Mechanosensitive ion channels in interstitial cells of Cajal and smooth muscle of the gastrointestinal tract

Neurogastroenterology and Motility

Volumn 19, Issue 4, 2007, Pages 245-252

  Kraichely, R E ^a   Farrugia, G ^a  

^a MAYO CLINIC   (United States)

Author keywords

Calcium channel; Patch clamp; Smooth muscle; Sodium channel; Stretch

Indexed keywords

CALCIUM CHANNEL; CATION CHANNEL; CHLORIDE CHANNEL; ION CHANNEL; SODIUM CHANNEL;

CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; ELECTRIC ACTIVITY; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; HUMAN; INTERSTITIAL CELL OF CAJAL; INTESTINE PARAMETERS; ION CURRENT; LEYDIG CELL; MECHANICAL STRESS; MECHANOTRANSDUCTION; MEMBRANE POTENTIAL; MUSCLE EXCITATION; MUSCLE FIBER MEMBRANE CONDUCTANCE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE;

CALCIUM CHANNELS; COILED BODIES; FOOD; GASTROINTESTINAL TRACT; GASTROINTESTINAL TRANSIT; HUMANS; ION CHANNELS; MECHANORECEPTORS; MECHANOTRANSDUCTION, CELLULAR; MUSCLE, SMOOTH; POTASSIUM CHANNELS; SODIUM CHANNELS;

EID: 33947513894     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2006.00880.x     Document Type: Review

References (53)

1. Gershon MD. Plasticity in serotonin control mechanisms in the gut. Curr Opin Pharmacol 2003; 3: 600-607.
2. Clerc N, Furness JB. Intrinsic primary afferent neurones of the digestive tract. Neurogastroenterol Motil 2004; 16(Suppl. 1): 24-7.
3. Zagorodnyuk VP, Chen BN, Brookes SJ. Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol 2001; 534: 255-68.
4. Barajas-Lopez C, Berezin I, Daniel EE, Huizinga JD. Pacemaker activity recorded in interstitial cells of Cajal of the gastrointestinal tract. Am J Physiol 1989; 257: C830-35.
5. 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.
6. Farrugia G, Lei S, Lin X et al. A major role for carbon monoxide as an endogenous hyperpolarizing factor in the gastrointestinal tract. Proc Natl Acad Sci USA 2003; 100: 8567-70.
7. Goodman MB, Lumpkin EA, Ricci A, Tracey WD, Kernan M, Nicolson T. Molecules and mechanisms of mechanotransduction. J Neurosci 2004; 24: 9220-22.
8. Sidi S, Friedrich RW, Nicolson T. NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 2003; 301: 96-9.
9. Driscoll M, Tavernarakis N. Molecules that mediate touch transduction in the nematode Caenorhabditis elegans. Gravit Space Biol Bull 1997; 10: 33-42.
10. Bulbring E. Correlation between membrane potential, spike discharge, and tension in smooth muscle. J Physiol 1955; 128: 200-21.
11. Sachs F. Mechanical transduction in biological systems. Crit Rev Biomed Eng 1988; 16: 141-69.
12. Markin VS, Martinac B. Mechanosensitive ion channels as reporters of bilayer expansion. A theoretical model. Biophys J 1991; 60: 1120-27.
13. Morris CE. Mechanosensitive ion channels. J Membr Biol 1990; 113: 93-107.
14. Hu H, Sachs F. Stretch-activated ion channels in the heart. J Mol Cell Cardiol 1997; 29: 1511-23.
15. Sukharev S, Corey DP. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci STKE 2004; 2004: re4.
16. Kung C. A possible unifying principle for mechanosensation. Nature 2005; 436: 647-54.
17. Gu CX, Juranka PF, Morris CE. Stretch-activation and stretch-inactivation of Shaker-IR, a voltage-gated K+ channel. Biophys J 2001; 80: 2678-93.
18. Patel AJ, Lazdunski M, Honore E. Lipid and mechanogated 2P domain K(+) channels. Curr Opin Cell Biol 2001; 13: 422-8.
19. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E. Lysophospholipids open the two-pore domain mechanogated K(+) channels TREK-1 and TRAAK. J Biol Chem 2000; 275: 10128-33.
20. 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.
21. Langton P, Ward SM, Carl A, Norell MA, Sanders KM. Spontaneous electrical activity of interstitial cells of Cajal isolated from canine proximal colon. Proc Natl Acad Sci USA 1989; 86: 7280-84.
22. Carl A, Bayguinov O, Shuttleworth CW, Ward SM, Sanders KM. Role of Ca(2+)-activated K+ channels in electrical activity of longitudinal and circular muscle layers of canine colon. Am J Physiol 1995; 268: C619-27.
23. Dopico AM, Kirber MT, Singer JJ, Walsh JV Jr. Membrane stretch directly activates large conductance Ca(2+)-activated K+ channels in mesenteric artery smooth muscle cells. Am J Hypertens 1994; 7: 82-9.
24. Kao CY. Ionic channel functions in some visceral smooth myocytes. In: Kao CY, Carsten ME, eds. Cellular Aspects of Smooth Muscle Function. Cambridge: Cambridge University Press, 1997: 98-131.
25. Farrugia G, Rich A, Rae JL, Sarr MG, Szurszewski JH. Calcium currents in human and canine jejunal circular smooth muscle cells. Gastroenterology 1995; 109: 707-17.
26. Imredy JP, Yue DT. Mechanism of Ca(2+)-sensitive inactivation of L-type Ca2+ channels. Neuron 1994; 12: 1301-18.
27. Farrugia G, Holm AN, Rich A, Sarr MG, Szurszewski JH, Rae JL. A mechanosensitive calcium channel in human intestinal smooth muscle cells. Gastroenterology 1999; 117: 900-905.
28. Lyford GL, Strege PR, Shepard A et al. Alpha(1C) (Ca(V)1.2) L-type calcium channel mediates mechanosensitive calcium regulation. Am J Physiol Cell Physiol 2002; 283: C1001-8.
29. Unno T, Komori S, Ohashi H. Microtubule cytoskeleton involvement in muscarinic suppression of voltage-gated calcium channel current in guinea-pig ileal smooth muscle. Br J Pharmacol 1999; 127: 1703-11.
30. Galli A, DeFelice LJ. Inactivation of L-type Ca channels in embryonic chick ventricle cells: dependence on the cytoskeletal agents colchicine and taxol. Biophys J 1994; 67: 2296-304.
31. Strege PR, Holm AN, Rich A et al. Cytoskeletal modulation of sodium current in human jejunal circular smooth muscle cells. Am J Physiol Cell Physiol 2003; 284: C60-66.
32. Kraichely RE, Strege PR, Sarr MG, Farrugia G. Regulation of mechanosensitivity of the L-type Ca2+ channel by composition of the lipid bilayer. Neurogastroenterol Motil 2005; 17: 610.
33. Lee HK, Sanders KM. Comparison of ionic currents from interstitial cells and smooth muscle cells of canine colon. J Physiol 1993; 460: 135-52.
34. Shin JB, Martinez-Salgado C, Heppenstall PA, Lewin GR. A T-type calcium channel required for normal function of a mammalian mechanoreceptor. Nat Neurosci 2003; 6: 724-30.
35. Calabrese B, Tabarean IV, Juranka P, Morris CE. Mechanosensitivity of N-type calcium channel currents. Biophys J 2002; 83: 2560-74.
36. Waniishi Y, Inoue R, Ito Y. Preferential potentiation by hypotonic cell swelling of muscarinic cation current in guinea pig ileum. Am J Physiol 1997; 272: C240-53.
37. Li L, Jin NG, Piao L et al. Hyposmotic membrane stretch potentiated muscarinic receptor agonist-induced depolarization of membrane potential in guinea-pig gastric myocytes. World J Gastroenterol 2002; 8: 724-7.
38. Kirber MT, Walsh JV Jr, Singer JJ. Stretch-activated ion channels in smooth muscle: a mechanism for the initiation of stretch-induced contraction. Pflugers Arch 1988; 412: 339-45.
39. Hisada T, Ordway RW, Kirber MT, Singer JJ, Walsh JV Jr. Hyperpolarization-activated cationic channels in smooth muscle cells are stretch sensitive. Pflugers Arch 1991; 417: 493-9.
40. Corey DP, Garcia-Anoveros J, Holt JR et al. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 2004; 432: 723-30.
41. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 2005; 7: 179-85.
42. Kim BJ, Lim HH, Yang DK et al. Melastatin-type transient receptor potential channel 7 is required for intestinal pacemaking activity. Gastroenterology 2005; 129: 1504-17.
43. Walker RL, Koh SD, Sergeant GP, Sanders KM, Horowitz B. TRPC4 currents have properties similar to the pacemaker current in interstitial cells of Cajal. Am J Physiol Cell Physiol 2002; 283: C1637-45.
44. Smirnov SV, Zholos AV, Shuba MF. Potential-dependent inward currents in single isolated smooth muscle cells of the rat ileum. J Physiol 1992; 454: 549-71.
45. Xiong Z, Sperelakis N, Noffsinger A, Fenoglio-Preiser C. Fast Na+ current in circular smooth muscle cells of the large intestine. Pflugers Arch 1993; 423: 485-91.
46. Muraki K, Imaizumi Y, Watanabe M. Sodium currents in smooth muscle cells freshly isolated from stomach fundus of the rat and ureter of the guinea-pig. J Physiol 1991; 442: 351-75.
47. Strege PR, Ou Y, Sha L et al. Sodium current in human intestinal interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 2003; 285: G1111-21.
48. Holm AN, Rich A, Miller SM et al. Sodium current in human jejunal circular smooth muscle cells. Gastroenterology 2002; 122: 178-87.
49. Ou Y, Strege P, Miller SM et al. Syntrophin gamma 2 regulates SCN5A gating by a PDZ domain-mediated interaction. J Biol Chem 2003; 278: 1915-23.
50. Bielefeldt K, Bass P. Sodium channel blockers alter slow-wave frequency of the rat stomach in vivo. Digestion 1991; 48: 43-50.
51. Locke GRI, Ackerman MJ, Zinsmeister AR, Thapa P, Farrugia G. Gastrointestinal symptoms in families patients with an SCN5A-Encoded cardiac channelopathy: evidence of an intestinal channelopathy. Am J Gastroenterol 2006; 101: 1-6.
52. Zhang Y, Miller DV, Paterson WG. Opposing roles of K(+) and Cl(-) channels in maintenance of opossum lower esophageal sphincter tone. Am J Physiol Gastrointest Liver Physiol 2000; 279: G1226-34.
53. Park SJ, McKay CM, Zhu Y, Huizinga JD. Volume-activated chloride currents in interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 2005; 289: G791-7.