Purinergic component of mechanosensory transduction is increased in a rat model of colitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 287, Issue 3 50-3, 2004, Pages

  Wynn, Gregory ^a   Ma, Bei ^a   Ruan, Huai Zhen ^a   Burnstock, Geoffrey ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

ATP; Dorsal root ganglia; Inflammation

Indexed keywords

2',3' O TRINITROPHENYL ADENOSINE TRIPHOSPHATE; ADENOSINE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; CALCITONIN GENE RELATED PEPTIDE; PURINE P2 RECEPTOR; PURINE RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; PYRIDOXYL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; COLON; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; FEMALE; MALE; MECHANOSENSORY TRANSDUCTION; NONHUMAN; PELVIC NERVE; PRIORITY JOURNAL; RAT; RECTUM; SIGNAL TRANSDUCTION; SPINAL GANGLION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; COLITIS; COLON; ELECTROPHYSIOLOGY; FEMALE; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MALE; MECHANOTRANSDUCTION, CELLULAR; PATCH-CLAMP TECHNIQUES; PELVIS; PHYSICAL STIMULATION; PRESSURE; PYRIDOXAL PHOSPHATE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC; RECEPTORS, PURINERGIC P2; RECTUM;

EID: 4143090377     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00020.2004     Document Type: Article

References (61)

1. Ardizzone S, Bollani S, Manzionna G, and Bianchi Porro G. Inflammatory bowel disease approaching the 3rd millennium: pathogenesis and therapeutic implications? Eur J Gastroenterol Hepatol 11: 27-32, 1999.
2. Ardizzone S and Porro GB. Inflammatory bowel disease: new insights into pathogenesis and treatment. J Intern Med 252: 475-496, 2002.
3. Barbara G, De Giorgio R, Stanghellini V, Cremon C, and Corinaldesi R. A role for inflammation in irritable bowel syndrome? Gut 51 Suppl I: 141-144, 2002.
4. Bjorck S, Dahlstrom A, Johansson L, and Ahlman H. Treatment of the mucosa with local anaesthetics in ulcerative colitis. Agents Actions C60-C72, 1992.
5. Bodin P and Burnstock G. Increased release of ATP from endothelial cells during acute inflammation. Inflamm Res 47: 351-354, 1998.
6. Bodin P and Burnstock G. Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J Cardiovasc Pharmacol 38: 900-908, 2001.
7. 3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 12: 256-268, 1998.
8. Bueno L and Fioramonti J. Visceral perception: inflammatory and non-inflammatory mediators. Gut 51, Suppl I: I19-I23, 2002.
9. Burnstock G. Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduction. J Anat 194: 335-342, 1999.
10. Burnstock G. P2X receptors in sensory neurones. Br J Anaesth 84: 476-488, 2000.
11. Burnstock G. Purine-mediated signalling in pain and visceral perception. Trends Pharmacol Sci 22: 182-188, 2001.
12. Burnstock G. Potential therapeutic targets in the rapidly expanding field of purinergic signalling. Clin Med 2: 45-53, 2002.
13. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, and Wood JN. A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377: 428-431, 1995.
14. Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB, and Ford AP. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 407: 1011-1015, 2000.
15. Cohen RD and Hanauer SB. Nicotine in ulcerative colitis. How does it work and how can we use it? Clin Immunother 5: 169-174, 1996.
16. Collins SM. The immunomodulation of enteric neuromuscular function: implications for motility and inflammatory disorders. Gastroenterology 111: 1683-1699, 1996.
17. De Giorgio R, Barbara G, Blennerhassett P, Wang L, Stanghellini V, Corinaldesi R, Collins SM, and Tougas G. Intestinal inflammation and activation of sensory nerve pathways: a functional and morphological study in the nematode-infected rat. Gut 49: 822-827, 2001.
18. Dray A. Inflammatory mediators of pain. Br J Anaesth 75: 125-131, 1995.
19. Driessen B, Reimann W, Selve N, Friderichs E, and Bultmann R. Antinociceptive effect of intrathecally administered P2-purinoceptor antagonists in rats. Brain Res 666: 182-188, 1994.
20. Ferguson DR, Kennedy I, and Burton TJ. ATP is released from rabbit urinary bladder epithelial cells by hydrostatic pressure changes - a possible sensory mechanism? J Physiol 505: 503-511, 1997.
21. Grundy D. Neuroanatomy of visceral nociception: vagal and splanchnic afferents. Gut 51, Suppl I: I2-I5, 2002.
22. Hamilton SG, McMahon SB, and Lewin GR. Selective activation of nociceptors by P2X receptor agonists in normal and inflamed rat skin. J Physiol 534: 437-445, 2001.
23. Hamilton SG, Wade A, and McMahon SB. The effects of inflammation and inflammatory mediators on nociceptive behaviour induced by ATP analogues in the rat. Br J Pharmacol 126: 326-332, 1999.
24. Hamilton SG, Warburton J, Bhattacharjee A, Ward J, and McMahon SB. ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain 123: 1238-1246, 2000.
25. Hannington-Kiff JG. Intravenous regional sympathetic block with guanethidine. Lancet 1: 1019-1020, 1974.
26. 3 receptors. J Physiol 544: 861-869, 2002.
27. Jacobson K, McHugh K, and Collins SM. Experimental colitis alters myenteric nerve function at inflamed and noninflamed sites in the rat. Gastroenterology 109: 718-722, 1995.
28. Jacobson K, McHugh K, and Collins SM. The mechanism of altered neural function in a rat model of acute colitis. Gastroenterology 112: 156-162, 1997.
29. 3 allosteric modulator, cibacron blue. Br J Pharmacol 132: 259-269, 2001.
30. 3 receptor expression and function following spinal nerve ligation in the rat. Exp Brain Res 147: 511-519, 2002.
31. 2 purinoceptor to ATP revealed by changing extracellular pH. Br J Pharmacol 117: 1371-1373, 1996.
32. Kirkup AJ, Booth CE, Chessell IP, Humphrey PP, and Grundy D. Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat. J Physiol 520: 551-563, 1999.
33. Knight GE, Bodin P, De Groat WC, and Burnstock G. ATP is released from guinea pig ureter epithelium on distension. Am J Physiol Renal Physiol 282: F281-F288, 2002.
34. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377: 432-435, 1995.
35. Madara JL. Loosening tight junctions. Lessons from the intestine. J Clin Invest 83: 1089-1094, 1989.
36. Mazelin L, Theodorou V, More J, Fioramonti J, and Bueno L. Protective role of vagal afferents in experimentally-induced colitis in rats. J Auton Nerv Syst 73: 38-45, 1998.
37. McCafferty DM, Wallace JL, and Sharkey KA. Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat. Am J Physiol Gastrointest Liver Physiol 272: G272-G280, 1997.
38. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 96: 795-803, 1989.
39. 3 purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain 80: 273-282, 1999.
40. Olivar T, Cervero F, and Laird JM. Responses of rat spinal neurones to natural and electrical stimulation of colonic afferents: effect of inflammation. Brain Res 866: 168-177, 2000.
41. Page AJ, O'Donnell TA, and Blackshaw LA. P2X purinoceptor-induced sensitisation of ferret vagal mechanoreceptors in oesophageal inflammation. J Physiol 523: 403-411, 2000.
42. Palmer JM, Wong-Riley M, and Sharkey KA. Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. Am J Physiol Gastrointest Liver Physiol 275: G922-G935, 1998.
43. 3 subunit. J Biol Chem 276: 21077-21082, 2001.
44. Reinshagen M, Flamig G, Ernst S, Geerling I, Wong H, Walsh JH, Eysselein VE, and Adler G. Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury. J Pharmacol Exp Ther 286: 657-661, 1998.
45. Rodriguez LA and Ruigomez A. Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. Br Med J 318: 565-566, 1999.
46. Rong W, Spyer KM, and Burnstock G. Activation and sensitisation of low- and high-threshold afferent fibres mediated by P2X receptors in the mouse urinary bladder. J Physiol 541: 591-600, 2002.
47. 2 co-released from the mouse colon: a new model to study nociceptive and inflammatory responses in viscera, in vitro. Pain 93: 213-219, 2001.
48. 4 receptors in dorsal root, nodose and trigeminal ganglia of the rat. Histochem Cell Biol 120: 415-426, 2003.
49. Sharkey KA and Kroese AB. Consequences of intestinal inflammation on the enteric nervous system: neuronal activation induced by inflammatory mediators. Anat Rec 262: 79-90, 2001.
50. 3 receptors. Nature 407: 1015-1017, 2000.
51. Stead RH, Rosecka-Janiszewska U, Oestreicher AB, Dixon MF, and Bienenstock J. Remodeling of B-50 (GAP-43)-and NSE-immunoreactive mucosal nerves in the intestines of rats infected with Nippostrongylus brasiliensis. J Neurosci 11: 3809-3821, 1991.
52. Sun Y, Keay S, DeDeyne PG, and Chai TC. Augmented stretch activated adenosine triphosphate release from bladder urothelial cells in patients with interstitial cystitis. J Urol 166: 1951-1956, 2001.
53. Tsuda M, Koizumi S, and Inoue K. Role of endogenous ATP at the incision area in a rat model of postoperative pain. Neuroreport 12: 1701-1704, 2001.
54. Tsuda M, Ueno S, and Inoue K. Evidence for the involvement of spinal endogenous ATP and P2X receptors in nociceptive responses caused by formalin and capsaicin in mice. Br J Pharmacol 128: 1497-1504, 1999.
55. 3 mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain 91: 351-360, 2001.
56. 3 knock-out mice reveal a major sensory role for urothelially released ATP. J Neurosci 21: 5670-5677, 2001.
57. 3 is expressed by DRG neurons that terminate in inner lamina. II. Eur J Neurosci 10: 3470-3478, 1998.
58. Wynn G, Rong W, Xiang Z, and Burnstock G. Purinergic mechanisms contribute to mechanosensory transduction in the rat colorectum. Gastroenterology 125: 1398-1409, 2003.
59. Xu GY and Huang LY. Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. J Neurosci 22: 93-102, 2002.
60. 3 is increased in human inflammatory bowel disease. Neurogastroenterol Motil 13: 365-369, 2001.
61. 3-deficient mice. Eur J Neurosci 14: 1784-1792, 2001.