Mechanically Evoked Reflex Electrogenic Chloride Secretion in Rat Distal Colon Is Triggered by Endogenous Nucleotides Acting at P2Y1, P2Y2, and P2Y4 Receptors

Journal of Comparative Neurology

Volumn 469, Issue 1, 2004, Pages 16-36

  Christofi, Fievos L ^a,c   Wunderlich, Jacqueline ^a   Yu, Jun Ge ^a   Wang, Y Z ^a   Xue, Jianjing ^a   Guzman, Jorge ^a   Javed, Najma ^b   Cooke, Helen ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b BALL STATE UNIVERSITY   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

5 adenosine triphosphate; Chloride secretion; Enteric nervous system; Fluo 4 AM Ca2+ imaging; Mechanical activation; Mucosal reflex; Nucleotides; P2X, P2Y1, P2Y2, P2Y4, P2Y6, P2Y12, or P1 receptors; P2Y antisera; Submucous plexus

Indexed keywords

2 METHYLTHIOADENOSINE DIPHOSPHATE; 2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; CALCITONIN GENE RELATED PEPTIDE; CALCIUM ION; CALRETININ; CHLORIDE; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; NUCLEOTIDE DERIVATIVE; PURINE NUCLEOTIDE; PURINE P2 RECEPTOR; PURINE P2Y1 RECEPTOR; PURINE P2Y1 RECEPTOR ANTAGONIST; PURINE P2Y2 RECEPTOR; PURINE P2Y2 RECEPTOR AGONIST; PURINE P2Y4 RECEPTOR; PURINE P2Y4 RECEPTOR AGONIST; PURINERGIC RECEPTOR BLOCKING AGENT; PURINERGIC RECEPTOR STIMULATING AGENT; SOMATOSTATIN; TETRODOTOXIN; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRUSH BORDER; CHLORIDE TRANSPORT; COLON; CONTROLLED STUDY; DESCENDING COLON; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; IN VITRO STUDY; INTESTINE MUCOSA; MALE; METABOLISM; METHODOLOGY; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; REFLEX; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHORT CIRCUIT CURRENT; STIMULATION; WESTERN BLOTTING;

ANIMALS; CHLORIDES; COLON; DOSE-RESPONSE RELATIONSHIP, DRUG; INTESTINAL MUCOSA; MALE; PHYSICAL STIMULATION; PURINE NUCLEOTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; REFLEX;

EID: 0348047630     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10961     Document Type: Article

References (60)

1. Barajas-Lopez C, Espinosa-Luna R, Gerzanich V. 1994. ATP closes a potassium and opens a cationic conductance through different receptors in neurons of guinea pig submucous plexus. J Pharmacol Exp Ther 268:1397-1402.
2. 2+ by activation of P2 Rs in submucosal neurons in short-term cultures. Eur J Pharmacol 409:243-257.
3. Brookes SJ. 2001. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262:58-70.
4. Browning KN, Lees GM. 1994. Reappraisal of the innervation of rat intestine by vasoactive intestinal polypeptide and neuropeptide Y-immunoreactive neurons. Neuroscience 62:1257-1266.
5. Buchan AMJ. 1991 Neurofilament M and calbindin D28k are present in mutually exclusive subpopulations of enteric neurons in the rat submucous plexus. Brain Res 538:171-175.
6. Buchan AM, Baimbridge KG. 1988. Distribution and co-localization of calbindin D28k with VIP and neuropeptide Y but not somatostatin, galanin and substance P in the enteric nervous system of the rat. Peptides 9:333-338.
7. Burnstock G. 2000. P2X Rs in sensory neurons. Br J Anaesth 84:476-488.
8. Burnstock G. 2001. Purinergic signaling in gut. In: Abbracchio MP, Williams M, editors. Handbook of experimental pharmacology. Volume 151/II, Purinergic and pyrimidinergic signaling II, cardiovascular, respiratory, immune, metabolic and gastrointestinal tract function. New York: Springer-Verlag. p 141-238.
9. Christofi FL. 2001. Unlocking mysteries of gut sensory transmission: is adenosine the key? News Physiol Sci 16:201-207.
10. 2+ signaling in myenteric neurons via P2 purinoceptors. Am J Physiol 272:463-473.
11. Christofi FL, Zhang H, Yu JG, Guzman, J, Xue J, Kim M, Wang Y-Z, Cooke HJ. 2001. Differential gene expression of adenosine A1, A2a, A2b, and A3 Rs in the human enteric nervous system. J Comp Neurol 439:46-64.
12. 1 receptors suppresses secretory reflexes in the guinea pig colon. Am J Physiol Gastrointest Liver Physiol 276:G451-G462.
13. Cooke HJ, Wunderlich J, Christofi FL. 2003. "The force be with you": ATP in gut mechanosensory transduction. NIPS 19:43-49.
14. Costa M, Brookes SJH, Steele PA, Gibbins I, Burcher E, Kandiah CJ. 1996. Neurochemical classification of myenteric neurons in the guinea-pig ileum. Neuroscience 75:949-967.
15. Cuthbert AW, Hickman ME. 1985. Indirect effects of adenosine triphosphate on chloride secretion in mammalian colon. J Membr Biol 86:157-166.
16. Dho S, Stewart K, Foskett JK. 1992. Purinergic receptor activation of C1-secretion in T84 cells. Am J Physiol 262:C67-C74.
17. Ekblad E, Ekman R, Hakanson R, Sundler F. 1988. Projections of peptide-containing neurons in rat colon. Neuroscience 27:655-674.
18. Galligan JJ, Bertrand PP. 1994. ATP mediates fast synaptic potentials in enteric neurons. J Neurosci 14:7563-7571.
19. Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JFB, Kelly JS, Evans RM, Rosenfeld MG. 1984. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101-3111.
20. Glushakov AV, Melishchuk AI, Skok VI. 1996. ATP-induced currents in submucous plexus neurons of the guinea-pig small intestine. Neurophysiology (Moscow) 28:77-85.
21. Grygorczyk R, Hanrahan JW. 1997. CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. Am J Physiol 272: C1058-C1066.
22. Hazama A, Shimizu T, Ando-Akatsuka Y, Hayashi S, Tanaka S, Maeno E, Okada Y. 1999. Swelling-induced, CFTR-independent ATP release from a human epithelial cell line. J Gen Physiol 114:525-533.
23. Heinemann A, Shahbazian A, Barthó L, Holzer P. 1999. Different receptors mediating the inhibitory action of exogenous ATP and endogenously released purines on guinea-pig intestinal peristalsis. Br J Pharmacol 128:313-320.
24. Homolya L, Steinberg TH, Boucher RC. 2000. Cell to cell communication in response to mechanical stress via bilateral release of ATP and UTP in polarized epithelia. J Cell Biol 150:1349-1360.
25. Hu HZ, Gao N, Lin Z, Gao C, Liu S, Ren J, Xia Y, Wood JD. 2001. P2X (7) receptors in the enteric nervous system of guinea-pig small intestine. J Comp Neurol 440:299-310.
26. Keast JR, de Groat WC. 1989. Immunohistochemical characterization of the pelvic neurons which project to the bladder, colon, or penis in rats. J Comp Neurol 288:387-400.
27. - secretion via afferent neurons and 5-HT4 receptors. Am J Physiol 277:G515-G520.
28. + secretion via a P2Y2 receptor in rat distal colonic mucosa. Pflugers Arch 436:712-716.
29. Khahn BS, Burnstock G, Kennedy C, King BF, North RA, Seguela P, Voigt M, Humphrey PPA. 2001. International Union of Pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 53:107-118.
30. Kim M, Cooke HJ, Javed NH, Carey HV, Christofi F, Raybould HE. 2001. D-glucose releases 5-Hydroxytryptamine from human BON cells as a model of enterochromaffin cells. Gastroenterology 121:1400-1406.
31. 2+ signaling in cultured myenteric neurons via a PLC-dependent mechanism. Am J Physiol 270:G587-G593.
32. Kishore BK, Ginns SM, Krane CM, Neilsen S, Knepper MA. 2000. Cellular localization of P2Y(2) purinoceptors in rat renal inner medulla and lung. Am J Physiol Renal Physiol 278:F43-F51.
33. Knight GE, Bodin P, DeGroat WC, Burnstock G. 2002. ATP is released from guinea pig ureter epithelium on distension. Am J Physiol Renal Physiol 282:F281-F288.
34. Korman LY, Lemp GF, Jackson MJ, Gardner JD. 1982. Mechanism of action of ATP on intestinal epithelial cells. Cyclic AMP-mediated stimulation of active ion transport. Biochim Biophys Acta 721:47-54.
35. Kunze WAA, Furness JB. 1999. The enteric nervous system and regulation of intestinal motility. Annu Rev Physiol 6:117-142.
36. Kuwahara A, Bowen S, Wang J, Condon C, Cooke HJ 1987. Epithelial responses evoked by stimulant of submucosal neurons in guinea pig distal colon. Am J Physiol 252:G667-G674.
37. Lawarowski ER, Boucher RC. 2001. UTP as an extracellular signaling molecule. News Physiol Sci 16:1-5.
38. Lazarowski ER, Homolya L, Boucher RC, Harden TK. 1997. Direct demonstration of mechanically induced release of cellular UTP and its implication for uridine nucleotide receptor activation. Am Soc Biochem Mol Biol 272:24348-24354.
39. i and ion secretion via a basolateral P2Y-receptor in rat distal colonic mucosa. Pflugers Arch 434:77-83.
40. 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.
41. 28 and calretinin varies with cell type: assessment with the fluorescent dye BODIPY forskolin in enteric ganglia. Cell Tissue Res 293:57-73.
42. McAlroy HL, Collett A, Ahmed S, Ko WH, Baines DL, Wilson SM. 1999. Expression of multiple P2Y receptor subtypes by Caco-2 human colonic adenocarcinoma cells [abstract]. J Physiol 517:97P.
43. Moore BA, Vanner S. 1998. Organization of intrinsic cholinergic neurons projecting within submucosal plexus of guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 275:G490-G497.
44. Moore D, Chambers J, Waldvogel H, Faull R, Emson P. 2000. Regional and cellular distribution of the P2Y(1) purinergic receptor in the human brain: striking neuronal localization. J Comp Neurol 421:374-384.
45. Moran-Jimenez MJ, Matute C. 2000. Immunohistochemical localization of the P2Y(1) purinergic receptor in neurons and glial cells of the central nervous system. Brain Res Mol Brain Res 78:50-58.
46. Nakamura F, Strittmatter SM. 1996. P2Y1 purinergic receptors in sensory neurons: contribution to touch-induced impulse generation. Proc Natl Acad Sci USA 93:10465-10470.
47. 12 receptor: a novel member of the P2Y family of receptors activated by extracellular nucleotides. Mol Pharm 60:416-420.
48. Ostrom RS, Gregorian C, Insel PA. 2000. Cellular release of and response to ATP as key determinants of the set-point of signal transduction pathways. J Biol Chem 275:11735-11739.
49. Pan H, Gershon MD. 2000. Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J Neurosci 20:3295-3309.
50. Pintor J, Diaz-Hernandes M, Gualix J, Gomez-Villafuertes R, Hernando F, Miras-Portugal MT. 2000. Diadenosine polyphosphate receptors. From rat and guinea-pig brain to human nervous system. Pharmacol Ther 87:103-115.
51. Ralevic V, Burnstock G. 1998. Receptors for purines and pyrimidines. Pharmacol Rev 50:413-492.
52. Reese JH, Cooper JR. 1982. Modulation of the release of acetylcholine from ileal synaptosomes by adenosine and adenosine 5′-triphosphate. J Pharmacol Exp Ther 223:612-616.
53. Roman RM, Fitz JG. 1999. Emerging roles of purinergic signaling in gastrointestinal epithelial secretion and hepatobiliary function. Gastroenterology 116:964-979.
54. Sidhu M, Cooke HJ. 1995. Role for 5-HT and ACh in submucosal reflexes mediating colonic secretion. Am J Physiol 269:G346-G351.
55. Song ZM, Costa M, Brookes SJ. 1998. Projections of submucous neurons to the myenteric plexus in the guinea pig small intestine. J Comp Neurol 399:255-268.
56. Spencer NJ, Walsh M, Smith TK. 2000. Purinergic and cholinergic neuroneuronal transmission underlying reflexes activated by mucosal stimulation in the isolated guinea-pig ileum. J Physiol 522:321-331.
57. von Kugelgen I, Wetter A. 2000. Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch Pharmacol 362:310-323.
58. Weber E, Neunlist M, Schemann M, Frieling T. 2001. Neural components of distension-evoked secretory responses in the guinea-pig distal colon. J Physiol 536:741-751.
59. Weisenfeld-Hallen A, Hokfelf T, Lundberg JM, Forssmann WG, Reinecke M, Tschopp FA, Fischer JA. 1984. Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioural responses of the rat. Neurosci Lett 52:199-204.
60. Windscheif U. 1996. Purinoceptors: from history to recent progress. A review. J Pharm Pharmacol 48:993-1011.