Fast adaptation in mouse olfactory sensory neurons does not require the activity of phosphodiesterase

Journal of General Physiology

Volumn 128, Issue 2, 2006, Pages 171-184

  Boccaccio, Anna ^a   Lagostena, Laura ^a   Hagen, Volker ^b   Menini, Anna ^a  

^a SISSA   (Italy)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC NUCLEOTIDE; PHOSPHODIESTERASE;

ANIMAL EXPERIMENT; ARTICLE; ENZYME ACTIVITY; EUKARYOTIC FLAGELLUM; KINETICS; MOUSE; NONHUMAN; SENSORY NERVE; SMELLING;

1-METHYL-3-ISOBUTYLXANTHINE; 8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ADENINE; ADENYLATE CYCLASE; ANIMALS; CALCIUM; CHLORIDE CHANNELS; CHLORIDES; CILIA; CYCLIC AMP; ENZYME INHIBITORS; GLUCONATES; ION CHANNELS; KINETICS; LIGHT; MICE; MICE, INBRED BALB C; NEURONAL PLASTICITY; OLFACTORY RECEPTOR NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; PHOTOCHEMISTRY;

EID: 33746588661     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609555     Document Type: Article

References (62)

1. Balasubramanian, S., J.W. Lynch, and P.H. Barry. 1996. Calcium-dependent modulation of the agonist affinity of the mammalian olfactory cyclic nucleotide-gated channel by calmodulin and a novel endogenous factor. J. Membr. Biol. 152:13-23.
2. Beltman, J., D.E. Becker, E. Butt, G.S. Jensen, S.D. Rybalkin, B. Jastorff, and J.A. Beavo. 1995. Characterization of cyclic nucleotide phosphodiesterases with cyclic GMP analogs: topology of the catalytic domains. Mol. Pharmacol. 47:330-339.
3. Boekhoff, I., C. Kroner, and H. Breer. 1996. Calcium controls second-messenger signalling in olfactory cilia. Cell. Signal. 8:167-171.
4. Borisy, F.F., G.V. Ronnett, A.M. Cunningham, D. Juilfs, J. Beavo, and S.H. Snyder. 1992. Calcium/calmodulin-activated phosphodiesterase expressed in olfactory receptor neurons. J. Neurosci. 12:915-923.
5. Bradley, J., W. Bonigk, K.W. Yau, and S. Frings. 2004. Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nat. Neurosci. 7:705-710.
6. Bradley, J., J. Reisert, and S. Frings. 2005. Regulation of cyclic nucleotide-gated channels. Curr. Opin. Neurobiol. 15:343-349.
7. Bradley, J., D. Reuter, and S. Frings. 2001. Facilitation of calmodulin-mediated odor adaptation by cAMP-gated channel subunits. Science. 294:2176-2178.
8. Braumann, T., C. Erneux, G. Petridis, W.D. Stohrer, and B. Jastorff. 1986. Hydrolysis of cyclic nucleotides by a purified cGMP-stimulated phosphodiesterase: structural requirements for hydrolysis. Biochim. Biophys. Acta. 871:199-206.
9. Butt, E., J. Beltman, D.E. Becker, G.S. Jensen, S.D. Rybalkin, B. Jastorff, and J.A. Beavo. 1995. Characterization of cyclic nucleotide phosphodiesterases with cyclic AMP analogs: topology of the catalytic sites and comparison with other cyclic AMP-binding proteins. Mol. Pharmacol. 47:340-347.
10. Chen, C., T. Nakamura, and Y. Koutalos. 1999. Cyclic AMP diffusion coefficient in frog olfactory cilia. Biophys. J. 76:2861-2867.
11. Chen, S., A.P. Lane, R. Bock, T. Leinders-Zufall, and F. Zufall. 2000. Blocking adenylyl cyclase inhibits olfactory generator currents induced by "IP(3)-odors". J. Neurophysiol. 84:575-580.
12. 2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature. 368:545-548.
13. Dubin, A.E., and V.E. Dionne. 1994. Action potentials and chemosensitive conductances in the dendrites of olfactory neurons suggest new features for odor transduction. J. Gen. Physiol. 103:181-201.
14. Firestein, S. 2001. How the olfactory system makes sense of scents. Nature. 413:211-218.
15. Firestein, S., B. Darrow, and G.M. Shepherd. 1991a. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 6:825-835.
16. Firestein, S., F. Zufall, and G.M. Shepherd. 1991b. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J. Neurosci. 11:3565-3572.
17. - channels-homing in on an elusive channel species. Prog. Neurobiol. 60:247-289.
18. Guellaen, G., J.L. Mahu, P. Mavier, P. Berthelot, and J. Hanoune. 1977. RMI 12330 A, an inhibitor of adenylate cyclase in rat liver. Biochim. Biophys. Acta. 484:465-475.
19. Hagen, V., J. Bendig, S. Frings, T. Eckardt, S. Helm, D. Reuter, and U.B. Kaupp. 2001. Highly efficient and ultrafast phototriggers for cAMP and cGMP by using long-wavelength UV/Vis-activation. Angew. Chem. Int. Ed. Engl. 40:1045-1048.
20. Hagen, V., K. Benndorf, and U.B. Kaupp. 2005. Photochemical release of second messengers-caged cyclic nucleotides. In Dynamic Studies in Biology: Phototriggers, Photoswitches and Caged Biomolecules. M. Goeldner and R.S. Givens, editors. Wiley-VCH, Weinheim, Germany. 155-178.
21. Harris, D.N., M.M. Asaad, M.B. Phillips, H.J. Goldenberg, and M.J. Antonaccio. 1979. Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives. J. Cyclic Nucleotide Res. 5:125-134.
22. Jung, A., F.W. Lischka, J. Engel, and D. Schild. 1994. Sodium/calcium exchanger in olfactory receptor neurones of Xenopus laevis. Neuroreport. 5:1741-1744.
23. 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.
24. Kaupp, U.B., and R. Seifert. 2002. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82:769-824.
25. Kleene, S.J. 1993. Origin of the chloride current in olfactory transduction. Neuron. 11:123-132.
26. Kleene, S.J. 1995. Block by external calcium and magnesium of the cyclic-nucleotide-activated current in olfactory cilia. Neuroscience. 66:1001-1008.
27. Kleene, S.J. 1999. Both external and internal calcium reduce the sensitivity of the olfactory cyclic-nucleotide-gated channel to cAMP. J. Neurophysiol. 81:2675-2682.
28. Kleene, S.J., and R.C. Gesteland. 1991. Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11:3624-3629.
29. 2+ regulates the sensitivity of cyclic nucleotide-gated channels in olfactory receptor neurons. Neuron. 9:897-906.
30. Kurahashi, T., and A. Menini. 1997. Mechanism of odorant adaptation in the olfactory receptor cell. Nature. 385:725-729.
31. 2+-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res. 515:261-268.
32. 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.
33. 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.
34. Leinders-Zufall, T., C.A. Greer, G.M. Shepherd, and F. Zufall. 1998. Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18:5630-5639.
35. Lowe, G., and G.H. Gold. 1993a. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature. 366:283-286.
36. Lowe, G., and G.H. Gold. 1993b. Contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the salamander. J. Physiol. 462:175-196.
37. 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.
38. Ma, M., X. Grosmaitre, C.L. Iwema, H. Baker, C.A. Greer, and G.M. Shepherd. 2003. Olfactory signal transduction in the mouse septal organ. J. Neurosci. 23:317-324.
39. Matthews, H.R., and J. Reisert. 2003. Calcium, the two-faced messenger of olfactory transduction and adaptation. Curr. Opin. Neurobiol. 13:469-475.
40. Menini, A. 1999. Calcium signalling and regulation in olfactory neurons. Curr. Opin. Neurobiol. 9:419-426.
41. Menini, A., L. Lagostena, and A. Boccaccio. 2004. Olfaction: from odorant molecules to the olfactory cortex. News Physiol. Sci. 19:101-104.
42. 2+-calmodulin-dependent odor adaptation. Science. 294:2172-2175.
43. 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.
44. Pifferi, S., A. Boccaccio, and A. Menini. 2006. Cyclic nucleotide-gated ion channels in sensory transduction. FEBS Lett. DOI:10.1016/j.febslet.2006.03. 086.
45. Reidl, J., P. Borowski, A. Sensse, J. Starke, M. Zapotocky, and M. Eiswirth. 2006. Model of calcium oscillations due to negative feedback in olfactory cilia. Biophys. J. 90:1147-1155.
46. - response in mouse olfactory receptor neurons. Neuron. 45:553-561.
47. 2+ extrusion governs response recovery in frog olfactory receptor cells. J. Gen. Physiol. 112:529-535.
48. Reisert, J., and H.R. Matthews. 1999. Adaptation of the odour-induced response in frog olfactory receptor cells. J. Physiol. 519:801-813.
49. Reisert, J., and H.R. Matthews. 2001. Response properties of isolated mouse olfactory receptor cells. J. Physiol. 530:113-122.
50. 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. 122:349-363.
51. Reuter, D., K. Zierold, W.H. Schroder, and S. Frings. 1998. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ. J. Neurosci. 18:6623-6630.
52. Schild, D., and D. Restrepo. 1998. Transduction mechanisms in vertebrate olfactory receptor cells. Physiol. Rev. 78:429-466.
53. Takeuchi, H., and T. Kurahashi. 2002. Photolysis of caged cyclic AMP in the ciliary cytoplasm of the newt olfactory receptor cell. J. Physiol. 541:825-833.
54. Takeuchi, H., and T. Kurahashi. 2003. Identification of second messenger mediating signal transduction in the olfactory receptor cell. J. Gen. Physiol. 122:557-567.
55. Takeuchi, H., and T. Kurahashi. 2005. Mechanism of signal amplification in the olfactory sensory cilia. J. Neurosci. 25:11084-11091.
56. Torre, V., J.F. Ashmore, T.D. Lamb, and A. Menini. 1995. Transduction and adaptation in sensory receptor cells. J. Neurosci. 15:7757-7768.
57. Trudeau, M.C., and W.N. Zagotta. 2003. Calcium/calmodulin modulation of olfactory and rod cyclic nucleotide-gated ion channels. J. Biol. Chem. 278:18705-18708.
58. 2+ inhibition of type III adenylate cyclase in vivo. J. Biol. Chem. 270:21480-21486.
59. Wei, J., G. Wayman, and D.R. Storm. 1996. Phosphorylation and inhibition of type III adenylate cyclase by calmodulin-dependent protein kinase II in vivo. J. Biol. Chem. 271:24231-24235.
60. Wei, J., A.Z. Zhao, G.C. Chan, L.P. Baker, S. Impey, J.A. Beavo, and D.R. Storm. 1998. Phosphorylation and inhibition of olfactory adenylate cyclase by CaM kinase II in neurons: a mechanism for attenuation of olfactory signals. Neuron. 21:495-504.
61. Yan, C., A.Z. Zhao, J.K. Bentley, K. Loughney, K. Ferguson, and J.A. Beavo. 1995. Molecular cloning and characterization of a calmodulin-dependent phosphodiesterase enriched in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA. 92:9677-9681.
62. Zimmerman, A.L., G. Yamanaka, F. Eckstein, D.A. Baylor, and L. Stryer. 1985. Interaction of hydrolysis-resistant analogs of cyclic GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments. Proc. Natl. Acad. Sci. USA. 82:8813-8817.