Nitric oxide and carbon monoxide act as inhibitory neurotransmitters in the longitudinal muscle of C57BL/6J mouse distal colon

Journal of Pharmacological Sciences

Volumn 112, Issue 2, 2010, Pages 231-241

  Hidaka, Ayako ^a   Azuma, Yasu Taka ^a   Nakajima, Hidemitsu ^a   Takeuchi, Tadayoshi ^a  

^a Osaka Prefecture University   (Japan)

Author keywords

Carbon oxide (CO); Cyclic guanosine 3 ,5 monophosphate (cyclic GMP) dependent protein kinase; Mouse distal colon; Nitric oxide (NO); Nonadrenergic noncholinergic (NANC) relaxation

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 4 METHYL 2 [HYDROXYIMINO] 5 NITRO 6 METHOXY 3 HEXENAMIDE; ATROPINE; CARBON MONOXIDE; CARBON MONOXIDE RELEASING MOLECULE 2; CYCLIC GMP; GUANETHIDINE; GUANYLATE CYCLASE; KT 5823; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; N(G) NITROARGININE; NEUROTRANSMITTER; NITRIC OXIDE; NITRIC OXIDE DONOR; ORGANONITROGEN DERIVATIVE; PROTOPORPHYRIN TIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DESCENDING COLON; ELECTROSTIMULATION; ENZYME ACTIVATION; MALE; MOUSE; MUSCLE EXCITATION; MUSCLE RELAXATION; NONHUMAN; RADIOIMMUNOASSAY; SMOOTH MUSCLE;

EID: 77249170899     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.09242FP     Document Type: Article

References (44)

1. Lecci A, Santicioli P, Maggi CA. Pharmacology of transmission to gastrointestinal muscle. Curr Opin Pharmacol. 2002;2: 630-641.
2. Hata F, Takeuchi T, Nishio H, Fujita A. Mediators and intracellular mechanisms of NANC relaxation of smooth muscle in the gastrointestinal tract. J Smooth Muscle Res. 2000;36:181-204.
3. Angel F, Go VL, Schmalz PF, Szurszewski JH. Vasoactive intestinal polypeptide: a putative transmitter in the canine gastric muscularis mucosa. J Physiol. 1983;341:641-654.
4. Cayabyab FS, Jimenez M, Vergara P, deBruin H, Daniel EE. Influence of nitric oxide and vasoactive intestinal peptide on the spontaneous and triggered electrical and mechanical activities of the canine ileum. Can J Physiol Pharmacol. 1997;75:383-397.
5. Okamura T, Tanobe Y, Fujioka H, Ayajiki K, Toda N. Mechanism of neurogenic relaxation and modification of the response by enteric substances in isolated dog colon. Eur J Pharmacol. 1998;358:245-252.
6. Baccari MC, Iacoviello C, Calamai F. Nitric oxide as modulator of cholinergic neurotransmission in gastric muscle of rabbits. Am J Physiol. 1997;273:G456-G463.
7. Ciccocioppo R, Onori L, Messori E, Candura SM, Coccini T, Tonini M. Role of nitric oxide-dependent and -independent mechanisms in peristalsis and accommodation in the rabbit distal colon. J Pharmacol Exp Ther. 1994;270:929-937.
8. Katsoulis S, Schmidt WE, Schwarzhoff R, Folsch UR, Jin JG, Grider JR, et al. Inhibitory transmission in guinea pig stomach mediated by distinct receptors for pituitary adenylate cyclase-activating peptide. J Pharmacol Exp Ther. 1996;278:199-204.
9. Gallego D, Vanden Berghe P, Farre R, Tack J, Jimenez M. P2Y1 receptors mediate inhibitory neuromuscular transmission and enteric neuronal activation in small intestine. Neurogastroenterol Motil. 2008;20:159-168.
10. Jin JG, Katsoulis S, Schmidt WE, Grider JR. Inhibitory transmission in tenia coli mediated by distinct vasoactive intestinal peptide and apamin-sensitive pituitary adenylate cyclase activating peptide receptors. J Pharmacol Exp Ther. 1994;270:433-439.
11. Curro D, De Marco T, Preziosi P. Involvement of peptide histidine isoleucine in non-adrenergic non-cholinergic relaxation of the rat gastric fundus induced by high-frequency neuronal firing. Naunyn Schmiedebergs Arch Pharmacol. 2002;366:578-586.
12. Waseda K, Takeuchi T, Ohta M, Okishio Y, Fujita A, Hata F, et al. Participation of ATP in nonadrenergic, noncholinergic relaxation of longitudinal muscle of wistar rat jejunum. J Pharmacol Sci. 2005;97:91-100.
13. Takeuchi T, Niioka S, Yamaji M, Okishio Y, Ishii T, Nishio H, et al. Decrease in participation of nitric oxide in nonadrenergic, noncholinergic relaxation of rat intestine with age. Jpn J Pharmacol. 1998;78:293-302.
14. Kishi M, Takeuchi T, Suthamnatpong N, Ishii T, Nishio H, Hata F, et al. VIP- and PACAP-mediated nonadrenergic, noncholinergic inhibition in longitudinal muscle of rat distal colon: involvement of activation of charybdotoxin- and apamin-sensitive K+ channels. Br J Pharmacol. 1996;119:623-630.
15. Van Geldre LA, Lefebvre RA. Interaction of NO and VIP in gastrointestinal smooth muscle relaxation. Curr Pharm Des. 2004;10:2483-2497.
16. Vetri T, Bonvissuto F, Marino A, Postorino A. Nitrergic and purinergic interplay in inhibitory transmission in rat gastric fundus. Auton Autacoid Pharmacol. 2007;27:151-157.
17. El-Yazbi AF, Schulz R, Daniel EE. Differential inhibitory control of circular and longitudinal smooth muscle layers of Balb/C mouse small intestine. Auton Neurosci. 2007;131:36-44.
18. Serio R, Zizzo MG, Mule F. Nitric oxide induces muscular relaxation via cyclic GMP-dependent and -independent mechanisms in the longitudinal muscle of the mouse duodenum. Nitric Oxide. 2003;8:48-52.
19. De Man JG, De Winter BY, Herman AG, Pelckmans PA. Study on the cyclic GMP-dependency of relaxations to endogenous and exogenous nitric oxide in the mouse gastrointestinal tract. Br J Pharmacol. 2007;150:88-96.
20. El-Yazbi AF, Cho WJ, Boddy G, Daniel EE. Caveolin-1 gene knockout impairs nitrergic function in mouse small intestine. Br J Pharmacol. 2005;145:1017-1026.
21. Satoh Y, Takeuchi T, Yamazaki Y, Okishio Y, Nishio H, Takatsuji K, et al. Mediators of nonadrenergic, noncholinergic relaxation in longitudinal muscle of the intestine of ICR mice. J Smooth Muscle Res. 1999;35:65-75.
22. Young HM, Ciampoli D, Johnson PJ, Stebbing MJ. Inhibitory transmission to the longitudinal muscle of the mouse caecum is mediated largely by nitric oxide acting via soluble guanylyl cyclase. J Auton Nerv Syst. 1996;61:103-108.
23. Zakhary R, Poss KD, Jaffrey SR, Ferris CD, Tonegawa S, Snyder SH. Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide. Proc Natl Acad Sci U S A. 1997;94:14848-14853.
24. Gibbons SJ, Farrugia G. The role of carbon monoxide in the gastrointestinal tract. J Physiol. 2004;556:325-336.
25. De Backer O, Lefebvre RA. Mechanisms of relaxation by carbon monoxide-releasing molecule-2 in murine gastric fundus and jejunum. Eur J Pharmacol. 2007;572:197-206.
26. Toda N, Herman AG. Gastrointestinal function regulation by nitrergic efferent nerves. Pharmacol Rev. 2005;57:315-338.
27. Satoh Y, Okishio Y, Azuma YT, Nakajima H, Hata F, Takeuchi T. Orexin A affects ascending contraction depending on downstream cholinergic neurons and descending relaxation through independent pathways in mouse jejunum. Neuropharmacology. 2006;51:466-473.
28. Hagi K, Azuma YT, Nakajima H, Shintani N, Hashimoto H, Baba A, et al. Involvements of PHI-nitric oxide and PACAP-BK channel in the sustained relaxation of mouse gastric fundus. Eur J Pharmacol. 2008;590:80-86.
29. Algara-Suarez P, Espinosa-Tanguma R. 8Br-cGMP mediates relaxation of tracheal smooth muscle through PKA. Biochem Biophys Res Commun. 2004;314:597-601.
30. Okishio Y, Niioka S, Yamaji M, Yamazaki Y, Nishio H, Takeuchi T, et al. Mediators of nonadrenergic, noncholinergic relaxation in Sprague Dawley rat intestine: comparison with the mediators of other strains. J Vet Med Sci. 2000;62:821-828.
31. Vannucchi MG, Corsani L, Bani D, Faussone-Pellegrini MS. Myenteric neurons and interstitial cells of Cajal of mouse colon express several nitric oxide synthase isoforms. Neurosci Lett. 2002;326:191-195.
32. Xue L, Farrugia G, Miller SM, Ferris CD, Snyder SH, Szurszewski JH. Carbon monoxide and nitric oxide as coneurotransmitters in the enteric nervous system: evidence from genomic deletion of biosynthetic enzymes. Proc Natl Acad Sci U S A. 2000;97:1851-1855.
33. Dulak J, Jozkowicz A. Carbon monoxide - a "new" gaseous modulator of gene expression. Acta Biochim Pol. 2003;50: 31-47.
34. Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev. 2005;57:585-630.
35. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, et al. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev. 2000;52:375-414.
36. Murthy KS. Signaling for contraction and relaxation in smooth muscle of the gut. Annu Rev Physiol. 2006;68:345-374.
37. Podda MV, Marcocci ME, Oggiano L, D'Ascenzo M, Tolu E, Palamara AT, et al. Nitric oxide increases the spontaneous firing rate of rat medial vestibular nucleus neurons in vitro via a cyclic GMP-mediated PKG-independent mechanism. Eur J Neurosci. 2004;20:2124-2132.
38. Sequeira SM, Carvalho AP, Carvalho CM. Both protein kinase G dependent and independent mechanisms are involved in the modulation of glutamate release by nitric oxide in rat hippocampal nerve terminals. Neurosci Lett. 1999;261:29-32.
39. Waniishi Y, Inoue R, Morita H, Teramoto N, Abe K, Ito Y. Cyclic GMP-dependent but G-kinase-independent inhibition of Ca2+-dependent Cl- currents by NO donors in cat tracheal smooth muscle. J Physiol. 1998;511:719-731.
40. Ward SM, Sanders KM, Hirst GD. Role of interstitial cells of Cajal in neural control of gastrointestinal smooth muscles. Neurogastroenterol Motil. 2004;16 Suppl 1:112-117.
41. Iino S, Horiguchi K, Nojyo Y. Interstitial cells of Cajal are innervated by nitrergic nerves and express nitric oxide-sensitive guanylate cyclase in the guinea-pig gastrointestinal tract. Neuroscience. 2008;152:437-448.
42. Giaroni C, Knight GE, Ruan HZ, Glass R, Bardini M, Lecchini S, et al. P2 receptors in the murine gastrointestinal tract. Neuropharmacology. 2002;43:1313-1323.
43. Zizzo MG, Mule F, Serio R. Evidence that ATP or a related purine is an excitatory neurotransmitter in the longitudinal muscle of mouse distal colon. Br J Pharmacol. 2007;151:73-81.
44. Zizzo MG, Mule F, Serio R. Mechanisms underlying hyperpolarization evoked by P2Y receptor activation in mouse distal colon. Eur J Pharmacol. 2006;544:174-180.