Gating modes of calcium-activated chloride channels TMEM16A and TMEM16B

Journal of Physiology

Volumn 593, Issue 24, 2015, Pages 5283-5298

  Cruz Rangel, Silvia ^a   De Jesús Pérez, José J ^a   Contreras Vite, Juan A ^a   Pérez Cornejo, Patricia ^a   Hartzell, H Criss ^b   Arreola, Jorge ^a  

^a UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; PROTEIN TMEM16A; PROTEIN TMEM16B; UNCLASSIFIED DRUG; CHLORIDE CHANNEL; TMEM16A PROTEIN, MOUSE; TMEM16B PROTEIN, MOUSE;

ACINAR CELL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL MEMBRANE CONDUCTANCE; CELL MEMBRANE DEPOLARIZATION; CHANNEL GATING; CHLORIDE CURRENT; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PAROTID GLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN MOTIF;

ACINAR CELLS; ACTION POTENTIALS; AMINO ACID MOTIFS; ANIMALS; CELLS, CULTURED; CHLORIDE CHANNELS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MICE; MICE, INBRED C57BL; MUTATION;

EID: 84952802869     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271256     Document Type: Article

References (56)

1. Adomaviciene A, Smith KJ, Garnett H & Tammaro P (2013). Putative pore-loops of TMEM16/anoctamin channels affect channel density in cell membranes. J Physiol 591, 3487-3505.
2. Arreola J, Melvin JE & Begenisich T (1996). Activation of calcium-dependent chloride channels in rat parotid acinar cells. J Gen Physiol 108, 35-47.
3. Bader CR, Bertrand D & Schwartz EA (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol 331, 253-284.
4. Betto G, Cherian OL, Pifferi S, Cenedese V, Boccaccio A & Menini A (2014). Interactions between permeation and gating in the TMEM16B/anoctamin2 calcium-activated chloride channel. J Gen Physiol 143, 703-718.
5. Bill A, Popa MO, van Diepen MT, Gutierrez A, Lilley S, Velkova M, Acheson K, Choudhury H, Renaud NA, Auld DS, Gosling M, Groot-Kormelink PJ & Gaither LA (2015). Variomics screen identifies the re-entrant loop of the calcium-activated chloride channel ANO1 that facilitates channel activation. J Biol Chem 290, 889-903.
6. Boton R, Dascal N, Gillo B, Lass Y (1989). Two calcium-activated chloride conductances in Xenopus laevis oocytes permeabilized with the ionophore A23187. J Physiol 408, 511-534.
7. Broadbent SD, Ramjeesingh M, Bear CE, Argent BE, Linsdell P & Gray MA (2015). The cystic fibrosis transmembrane conductance regulator is an extracellular chloride sensor. Pflugers Arch 467, 1783-1794.
8. Brunner JD, Lim NK, Schenck S, Duerst A & Dutzler R (2014). X-ray structure of a calcium-activated TMEM16 lipid scramblase. Nature 516, 207-212.
9. Bykova EA, Zhang XD, Chen TY & Zheng J (2006). Large movement in the C terminus of CLC-0 chloride channel during slow gating. Nat Struct Mol Biol 13, 1115-1119.
10. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O & Galietta LJ (2008). TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322, 590-594.
11. Casas-Pruneda G, Reyes JP, Pérez-Flores G, Pérez-Cornejo P & Arreola J (2009). Functional interactions between P2×4 and P2×7 receptors from mouse salivary epithelia. J Physiol 587, 2887-2901.
12. Catalán MA, Kondo Y, Peña-Munzenmayer G, Jaramillo Y, Liu F, Choi S, Crandall E, Borok Z, Flodby P, Shull GE & Melvin JE (2015). A fluid secretion pathway unmasked by acinar-specific Tmem16A gene ablation in the adult mouse salivary gland. Proc Natl Acad Sci USA 112, 2263-2268.
13. Cenedese V, Betto G, Celsi F, Cherian OL, Pifferi S & Menini A (2012). The voltage dependence of the TMEM16B/anoctamin2 calcium-activated chloride channel is modified by mutations in the first putative intracellular loop. J Gen Physiol 139, 285-294.
14. Chen TY (2005). Structure and function of ClC channels. Annu Rev Physiol 67, 809-839.
15. Dauner K, Möbus C, Frings S & Möhrlen F (2013). Targeted expression of anactamin calcium-activated chloride channels in rod photoreceptor terminals of the rodent retina. Invest Ophthalmol Vis Sci 54, 3126-3136.
16. Duan DY (2009). Phenomics of cardiac chloride channels: the systematic study of chloride channel function in the heart. J Physiol 587, 2163-2177.
17. Dutzler R, Campbell EB, Cadene M, Chait BT & MacKinnon R (2002). X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415, 287-294.
18. Dutzler R, Campbell EB & MacKinnon R (2003). Gating the selectivity filter in ClC chloride channels. Science 300, 108-112.
19. Duvvuri U, Shiwarski DJ, Xiao D, Bertrand C, Huang X, Edinger RS, Rock JR, Harfe BD, Henson BJ, Kunzelmann K, Schreiber R, Seethala RS, Egloff AM, Chen X, Lui VW, Grandis JR & Gollin SM (2012). TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression. Cancer Res 72, 3270-3281.
20. Fallah G, Römer T, Detro-Dassen S, Braam U, Markwardt F & Schmalzing G (2011). TMEM16A(a)/anoctamin-1 shares a homodimeric architecture with CLC chloride channels. Mol Cell Proteomics 10, M110.004697.
21. Ferrera L, Caputo A, Ubby I, Bussani E, Zegarra-Moran O, Ravazzolo R, Pagani F & Galietta LJ (2009). Regulation of TMEM16A chloride channel properties by alternative splicing. J Biol Chem 284, 33360-33368.
22. - content controls cell volume in single salivary acinar cells during fluid secretion. Am J Physiol 259, C998-C1004.
23. Glahn D & Nuccitelli R (2003). Voltage-clamp study of the activation currents and fast block to polyspermy in the egg of Xenopus laevis. Develop Growth Diff 45, 187-197.
24. Garcia-Olivares J, Alekov A, Boroumand MR, Begemann B, Hidalgo P & Fahlke C (2008). Gating of human ClC-2 chloride channels and regulation by carboxy-terminal domains. J Physiol 586, 5325-5336.
25. - currents in rabbit portal vein smooth muscle cells by external anions. J Physiol 516, 365-376.
26. Hartzell HC, Putzier I & Arreola J (2005). Calcium-activated chloride channels. Annu Rev Physiol 67, 719-758.
27. Hernández-Carballo CY, De Santiago-Castillo JA, Rosales-Saavedra T, Pérez-Cornejo P & Arreola J (2010). Control of volume-sensitive chloride channel inactivation by the coupled action of intracellular chloride and extracellular protons. Pflugers Arch 460, 633-644.
28. 2+ signals. J Gen Physiol 115, 59-80.
29. Kuruma A & Hartzell HC (1999b). Dynamics of calcium regulation of chloride currents in Xenopus oocytes. Am J Physiol 276, C161-C175.
30. - conductance in smooth muscle. Am J Physiol 271, C435-C454.
31. - channels in blood pressure control. Curr Opin Pharmacol 21, 127-137.
32. - currents in salivary and lacrimal glands. In Calcium-Activated Chloride Channels, ed. Fuller C, pp. 209-230. Academic Press, New York.
33. Melvin JE, Yule D, Shuttleworth T & Begenisich T (2005). Regulation of fluid and electrolyte secretion in salivary gland acinar cells. Ann Rev Physiol 67, 445-469.
34. Miledi R (1982). A calcium-dependent transient outward current in Xenopus laevis oocytes. Proc R Soc Lond B Biol Sci 215, 491-497.
35. Miller C (2006). ClC chloride channels viewed through a transporter lens. Nature 440, 484-489.
36. Nilius B, Prenen J, Sziics G, Wei L, Tanzi F, Voets T & Droogmans G (1997). Calcium-activated chloride channels in bovine pulmonary artery endothelial cells. J Physiol 498, 381-396.
37. Pérez-Cornejo P, De Santiago JA & Arreola J (2004). Permeant anions control gating of calcium-dependent chloride channels. J Membr Biol 198, 125-133.
38. Peters CJ, Yu H, Tiena J, Jan JN, Li M, & Jan LY. (2015). Four basic residues critical for the ion selectivity and pore blocker sensitivity of TMEM16A calcium-activated chloride channels. Proc Natl Acad Sci USA 112, 3547-3552.
39. Pifferi S, Dibattista M & Menini A (2009). TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch 458, 1023-1038.
40. - channel, ANO1 (TMEM16A), is a double-edged sword in cell proliferation and tumorigenesis. Cancer Med 3, 453-461.
41. Reyes JP, Huanosta-Gutiérrez A, López-Rodríguez A & Martínez-Torres A (2015). Study of permeation and blocker binding in TMEM16A calcium-activated chloride channels. Channels 9, 88-95.
42. Reyes JP, López-Rodríguez A, Espino-Saldaña AE, Huanosta-Gutiérrez A, Miledi R & Martínez-Torres A (2014). Anion permeation in calcium-activated chloride channels formed by TMEM16A from Xenopus tropicalis. Pflugers Arch 466, 1769-1777.
43. - channel in mouse submandibular salivary gland acinar cells. J Biol Chem 285, 12990-13001.
44. Schroeder BC, Cheng T, Jan YN & Jan LY (2008). Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134, 1019-1029.
45. Scudieri P, Sondo E, Caci E, Ravazzolo R & Galietta LJ (2013). TMEM16A-TMEM16B chimaeras to investigate the structure-function relationship of calcium-activated chloride channels. Biochem J 452, 443-55.
46. Sui Y, Sun M, Wu F, Yang L, Di W, Zhang G, Zhong L, Ma Z, Zheng J, Fang X & Ma T (2014). Inhibition of TMEM16A expression suppresses growth and invasion in human colorectal cancer cells. PLoS ONE 9, e115443.
47. 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 USA 106, 11776-11781.
48. Tien J, Peters CJ, Wong XM, Cheng T, Jan YN, Jan LY & Yang H (2014). A comprehensive search for calcium binding sites critical for TMEM16A calcium-activated chloride channel activity. Elife 3:e02772 doi: 10.7554/eLife.02772.
49. Vocke K, Dauner K, Hahn A, Ulbrich A, Broecker J, Keller S, Frings S & Mohrlen F (2013). Calmodulin-dependent activation and inactivation of anoctamin calcium-gated chloride channel. J Gen Physiol 142, 381-404.
50. Webb DJ & Nuccitelli R (1985). Fertilization potential and electrical properties of the Xenopus laevis egg. Dev Biol 107, 395-406.
51. Xiao Q, Yu K, Pérez-Cornejo P, Cui Y, Arreola J & Hartzell HC (2011). Voltage- and calcium-dependent gating of TMEM16A/Ano1 chloride channels are physically coupled by the first intracellular loop. Proc Natl Acad Sci USA 108, 8891-8896.
52. Xiao Q & Cui Y (2014). Acidic amino acids in the first intracellular loop contribute to voltage- and calcium-dependent gating of anoctamin1/TMEM16A. PLoS One 9, e99376.
53. 2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151, 111-22.
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. Yu K, Duran C, Qu Z, Cui YY & Hartzell HC (2012). Explaining calcium-dependent gating of anoctamin-1 chloride channels requires a revised topology. Circ Res 110, 990-999.
56. Yu K, Whitlock JM, Lee K, Ortlund EA, Cui YY & Hartzell HC (2015). Identification of a lipid scrambling domain in ANO6/TMEM16F. Elife 4:e06901. doi: 10.7554/eLife.06901.