ANO1 in intramuscular interstitial cells of Cajal plays a key role in the generation of slow waves and tone in the internal anal sphincter

Journal of Physiology

Volumn 595, Issue 6, 2017, Pages 2021-2041

  Cobine, C A ^a   Hannah, E E ^a   Zhu, M H ^a   Lyle, H E ^a   Rock, J R ^b   Sanders, K M ^a   Ward, S M ^a   Keef, K D ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

calcium activated chloride channels; excitation contraction coupling; gastrointestinal motility; interstitial cells of Cajal

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CACNA1C PROTEIN, MOUSE; CALCIUM CHANNEL L TYPE; CHLORIDE CHANNEL; STEM CELL FACTOR RECEPTOR; TMEM16A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ANUS SPHINCTER; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; INTRAMUSCULAR INTERSTITIAL CELL OF CAJAL; LIMIT OF QUANTITATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SMOOTH MUSCLE CELL; ANAL CANAL; ANIMAL; C57BL MOUSE; GENE EXPRESSION; GENETICS; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; SMOOTH MUSCLE; TRANSGENIC MOUSE;

ANAL CANAL; ANIMALS; CALCIUM CHANNELS, L-TYPE; CHLORIDE CHANNELS; FEMALE; GENE EXPRESSION; IN VITRO TECHNIQUES; INTERSTITIAL CELLS OF CAJAL; MALE; MEMBRANE POTENTIALS; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE, SMOOTH; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 85013059149     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP273618     Document Type: Article

References (59)

1. Aickin CC & Brading AF (1982). Measurement of intracellular chloride in guinea-pig vas deferens by ion analysis, chloride efflux and micro-electrodes. J Physiol 326, 139–154.
2. 2+ transients in interstitial cells of Cajal located within the deep muscular plexus of the murine small intestine. J Physiol 594, 3317–3338.
3. Baker SA, Hennig GW, Ward SM & Sanders KM (2015). Temporal sequence of activation of cells involved in purinergic neurotransmission in the colon. J Physiol 593, 1945–1963.
4. Bayguinov O, Hagen B, Bonev AD, Nelson MT & Sanders KM (2000). Intracellular calcium events activated by ATP in murine colonic myocytes. Am J Physiol Cell Physiol 279, C126–C135.
5. 2+ currents are necessary for slow-wave propagation in the canine gastric antrum. Am J Physiol Cell Physiol 293, C1645–C1659.
6. Boedtkjer DM, Kim S, Jensen AB, Matchkov VM & Andersson KE (2015). New selective inhibitors of calcium-activated chloride channels - T16A(inh) -A01, CaCC(inh) -A01 and MONNA – what do they inhibit? Br J Pharmacol 172, 4158–4172.
7. Bradley E, Fedigan S, Webb T, Hollywood MA, Thornbury KD, McHale NG & Sergeant GP (2014). Pharmacological characterization of TMEM16A currents. Channels (Austin) 8, 308–320.
8. – channels in smooth muscle cells. Pflugers Arch 466, 861–872.
9. Chen H, Ordog T, Chen J, Young DL, Bardsley MR, Redelman D, Ward SM & Sanders KM (2007). Differential gene expression in functional classes of interstitial cells of Cajal in murine small intestine. Physiol Genomics 31, 492–509.
10. Cobine CA, Fong M, Hamilton R & Keef KD (2007). Species dependent differences in the actions of sympathetic nerves and noradrenaline in the internal anal sphincter. Neurogastroenterol Motil 19, 937–945.
11. Cobine CA, Hennig GW, Bayguinov YR, Hatton WJ, Ward SM & Keef KD (2010). Interstitial cells of Cajal in the cynomolgus monkey rectoanal region and their relationship to sympathetic and nitrergic nerves. Am J Physiol Gastrointest Liver Physiol 298, G643–G656.
12. Cobine CA, Hennig GW, Kurahashi M, Sanders KM, Ward SM & Keef KD (2011). Relationship between interstitial cells of Cajal, fibroblast-like cells and inhibitory motor nerves in the internal anal sphincter. Cell Tissue Res 344, 17–30.
13. Cobine CA, Sotherton AG, Peri LE, Sanders KM, Ward SM & Keef KD (2014). Nitrergic neuromuscular transmission in the mouse internal anal sphincter is accomplished by multiple pathways and post-junctional effector cells. Am J Physiol Gastrointest Liver Physiol 307, G1057–G1072.
14. Cook TA, Brading AF & Mortensen NJ (1999). Differences in contractile properties of anorectal smooth muscle and the effects of calcium channel blockade. Br J Surg 86, 70–75.
15. Cooke PH & Fay FS (1972). Correlation between fibre length, ultrastructure, and the length–tension relationship of mammalian smooth muscle. J Cell Biol 52, 105–116.
16. Davis AJ, Shi J, Pritchard HA, Chadha PS, Leblanc N, Vasilikostas G, Yao Z, Verkman AS, Albert AP & Greenwood IA (2013). Potent vasorelaxant activity of the TMEM16A inhibitor T16A(inh) -A01. Br J Pharmacol 168, 773–784.
17. v mouse internal anal sphincter. Neurogastroenterol Motil 24, e41–e55.
18. Gil V, Gallego D, Moha Ou MH, Peyronnet R, Martinez-Cutillas M, Heurteaux C, Borsotto M & Jimenez M (2012). Relative contribution of SKCa and TREK1 channels in purinergic and nitrergic neuromuscular transmission in the rat colon. Am J Physiol Gastrointest Liver Physiol 303, G412–G423.
19. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, Van de Rijn M, 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.
20. + channels. Trends Pharmacol Sci 28, 1–5.
21. Hall KA, Ward SM, Cobine CA & Keef KD (2014). Spatial organization and coordination of slow waves in the mouse anorectum. J Physiol 592, 3813–3829.
22. Hirst GD & Edwards FR (2006). Electrical events underlying organized myogenic contractions of the guinea pig stomach. J Physiol 576, 659–665.
23. V1.2 calcium channels: from in vitro findings to in vivo function. Physiol Rev 94, 303–326.
24. Horiguchi K, Keef KD & Ward SM (2003). Distribution of interstitial cells of Cajal in tunica muscularis of the canine rectoanal region. Am J Physiol Gastrointest Liver Physiol 284, G756–G767.
25. Huang F, Zhang H, Wu M, Yang H, Kudo M, Peters CJ, Woodruff PG, Solberg OD, Donne ML, Huang X, Sheppard D, Fahy JV, Wolters PJ, Hogan BL, Finkbeiner WE, Li M, Jan YN, Jan LY & Rock JR (2012). Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc Natl Acad Sci USA 109, 16354–16359.
26. Huizinga JD, Zarate N & Farrugia G (2009). Physiology, injury, and recovery of interstitial cells of Cajal: basic and clinical science. Gastroenterology 137, 1548–1556.
27. Hwang SJ, Basma N, Sanders KM & Ward SM (2016). Effects of new-generation inhibitors of the calcium-activated chloride channel anoctamin 1 on slow waves in the gastrointestinal tract 3. Br J Pharmacol 173, 1339–1349.
28. 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.
29. Iino S, Horiguchi K, Horiguchi S & Nojyo Y (2009). c-Kit-negative fibroblast-like cells express platelet-derived growth factor receptor alpha in the murine gastrointestinal musculature. Histochem Cell Biol 131, 691–702.
30. Iino S, Horiguchi S, Horiguchi K & Nojyo Y (2007). Interstitial cells of Cajal in the gastrointestinal musculature of W mutant mice. Arch Histol Cytol 70, 163–173.
31. Keef KD, Saxton SN, McDowall RA, Kaminski RE, Duffy AM & Cobine CA (2013). Functional role of vasoactive intestinal polypeptide in inhibitory motor innervation in the mouse internal anal sphincter. J Physiol 591, 1489–1506.
32. Kito Y, Kurahashi M, Mitsui R, Ward SM & Sanders KM (2014). Spontaneous transient hyperpolarizations in the rabbit small intestine. J Physiol 592, 4733–4745.
33. Kubota M, Suita S & Szurszewski JH (1998). Membrane properties and the neuro-effector transmission of smooth muscle cells in the canine internal anal sphincter. J Smooth Muscle Res 34, 173–184.
34. Kurahashi M, Mutafova-Yambolieva V, Koh SD & Sanders KM (2014). Platelet-derived growth factor receptor alpha-positive cells and not smooth muscle cells mediate purinergic hyperpolarization in murine colonic muscles. Am J Physiol Cell Physiol 307, C561–C570.
35. Kurahashi M, Zheng H, Dwyer L, Ward SM, Koh SD & Sanders KM (2011). A functional role for the ‘fibroblast-like cells’ in gastrointestinal smooth muscles. J Physiol 589, 697–710.
36. Lee MY, Park C, Berent RM, Park PJ, Fuchs R, Syn H, Chin A, Townsend J, Benson CC, Redelman D, Shen TW, Park JK, Miano JM, Sanders KM & Ro S (2015). Smooth muscle cell genome browser: enabling the identification of novel serum response factor target genes. PLoS One 10, e0133751.
37. Lees-Green R, Gibbons SJ, Farrugia G, Sneyd J & Cheng LK (2014). Computational modeling of anoctamin 1 calcium-activated chloride channels as pacemaker channels in interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 306, G711–G727.
38. McDonnell B, Hamilton R, Fong M, Ward SM & Keef KD (2008). Functional evidence for purinergic inhibitory neuromuscular transmission in the mouse internal anal sphincter. Am J Physiol Gastrointest Liver Physiol 294, G1041–G1051.
39. Mutafova-Yambolieva VN, O'Driscoll K, Farrelly A, Ward SM & Keef KD (2003). Spatial localization and properties of pacemaker potentials in the canine rectoanal region. Am J Physiol Gastrointest Liver Physiol 284, G748–G755.
40. Nakamura Y, Ohya Y, Abe I & Fujishima M (1999). Sodium–potassium pump current in smooth muscle cells from mesenteric resistance arteries of the guinea-pig. J Physiol 519, 203–212.
41. Nocka K, Tan JC, Chiu E, Chu TY, Ray P, Traktman P & Besmer P (1990). Molecular bases of dominant negative and loss of function mutations at the murine c-kit/white spotting locus: W37, Wv, W41 and W. EMBO J 9, 1805–1813.
42. Opazo A, Lecea B, Gil V, Jimenez M, Clave P & Gallego D (2011). Specific and complementary roles for nitric oxide and ATP in the inhibitory motor pathways to rat internal anal sphincter. Neurogastroenterol Motil 23, e11–e25.
43. Patel CA & Rattan S (2006). Spontaneously tonic smooth muscle has characteristically higher levels of RhoA/ROK compared with the phasic smooth muscle. Am J Physiol Gastrointest Liver Physiol 291, G830–G837.
44. Rothberg BS (2012). The BK channel: a vital link between cellular calcium and electrical signalling. Protein Cell 3, 883–892.
45. Sanders KM & Ward SM (2007). Kit mutants and gastrointestinal physiology. J Physiol 578, 33–42.
46. Sanders KM, Ward SM & Koh SD (2014). Interstitial cells: regulators of smooth muscle function. Physiol Rev 94, 859–907.
47. Sanders KM, Zhu MH, Britton F, Koh SD & Ward SM (2012). Anoctamins and gastrointestinal smooth muscle excitability. Exp Physiol 97, 200–206.
48. 2+ transient coordination between interstitial cells of Cajal. J Physiol 592, 4051–4068.
49. 2+ and alternative splicing on the pharmacological profile of ANO1 channels. Am J Physiol Cell Physiol 311, C437–C451.
50. Szurszewski JH (1987). Electrical basis for gastrointestinal motility. In Physiology of the Gastrointestinal Tract, ed. Johnson LR, pp. 383–423. Raven Press, New York.
51. Todorov LD (1982). On certain characteristics of the internal anal sphincter of cats. C R Acad Bulg Sci 35, 1435–1437.
52. 2+ phase waves: a basis for cellular pacemaking and long-range synchronicity in the guinea-pig gastric pylorus. J Physiol 548, 271–296.
53. 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.
54. Ward SM & Sanders KM (1992). Upstroke component of electrical slow waves in canine colonic smooth muscle due to nifedipine-resistant calcium current. J Physiol (Lond) 455, 321–337.
55. Zhang CH, Wang P, Liu DH, Chen CP, Zhao W, Chen X, Chen C, He WQ, Qiao YN, Tao T, Sun J, Peng YJ, Lu P, Zheng K, Craige SM, Lifshitz LM, Keaney JF, Jr, Fogarty KE, ZhuGe R & Zhu MS (2016). The molecular basis of the genesis of basal tone in internal anal sphincter. Nat Commun 7, 11358.
56. v mutant mice. Am J Physiol Gastrointest Liver Physiol 298, G14–G24.
57. 2+ conductance in interstitial cells of Cajal of the murine small intestine. Am J Physiol Cell Physiol 306, C705–C713.
58. – conductance in interstitial cells of Cajal linked to slow wave currents and pacemaker activity. J Physiol 587, 4905–4918.
59. 2+ release from endoplasmic reticulum regulates slow wave currents and pacemaker activity of interstitial cells of Cajal. Am J Physiol Cell Physiol 308, C608–C620.