Modulation of the activity of two pacemakers by transmural nerve stimulation in circular smooth muscle preparations isolated from the rat proximal colon

Journal of Smooth Muscle Research

Volumn 45, Issue 6, 2010, Pages 249-268

  Kato, Takashi ^a   Nakamura, Eri ^a   Imaeda, Kenro ^a   Suzuki, Hikaru ^a  

^a NAGOYA CITY UNIV MEDICAL SCHOOL   (Japan)

Author keywords

Enteric nerves; P region; Pacemaker cells; Phasic contraction; Proximal colon

Indexed keywords

AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; APAMIN; ATROPINE; CAPSAICIN; CHOLINERGIC RECEPTOR BLOCKING AGENT; ENZYME INHIBITOR; N(G) NITROARGININE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; SURAMIN;

ANIMAL; ARTICLE; BIOLOGICAL RHYTHM; COLON; DRUG EFFECT; ELECTROSTIMULATION; INNERVATION; MALE; MUSCLE CONTRACTION; MYENTERIC PLEXUS; NERVE CELL INHIBITION; PHYSIOLOGY; RAT; SMOOTH MUSCLE; WISTAR RAT;

ANIMALS; APAMIN; ATROPINE; BIOLOGICAL CLOCKS; CAPSAICIN; COLON; ELECTRIC STIMULATION; ENZYME INHIBITORS; MALE; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYENTERIC PLEXUS; NEURAL INHIBITION; NITRIC OXIDE DONORS; NITROARGININE; NITROPRUSSIDE; PARASYMPATHOLYTICS; RATS; RATS, WISTAR; SENSORY SYSTEM AGENTS; SURAMIN;

EID: 77949335169     PISSN: 09168737     EISSN: None     Source Type: Journal    
DOI: 10.1540/jsmr.45.249     Document Type: Article

References (44)

1. Dalziel, H.H., Thornbury, K.D., Ward, S.M. and Sanders, K.M. (1991). Involvement of nitric oxide synthetic pathway in inhibitory junction potentials in canine proximal colon. Am. J. Physiol. 261: G789-G792.
2. Dunn, P.M. and Blakeley, A.G.H. (1988). Suramin, a reversible P2-purinoceptor antagonist in the mouse vas deferens. Br. J. Pharmacol. 93: 243-247.
3. Hata, F., Takeuchi, S.T., Nishio, H. and Fujita, A. (2000). Mediators and intracellular mechanisms of NANC relaxation of smooth muscle in the gastrointestinal tract. J. Smooth Muscle Res. 36: 181-204.
4. Hirst, G.D.S. and Ward, S.M. (2003). Interstitial cells: involvement in rhythmicity and neural control of gut smooth muscle. J. Physiol. (Lond.) 550: 337-346.
5. Horiguchi, K., Sanders, K.M. and Ward, S.M. (2003). Enteric motor neurons form synaptic-like junctions with interstitial cells of Cajal in the canine gastric antrum. Cell Tissue Res. 311: 299-313.
6. Hoyle, C.H.V. and Burnstock, G. (1989). Neuromuscular transmission in the gastrointestinal tract. Handbook of Physiology Section 6, The Gastrointestinal System, Vol. 1, Part 1. Am. Physiol. Society, Bethesda, Maryland, USA, pp. 435-464.
7. Huizinga, J.D., Thuneberg, L., Vanderwinden, J.M. and Rumessen, J. (1997). Interstitial cells of Cajal as targets for pharmacological intervention in gastrointestinal motor disorders. Trends Pharmacol. Sci. 8: 393-403.
8. Hukuhara, T. and Neya, T. (1968). The movements of the colon of rats and guinea pigs. Jpn. J. Physiol. 18: 551-562.
9. Kato, T., Imaeda, K., Nakamura, E. and Suzuki, H. (2009). Modulation of phasic contractions by nerve stimulation in circular smooth muscle tissues isolated from the rat proximal colon. Nippon Heikatsukin Gakkaizassi 13: J-25 (in Japanese).
10. Keef, K.D., Anderson, U., O'Driscoll, K., Ward, S.M. and Sanders, K.M. (2002). Electrical activity induced by nitric oxide in canine colonic circular muscle. Am. J. Physiol. 282: G123-G129.
11. Kobayashi, S., Torihashi, S., Iino, S., Pang, Y.W., Chowdhury, J.U. and Tomita, T. (1995). The inner sublayer of the circular muscle coat in the canine proximal colon: origins of spontaneous electrical and mechanical activity. Arch. Histol. Cytol. 58: 45-63.
12. Kobayashi, S., Chowdhury, J.U., Tokuno, H., Nahar, N.S. and Iino, S. (1996). A smooth muscle nodule producing 10-12 cycle/min regular contractions at the mesenteric border of the pacemaker area in the guinea-pig colon. Arch. Histol. Cytol. 59: 159-168.
13. Komori, K. and Suzuki, H. (1986). Distribution and properties of excitatory and inhibitory junction potentials in circular muscle of the guinea-pig stomach. J. Physiol. (Lond.) 370: 339-355.
14. Komuro, T., Seki, K. and Horiguchi, K. (1999). Ultrastructural characterization of the interstitial cells of Cajal. Arch. Histol. Cytol. 62: 295-316.
15. Lentle, R.G. and Janssen, P.W. (2008). Physical characteristics of digesta and their influence on flow and mixing in the mammalian intestine: a review. J. Comp. Physiol. B. 178: 673-690.
16. Lyster, D.J., Bywater, R.A.R., Taylor, G.S. and Watson, M.J. (1992). Effects of a nitric oxide synthase inhibitor on non-cholinergic junction potentials in the circular muscle of the guinea pig ileum. J. Auton. Nerv. Syst. 41: 187-196.
17. Lyster, D.J., Bywater, R.A. and Taylor, G.S. (1995). Neurogenic control of myoelectric complexes in the mouse isolated colon. Gastroenterol. 108: 1371-1378.
18. McDonnell, B., Hamilton, R., Fong, M., Ward, S.M. and Keef, K.D. (2008). Functional evidence for purinergic inhibitory neuromuscular transmission in the mouse internal anal sphincter. Am. J. Physiol. 294: G1041-G1051.
19. Nahar, N.S., Chowdhury, J.U., Tokuno, H., Tomita, T., Torihashi, S., Iino, S. and Kobayashi, S. (1996). Nitrinergic nerves controlling pacemaker activities of the inner sublayer (P-layer) in the canine proximal colon circular muscles. Arch. Histol. Cytol. 59: 37-46.
20. Nahar, N.S., Torihashi, S., Iino, S., Senda, T., Chowdhury, J.U. and Kobayashi, S. (1998). Special smooth muscle cells along the submucosal surface of the guinea pig colon with reference to its spontaneous contractions. Cell Tissue Res. 293: 143-154.
21. Nakamura, K. and Shibata, Y. (1999). Connexin 43 expression in network-forming cells at the submucosal-muscular border of guinea pig and dog colon. Cells Tissues Organs 165: 16-21.
22. Ohno, N., Ito, K.M., Yamamoto, Y. and Suzuki, H. (1993). Suramin selectively inhibits the nonadrenergic non-cholinergic inhibitory junction potential in the guinea-pig stomach. Eur. J. Pharmacol. 249: 121-123.
23. Ohno, N., Xue, L., Yamamoto, Y. and Suzuki, H. (1996). Properties of inhibitory junction potential in smooth muscle of the guinea-pig gastric fundus. Br. J. Pharmacol. 117: 974-978.
24. Plujà, L., Fernández, E. and Jiménez, M. (1999). Neural modulation of the cyclic electrical and mechanical activity in the rat colonic circular muscle: putative role of ATP and NO. Br. J. Pharmacol. 126: 883-892.
25. Plujà, L., Alberti, E., Fernández, E., Mikkelsen, H.B., Thuneberg, L. and Jiménez, M. (2001). Evidence supporting presence of two pacemakers in rat colon. Am. J. Physiol. 281: G255-G266.
26. Rae, M.G. and Muir, T.C. (1996). Neuronal mediators of inhibitory junction potentials and relaxation in the guinea-pig internal anal sphincter. J. Physiol. (Lond.) 493: 517-527.
27. Sanders, K.M. (1996). A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterol. 111: 492-515.
28. Sanders, K.M., Ördog, T., Koh, S.D., Torihashi, S. and Ward, S.M. (1999). Development and plasticity of interstitial cells of Cajal. Neurogastroenterol. Motil. 11: 311-338.
29. Shuba, M.F. and Vladimirova, I.A. (1980). Effect of apamin on the electrical responses of smooth muscle to adenosine 5'-triphosphate and to non-adrenergic, non-cholinergic nerve stimulation. Neurosci. 5: 853-859.
30. Smith, T.K., Reed, J.B. and Sanders, K.M. (1987a). Origin and propagation of electrical slow waves in circular muscle of canine proximal colon. Am. J. Physiol. 252: C215-C224.
31. Smith, T.K., Reed, J.B. and Sanders, K.M. (1987b). Interaction of two electrical pacemakers in muscularis of canine proximal colon. Am. J. Physiol. 252: C290-C299.
32. Smith, T.K., Reed, J.B. and Sanders, K.M. (1989). Electrical pacemakers of canine proximal colon are functionally innervated by inhibitory motor neurons. Am. J. Physiol. 256: C466-C477.
33. Suzuki, H., Kito, Y., Hashitani, H. and Nakamura, E. (2006). Factors modifying the frequency of spontaneous activity in gastric muscle. J. Physiol. (Lond.) 576: 667-694.
34. Tanaka, C., Domae, K., Hashitani, H. and Suzuki, H. (2009). Modulation of slow waves by transmural nerve stimulation of smooth muscle tissue isolated from the corpus of the guinea-pig stomach. J. Smooth Muscle Res. 45: 109-124.
35. Tomita, T. (1981). Electrical activity (spikes and slow wave) in gastrointestinal smooth muscles. In: Smooth Muscle, ed. by E. Bülbring, A.F. Brading, A.W. Jones and T. Tomita, Edward Arnold, London, pp. 127-156.
36. Ward, S.M., Beckett, E.A., Wang, X., Baker, F., Khoyi, M. and Sanders, K.M. (2000). Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J. Neurosci. 20: 1393-1403.
37. Ward, S.M., Burns, A.J., Torihashi, S. and Sanders, K.M. (1994). Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J. Physiol. (Lond.) 480: 91-97.
38. Ward, S.M. and Sanders, K.M. (2001). Interstitial cells of Cajal: primary targets of enteric motor innervation. Anat. Rec. 262: 125-135.
39. Xue, L., Farrugia, G., Sarr, M.G. and Szurszewski, J.H. (1999). ATP is a mediator of the fast inhibitory junction potential in human jejunal circular smooth muscle. Am. J. Physiol. 276: G1373-G1379.
40. Xue, L., Fukuta, H., Yamamoto, Y. and Suzuki, H. (1996). Properties of junction potentials in gastric smooth muscle of the rat. Jpn. J. Physiol. 46: 123-130.
41. Xue, L., Imaeda, K., Yamamoto, Y. and Suzuki, H. (1998). Effects of suramin on electrical and mechanical activities of antrum smooth muscle of the guinea-pig stomach. J. Autonom. Pharmacol. 18: 325-331.
42. Yoneda, S., Fukui, H. and Takaki, M. (2004). Pacemaker activity from submucosal interstitial cells of Cajal derives high-frequency and low-amplitude circular muscle contractions in the mouse proximal colon. Neurogastroenterol. Motil. 16: 621-627.
43. Yoneda, S., Takano, H., Takaki, M. and Suzuki, H. (2002). Properties of spontaneously active cells distributed in submucosal layer of the mouse proximal colon. J. Physiol. (Lond.) 542: 887-897.
44. Zizzo, M.G., Mule, F. and Serio, R. (2007). Inhibitory purinergic transmission in mouse caecum: role for P2Y1 receptors as prejunctional modulators of ATP release. Neuroscience 150: 658-664.