The Ca2+-activated Cl- channel TMEM16B regulates action potential firing and axonal targeting in olfactory sensory neurons

Journal of General Physiology

Volumn 148, Issue 4, 2016, Pages

  Pietra, Gianluca ^a   Dibattista, Michele ^b   Menini, Anna ^a   Reisert, Johannes ^b   Boccaccio, Anna ^c  

^a SISSA   (Italy)

^b MONELL CHEMICAL SENSES CENTER   (United States)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANO2 PROTEIN, MOUSE; ANOCTAMIN;

ACTION POTENTIAL; ANIMAL; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; ODOR; OLFACTORY RECEPTOR; OLFACTORY RECEPTOR NEURON; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ANOCTAMINS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; SMELL;

EID: 84991492534     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201611622     Document Type: Article

References (80)

1. - currents are dispensable for olfaction. Nat. Neurosci. 14:763-769. doi:10.1038/nn.2821.
2. - currents in isolated mouse olfactory sensory neurons. J. Neurophysiol. 98:153-160. doi:10.1152/jn.00270.2007.
3. Boccaccio, A., L. Lagostena, V. Hagen, and A. Menini. 2006. Fast adaptation in mouse olfactory sensory neurons does not require the activity of phosphodiesterase. J. Gen. Physiol. 128:171-184. doi:10.1085/jgp.200609555.
4. Boccaccio, A., C. Sagheddu, and A. Menini. 2011. Flash photolysis of caged compounds in the cilia of olfactory sensory neurons. J. Vis. Exp. (55):e3195.
5. Bozza, T., P. Feinstein, C. Zheng, and P. Mombaerts. 2002. Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22:3033-3043.
6. Bozza, T., J.P. McGann, P. Mombaerts, and M. Wachowiak. 2004. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron. 42:9-21. doi:10.1016/S0896-6273(04)00144-8.
7. Connelly, T., A. Savigner, and M. Ma. 2013. Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors. J. Neurophysiol. 110:55-62. doi:10.1152/jn.00910.2012.
8. Delay, R., and D. Restrepo. 2004. Odorant responses of dual polarity are mediated by cAMP in mouse olfactory sensory neurons. J. Neurophysiol. 92:1312-1319. doi:10.1152/jn.00140.2004.
9. Dewan, A., R. Pacifico, R. Zhan, D. Rinberg, and T. Bozza. 2013. Non-redundant coding of aversive odours in the main olfactory pathway. Nature. 497:486-489. doi:10.1038/nature12114.
10. Dibattista, M., and J. Reisert. 2016. The odorant receptor-dependent role of olfactory marker protein in olfactory receptor neurons. J. Neurosci. 36:2995-3006. doi:10.1523/JNEUROSCI.4209-15.2016.
11. Dörrscheidt, G.H. 1981. The statistical significance of the peristimulus time histogram (PSTH). Brain Res. 220:397-401. doi:10.1016/0006-8993(81)91232-4.
12. Duchamp-Viret, P., A. Duchamp, and M.A. Chaput. 2000. Peripheral odor coding in the rat and frog: quality and intensity specification. J. Neurosci. 20:2383-2390.
13. Firestein, S., and G.M. Shepherd. 1995. Interaction of anionic and cationic currents leads to a voltage dependence in the odor response of olfactory receptor neurons. J. Neurophysiol. 73:562-567.
14. Frings, S., and B. Lindemann. 1991. Current recording from sensory cilia of olfactory receptor cells in situ. I. The neuronal response to cyclic nucleotides. J. Gen. Physiol. 97:1-16. doi:10.1085/jgp.97.1.1.
15. Ghatpande, A.S., and J. Reisert. 2011. Olfactory receptor neuron responses coding for rapid odour sampling. J. Physiol. 589:2261-2273. doi:10.1113/jphysiol.2010.203687.
16. Grosmaitre, X., L.C. Santarelli, J. Tan, M. Luo, and M. Ma. 2007. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10:348-354. doi:10.1038/nn1856.
17. Hall, S.E., W.B. Floriano, N. Vaidehi, and W.A. Goddard III. 2004. Predicted 3-D structures for mouse I7 and rat I7 olfactory receptors and comparison of predicted odor recognition profiles with experiment. Chem. Senses. 29:595-616. doi:10.1093/chemse/bjh063.
18. Huberman, A.D., M.B. Feller, and B. Chapman. 2008. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31:479-509. doi:10.1146/annurev.neuro.31.060407.125533.
19. Imai, T., M. Suzuki, and H. Sakano. 2006. Odorant receptor-derived cAMP signals direct axonal targeting. Science. 314:657-661. doi:10.1126/science.1131794.
20. Jarriault, D., and X. Grosmaitre. 2015. Perforated patch-clamp recording of mouse olfactory sensory neurons in intact neuroepithelium: functional analysis of neurons expressing an identified odorant receptor. J. Vis. Exp. (101):e52652.
21. 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. doi:10.1523/JNEUROSCI.2115-04.2004.
22. Kermen, F., M. Midroit, N. Kuczewski, J. Forest, M. Thévenet, J. Sacquet, C. Benetollo, M. Richard, A. Didier, and N. Mandairon. 2016. Topographical representation of odor hedonics in the olfactory bulb. Nat. Neurosci. 19:876-878. doi:10.1038/nn.4317.
23. Kleene, S.J. 1993. Origin of the chloride current in olfactory transduction. Neuron. 11:123-132. doi:10.1016/0896-6273(93)90276-W.
24. Kleene, S.J. 1997. High-gain, low-noise amplification in olfactory transduction. Biophys. J. 73:1110-1117. doi:10.1016/S0006-3495(97)78143-8.
25. Kleene, S.J. 2008. The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chem. Senses. 33:839-859. doi:10.1093/chemse/bjn048.
26. Kleene, S.J., and R.C. Gesteland. 1991. Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11:3624-3629.OpenUrlAbstract.
27. Kobayakawa, K., R. Kobayakawa, H. Matsumoto, Y. Oka, T. Imai, M. Ikawa, M. Okabe, T. Ikeda, S. Itohara, T. Kikusui, et al. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature. 450:503-508. doi:10.1038/nature06281.
28. Krautwurst, D., K.W. Yau, and R.R. Reed. 1998. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 95:917-926. doi:10.1016/S0092-8674(00)81716-X.
29. 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. doi:10.1038/363071a0.
30. Lagostena, L., and A. Menini. 2003. Whole-cell recordings and photolysis of caged compounds in olfactory sensory neurons isolated from the mouse. Chem. Senses. 28:705-716. doi:10.1093/chemse/bjg063.
31. Lam, R.S., and P. Mombaerts. 2013. Odorant responsiveness of embryonic mouse olfactory sensory neurons expressing the odorant receptors S1 or MOR23. Eur. J. Neurosci. 38:2210-2217. doi:10.1111/ejn.12240.
32. 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 G13 is critical to olfaction. J. Neurosci. 33:7975-7984. doi:10.1523/JNEUROSCI.5563-12.2013.
33. Lodovichi, C., and L. Belluscio. 2012. Odorant receptors in the formation of the olfactory bulb circuitry. Physiology (Bethesda). 27:200-212. doi:10.1152/physiol.00015.2012.
34. Lorenzon, P., N. Redolfi, M.J. Podolsky, I. Zamparo, S.A. Franchi, G. Pietra, A. Boccaccio, A. Menini, V.N. Murthy, and C. Lodovichi. 2015. Circuit formation and function in the olfactory bulb of mice with reduced spontaneous afferent activity. J. Neurosci. 35:146-160. doi:10.1523/JNEUROSCI.0613-14.2015.
35. Lowe, G., and G.H. Gold. 1991. The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J. Physiol. 442:147-168. doi:10.1113/jphysiol.1991.sp018787.
36. Lowe, G., and G.H. Gold. 1993. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature. 366:283-286. doi:10.1038/366283a0.
37. Lowe, G., and G.H. Gold. 1995. Olfactory transduction is intrinsically noisy. Proc. Natl. Acad. Sci. USA. 92:7864-7868. doi:10.1073/pnas.92.17.7864.
38. Ma, M., W.R. Chen, and G.M. Shepherd. 1999. Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation. J. Neurosci. Methods. 92:31-40. doi:10.1016/S0165-0270(99)00089-8.
39. Mainland, J.D., J.N. Lundström, J. Reisert, and G. Lowe. 2014. From molecule to mind: an integrative perspective on odor intensity. Trends Neurosci. 37:443-454. doi:10.1016/j.tins.2014.05.005.
40. Matthews, H.R. 1999. A compact modular flow heater for the superfusion of mammalian cells. J. Physiol. 518:13P.
41. Maurya, D.K., and A. Menini. 2014. Developmental expression of the calcium-activated chloride channels TMEM16A and TMEM16B in the mouse olfactory epithelium. Dev. Neurobiol. 74:657-675. doi:10.1002/dneu.22159.
42. Mobley, A.S., A.M. Miller, R.C. Araneda, L.R. Maurer, F. Müller, and C.A. Greer. 2010. Hyperpolarization-activated cyclic nucleotide-gated channels in olfactory sensory neurons regulate axon extension and glomerular formation. J. Neurosci. 30:16498-16508. doi:10.1523/JNEUROSCI.4225-10.2010.
43. Nakamura, T., and G.H. Gold. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature. 325:442-444. doi:10.1038/325442a0.
44. Nakashima, A., H. Takeuchi, T. Imai, H. Saito, H. Kiyonari, T. Abe, M. Chen, L.S. Weinstein, C.R. Yu, D.R. Storm, et al. 2013b. Agonist-independent GPCR activity regulates anterior-posterior targeting of olfactory sensory neurons. Cell. 154:1314-1325. doi:10.1016/j.cell.2013.08.033.
45. Nakashima, N., T.M. Ishii, Y. Bessho, R. Kageyama, and H. Ohmori. 2013a. Hyperpolarisation-activated cyclic nucleotide-gated channels regulate the spontaneous firing rate of olfactory receptor neurons and affect glomerular formation in mice. J. Physiol. 591:1749-1769. doi:10.1113/jphysiol.2012.247361.
46. Nickell, W.T., N.K. Kleene, R.C. Gesteland, and S.J. Kleene. 2006. Neuronal chloride accumulation in olfactory epithelium of mice lacking NKCC1. J. Neurophysiol. 95:2003-2006. doi:10.1152/jn.00962.2005.
47. Nishizumi, H., and H. Sakano. 2015. Developmental regulation of neural map formation in the mouse olfactory system. Dev. Neurobiol. 75:594-607. doi:10.1002/dneu.22268.
48. Nunemaker, C.S., R.A. DeFazio, and S.M. Moenter. 2003. A targeted extracellular approach for recording long-term firing patterns of excitable cells: a practical guide. Biol. Proced. Online. 5:53-62. doi:10.1251/bpo46.
49. O'Connell, R.J., and M.M. Mozell. 1969. Quantitative stimulation of frog olfactory receptors. J. Neurophysiol. 32:51-63.
50. Pedemonte, N., and L.J.V. Galietta. 2014. Structure and function of TMEM16 proteins (anoctamins). Physiol. Rev. 94:419-459. doi:10.1152/physrev.00039.2011.
51. Pifferi, S., A. Boccaccio, and A. Menini. 2006. Cyclic nucleotide-gated ion channels in sensory transduction. FEBS Lett. 580:2853-2859. doi:10.1016/j.febslet.2006.03.086.
52. Pifferi, S., M. Dibattista, and A. Menini. 2009. TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch. 458:1023-1038. doi:10.1007/s00424-009-0684-9.
53. A. MeniniPifferi, S., A. Menini, and T. Kurahashi. 2010. Signal transduction in vertebrate olfactory cilia. In The Neurobiology of Olfaction. Frontiers in Neuroscience. First edition. A. Menini, editor. CRC Press, Boca Raton, FL. 203-224.
54. Pifferi, S., V. Cenedese, and A. Menini. 2012. Anoctamin 2/TMEM16B: a calcium-activated chloride channel in olfactory transduction. Exp. Physiol. 97:193-199. doi:10.1113/expphysiol.2011.058230.
55. Ponissery Saidu, S., M. Dibattista, H.R. Matthews, and J. Reisert. 2012. Odorant-induced responses recorded from olfactory receptor neurons using the suction pipette technique. J. Vis. Exp. (62):e3862.
56. Reisert, J. 2010. Origin of basal activity in mammalian olfactory receptor neurons. J. Gen. Physiol. 136:529-540. doi:10.1085/jgp.201010528.
57. Reisert, J., and H.R. Matthews. 1999. Adaptation of the odour-induced response in frog olfactory receptor cells. J. Physiol. 519:801-813. doi:10.1111/j.1469-7793.1999.0801n.x.
58. Reisert, J., and H.R. Matthews. 2001. Response properties of isolated mouse olfactory receptor cells. J. Physiol. 530:113-122. doi:10.1111/j.1469-7793.2001.0113m.x.
59. Reisert, J., P.J. Bauer, K.-W. Yau, and S. Frings. 2003. The Ca-activated Cl channel and its control in rat olfactory receptor neurons. J. Gen. Physiol. 122:349-364. doi:10.1085/jgp.200308888.
60. - response in mouse olfactory receptor neurons. Neuron. 45:553-561. doi:10.1016/j.neuron.2005.01.012.
61. Reisert, J., K.-W. Yau, and F.L. Margolis. 2007. Olfactory marker protein modulates the cAMP kinetics of the odour-induced response in cilia of mouse olfactory receptor neurons. J. Physiol. 585:731-740. doi:10.1113/jphysiol.2007.142471.
62. Reuter, D., K. Zierold, W.H. Schröder, and S. Frings. 1998. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ. J. Neurosci. 18:6623-6630.
63. Rospars, J.-P., P. Lánskỳ, A. Duchamp, and P. Duchamp-Viret. 2003. Relation between stimulus and response in frog olfactory receptor neurons in vivo. Eur. J. Neurosci. 18:1135-1154. doi:10.1046/j.1460-9568.2003.02766.x.
64. 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. doi:10.1113/jphysiol.2010.194407.
65. Savigner, A., P. Duchamp-Viret, X. Grosmaitre, M. Chaput, S. Garcia, M. Ma, and B. Palouzier-Paulignan. 2009. Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. J. Neurophysiol. 101:2898-2906. doi:10.1152/jn.91169.2008.
66. Schild, D., and D. Restrepo. 1998. Transduction mechanisms in vertebrate olfactory receptor cells. Physiol. Rev. 78:429-466.
67. Shimazaki, H., and S. Shinomoto. 2007. A method for selecting the bin size of a time histogram. Neural Comput. 19:1503-1527. doi:10.1162/neco.2007.19.6.1503.
68. 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. doi:10.1073/pnas.0903304106.
69. 2+ exchanger NCKX4 governs termination and adaptation of the mammalian olfactory response. Nat. Neurosci. 15:131-137. doi:10.1038/nn.2943.
70. Tan, J., A. Savigner, M. Ma, and M. Luo. 2010. Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron. 65:912-926. doi:10.1016/j.neuron.2010.02.011.
71. Trotier, D. 1994. Intensity coding in olfactory receptor cells. Semin. Cell Biol. 5:47-54. doi:10.1006/scel.1994.1007.
72. Trotier, D. 1998. Electrophysiological properties of frog olfactory supporting cells. Chem. Senses. 23:363-369. doi:10.1093/chemse/23.3.363.
73. Trotier, D., and P. MacLeod. 1983. Intracellular recordings from salamander olfactory receptor cells. Brain Res. 268:225-237. doi:10.1016/0006-8993(83)90488-2.
74. Vincis, R., O. Gschwend, K. Bhaukaurally, J. Beroud, and A. Carleton. 2012. Dense representation of natural odorants in the mouse olfactory bulb. Nat. Neurosci. 15:537-539. doi:10.1038/nn.3057.
75. Wachowiak, M., and L.B. Cohen. 2001. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron. 32:723-735. doi:10.1016/S0896-6273(01)00506-2.
76. Wang, H.C., C.-C. Lin, R. Cheung, Y. Zhang-Hooks, A. Agarwal, G. Ellis-Davies, J. Rock, and D.E. Bergles. 2015. Spontaneous activity of cochlear hair cells triggered by fluid secretion mechanism in adjacent support cells. Cell. 163:1348-1359. doi:10.1016/j.cell.2015.10.070.
77. Yu, C.R., J. Power, G. Barnea, S. O'Donnell, H.E.V. Brown, J. Osborne, R. Axel, and J.A. Gogos. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron. 42:553-566. doi:10.1016/S0896-6273(04)00224-7.
78. Zhainazarov, A.B., and B.W. Ache. 1995. Odor-induced currents in Xenopus olfactory receptor cells measured with perforated-patch recording. J. Neurophysiol. 74:479-483.
79. Zhao, H., L. Ivic, J.M. Otaki, M. Hashimoto, K. Mikoshiba, and S. Firestein. 1998. Functional expression of a mammalian odorant receptor. Science. 279:237-242. doi:10.1126/science.279.5348.237.
80. Zheng, C., P. Feinstein, T. Bozza, I. Rodriguez, and P. Mombaerts. 2000. Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron. 26:81-91. doi:10.1016/S0896-6273(00)81140-X.