Channel properties of the splicing isoforms of the olfactory calcium-activated chloride channel Anoctamin 2

Journal of General Physiology

Volumn 141, Issue 6, 2013, Pages 691-703

  Ponissery Saidu, Samsudeen ^a   Stephan, Aaron B ^b,c   Talaga, Anna K ^b   Zhao, Haiqing ^b   Reisert, Johannes ^a  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHLORIDE CHANNEL; ISOPROTEIN; MESSENGER RNA; TMEM16B PROTEIN, MOUSE;

5' UNTRANSLATED REGION; ACTION POTENTIAL; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; C57BL MOUSE; CELL STRAIN HEK293; CHEMISTRY; EXON; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT;

5' UNTRANSLATED REGIONS; ACTION POTENTIALS; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CHLORIDE CHANNELS; EXONS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RNA, MESSENGER;

EID: 84878655983     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210937     Document Type: Article

References (39)

1. 2+- activated Cl currents are dispensable for olfaction. Nat. Neurosci. 14:763-769. http://dx.doi.org/10.1038/nn.2821
2. 2+-activated Cl currents in isolated mouse olfactory sensory neurons. J. Neurophysiol. 98:153-160. http://dx.doi.org/10.1152/jn.00270.2007
3. Caputo, A., E. Caci, L. Ferrera, N. Pedemonte, C. Barsanti, E. Sondo, U. Pfeffer, R. Ravazzolo, O. Zegarra-Moran, and L.J. 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
4. 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 nociceptiveneurons. Nat. Neurosci. 15:1015-1021. http://dx.doi.org/10 .1038/nn.3111
5. Das, S., Y. Hahn, D.A. Walker, S. Nagata, M.C. Willingham, D.M. Peehl, T.K. Bera, B. Lee, and I. Pastan. 2008. Topology of NGEP, a prostate-specific cell:cell junction protein widely expressed in many cancers of different grade level. Cancer Res. 68:6306-6312. http://dx.doi.org/10.1158/0008-5472.CAN-08-0870
6. 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
7. 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
8. 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
9. Duran, C., Z. Qu, A.O. Osunkoya, Y. Cui, and H.C. Hartzell. 2012. ANOs 3-7 in the anoctamin/Tmem16 Cl channel family are intracellular proteins. Am. J. Physiol. Cell Physiol. 302:C482-C493. http://dx.doi.org/10.1152/ajpcell.00140.2011
10. Fallah, G., T. Romer, 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.
11. Ferrera, L., A. Caputo, I. Ubby, E. Bussani, O. Zegarra-Moran, R. Ravazzolo, F. Pagani, and L.J. 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
12. 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
13. Kaupp, U.B. 2010. Olfactory signalling in vertebrates and insects: differences and commonalities. Nat. Rev. Neurosci. 11:188-200.
14. Kim, S., L. Ma, and C.R. Yu. 2011. Requirement of calcium-activated chloride channels in the activation of mouse vomeronasal neurons. Nat Commun. 2:365. http://dx.doi.org/10.1038/ncomms1368
15. Kleene, S.J. 2008. The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chem. Senses. 33:839-859. http://dx.doi.org/10.1093/chemse/bjn048
16. 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
17. Kurahashi, T., and K.W. Yau. 1993. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature. 363:71-74. http://dx.doi.org/10.1038/363071a0
18. Lowe, G., and G.H. Gold. 1993. Nonlinear amplification by calciumdependent chloride channels in olfactory receptor cells. Nature. 366:283-286. http://dx.doi.org/10.1038/366283a0
19. 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
20. O'Driscoll, K.E., R.A. Pipe, and F.C. Britton. 2011. Increased complexity of Tmem16a/Anoctamin 1 transcript alternative splicing. BMC Mol. Biol. 12:35. http://dx.doi.org/10.1186/1471-2199-12-35
21. 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
22. Pifferi, S., G. Pascarella, A. Boccaccio, A. Mazzatenta, S. Gustincich, A. Menini, and S. Zucchelli. 2006. Bestrophin-2 is a candidate calcium- activated chloride channel involved in olfactory transduction. Proc. Natl. Acad. Sci. USA. 103:12929-12934. http://dx.doi.org/10.1073/pnas.0604505103
23. 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
24. Pifferi, S., V. Cenedese, and A. Menini. 2012. Anoctamin 2/TMEM16B: a calcium-activated chloride channel in olfactory transduction. Exp. Physiol. 97:193-199.
25. 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
26. 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
27. - response in mouse olfactory receptor neurons. Neuron. 45:553-561. http://dx.doi.org/10.1016/j.neuron.2005.01.012
28. Sagheddu, C., A. Boccaccio, M. Dibattista, G. Montani, R. Tirindelli, and A. Menini. 2010. Calcium concentration jumps reveal dynamic ion selectivity of calcium-activated chloride currents in mouse olfactory sensory neurons and TMEM16b-transfected HEK 293T cells. J. Physiol. 588:4189-4204. http://dx.doi.org/10.1113/jphysiol.2010.194407
29. 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
30. 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
31. Scotto-Lavino, E., G. Du, and M.A. Frohman. 2006. 5 end cDNA amplification using classic RACE. Nat. Protoc. 1:2555-2562. http://dx.doi.org/10.1038/nprot.2006.480
32. 2+-activated Cl channel Ano1/TMEM16A. J. Biol. Chem. 286:1381-1388. http://dx.doi.org/10.1074/jbc.M110.174847
33. 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
34. Stöhr, H., J.B. Heisig, P.M. Benz, S. Schöberl, V.M. Milenkovic, O. Strauss, W.M. Aartsen, J. Wijnholds, B.H. 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
35. 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
36. 2+-activated Cl channels. J. Cell Sci. 125:4991-4998. http://dx.doi.org/10.1242/jcs.109553
37. 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
38. Yang, Y.D., H. Cho, J.Y. Koo, M.H. Tak, 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/nature07313
39. 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