Ano1, a Ca2+-activated Cl- channel, coordinates contractility in mouse intestine by Ca2+ transient coordination between interstitial cells of Cajal

Journal of Physiology

Volumn 592, Issue 18, 2014, Pages 4051-4068

  Singh, Raman Deep ^a   Gibbons, Simon J ^a   Saravanaperumal, Siva Arumugam ^a   Du, Peng ^b   Hennig, Grant W ^c   Eisenman, Seth T ^a   Mazzone, Amelia ^a   Hayashi, Yujiro ^a   Cao, Chike ^a   Stoltz, Gary J ^a   Ordog, Tamas ^a   Rock, Jason R ^d   Harfe, Brian D ^e   Szurszewski, Joseph H ^a   Farrugia, Gianrico ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

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

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ION; PROTEIN ANO1; UNCLASSIFIED DRUG; CALCIUM; CHLORIDE CHANNEL; TMEM16A PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; INTERSTITIAL CELL OF CAJAL; INTESTINE CONTRACTION; JEJUNUM; MOUSE; NONHUMAN; PROTEIN FUNCTION; SMALL INTESTINE; TISSUE CULTURE; ANIMAL; CALCIUM SIGNALING; GENETICS; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CHLORIDE CHANNELS; INTERSTITIAL CELLS OF CAJAL; JEJUNUM; MICE; MUSCLE CONTRACTION;

EID: 84907851834     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.277152     Document Type: Article

References (55)

1. Abramoff MD, Magalhaes PJ & Ram SJ (2004). Image processing with ImageJ. Biophotonics Int 11, 7.
2. 2+-activated Cl- channels at a glance. J Cell Sci 125, 1367-1371.
3. Beyder A & Farrugia G (2012). Targeting ion channels for the treatment of gastrointestinal motility disorders. Therap Adv Gastroenterol 5, 5-21.
4. Bogeski G, Shafton AD, Kitchener PD, Ferens DM & Furness JB (2005). A quantitative approach to recording peristaltic activity from segments of rat small intestine in vivo. Neurogastroenterol Motil 17, 262-272.
5. Bulley S & Jaggar JH (2013). Cl channels in smooth muscle cells. Pflugers Arch 466, 861-872.
6. Collins SM, Khan I, Vallance B & Hogaboam C (1994). The role of smooth muscle in intestinal inflammation. In Inflammatory Bowel Disease Basic Research, Clinical Implications and Trends in Therapy, ed. Sutherland LR, Collins SM, Martin F, McLeod RS & Targan SR, pp. 162-169. Springer, Dordrecht.
7. Dixon RE, Hennig GW, Baker SA, Britton FC, Harfe BD, Rock JR, Sanders KM &Ward SM (2012). Electrical slow waves in the mouse oviduct are dependent upon a calcium activated chloride conductance encoded by Tmem16a. Biol Reprod 86, 1-7.
8. Farrugia G (1999). Ionic conductances in gastrointestinal smooth muscles and interstitial cells of Cajal. Annu Rev Physiol 61, 45-84.
9. Farrugia G, Lei S, Lin X, Miller SM, Nath KA, Ferris CD, Levitt M & Szurszewski JH (2003). A major role for carbon monoxide as an endogenous hyperpolarizing factor in the gastrointestinal tract. Proc Natl Acad Sci U S A 100, 8567-8570.
10. Fernandez D, Sargent J, Sachse FB & Sanguinetti MC (2008). Structural basis for ether-a-go-go-related gene K+ channel subtype-dependent activation by niflumic acid. Mol Pharmacol 73, 1159-1167.
11. Gershon MD & Tack J (2007). The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132, 397-414.
12. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, de Rijn MV,West RB, Sarr MG, Kendrick ML, Cima RR, Dozois EJ, Larson DW, Ordog T & Farrugia G (2009). Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 296 G1370-G1381
13. Hanani M, Belzer V, Rich A & Faussone-Pellegrini SM (1999). Visualization of interstitial cells of Cajal in living, intact tissues. Microsc Res Tech 47, 336-343.
14. 2+ waves in the longitudinal muscle layer of the murine large intestine in vitro. J Physiol 543, 233-253.
15. Horvath VJ, Vittal H, Lorincz A, Chen H, Almeida-Porada G, Redelman D & Ordog T (2006). Reduced stem cell factor links smooth myopathy and loss of interstitial cells of Cajal in murine diabetic gastroparesis. Gastroenterology 130, 759-770.
16. 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.
17. Hwang SJ, Blair PJ, Britton FC, O'Driscoll KE, Hennig G, Bayguinov YR, Rock JR, Harfe BD, Sanders KM &Ward SM (2009). Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587, 4887-4904.
18. 2+-inhibited non-selective cation conductance contributes to pacemaker currents in mouse interstitial cell of Cajal. J Physiol 540, 803-814.
19. Kraichely RE & Farrugia G (2007). Mechanosensitive ion channels in interstitial cells of Cajal and smooth muscle of the gastrointestinal tract. Neurogastroenterol Motil 19, 245-252.
20. Kunze WA & Furness JB (1999). The enteric nervous system and regulation of intestinal motility. Annu Rev Physiol 61, 117-142.
21. Kunzelmann K, Tian Y, Martins JR, Faria D, Kongsuphol P, Ousingsawat J, Wolf L & Schreiber R (2012). Airway epithelial cells-functional links between CFTR and anoctamin dependent Cl- secretion. Int J Biochem Cell Biol 44, 1897-1900.
22. Lammers WJ, Al-Bloushi HM, Al-Eisaei SA, Al-Dhaheri FA, Stephen B, John R, Dhanasekaran S & Karam SM (2011). Slow wave propagation and plasticity of interstitial cells of Cajal in the small intestine of diabetic rats. Exp Physiol 96, 1039-1048.
23. Lowie BJ, Wang XY, White EJ & Huizinga JD (2011). On the origin of rhythmic calcium transients in the ICC-MP of the mouse small intestine. Am J Physiol Gastrointest Liver Physiol 301, 11.
24. Martins JR, Faria D, Kongsuphol P, Reisch B, Schreiber R & Kunzelmann K (2011). Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc Natl Acad Sci U S A 108, 18168-18172.
25. -) channel, Ano1. Biochem Biophys Res Commun 427, 248-253.
26. 2+-activated Cl channel using Xenopus laevis oocytes with an improved drug screening strategy. Mol Brain 1, 1756-6606.
27. Park KJ, Hennig GW, Lee HT, Spencer NJ,Ward SM, Smith TK & Sanders KM (2006). Spatial and temporal mapping of pacemaker activity in interstitial cells of Cajal in mouse ileum in situ. Am J Physiol Cell Physiol 290, 28.
28. Quian Quiroga R, Kreuz T & Grassberger P (2002). Event synchronization: a simple and fast method to measure synchronicity and time delay patterns. Phys Rev E Stat Nonlin Soft Matter Phys 66, 15.
29. Rich A, Hanani M, Ermilov LG, Malysz J, Belzer V, Szurszewski JH & Farrugia G (2002). Physiological study of interstitial cells of Cajal identified by vital staining. Neurogastroenterol Motil 14, 189-196.
30. Roberts RR, Murphy JF, Young HM & Bornstein JC (2007). Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am J Physiol Gastrointest Liver Physiol 292, G930-G938.
31. Rock JR, Futtner CR & Harfe BD (2008). The transmembrane protein TMEM16A is required for normal development of the murine trachea. Dev Biol 321, 141-149.
32. Sagheddu C, Boccaccio A, Dibattista M, Montani G, Tirindelli R & Menini A (2010). Calcium concentration jumps reveal dynamic ion selectivity of calcium-activated chloride currents in mouse olfactory sensory neurons and TMEM16btransfected HEK 293T cells. J Physiol 588, 4189-4204.
33. Sanders KM (1996). A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111, 492-515.
34. Sanders KM (2008). Regulation of smooth muscle excitation and contraction. Neurogastroenterol Motil 20, 39-53.
35. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R & Sofroniew MV (2007). Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132, 1344-1358.
36. Schreiber R, Uliyakina I, Kongsuphol P,Warth R, Mirza M, Martins JR & Kunzelmann K (2010). Expression and function of epithelial anoctamins. J Biol Chem 285, 7838-7845.
37. Schroeder BC, Cheng T, Jan YN & Jan LY (2008). Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134, 1019-1029.
38. Shi XZ, Lin YM, Powell DW& Sarna SK (2011). Pathophysiology of motility dysfunction in bowel obstruction: role of stretch-induced COX-2. Am J Physiol Gastrointest Liver Physiol 300, G99-G108.
39. Stanich JE, Gibbons SJ, Eisenman ST, Bardsley MR, Rock JR, Harfe BD, Ordog T & Farrugia G (2011). Ano1 as a regulator of proliferation. Am J Physiol Gastrointest Liver Physiol 301, G1044-G1051.
40. Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J & Zhao H (2009). ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci U S A 106, 11776-11781.
41. Szurszewski JH (1987). Electrophysiological basis of gastrointestinal motility. In Physiology of the Gastrointestinal Tract, 2nd edn, ed. Johnson LR, pp. 383-422. Raven Press, New York.
42. Thuneberg L (1982). Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71, 1-130.
43. 2+-activated Cl- channels. J Cell Sci 125, 4991-4998.
44. Torihashi S, Fujimoto T, Trost C & Nakayama S (2002). Calcium oscillation linked to pacemaking of interstitial cells of Cajal: requirement of calcium influx and localization of TRP4 in caveolae. J Biol Chem 277, 19191-19197.
45. 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.
46. Tran TT, Tobiume K, Hirono C, Fujimoto S, Mizuta K, Kubozono K, Inoue H, Itakura M, Sugita M & Kamata N (2014). TMEM16E (GDD1) exhibits protein instability and distinct characteristics in chloride channel/pore forming ability. J Cell Physiol 229, 181-190.
47. Ward SM, Beckett EA,Wang X, Baker F, Khoyi M & Sanders KM (2000). Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 20, 1393-1403.
48. 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.
49. Ward SM, Harney SC, Bayguinov JR, McLaren GJ & Sanders KM (1997). Development of electrical rhythmicity in the murine gastrointestinal tract is specifically encoded in the tunica muscularis. J Physiol 505, 241-258.
50. Ward SM & Sanders KM (2006). Involvement of intramuscular interstitial cells of Cajal in neuroeffector transmission in the gastrointestinal tract. J Physiol 576, 675-682.
51. Xue L, Farrugia G, Miller SM, Ferris CD, Snyder SH & Szurszewski JH (2000). 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 97, 1851-1855.
52. 2+ signals in interstitial cells of Cajal and longitudinal smooth muscle cells during rhythmic activity in mouse ileum. J Physiol 538, 823-835.
53. 2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151, 111-122.
54. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK & Oh U (2008). TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455, 1210-1215.
55. 2+-activated Cl- conductance in interstitial cells of Cajal linked to slow wave currents and pacemaker activity. J Physiol 587, 4905-4918.