Interstitial cells of Cajal contain signalling molecules for transduction of nitrergic stimulation in guinea pig caecum

Neurogastroenterology and Motility

Volumn 21, Issue 5, 2009, Pages

  Iino, S ^a   Horiguchi, K ^a   Nojyo, Y ^a   Ward, S M ^b   Sanders, K M ^b  

^a UNIVERSITY OF FUKUI   (Japan)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Cyclic guanosine 3 ,5 monophospate; Cyclic guanosine 3 ,5 monophospate dependent protein kinase; Enteric nervous system; Kit receptor tyrosine kinase; Nitric oxide; Soluble guanylate cyclase

Indexed keywords

3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; NITRIC OXIDE; NITROPRUSSIDE SODIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GASTROINTESTINAL TRACT; GUINEA PIG; IMMUNOREACTIVITY; INTERSTITIAL CELL OF CAJAL; MOLECULE; NERVE STIMULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER;

ANIMALS; CECUM; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; FEMALE; GUANYLATE CYCLASE; GUINEA PIGS; HUMANS; ISOENZYMES; MICE; MICE, INBRED BALB C; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITROPRUSSIDE; PHOSPHODIESTERASE INHIBITORS; PURINONES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; STEM CELL FACTOR;

EID: 65349152470     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2008.01236.x     Document Type: Article

References (43)

1. Zabel U, Kleinschnitz C, Oh P et al. Calcium-dependent membrane association sensitizes soluble guanylyl cyclase to nitric oxide. Nat Cell Biol 2002 4 : 307 11. (Pubitemid 34308857)
2. Arnold WP, Mittal CK, Katsuki S, Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 1977 74 : 3203 7.
3. Poulos TL. Soluble guanylate cyclase. Curr Opin Struct Biol 2006 16 : 736 43.
4. Hofmann F, Ammendola A, Schlossmann J. Rising behind NO: cGMP-dependent protein kinases. J Cell Sci 2000 113 : 1671 6. (Pubitemid 30333116)
5. Mergia E, Friebe A, Dangel O, Russwurm M, Koesling D. Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J Clin Invest 2006 116 : 1731 7. (Pubitemid 43911028)
6. Huber A, Trudrung P, Storr M et al. Protein kinase G expression in the small intestine and functional importance for smooth muscle relaxation. Am J Physiol Gastrointest Liver Physiol 1998 275 : G629 37. (Pubitemid 28491815)
7. Pfeifer A, Klatt P, Massberg S et al. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 1998 17 : 3045 51. (Pubitemid 28254377)
8. Geiselhoringer A, Werner M, Sigl K et al. IRAG is essential for relaxation of receptor-triggered smooth muscle contraction by cGMP kinase. EMBO J 2004 23 : 4222 31. (Pubitemid 39546160)
9. Koh SD, Monaghan K, Sergeant GP et al. TREK-1 regulation by nitric oxide and cGMP-dependent protein kinase. An essential role in smooth muscle inhibitory neurotransmission. J Biol Chem 2001 276 : 44338 46. (Pubitemid 37384009)
10. Koh SD, Sanders KM. Stretch-dependent potassium channels in murine colonic smooth muscle cells. J Physiol (Lond) 2001 533 : 155 63. (Pubitemid 32499368)
11. Ward SM, Sanders KM. Interstitial cells of Cajal: primary targets of enteric motor innervation. Anat Rec 2001 262 : 125 35. (Pubitemid 32061919)
12. Rumessen JJ, Vanderwinden JM. Interstitial cells in the musculature of the gastrointestinal tract: Cajal and beyond. Int Rev Cytol 2003 229 : 115 208. (Pubitemid 41782964)
13. Ward SM, Sanders KM, Hirst GDS. Role of interstitial cells of Cajal in neural control of gastrointestinal smooth muscles. Neurogastroenterol Motil 2004 16 (Suppl. 1 112 7. (Pubitemid 38580951)
14. Wang XY, Sanders KM, Ward SM. Intimate relationship between interstitial cells of Cajal and enteric nerves in the guinea-pig small intestine. Cell Tissue Res 1999 295 : 247 56. (Pubitemid 29050257)
15. Ward SM, Beckett EA, Wang X, Baker F, Khoyi M, Sanders KM. Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 2000 20 : 1393 403. (Pubitemid 30220419)
16. Horiguchi K, Sanders KM, Ward SM. Enteric motor neurons form synaptic-like junctions with interstitial cells of Cajal in the canine gastric antrum. Cell Tissue Res 2003 311 : 299 313. (Pubitemid 36459669)
17. Beckett EA, Takeda Y, Yanase H, Sanders KM, Ward SM. Synaptic specializations exist between enteric motor nerves and interstitial cells of Cajal in the murine stomach. J Comp Neurol 2005 493 : 193 206. (Pubitemid 41677477)
18. Burns AJ, Lomax AE, Torihashi S, Sanders KM, Ward SM. Interstitial cells of Cajal mediate inhibitory neurotransmission in the stomach. Proc Natl Acad Sci USA 1996 93 : 12008 13. (Pubitemid 26347239)
19. Ward SM, Morris G, Reese L, Wang XY, Sanders KM. Interstitial cells of Cajal mediate enteric inhibitory neurotransmission in the lower esophageal and pyloric sphincters. Gastroenterology 1998 115 : 314 29. (Pubitemid 28363424)
20. d mice. J Physiol (Lond) 2002 543 : 871 87.
21. Ward SM, McLaren GJ, Sanders KM. Interstitial cells of Cajal in the deep muscular plexus mediate enteric motor neurotransmission in the mouse small intestine. J Physiol (Lond) 2006 573 : 147 59. (Pubitemid 43670864)
22. Shuttleworth CW, Xue C, Ward SM, de Vente J, Sanders KM. Immunohistochemical localization of 3′,5′-cyclic guanosine monophosphate in the canine proximal colon: responses to nitric oxide and electrical stimulation of enteric inhibitory neurons. Neuroscience 1993 56 : 513 22. (Pubitemid 23274768)
23. Young HM, McConalogue K, Furness JB, De Vente J. Nitric oxide targets in the guinea-pig intestine identified by induction of cyclic GMP immunoreactivity. Neuroscience 1993 55 : 583 96. (Pubitemid 23211369)
24. Salmhofer H, Neuhuber WL, Ruth P, Huber A, Russwurm M, Allescher HD. Pivotal role of the interstitial cells of Cajal in the nitric oxide signaling pathway of rat small intestine. Morphological evidence. Cell Tissue Res 2001 305 : 331 40. (Pubitemid 34212126)
25. 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 48.
26. Sivarao DV, Mashimo HL, Thatte HS, Goyal RK. Lower esophageal sphincter is achalasic in nNOS(-/-) and hypotensive in W/Wv mutant mice. Gastroenterology 2001 121 : 34 42. (Pubitemid 32591513)
27. 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 8. (Pubitemid 26384331)
28. Shuttleworth CW, Sweeney KM, Sanders KM. Evidence that nitric oxide acts as an inhibitory neurotransmitter supplying taenia from the guinea-pig caecum. Br J Pharmacol 1999 127 : 1495 501. (Pubitemid 29358952)
29. Burns AJ, Herbert TM, Ward SM, Sanders KM. Interstitial cells of Cajal in the guinea-pig gastrointestinal tract as revealed by c-Kit immunohistochemistry. Cell Tissue Res 1997 290 : 11 20. (Pubitemid 27460120)
30. 2 acetylcholine receptor distribution in the guinea-pig gastrointestinal tract. Neuroscience 2006 138 : 549 59. (Pubitemid 43255564)
31. Tanaka J, Markerink-van Ittersum M, Steinbusch HW, De Vente J. Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia 1997 19 : 286 97. (Pubitemid 27165236)
32. Herbison AE, Simonian SX, Norris PJ, Emson PC. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J Neuroendocrinol 1996 8 : 73 82. (Pubitemid 26053031)
33. Hunyady B, Krempels K, Harta G, Mezey E. Immunohistochemical signal amplification by catalyzed reporter deposition and its application in double immunostaining. J Histochem Cytochem 1996 44 : 1353 62. (Pubitemid 27009081)
34. Iino S, Ward SM, Sanders KM. Interstitial cells of Cajal are functionally innervated by excitatory motor neurones in the murine intestine. J Physiol (Lond) 2004 556 : 521 30. (Pubitemid 38579004)
35. Suzuki H, Ward SM, Bayguinov YR, Edwards FR, Hirst GD. Involvement of intramuscular interstitial cells in nitrergic inhibition in the mouse gastric antrum. J Physiol (Lond) 2003 546 : 751 63. (Pubitemid 36204510)
36. Sanders KM, Ward SM, Daniel EE. ICC in neurotransmission: hard to swallow a lack of involvement. Gastroenterology 2002 122 : 1185 6 (Author Reply 1).
37. de Lorijn F, de Jonge WJ, Wedel T, Vanderwinden JM, Benninga MA, Boeckxstaens GE. Interstitial cells of Cajal are involved in the afferent limb of the rectoanal inhibitory reflex. Gut 2005 54 : 1107 13. (Pubitemid 41025903)
38. Tsujimura T, Hirota S, Nomura S et al. Characterization of Ws mutant allele of rats: a 12-base deletion in tyrosine kinase domain of c-kit gene. Blood 1991 78 : 1942 6.
39. Farre R, Wang XY, Vidal E et al. Interstitial cells of Cajal and neuromuscular transmission in the rat lower oesophageal sphincter. Neurogastroenterol Motil 2007 19 : 484 96. (Pubitemid 46905391)
40. Alberti E, Mikkelsen HB, Wang XY et al. Pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats. Am J Physiol Gastrointest Liver Physiol 2007 292 : G1499 510. (Pubitemid 47080602)
41. Koh SD, Campbell JD, Carl A, Sanders KM. Nitric oxide activates multiple potassium channels in canine colonic smooth muscle. J Physiol (Lond) 1995 489 : 735 43. (Pubitemid 26015844)
42. + (BKCa) channels in myocytes of the guinea-pig taenia caeci. J Physiol (Lond) 2000 525 : 363 76. (Pubitemid 30398367)
43. Tanovic A, Jimenez M, Fernandez E. Actions of NO donors and endogenous nitrergic transmitter on the longitudinal muscle of rat ileum in vitro: mechanisms involved. Life Sci 2001 69 : 1143 54. (Pubitemid 32722080)