. Amitai Y (2010). Physiologic role for "inducible" nitric oxide synthase: A new form of astrocytic-neuronal interface. Glia 58, 1775-1781.
2. Barrett KE & Keely SJ (2000). Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu Rev Physiol 62, 535-572.
3. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH & Sofroniew MV (1998). Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93, 189-201.
4. Cooke HJ (1989). Role of the "little brain" in the gut in water and electrolyte homeostasis. FASEB J 3, 127-138.
5. Cross RK & Wilson KT (2003). Nitric oxide in inflammatory bowel disease. Inflamm Bowel Dis 9, 179-189.
6. Diener M, Knobloch SF, Bridges RJ, Keilmann T & Rummel W (1989). Cholinergic-mediated secretion in the rat colon: neuronal and epithelial muscarinic responses. Eur J Pharmacol 168, 219-229.
7. Ferri GL, Probert L, Cocchia D, Michetti F, Marangos PJ & Polak JM (1982). Evidence for the presence of S-100 protein in the glial component of the human enteric nervous system. Nature 297, 409-410.
8. Flamant M, Aubert P, Rolli-Derkinderen M, Bourreille A, Neunlist MR, Mahe MM, Meurette G, Marteyn B, Savidge T, Galmiche JP, Sansonetti PJ & Neunlist M (2010). Enteric glia protect against Shigella flexneri invasion in intestinal epithelial cells: a role for S-nitrosoglutathione. Gut 60, 473-484
9. Furness JB (2006) The Enteric Nervous System. Blackwell Publishing, Malden, MA
10. Furness JB, Li ZS, Young HM & Forstermann U (1994). Nitric oxide synthase in the enteric nervous system of the guinea-pig: a quantitative description. Cell Tissue Res 277, 139-149.
11. Gabella G (1981). Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6, 425-436.
12. Gabella G & Trigg P (1984). Size of neurons and glial cells in the enteric ganglia of mice, guinea-pigs, rabbits and sheep. J Neurocytol 13, 49-71.
13. Galea E, Feinstein DL & Reis DJ (1992). Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures. Proc Natl Acad Sci U S A 89, 10945-10949.
14. Green CL, Ho W, Sharkey KA & McKay DM (2004). Dextran sodium sulfate-induced colitis reveals nicotinic modulation of ion transport via iNOS-derived NO. Am J Physiol Gastrointest Liver Physiol 287, G706-G714.
15. Gulbransen BD, Bains JS & Sharkey KA (2010). Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci 30, 6801-6809.
16. Gulbransen BD & Sharkey KA (2009). Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 136, 1349-1358.
17. Hebeiss K & Kilbinger H (1998). Nitric oxide-sensitive guanylyl cyclase inhibits acetylcholine release and excitatory motor transmission in the guinea-pig ileum. Neuroscience 82, 623-629.
18. Izzo AA, Mascolo N & Capasso F (1998). Nitric oxide as a modulator of intestinal water and electrolyte transport. Dig Dis Sci 43, 1605-1620.
19. Jodal M, Holmgren S, Lundgren O & Sjoqvist A (1993). Involvement of the myenteric plexus in the cholera toxin-induced net fluid secretion in the rat small intestine. Gastroenterology 105, 1286-1293.
20. Kirchgessner AL & Liu MT (1998). Immunohistochemical localization of nicotinic acetylcholine receptors in the guinea pig bowel and pancreas. J Comp Neurol 390, 497-514.
21. Knowles RG & Moncada S (1994). Nitric oxide synthases in mammals. Biochem J 298, 249-258.
22. Kojima H, Hirotani M, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, Hirata Y & Nagano T (2001). Bioimaging of nitric oxide with fluorescent indicators based on the rhodamine chromophore. Anal Chem 73, 1967-1973.
23. Mang CF, Truempler S, Erbelding D & Kilbinger H (2002). Modulation by NO of acetylcholine release in the ileum of wild-type and NOS gene knockout mice. Am J Physiol Gastrointest Liver Physiol 283, G1132-G1138.
24. Mawe GM & Gershon MD (1986). Functional heterogeneity in the myenteric plexus: demonstration using cytochrome oxidase as a verified cytochemical probe of the activity of individual enteric neurons. J Comp Neurol 249, 381-391.
25. Miampamba M & Sharkey KA (1999). Temporal distribution of neuronal and inducible nitric oxide synthase and nitrotyrosine during colitis in rats. Neurogastroenterol Motil 11, 193-206.
26. Moncada S & Bolanos JP (2006). Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97, 1676-1689.
27. Mourad FH, Barada KA, bdel-Malak N, Bou Rached NA, Khoury CI, Saade NE & Nassar CF (2003). Interplay between nitric oxide and vasoactive intestinal polypeptide in inducing fluid secretion in rat jejunum. J Physiol 550, 863-871.
28. Mourad FH, Barada KA, Bou Rached NA, Khoury CI, Saade NE & Nassar CF (2006). Inhibitory effect of experimental colitis on fluid absorption in rat jejunum: role of the enteric nervous system, VIP, and nitric oxide. Am J Physiol Gastrointest Liver Physiol 290, G262-G268.
29. Mourad FH, Turvill JL & Farthing MJ (1999). Role of nitric oxide in intestinal water and electrolyte transport. Gut 44, 143-147.
30. Murphy S, Simmons ML, Agullo L, Garcia A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D & Schwartz JP (1993). Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 16, 323-328.
31. 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.
32. Neunlist M, Michel K, Aube AC, Galmiche JP & Schemann M (2001). Projections of excitatory and inhibitory motor neurones to the circular and longitudinal muscle of the guinea pig colon. Cell Tissue Res 305, 325-330.
33. Obaid AL, Nelson ME, Lindstrom J & Salzberg BM (2005). Optical studies of nicotinic acetylcholine receptor subtypes in the guinea-pig enteric nervous system. J Exp Biol 208, 2981-3001.
34. Patel BA (2008). Continuous amperometric detection of co-released serotonin and melatonin from the mucosa in the ileum. Analyst 133, 516-524.
35. Patel BA, Bian X, Quaiserova-Mocko V, Galligan JJ & Swain GM (2007). In vitro continuous amperometric monitoring of 5-hydroxytryptamine release from enterochromaffin cells of the guinea pig ileum. Analyst 132, 41-47.
36. Patel BA, Galligan JJ, Swain GM & Bian X (2008). Electrochemical monitoring of nitric oxide released by myenteric neurons of the guinea pig ileum. Neurogastroenterol Motil 20, 1243-1250.
37. Qu ZD, Thacker M, Castelucci P, Bagyanszki M, Epstein ML & Furness JB (2008). Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 334, 147-161.
38. Rao RK, Riviere PJ, Pascaud X, Junien JL & Porreca F (1994). Tonic regulation of mouse ileal ion transport by nitric oxide. J Pharmacol Exp Ther 269, 626-631.
39. Reddix RA, Liu X, Miller MJ, Niu X & Powell A (2000). Constitutive nitric oxide release modulates neurally-evoked chloride secretion in guinea pig colon. Auton Neurosci 86, 47-57.
40. Rolfe VE & Levin RJ (1998). Neural and non-neural activation of electrogenic secretion by 5-hydroxytryptamine in the rat ileum in vitro. Acta Physiol Scand 162, 469-474.
41. Rolfe VE & Milla PJ (1999). Nitric oxide stimulates cyclic guanosine monophosphate production and electrogenic secretion in Caco-2 colonocytes. Clin Sci (Lond) 96, 165-170.
42. Sang Q & Young HM (1996). Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284, 39-53.
43. Savidge TC (2007). MIND the gap: an astroglial perspective on barrier regulation. Neuron Glia Biol 3, 191-197.
44. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R & Sofroniew MV (2007). Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132, 1344-1358.
45. See NA & Bass P (1993). Glucose-induced ion secretion in rat jejunum: a mucosal reflex that requires integration by the myenteric plexus. J Auton Nerv Syst 42, 33-40.
46. Simmons ML & Murphy S (1992). Induction of nitric oxide synthase in glial cells. J Neurochem 59, 897-905.
47. Stack WA, Filipowicz B & Hawkey CJ (1996). Nitric oxide donating compounds stimulate human colonic ion transport in vitro. Gut 39, 93-99.
48. Tamai H & Gaginella TS (1993). Direct evidence for nitric oxide stimulation of electrolyte secretion in the rat colon. Free Radic Res Commun 19, 229-239.
49. Tang Q, Svensson CI, Fitzsimmons B, Webb M, Yaksh TL & Hua XY (2007). Inhibition of spinal constitutive NOS-2 by 1400W attenuates tissue injury and inflammation-induced hyperalgesia and spinal p38 activation. Eur J Neurosci 25, 2964-2972.
50. Tapper EJ & Lewand DL (1981). Actions of a nicotinic agonist, DMPP, on intestinal ion transport in vitro. Life Sci 28, 155-162.
51. Van Landeghem L, Mahe MM, Teusan R, Leger J, Guisle I, Houlgatte R & Neunlist M (2009). Regulation of intestinal epithelial cells transcriptome by enteric glial cells: impact on intestinal epithelial barrier functions. BMC Genomics 10, 507.
52. Vives V, Alonso G, Solal AC, Joubert D & Legraverend C (2003). Visualization of S100B-positive neurons and glia in the central nervous system of EGFP transgenic mice. J Comp Neurol 457, 404-419.
53. Wang S, Paton JF & Kasparov S (2006). The challenge of real-time measurements of nitric oxide release in the brain. Auton Neurosci 126-127, 59-67.
54. Wapnir RA, Wingertzahn MA & Teichberg S (1997). L-Arginine in low concentration improves rat intestinal water and sodium absorption from oral rehydration solutions. Gut 40, 602-607.
55. Wilson KT, Xie Y, Musch MW & Chang EB (1993). Sodium nitroprusside stimulates anion secretion and inhibits sodium chloride absorption in rat colon. J Pharmacol Exp Ther 266, 224-230.
56. Yajima T, Inoue R, Matsumoto M & Yajima M (2011). Non-neuronal release of ACh plays a key role in secretory response to luminal propionate in rat colon. J Physiol 589, 953-962.