Calmodulin-dependent activation and inactivation of anoctamin calcium-gated chloride channels

Journal of General Physiology

Volumn 142, Issue 4, 2013, Pages 381-404

  Vocke, Kerstin ^a   Dauner, Kristin ^a   Hahn, Anne ^a   Ulbrich, Anne ^a   Broecker, Jana ^b   Keller, Sandro ^b   Frings, Stephan ^a   Möhrlen, Frank ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANO1 PROTEIN, RAT; ANOCTAMIN 2 PROTEIN, RAT; CALCIUM; CALMODULIN; CHLORIDE CHANNEL; ISOPROTEIN;

ACTION POTENTIAL; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BINDING SITE; BRAIN; CHANNEL GATING; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTATION; NERVE CELL; PHYSIOLOGY; PROTEIN BINDING; RAT; RETINA;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BRAIN; CALCIUM; CALMODULIN; CHLORIDE CHANNELS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NEURONS; PROTEIN BINDING; PROTEIN ISOFORMS; RATS; RETINA;

EID: 84885454101     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311015     Document Type: Article

References (112)

1. Adomaviciene, A., K.J. Smith, H. Garnett, and P. Tammaro. 2013. Putative pore-loops of TMEM16/anoctamin channels affect channel density in cell membranes. J. Physiol. 591:3487-3505. http://dx.doi.org/10.1113/jphysiol.2013.251660
2. Alseikhan, B.A., C.D. DeMaria, H.M. Colecraft, and D.T. Yue. 2002. Engineered calmodulins reveal the unexpected eminence of Ca2+ channel inactivation in controlling heart excitation. Proc. Natl. Acad. Sci. USA. 99:17185-17190. http://dx.doi.org/10 .1073/pnas.262372999
3. - currents by phosphorylation in pulmonary arterial smooth muscle cells. J. Gen. Physiol. 128:73-87. http://dx.doi .org/10.1085/jgp.200609507
4. - currents in pulmonary arterial smooth muscle cells. J. Biol. Chem. 284:32507-32521. http://dx.doi.org/10.1074/jbc.M109.050401
5. Bähler, M., and A. Rhoads. 2002. Calmodulin signaling via the IQ motif. FEBS Lett. 513:107-113. http://dx.doi.org/10 .1016/S0014-5793(01)03239-2
6. - channels at a glance. J. Cell Sci. 125:1367-1371. http://dx.doi.org/10.1242/ jcs.093260
7. - currents are dispensable for olfaction. Nat. Neurosci. 14:763-769. http://dx.doi.org/10.1038/nn.2821
8. Biskup, C., J. Kusch, E. Schulz, V. Nache, F. Schwede, F. Lehmann, V. Hagen, and K. Benndorf. 2007. Relating ligand binding to activation gating in CNGA2 channels. Nature. 446:440-443. http://dx.doi.org/10.1038/nature05596
9. Biswas, S., I. Deschênes, D. Disilvestre, Y. Tian, V.L. Halperin, and G.F. Tomaselli. 2008. Calmodulin regulation of Nav1.4 current: role of binding to the carboxyl terminus. J. Gen. Physiol. 131:197- 209. http://dx.doi.org/10.1085/jgp.200709863
10. Blaesse, P., M.S. Airaksinen, C. Rivera, and K. Kaila. 2009. Cationchloride cotransporters and neuronal function. Neuron. 61:820- 838. http://dx.doi.org/10.1016/j.neuron.2009.03.003
11. - currents in isolated mouse olfactory sensory neurons. J. Neurophysiol. 98:153-160. http://dx.doi.org/10.1152/jn.00270.2007
12. Boccaccio, A., C. Sagheddu, and A. Menini. 2011. Flash photolysis of caged compounds in the cilia of olfactory sensory neurons. J. Vis. Exp. e3195. http://dx.doi.org/10.3791/3195
13. Bradley, J., D. Reuter, and S. Frings. 2001. Facilitation of calmodulinmediated odor adaptation by cAMP-gated channel subunits. Science. 294:2176-2178. http://dx.doi.org/10.1126/science.1063415
14. Bradley, J., W. Bönigk, K.W. Yau, and S. Frings. 2004. Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nat. Neurosci. 7:705-710. http://dx.doi.org/10.1038/nn1266
15. Caporale, N., and Y. Dan. 2008. Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31:25-46. http://dx.doi.org/10.1146/annurev.neuro.31.060407.125639
16. Caputo, A., E. Caci, L. Ferrera, N. Pedemonte, C. Barsanti, E. Sondo, U. Pfeffer, R. Ravazzolo, O. Zegarra-Moran, and L.J.V. Galietta. 2008. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science. 322:590- 594. http://dx.doi.org/10.1126/science.1163518
17. Cenedese, V., G. Betto, F. Celsi, O.L. Cherian, S. Pifferi, and A. Menini. 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. http://dx.doi.org/10.1085/jgp.201110764
18. Cho, H., Y.D. Yang, J. Lee, B. Lee, T. Kim, Y. Jang, S.K. Back, H.S. Na, B.D. Harfe, F. Wang, et al. 2012. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat. Neurosci. 15:1015-1021. http://dx.doi.org/10.1038/nn.3111
19. Craven, C.J., B. Whitehead, S.K. Jones, E. Thulin, G.M. Blackburn, and J.P. Waltho. 1996. Complexes formed between calmodulin and the antagonists J-8 and TFP in solution. Biochemistry. 35:10287-10299. http://dx.doi.org/10.1021/bi9605043
20. Dauner, K., J. Lissmann, S. Jeridi, S. Frings, and F. Möhrlen. 2012. Expression patterns of anoctamin 1 and anoctamin 2 chloride channels in the mammalian nose. Cell Tissue Res. 347:327-341. http://dx.doi.org/10.1007/s00441-012-1324-9
21. Dauner, K., C. Möbus, S. Frings, and F. Möhrlen. 2013. Targeted expression of anoctamin calcium-activated chloride channels in rod photoreceptor terminals of the rodent retina. Invest. Ophthalmol. Vis. Sci. 54:3126-3136. http://dx.doi.org/10.1167/iovs.13-11711
22. Davis, A.J., A.S. Forrest, T.A. Jepps, M.L. Valencik, M. Wiwchar, C.A. Singer, W.R. Sones, I.A. Greenwood, and N. Leblanc. 2010. Expression profile and protein translation of TMEM16A in murine smooth muscle. Am. J. Physiol. Cell Physiol. 299:C948-C959. http://dx.doi.org/10.1152/ajpcell.00018.2010
23. Del Carlo, B., M. Pellegrini, and M. Pellegrino. 2002. Calmodulin antagonists do not inhibit IK(Ca) channels of human erythrocytes. Biochim. Biophys. Acta. 1558:133-141. http://dx.doi.org/10.1016/S0005-2736(01)00419-9
24. DeMaria, C.D., T.W. Soong, B.A. Alseikhan, R.S. Alvania, and D.T. Yue. 2001. Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature. 411:484-489. http://dx.doi.org/10.1038/35078091
25. Derler, I., M. Hofbauer, H. Kahr, R. Fritsch, M. Muik, K. Kepplinger, M.E. Hack, S. Moritz, R. Schindl, K. Groschner, and C. Romanin. 2006. Dynamic but not constitutive association of calmodulin with rat TRPV6 channels enables fine tuning of Ca2+- dependent inactivation. J. Physiol. 577:31-44. http://dx.doi .org/10.1113/jphysiol.2006.118661
26. Dibattista, M., A. Amjad, D.K. Maurya, C. Sagheddu, G. Montani, R. Tirindelli, and A. Menini. 2012. Calcium-activated chloride channels in the apical region of mouse vomeronasal sensory neurons. J. Gen. Physiol. 140:3-15. http://dx.doi.org/10.1085/jgp.201210780
27. Dick, I.E., M.R. Tadross, H. Liang, L.H. Tay, W. Yang, and D.T. Yue. 2008. A modular switch for spatial Ca2+ selectivity in the calmodulin regulation of CaV channels. Nature. 451:830-834. http://dx.doi.org/10.1038/nature06529
28. Duran, C., and H.C. Hartzell. 2011. Physiological roles and diseases of Tmem16/Anoctamin proteins: are they all chloride channels? Acta Pharmacol. Sin. 32:685-692. http://dx.doi.org/10.1038/aps.2011.48
29. - channel family are intracellular proteins. Am. J. Physiol. Cell Physiol. 302:C482-C493. http://dx.doi.org/10.1152/ajpcell.00140.2011
30. Durham, A.C. 1983. A survey of readily available chelators for buffering calcium ion concentrations in physiological solutions. Cell Calcium. 4:33-46. http://dx.doi.org/10.1016/0143-4160(83)90047-7
31. Dzeja, C., V. Hagen, U.B. Kaupp, and S. Frings. 1999. Ca2+ permeation in cyclic nucleotide-gated channels. EMBO J. 18:131-144. http://dx.doi.org/10.1093/emboj/18.1.131
32. Erickson, M.G., B.A. Alseikhan, B.Z. Peterson, and D.T. Yue. 2001. Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells. Neuron. 31:973-985. http://dx.doi.org/10.1016/S0896-6273(01)00438-X
33. Erickson, M.G., H. Liang, M.X. Mori, and D.T. Yue. 2003. FRET two-hybrid mapping reveals function and location of L-type Ca2+ channel CaM preassociation. Neuron. 39:97-107. http://dx.doi.org/10.1016/S0896-6273(03)00395-7
34. Fallah, G., T. Römer, S. Detro-Dassen, U. Braam, F. Markwardt, and G. Schmalzing. 2011. TMEM16A(a)/anoctamin-1 shares a homodimeric architecture with CLC chloride channels. Mol. Cell. Proteomics. 10:M110.004697.
35. Feldkamp, M.D., S.E. O'Donnell, L. Yu, and M.A. Shea. 2010. Allosteric effects of the antipsychotic drug trifluoperazine on the energetics of calcium binding by calmodulin. Proteins. 78:2265- 2282. http://dx.doi.org/10.1002/prot.22739
36. Ferrera, L., A. Caputo, I. Ubby, E. Bussani, O. Zegarra-Moran, R. Ravazzolo, F. Pagani, and L.J.V. Galietta. 2009. Regulation of TMEM16A chloride channel properties by alternative splicing. J. Biol. Chem. 284:33360-33368. http://dx.doi.org/10.1074/jbc .M109.046607
37. Ferrera, L., P. Scudieri, E. Sondo, A. Caputo, E. Caci, O. Zegarra- Moran, R. Ravazzolo, and L.J.V. Galietta. 2011. A minimal isoform of the TMEM16A protein associated with chloride channel activity. Biochim. Biophys. Acta. 1808:2214-2223. http://dx.doi.org/10.1016/j.bbamem.2011.05.017
38. Gangopadhyay, J.P., Z. Grabarek, and N. Ikemoto. 2004. Fluorescence probe study of Ca2+-dependent interactions of calmodulin with calmodulin-binding peptides of the ryanodine receptor. Biochem. Biophys. Res. Commun. 323:760-768. http://dx.doi.org/10.1016/j.bbrc.2004.08.154
39. Ghatpande, A.S., and J. Reisert. 2011. Olfactory receptor neuron responses coding for rapid odour sampling. J. Physiol. 589:2261-2273. http://dx.doi.org/10.1113/jphysiol.2010.203687
40. Grubb, S., K.A. Poulsen, C.A. Juul, T. Kyed, T.K. Klausen, E.H. Larsen, and E.K. Hoffmann. 2013. TMEM16F (Anoctamin 6), an anion channel of delayed Ca(2+) activation. J. Gen. Physiol. 141:585-600. http://dx.doi.org/10.1085/jgp.201210861
41. Guo, T., B.R. Fruen, F.R. Nitu, T.D. Nguyen, Y. Yang, R.L. Cornea, and D.M. Bers. 2011. FRET detection of calmodulin binding to the cardiac RyR2 calcium release channel. Biophys. J. 101:2170-2177. http://dx.doi.org/10.1016/j.bpj.2011.09.030
42. Halling, D.B., P. Aracena-Parks, and S.L. Hamilton. 2006. Regulation of voltage-gated Ca2+ channels by calmodulin. Sci. STKE. 2006:er1. Hartzell, C., I. Putzier, and J. Arreola. 2005. Calcium-activated chloride channels. Annu. Rev. Physiol. 67:719-758. http://dx.doi.org/10.1146/annurev.physiol.67.032003.154341
43. Hartzell, C., I. Putzier, and J. Arreola. 2005. Calcium-activated chloride channels. Annu. Rev. Physiol. 67:719-758. http://dx.doi.org/10.1146/annurev.physiol.67.032003.154341
44. - channels. J. Physiol. 587:2127-2139. http://dx.doi.org/10.1113/jphysiol.2008.163709
45. Hengl, T., H. Kaneko, K. Dauner, K. Vocke, S. Frings, and F. Möhrlen. 2010. Molecular components of signal amplification in olfactory sensory cilia. Proc. Natl. Acad. Sci. USA. 107:6052-6057. http://dx.doi.org/10.1073/pnas.0909032107
46. Huang, F., J.R. Rock, B.D. Harfe, T. Cheng, X.Z. Huang, Y.N. Jan, and L.Y. Jan. 2009. Studies on expression and function of the TMEM16A calcium-activated chloride channel. Proc. Natl. Acad. Sci. USA. 106:21413-21418. http://dx.doi.org/10.1073/pnas.0911935106
47. Huang, F., X. Wong, and L.Y. Jan. 2012a. International Union of Basic and Clinical Pharmacology. LXXXV: calcium-activated chloride channels. Pharmacol. Rev. 64:1-15. http://dx.doi.org/10.1124/pr.111.005009
48. Huang, F., H. Zhang, M. Wu, H. Yang, M. Kudo, C.J. Peters, P.G. Woodruff, O.D. Solberg, M.L. Donne, X. Huang, et al. 2012b. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc. Natl. Acad. Sci. USA. 109:16354-16359. http://dx.doi.org/10.1073/pnas .1214596109
49. Huang, W.C., S. Xiao, F. Huang, B.D. Harfe, Y.N. Jan, and L.Y. Jan. 2012c. Calcium-activated chloride channels (CaCCs) regulate action potential and synaptic response in hippocampal neurons. Neuron. 74:179-192. http://dx.doi.org/10.1016/j.neuron.2012.01.033
50. Huelsenbeck, J.P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17:754-755. http://dx.doi.org/10.1093/bioinformatics/17.8.754
51. Jach, G., M. Pesch, K. Richter, S. Frings, and J.F. Uhrig. 2006. An improved mRFP1 adds red to bimolecular fluorescence complementation. Nat. Methods. 3:597-600. http://dx.doi.org/10.1038/nmeth901
52. Jeon, J.H., S.S. Paik, M.H. Chun, U. Oh, and I.B. Kim. 2013. Presynaptic localization and possible function of calciumactivated chloride channel anoctamin 1 in the mammalian retina. PLoS ONE. 8:e67989. http://dx.doi.org/10.1371/journal.pone .0067989
53. Jung, J., J.H. Nam, H.W. Park, U. Oh, J.H. Yoon, and M.G. Lee. 2013. Dynamic modulation of ANO1/TMEM16A HCO3(-) permeability by Ca2+/calmodulin. Proc. Natl. Acad. Sci. USA. 110:360-365. http://dx.doi.org/10.1073/pnas.1211594110
54. Kaneko, H., I. Putzier, S. Frings, U.B. Kaupp, and T. Gensch. 2004. Chloride accumulation in mammalian olfactory sensory neurons. J. Neurosci. 24:7931-7938. http://dx.doi.org/10.1523/JNEUROSCI.2115-04.2004
55. Kaneko, H., F. Möhrlen, and S. Frings. 2006. Calmodulin contributes to gating control in olfactory calcium-activated chloride channels. J. Gen. Physiol. 127:737-748. http://dx.doi.org/10.1085/jgp.200609497
56. Kasri, N.N., K. Török, A. Galione, C. Garnham, G. Callewaert, L. Missiaen, J.B. Parys, and H. De Smedt. 2006. Endogenously bound calmodulin is essential for the function of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 281:8332-8338. http://dx.doi.org/10.1074/jbc.M510971200
57. Kim, S., L. Ma, and C.R. Yu. 2011. Requirement of calciumactivated chloride channels in the activation of mouse vomeronasal neurons. Nat Commun. 2:365. http://dx.doi.org/10.1038/ncomms1368
58. Kunzelmann, K., Y. Tian, J.R. Martins, D. Faria, P. Kongsuphol, J. Ousingsawat, F. Thevenod, E. Roussa, J. Rock, and R. Schreiber. 2011. Anoctamins. Pflugers Arch. 462:195-208. http://dx.doi.org/10.1007/s00424-011-0975-9
59. Kunzelmann, K., B. Nilius, G. Owsianik, R. Schreiber, J. Ousingsawat, L. Sirianant, P. Wanitchakool, E.M. Bevers, and J.W. Heemskerk. 2013. Molecular functions of anoctamin 6 (TMEM16F): a chloride channel, cation channel, or phospholipid scramblase? Pflugers Arch. In press. http://dx.doi.org/10.1007/s00424-013-1305-1
60. Kursula, P., and V. Majava. 2007. A structural insight into lead neurotoxicity and calmodulin activation by heavy metals. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63:653-656. http://dx.doi.org/10.1107/S1744309107034525
61. Lee, A., S.T. Wong, D. Gallagher, B. Li, D.R. Storm, T. Scheuer, and W.A. Catterall. 1999. Ca2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature. 399:155-159. http://dx.doi.org/10.1038/20194
62. Li, F., S. Ponissery-Saidu, K.K. Yee, H. Wang, M.L. Chen, N. Iguchi, G. Zhang, P. Jiang, J. Reisert, and L. Huang. 2013. Heterotrimeric G protein subunit G?13 is critical to olfaction. J. Neurosci. 33:7975-7984. http://dx.doi.org/10.1523/JNEUROSCI.5563-12.2013
63. Lindemann, B. 2001. Predicted profiles of ion concentrations in olfactory cilia in the steady state. Biophys. J. 80:1712-1721. http://dx.doi.org/10.1016/S0006-3495(01)76142-5
64. - channels. J. Clin. Invest. 120:1240-1252. http://dx.doi.org/10.1172/JCI41084
65. Martins, J.R., D. Faria, P. Kongsuphol, B. Reisch, R. Schreiber, and K. Kunzelmann. 2011. Anoctamin 6 is an essential component of the outwardly rectifying chloride channel. Proc. Natl. Acad. Sci. USA. 108:18168-18172. http://dx.doi.org/10.1073/pnas.1108094108
66. Mercer, A.J., K. Rabl, G.E. Riccardi, N.C. Brecha, S.L. Stella Jr., and W.B. Thoreson. 2011. Location of release sites and calcium-activated chloride channels relative to calcium channels at the photoreceptor ribbon synapse. J. Neurophysiol. 105:321-335. http://dx.doi.org/10.1152/jn.00332.2010
67. Mori, M.X., M.G. Erickson, and D.T. Yue. 2004. Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels. Science. 304:432-435. http://dx.doi.org/10.1126/science.1093490
68. Owenius, R., M. Osterlund, M. Lindgren, M. Svensson, O.H. Olsen, E. Persson, P.O. Freskgård, and U. Carlsson. 1999. Properties of spin and fluorescent labels at a receptor-ligand interface. Biophys. J. 77:2237-2250. http://dx.doi.org/10.1016/S0006-3495(99)77064-5
69. Patton, C., S. Thompson, and D. Epel. 2004. Some precautions in using chelators to buffer metals in biological solutions. Cell Calcium. 35:427-431. http://dx.doi.org/10.1016/j.ceca.2003.10.006
70. Payne, J.A., C. Rivera, J. Voipio, and K. Kaila. 2003. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 26:199-206. http://dx.doi.org/10.1016/S0166-2236(03)00068-7
71. Peersen, O.B., T.S. Madsen, and J.J. Falke. 1997. Intermolecular tuning of calmodulin by target peptides and proteins: differential effects on Ca2+ binding and implications for kinase activation. Protein Sci. 6:794-807. http://dx.doi.org/10.1002/pro.5560060406
72. Peterson, B.Z., C.D. DeMaria, J.P. Adelman, and D.T. Yue. 1999. Calmodulin is the Ca2+ sensor for Ca2+ -dependent inactivation of L-type calcium channels. Neuron. 22:549-558. http://dx.doi.org/10.1016/S0896-6273(00)80709-6
73. Pifferi, S., M. Dibattista, and A. Menini. 2009. TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch. 458:1023-1038. http://dx.doi.org/10.1007/s00424-009-0684-9
74. Pitt, G.S., R.D. Zühlke, A. Hudmon, H. Schulman, H. Reuter, and R.W. Tsien. 2001. Molecular basis of calmodulin tethering and Ca2+-dependent inactivation of L-type Ca2+ channels. J. Biol. Chem. 276:30794-30802. http://dx.doi.org/10.1074/jbc .M104959200
75. Ponissery Saidu, S., A.B. Stephan, A.K. Talaga, H. Zhao, and J. Reisert. 2013. Channel properties of the splicing isoforms of the olfactory calcium-activated chloride channel Anoctamin 2. J. Gen. Physiol. 141:691-703. http://dx.doi.org/10.1085/jgp.201210937
76. Qu, Z., and H.C. Hartzell. 2000. Anion permeation in Ca(2+)-activated Cl(-) channels. J. Gen. Physiol. 116:825-844. http://dx.doi.org/10.1085/jgp.116.6.825
77. Rasche, S., B. Toetter, J. Adler, A. Tschapek, J.F. Doerner, S. Kurtenbach, H. Hatt, H. Meyer, B. Warscheid, and E.M. Neuhaus. 2010. Tmem16b is specifically expressed in the cilia of olfactory sensory neurons. Chem. Senses. 35:239-245. http://dx.doi.org/10.1093/chemse/bjq007
78. Reisert, J., P.J. Bauer, K.W. Yau, and S. Frings. 2003. The Caactivated Cl channel and its control in rat olfactory receptor neurons. J. Gen. Physiol. 122:349-363. http://dx.doi.org/10.1085/jgp .200308888
79. - response in mouse olfactory receptor neurons. Neuron. 45:553-561. http://dx.doi.org/10.1016/j.neuron.2005 .01.012
80. Schreiber, R., I. Uliyakina, P. Kongsuphol, R. Warth, M. Mirza, J.R. Martins, and K. Kunzelmann. 2010. Expression and function of epithelial anoctamins. J. Biol. Chem. 285:7838-7845. http://dx.doi.org/10.1074/jbc.M109.065367
81. Schroeder, B.C., T. Cheng, Y.N. Jan, and L.Y. Jan. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell. 134:1019-1029. http://dx.doi.org/10.1016/j.cell.2008.09.003
82. Scudieri, P., E. Sondo, E. Caci, R. Ravazzolo, and L.J. Galietta. 2013. TMEM16A-TMEM16B chimaeras to investigate the structurefunction relationship of calcium-activated chloride channels. Biochem. J. 452:443-455. http://dx.doi.org/10.1042/BJ20130348
83. Shen, Y., D. Yu, H. Hiel, P. Liao, D.T. Yue, P.A. Fuchs, and T.W. Soong. 2006. Alternative splicing of the Ca(v)1.3 channel IQ domain, a molecular switch for Ca2+-dependent inactivation within auditory hair cells. J. Neurosci. 26:10690-10699. http://dx.doi.org/10.1523/JNEUROSCI.2093-06.2006
84. - channel Ano1/TMEM16A. J. Biol. Chem. 286:1381-1388. http://dx.doi.org/10.1074/jbc .M110.174847
85. - channel. Am. J. Physiol. Cell Physiol. 304:C748-C759. http://dx.doi.org/10.1152/ajpcell.00228.2012
86. Sigworth, F.J. 1980. The variance of sodium current fluctuations at the node of Ranvier. J. Physiol. 307:97-129.
87. Stephan, A.B., E.Y. Shum, S. Hirsh, K.D. Cygnar, J. Reisert, and H. Zhao. 2009. ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc. Natl. Acad. Sci. USA. 106:11776-11781. http://dx.doi.org/10.1073/pnas .0903304106
88. Stephan, A.B., S. Tobochnik, M. Dibattista, C.M. Wall, J. Reisert, and H. Zhao. 2011. The Na(+)/Ca(2+) exchanger NCKX4 governs termination and adaptation of the mammalian olfactory response. Nat. Neurosci. 15:131-137. http://dx.doi.org/10.1038/nn.2943
89. Stöhr, H., J.B. Heisig, P.M. Benz, S. Schöberl, V.M. Milenkovic, O. Strauss, W.M. Aartsen, J. Wijnholds, B.H.F. Weber, and H.L. Schulz. 2009. TMEM16B, a novel protein with calcium-dependent chloride channel activity, associates with a presynaptic protein complex in photoreceptor terminals. J. Neurosci. 29:6809-6818. http://dx.doi.org/10.1523/JNEUROSCI.5546-08.2009
90. Stroffekova, K. 2008. Ca2+/CaM-dependent inactivation of the skeletal muscle L-type Ca2+ channel (Cav1.1). Pflugers Arch. 455:873-884. http://dx.doi.org/10.1007/s00424-007-0344-x
91. Szteyn, K., E. Schmid, M.K. Nurbaeva, W. Yang, P. Münzer, K. Kunzelmann, F. Lang, and E. Shumilina. 2012. Expression and functional significance of the Ca(2+)-activated Cl(-) channel ANO6 in dendritic cells. Cell. Physiol. Biochem. 30:1319-1332. http://dx.doi.org/10.1159/000343321
92. Thoreson, W.B., R. Nitzan, and R.F. Miller. 2000. Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors: chloride imaging and cell-attached patch-clamp recordings. Vis. Neurosci. 17:197-206. http://dx.doi.org/10.1017/S0952523800172025
93. Thoreson, W.B., S.L. Stella Jr., E.I. Bryson, J. Clements, and P. Witkovsky. 2002. D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. Vis. Neurosci. 19:235-247. http://dx.doi.org/10.1017/S0952523802192017
94. Thoreson, W.B., E.J. Bryson, and K. Rabl. 2003. Reciprocal interactions between calcium and chloride in rod photoreceptors. J. Neurophysiol. 90:1747-1753. http://dx.doi.org/10.1152/jn.00932.2002
95. Tian, Y., P. Kongsuphol, M. Hug, J. Ousingsawat, R. Witzgall, R. Schreiber, and K. Kunzelmann. 2011. Calmodulin-dependent activation of the epithelial calcium-dependent chloride channel TMEM16A. FASEB J. 25:1058-1068. http://dx.doi.org/10 .1096/fj.10-166884
96. - channels. J. Cell Sci. 125:4991-4998. http://dx.doi.org/10.1242/jcs.109553
97. Tien, J., H.Y. Lee, D.L. Minor Jr., Y.N. Jan, and L.Y. Jan. 2013. Identification of a dimerization domain in the TMEM16A calciumactivated chloride channel (CaCC). Proc. Natl. Acad. Sci. USA. 110 :6352-6357. http://dx.doi.org/10.1073/pnas.1303672110
98. Tran, T.T., K. Tobiume, C. Hirono, S. Fujimoto, K. Mizuta, K. Kubozono, H. Inoue, M. Itakura, M. Sugita, and N. Kamata. 2013. TMEM16E (GDD1) exhibits protein instability and distinct characteristics in chloride channel/pore forming ability. J. Cell. Physiol. In press. http://dx.doi.org/10.1002/jcp.24431
99. Trudeau, M.C., and W.N. Zagotta. 2004. Dynamics of Ca2+-calmodulin-dependent inhibition of rod cyclic nucleotide-gated channels measured by patch-clamp fluorometry. J. Gen. Physiol. 124:211-223. http://dx.doi.org/10.1085/jgp.200409101
100. Ungerer, N., N. Mücke, J. Broecker, S. Keller, S. Frings, and F. Möhrlen. 2011. Distinct binding properties distinguish LQ-type calmodulinbinding domains in cyclic nucleotide-gated channels. Biochemistry. 50:3221-3228. http://dx.doi.org/10.1021/bi200115m
101. Whelan, S., and N. Goldman. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18:691-699. http://dx.doi.org/10.1093/oxfordjournals.molbev.a003851
102. Williams, D.A., and F.S. Fay. 1990. Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium. 11:75-83. http://dx.doi.org/10.1016/0143-4160(90)90061-X
103. Xia, X.M., B. Fakler, A. Rivard, G. Wayman, T. Johnson-Pais, J.E. Keen, T. Ishii, B. Hirschberg, C.T. Bond, S. Lutsenko, et al. 1998. Mechanism of calcium gating in small-conductance calciumactivated potassium channels. Nature. 395:503-507. http://dx .doi.org/10.1038/26758
104. Xiao, Q., K. Yu, P. Perez-Cornejo, Y. Cui, J. Arreola, and H.C. Hartzell. 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. http://dx.doi.org/10.1073/pnas.1102147108
105. Yamazaki, J., T. Urushidani, and T. Nagao. 1996. Barium activates rat cerebellar nitric oxide synthase. Jpn. J. Pharmacol. 70:351-354. http://dx.doi.org/10.1254/jjp.70.351
106. Yang, C., and R.J. Delay. 2010. Calcium-activated chloride current amplifies the response to urine in mouse vomeronasal sensory neurons. J. Gen. Physiol. 135:3-13. http://dx.doi.org/10.1085/jgp .200910265
107. Yang, P.S., B.A. Alseikhan, H. Hiel, L. Grant, M.X. Mori, W. Yang, P.A. Fuchs, and D.T. Yue. 2006. Switching of Ca2+-dependent inactivation of Ca(v)1.3 channels by calcium binding proteins of auditory hair cells. J. Neurosci. 26:10677-10689. http://dx.doi.org/10.1523/JNEUROSCI.3236-06.2006
108. Yang, Y.D., H.W. Cho, J.Y. Koo, M.H. Tak, Y.Y. Cho, W.S. Shim, S.P. Park, J. Lee, B. Lee, B.M. Kim, et al. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature. 455:1210-1215. http://dx.doi.org/10.1038/nature 07313
109. Yang, H., A. Kim, T. David, D. Palmer, T. Jin, J. Tien, F. Huang, T. Cheng, S.R. Coughlin, Y.N. Jan, and L.Y. Jan. 2012. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell. 151:111-122. http://dx.doi.org/10.1016/j.cell.2012.07.036
110. Yap, K.L., J. Kim, K. Truong, M. Sherman, T. Yuan, and M. Ikura. 2000. Calmodulin target database. J. Struct. Funct. Genomics. 1:8-14. http://dx.doi.org/10.1023/A:1011320027914
111. Yu, K., C. Duran, Z. Qu, Y.Y. Cui, and H.C. Hartzell. 2012. Explaining calcium-dependent gating of anoctamin-1 chloride channels requires a revised topology. Circ. Res. 110:990-999. http://dx.doi.org/10.1161/CIRCRESAHA.112.264440
112. Zühlke, R.D., G.S. Pitt, K. Deisseroth, R.W. Tsien, and H. Reuter. 1999. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 399:159-162. http://dx.doi.org/10.1038/20200