Nitrergic signalling via interstitial cells of Cajal regulates motor activity in murine colon

Journal of Physiology

Volumn 593, Issue 20, 2015, Pages 4589-4601

  Lies, Barbara ^a   Beck, Katharina ^a   Keppler, Jonas ^a   Saur, Dieter ^b   Groneberg, Dieter ^a   Friebe, Andreas ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANYLATE CYCLASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; TETRODOTOXIN; CELL RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLON; COLON MOTILITY; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME ACTIVITY; ENZYME RELEASE; EX VIVO STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; INTESTINE CONTRACTION; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; MALE; MOUSE; NERVE BLOCK; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; WILD TYPE; ANIMAL; C57BL MOUSE; GENETICS; MUSCLE CONTRACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; SMOOTH MUSCLE CELL;

ANIMALS; COLON; GUANYLATE CYCLASE; INTERSTITIAL CELLS OF CAJAL; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; SOLUBLE GUANYLYL CYCLASE;

EID: 84944276144     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270511     Document Type: Article

References (31)

1. Boeckxstaens GE, Hirsch DP, Kodde A, Moojen TM, Blackshaw A, Tytgat GN & Blommaart PJ (1999). Activation of an adrenergic and vagally-mediated NANC pathway in surgery-induced fundic relaxation in the rat. Neurogastroenterol Motil 11, 467-474.
2. Boeckxstaens GE, Pelckmans PA, Bult H, DeMan JG, Herman AG & Van Maercke YM (1990). Non-adrenergic non-cholinergic relaxation mediated by nitric oxide in the canine ileocolonic junction. Eur J Pharmacol 190, 239-246.
3. Burns AJ, Lomax AE, Torihashi S, Sanders KM & Ward SM (1996). Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci USA 93, 12008-12013.
4. Costa M, Dodds KN, Wiklendt L, Spencer NJ, Brookes SJ & Dinning PG (2013). Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat. Am J Physiol Gastrointest Liver Physiol 305, G749-G759.
5. Cousins HM, Edwards FR, Hickey H, Hill CE & Hirst GD (2003). Electrical coupling between the myenteric interstitial cells of Cajal and adjacent muscle layers in the guinea-pig gastric antrum. J Physiol 550, 829-844.
6. G-monomethyl l-arginine on the response of the rat anococcygeus muscle to NANC nerve stimulation. Br J Pharmacol 98, 1080-1082.
7. Gershon MD (1967). Effects of tetrodotoxin on innervated smooth muscle preparations. Br J Pharmacol Chemother 29, 259-279.
8. Groneberg D, Konig P, Koesling D & Friebe A (2011). Nitric oxide-sensitive guanylyl cyclase is dispensable for nitrergic signaling and gut motility in mouse intestinal smooth muscle. Gastroenterology 140, 1608-1617.
9. Groneberg D, Lies B, Konig P, Jager R, Seidler B, Klein S, Saur D & Friebe A (2013). Cell-specific deletion of nitric oxide-sensitive guanylyl cyclase reveals a dual pathway for nitrergic neuromuscular transmission in the murine fundus nitrergic relaxation in nitric oxide-sensitive guanylyl cyclase knockout mice. Gastroenterology 145, 188-196.
10. Hennig GW, Spencer NJ, Jokela-Willis S, Bayguinov PO, Lee HT, Ritchie LA, Ward SM, Smith TK & Sanders KM (2010). ICC-MY coordinate smooth muscle electrical and mechanical activity in the murine small intestine. Neurogastroenterol Motil 22, e138-e151.
11. Huh WJ, Khurana SS, Geahlen JH, Kohli K, Waller RA & Mills JC (2012). Tamoxifen induces rapid, reversible atrophy, and metaplasia in mouse stomach. Gastroenterology 142, 21-24.e7.
12. Huizinga JD & Chen JH (2014). The myogenic and neurogenic components of the rhythmic segmentation motor patterns of the intestine. Front Neurosci 8, 78.
13. Huizinga JD, Martz S, Gil V, Wang XY, Jimenez M & Parsons S (2011). Two independent networks of interstitial cells of Cajal work cooperatively with the enteric nervous system to create colonic motor patterns. Front Neurosci 5, 93.
14. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB & Bernstein A (1995). W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373, 347-349.
15. Huizinga JD, Zarate N & Farrugia G (2009). Physiology, injury, and recovery of interstitial cells of Cajal: basic and clinical science. Gastroenterology 137, 1548-1556.
16. Keef KD, Murray DC, Sanders KM & Smith TK (1997). Basal release of nitric oxide induces an oscillatory motor pattern in canine colon. J Physiol 499, 773-786.
17. Klein S, Seidler B, Kettenberger A, Sibaev A, Rohn M, Feil R, Allescher HD, Vanderwinden JM, Hofmann F, Schemann M, Rad R, Storr MA, Schmid RM, Schneider G & Saur D (2013). Interstitial cells of Cajal integrate excitatory and inhibitory neurotransmission with intestinal slow-wave activity. Nat Commun 4, 1630.
18. Li CG & Rand MJ (1989). Evidence for a role of nitric oxide in the neurotransmitter system mediating relaxation of the rat anococcygeus muscle. Clin Exp Pharmacol Physiol 16, 933-938.
19. Lies B, Gil V, Groneberg D, Seidler B, Saur D, Wischmeyer E, Jimenez M & Friebe A (2014). Interstitial cells of Cajal mediate nitrergic inhibitory neurotransmission in the murine gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 307, G98-G106.
20. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S & Nishi K (1992). Requirement of c-kit for development of intestinal pacemaker system. Development 116, 369-375.
21. Mitsui R & Komuro T (2003). Distribution and ultrastructure of interstitial cells of Cajal in the gastric antrum of wild-type and Ws/Ws rats. Anat Embryol (Berl) 206, 453-460.
22. Narahashi T (1972). Mechanism of action of tetrodotoxin and saxitoxin on excitable membranes. Fed Proc 31, 1124-1132.
23. Pluja L, Alberti E, Fernandez E, Mikkelsen HB, Thuneberg L & Jimenez M (2001). Evidence supporting presence of two pacemakers in rat colon. Am J Physiol Gastrointest Liver Physiol 281, G255-G266.
24. Pluja L, Fernandez E & Jimenez 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. Sanders KM, Koh SD & Ward SM (2006). Interstitial cells of cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 68, 307-343.
26. Thuneberg L (1982). Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71, 1-130.
27. Torihashi S, Ward SM, Nishikawa S, Nishi K, Kobayashi S & Sanders KM (1995). c-kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res 280, 97-111.
28. Ward SM, Burns AJ, Torihashi S & Sanders KM (1994). Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 480, 91-97.
29. Ward SM, Dalziel HH, Bradley ME, Buxton IL, Keef K, Westfall DP & Sanders KM (1992). Involvement of cyclic GMP in non-adrenergic, non-cholinergic inhibitory neurotransmission in dog proximal colon. Br J Pharmacol 107, 1075-1082.
30. Ward SM, Morris G, Reese L, Wang XY & Sanders KM (1998). Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 115, 314-329.
31. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horvath B, Maser-Gluth C, Greiner E, Lemmer B, Schutz G, Gutkind JS & Offermanns S (2008). G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med 14, 64-68.