Role of enteric glia in intestinal physiology: Effects of the gliotoxin fluorocitrate on motor and secretory function

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 291, Issue 5, 2006, Pages

  Nasser, Yasmin ^a,b   Fernandez, Ester ^c   Keenan, Catherine M ^a,b   Ho, Winnie ^a,b   Oland, Lorraine D ^a,b   Tibbles, Lee Anne ^a   Schemann, Michael ^d   MacNaughton, Wallace K ^a   Rühl, Anne ^d   Sharkey, Keith A ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Colonic ion transport; Enteric glia; Myenteric plexus

Indexed keywords

2 [N (7 NITROBENZENE 2 OXA 1,3 DIAZ 4 YL)AMINO] 2 DEOXYGLUCOSE; ALANYLLYSYL 7 AMINO 4 METHYLCOUMARIN 3 ACETIC ACID; DEOXYGLUCOSE; DIPEPTIDE; FLUORESCENT DYE; FLUOROCITRIC ACID; GLIOTOXIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLON; COLON ABSORPTION; CONTROLLED STUDY; ELECTROSTIMULATION; ENTERIC GLIA; ENTERITIS; GLIA; GUINEA PIG; ILEUM; IN VITRO STUDY; IN VIVO STUDY; INTESTINE ABSORPTION; INTESTINE CONTRACTION; INTESTINE FUNCTION; INTESTINE INNERVATION; INTESTINE MOTILITY; INTESTINE SECRETION; ION TRANSPORT; MALE; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

4-CHLORO-7-NITROBENZOFURAZAN; ANIMALS; CELLS, CULTURED; CITRATES; COLITIS; DEOXYGLUCOSE; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL DISEASES; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRANSIT; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTESTINES; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; NEUROGLIA; NEURONS; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33751119918     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00067.2006     Document Type: Article

References (61)

1. Araque A, Parpura V, Sanzgiri RP, and Haydon PG. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22: 208-215, 1999.
2. Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, and Neunlist M. Changes in enteric neurone phenotype and intestinal functions in a transgenic mice model of enteric glia disruption. Gut 55: 630-637, 2005.
3. Bishop AE, Carlei F, Lee V, Trojanowski J, Marangos PJ, Dahl D, and Polak JM. Combined immunostaining of neurofilaments, neuron specific enolase, GFAP and S-100. A possible means for assessing the morphological and functional status of the enteric nervous system. Histochemistry 82: 93-97, 1985.
4. Brookes SJ. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262: 58-70, 2001.
5. Broussard DL, Bannerman PG, Tang CM, Hardy M, and Pleasure D. Electrophysiologic and molecular properties of cultured enteric glia. J Neurosci Res 34: 24-31, 1993.
6. Brown AM, Baltan TS, and Ransom BR. Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem Int 45: 529-536, 2004.
7. Buresi MC, Vergnolle N, Sharkey KA, Keenan CM, Andrade-Gordon P, Cirino G, Cirillo D, Hollenberg MD, and MacNaughton WK. Activation of proteinase-activated receptor-1 inhibits neurally evoked chloride secretion in the mouse colon in vitro. Am J Physiol Gastrointest Liver Physiol 288: G337-G345, 2005.
8. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, and Sofroniew MV. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93: 189-201, 1998.
9. Cabarrocas J, Savidge TC, and Liblau RS. Role of enteric glial cells in inflammatory bowel disease. Glia 41: 81-93, 2003.
10. Cornet A, Savidge TC, Cabarrocas J, Deng WL, Colombel JF, Lassmann H, Desreumaux P, and Liblau RS. Enterocolitis induced by autoimmune targeting of enteric glial cells: a possible mechanism in Crohn's disease? Proc Natl Acad Sci USA 98: 13306-13311, 2001.
11. ε-AMCA in astrocytes. Glia 25: 10-20, 1999.
12. Fletcher EL, Clark MJ, and Furness JB. Neuronal and glial localization of GABA transporter immunoreactivity in the myenteric plexus. Cell Tissue Res 308: 339-346, 2002.
13. Fonnum F, Johnsen A, and Hassel B. Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia 21: 106-113, 1997.
14. Furness JB, Clerc N, Vogalis F, and Stebbing MJ. The enteric nervous system and its extrinsic connections. In: Textbook of Gastroenterology, edited by Yamada T, Alpers DH, Kaplowitz N, Laine L, Owyang C, and Powell DW. Philadelphia, PA: Lippincott Williams & Wilkins, 2003, p. 12-33.
15. Gabella G. Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6: 425-436, 1981.
16. Gardner PR, Nguyen DD, and White CW. Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proc Natl Acad Sci USA 91: 12248-12252, 1994.
17. Gershon MD, Kirchgessner AL, and Wade PR. Functional anatomy of the enteric nervous system. In: Physiology of the Gastrointestinal Tract, edited by Johnson LR. New York: Raven, 1994.
18. Gordon GR, Baimoukhametova DV, Hewitt SA, Rajapaksha WR, Fisher TE, and Bains JS. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 8: 1078-1086, 2005.
19. Groneberg DA, Doring F, Eynott PR, Fischer A, and Daniel H. Intestinal peptide transport: ex vivo uptake studies and localization of peptide carrier PEPT1. Am J Physiol Gastrointest Liver Physiol 281: G697-G704, 2001.
20. Hanani M, Francke M, Hartig W, Grosche J, Reichenbach A, and Pannicke T. Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 278: G644-G651, 2000.
21. Hassel B, Paulsen RE, Johnsen A, and Fonnum F. Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res 576: 120-124, 1992.
22. Hassel B, Sonnewald U, Unsgard G, and Fonnum F. NMR spectroscopy of cultured astrocytes: effects of glutamine and the gliotoxin fluorocitrate. J Neurochem 62: 2187-2194, 1994.
23. Heffron DS and Mandell JW. Opposing roles of ERK and p38 MAP kinases in FGF2-induced astroglial process extension. Mol Cell Neurosci 28: 779-790, 2005.
24. Hornfeldt CS and Larson AA. Seizures induced by fluoroacetic acid and fluorocitric acid may involve chelation of divalent cations in the spinal cord. Eur J Pharmacol 179: 307-313, 1990.
25. Irving EA and Bamford M. Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 22: 631-647, 2002.
26. Itoh Y, Abe T, Takaoka R, and Tanahashi N. Fluorometric determination of glucose utilization in neurons in vitro and in vivo. J Cereb Blood Flow Metab 24: 993-1003, 2004.
27. Jessen KR and Mirsky R. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286: 736-737, 1980.
28. Jessen KR and Mirsky R. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3: 2206-2218, 1983.
29. Kimball BC and Mulholland MW. Enteric glia exhibit P2U receptors that increase cytosolic calcium by a phospholipase C-dependent mechanism. J Neurochem 66: 604-612, 1996.
30. Kofuji P and Newman EA. Potassium buffering in the central nervous system. Neuroscience 129: 1045-1056, 2004.
31. Largo C, Cuevas P, Somjen GG, Martin del Rio R, and Herreras O. The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival. J Neurosci 16: 1219-1229, 1996.
32. Lian XY and Stringer JL. Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression. Brain Res 1012: 177-184, 2004.
33. Lian XY and Stringer JL. Energy failure in astrocytes increases the vulnerability of neurons to spreading depression. Eur J Neurosci 19: 2446-2454, 2004.
34. Lian XY and Stringer JL. Inhibition of aconitase in astrocytes increases the sensitivity to chemical convulsants. Epilepsy Res 60: 41-52, 2004.
35. Loaiza A, Porras OH, and Barros LF. Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23: 7337-7342, 2003.
36. Marcus JS, Karackattu SL, Fleegal MA, and Sumners C. Cytokine-stimulated inducible nitric oxide synthase expression in astroglia: role of Erk mitogen-activated protein kinase and NF-kappaB. Glia 41: 152-160, 2003.
37. McCafferty DM, Miampamba M, Sihota E, Sharkey KA, and Kubes P. Role of inducible nitric oxide synthase in trinitrobenzene sulphonic acid induced colitis in mice. Gut 45: 864-873, 1999.
38. 2-mediated action on gastric transit in rats. Am J Physiol Gastrointest Liver Physiol 282: G34-G40, 2002.
39. Nasser Y, Ho W, and Sharkey KA. Distribution of adrenergic receptors in the enteric nervous system of the guinea pig, mouse, and rat. J Comp Neurol 495: 529-553, 2006.
40. Newman EA. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 26: 536-542, 2003.
41. Omara F and Sisodia CS. Evaluation of potential antidotes for sodium fluoroacetate in mice. Vet Hum Toxicol 32: 427-431, 1990.
42. Paulsen RE, Contestabile A, Villani L, and Fonnum F. An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J Neurochem 48: 1377-1385, 1987.
43. Rist RJ, Romero IA, Chan MW, and Abbott NJ. Effects of energy deprivation induced by fluorocitrate in immortalised rat brain microvessel endothelial cells. Brain Res 730: 87-94, 1996.
44. Ruhl A. Glial cells in the gut. Neurogastroenterol Motil 17: 1-14, 2005.
45. Ruhl A, Hoppe S, Frey I, Daniel H, and Schemann M. Functional expression of the peptide transporter PEPT2 in the mammalian enteric nervous system. J Comp Neurol 490: 1-11, 2005.
46. Ruhl A, Nasser Y, and Sharkey KA. Enteric glia. Neurogastroenterol Motil 16, Suppl 1: 44-49, 2004.
47. Ruhl A, Trotter J, and Stremmel W. Isolation of enteric glia and establishment of transformed enteroglial cell lines from the myenteric plexus of adult rat. Neurogastroenterol Motil 13: 95-106, 2001.
48. Schousboe A, Sarup A, Bak LK, Waagepetersen HS, and Larsson OM. Role of astrocytic transport processes in glutamatergic and GABAergic neurotransmission. Neurochem Int 45: 521-527, 2004.
49. Sharkey KA, Coggins PJ, Tetzlaff W, Zwiers H, Bisby MA, and Davision JS. Distribution of growth-associated protein, B-50 (GAP-43) in the mammalian enteric nervous system. Neuroscience 38: 13-20, 1990.
50. Swanson RA and Graham SH. Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res 664: 94-100, 1994.
51. Tibbles LA and Woodgett JR. The stress-activated protein kinase pathways. Cell Mol Life Sci 55: 1230-1254, 1999.
52. Tjwa ET, Bradley JM, Keenan CM, Kroese AB, and Sharkey KA. Interleukin-1beta activates specific populations of enteric neurons and enteric glia in the guinea pig ileum and colon. Am J Physiol Gastrointest Liver Physiol 285: G1268-G1276, 2003.
53. 2-terminal kinase). Eur J Biochem 244: 587-595, 1997.
54. Vanderwinden JM, Timmermans JP, and Schiffmann SN. Glial cells, but not interstitial cells, express P2X7, an ionotropic purinergic receptor, in rat gastrointestinal musculature. Cell Tissue Res 312: 149-154, 2003.
55. Vannucci SJ, Maher F, and Simpson IA. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 21: 2-21, 1997.
56. Wang X, Zhu C, Qiu L, Hagberg H, Sandberg M, and Blomgren K. Activation of ERK1/2 after neonatal rat cerebral hypoxia-ischaemia. J Neurochem 86: 351-362, 2003.
57. Wiesinger H, Hamprecht B, and Dringen R. Metabolic pathways for glucose in astrocytes. Glia 21: 22-34, 1997.
58. Willoughby JO, Mackenzie L, Broberg M, Thoren AE, Medvedev A, Sims NR, and Nilsson M. Fluorocitrate-mediated astroglial dysfunction causes seizures. J Neurosci Res 74: 160-166, 2003.
59. Wilson JE. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057, 2003.
60. Xiong ZQ and Stringer JL. Astrocytic regulation of the recovery of extracellular potassium after seizures in vivo. Eur J Neurosci 11: 1677-1684, 1999.
61. Zhang W, Segura BJ, Lin TR, Hu Y, and Mulholland MW. Intercellular calcium waves in cultured enteric glia from neonatal guinea pig. Glia 42: 252-262, 2003.