Amplification of odor-induced Ca2+ transients by store-operated Ca2+ release and its role in olfactory signal transduction

Journal of Neurophysiology

Volumn 83, Issue 1, 2000, Pages 501-512

  Zufall, Frank ^a   Leinders Zufall, Trese ^a,d   Greer, Charles A ^b,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b YALE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEINE; CALCIUM; RYANODINE; RYANODINE RECEPTOR; THAPSIGARGIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; DENDRITE; NONHUMAN; ODOR; OLFACTORY SYSTEM; PATCH CLAMP; PRIORITY JOURNAL; RECEPTOR POTENTIAL; SALAMANDER; SIGNAL TRANSDUCTION; VOLTAGE CLAMP;

EID: 0033985509     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.1.501     Document Type: Article

References (63)

1. ACHE, B. W. AND ZHAINAZAROV, A. Dual second messenger pathways in olfactory transduction. Curr. Opin. Neurobiol. 5: 461-466, 1995.
2. olf, are anosmic. Neuron 20: 69-81, 1998.
3. BERRIDGE, M. J. Neuronal calcium signaling. Neuron 21: 13-26, 1998.
4. BOEKHOFF, I., TAREILUS, E., STROTMANN, J., AND BREER, H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 9: 2453-2458, 1990.
5. BOZZA, T. C. AND KAUER, J. S. Odorant response properties of convergent olfactory receptor neurons. J. Neurosci. 18: 4560-4569, 1998.
6. BRUNET, L. J., GOLD, G. H., AND NGAI, J. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17: 681-693, 1996.
7. 2+ response amplitude and duration. Nature 386: 855-858, 1997.
8. DUCHAMP-VIRET, P., CHAPUT, M. A., AND DUCHAMP, A. Odor response properties of rat olfactory receptor neurons. Science 284: 2171-2174, 1999.
9. 2+ permeation in cyclic nucleotide-gated channels. EMBO J. 18: 131-144, 1999.
10. FIRESTEIN, S., DARROW, B., AND SHEPHERD, G. M. Activation of the sensory current in salamander olfactory receptor neurons depends on a G-protein mediated cAMP second messenger system. Neuron 6: 825-835, 1991a.
11. FIRESTEIN, S. AND WERBLIN, F. Gated currents in isolated olfactory receptor neurons of the larval tiger salamander. Proc. Natl. Acad. Sci. USA 84: 6292-6296, 1987.
12. FIRESTEIN, S., ZUFALL, F., AND SHEPHERD, G. M. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J. Neurosci. 11: 3565-3572, 1991b.
13. FRINGS, S., SEIFERT, R., GODDE, M., AND KAUPP, U. B. Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron 15: 169-179, 1995.
14. GARASCHUK, O., YAARI, Y., AND KONNERTH, A. Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones. J. Physiol. (Lond.) 502: 13-30, 1997.
15. HARDINGHAM, G. E., CHAWLA, S., JOHNSON, C. M., AND BADING, H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385: 260-265, 1997.
16. JUNG, A., LISCHKA, F. W., ENGEL, J., AND SCHILD, D. Sodium/calcium exchanger in olfactory receptor neurones of Xenopus laevis. NeuroReport 5: 1741-1744, 1994.
17. KAUER, J. S. Olfactory receptor cell staining using horseradish peroxidase. Anat. Rec. 200: 331-336, 1981
18. KLEENE, S. J. Origin of the chloride current in olfactory transduction. Neuron 11: 123-132, 1993.
19. KLEENE, S. J. AND GESTELAND, R. C. Calcium-activated chloride conductance in frog olfactory cilia. J. Neurosci. 11: 3624-3629, 1991.
20. 2+ release in peptidergic neurons of Aplysia californica. J. Physiol. (Lond.) 494: 627-639, 1996.
21. KRIZAJ, D. AND COPENHAGEN, D. R. Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 21: 249-256, 1998.
22. KURAHASHI, T. The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt. J. Physiol. (Lond.) 430: 355-371, 1990.
23. KURAHASHI, T. AND MENINI, A. Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385: 725-729, 1997.
24. KURAHASHI, T. AND YAU, K.-W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature 363: 71-74, 1993.
25. 2+/calmodulin kinase II. J. Neurosci. 19: RC19 (1-6), 1999.
26. LEINDERS-ZUFALL, T., RAND, M. N., SHEPHERD, G. M., GREER, C. A., AND ZUFALL, F. Calcium entry through cyclic nucleotide-gated channels in individual cilia of olfactory receptor cells: spatio-temporal dynamics. J. Neurosci. 17: 4136-4148, 1997.
27. LEINDERS-ZUFALL, T., SHEPHERD, G. M., GREER, C. A., AND ZUFALL, F. Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18: 5630-5639, 1998.
28. LEINDERS-ZUFALL, T., SHEPHERD, G. M., AND ZUFALL, F. Regulation of cyclic nucleotide-gated channels and membrane excitability in olfactory receptor cells by carbon monoxide. J. Neurophysiol. 74: 1498-1508, 1995.
29. 2+ spike frequency can optimize gene expression. Nature 392: 936-941, 1998.
30. LIU, M., CHEN, T.-Y., AHAMED, B., LI, J., AND YAU, K.-W. Calcium-calmodulin modulation of the olfactory cyclic nucleotide-gated cation channel. Science 266: 1348-1354, 1994.
31. 2+-ATPase in plasma membrane-rich preparations from olfactory epithelium of Atlantic salmon. Biochim. Biophys. Acta 1192: 153-158, 1994.
32. LOWE, G. AND GOLD, G. H. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature 366: 283-286, 1993.
33. MALNIC, B., HIRONO, J., SATO, T., AND BUCK, L. B. Combinatorial receptor codes for odors. Cell 96: 713-723, 1999.
34. MAUE, R. A. AND DIONNE, V. E. Patch-clamp studies of isolated mouse olfactory receptor neurons. J. Gen. Physiol. 90: 95-125, 1987.
35. MCPHERSON, P. S., KIM, Y. K., VALDIVIA, H., KNUDSON, C. M., TAKEKURA, H., FRANZINI-ARMSTRONG, C., CORONADO, R., AND CAMPBELL, K. P. The brain ryanodine receptor: a caffeine-sensitive calcium release channel. Neuron 7: 17-25, 1991.
36. MEECH, R. W. AND STANDEN, N. B. Potassium activation in Helix aspersa neurones under voltage-clamp: a component mediated by calcium influx. J. Physiol. (Lond.) 249: 211-239, 1975.
37. 2+ homeostasis. Prog. Neurobiol. 37: 255-285, 1991.
38. MORALES, B., MADRID, R., AND BACIGALUPO, J. Calcium mediates the activation of the inhibitory current induced by odorants in toad olfactory receptor neurons. FEBS Lett. 402: 259-264, 1997.
39. NOÉ, J., TAREILUS, E., BOEKHOFF, I., AND BREER, H. Sodium/calcium exchanger in rat olfactory neurons. Neurochem. Int. 30: 523-531, 1997.
40. PAREKH, A. B. AND PENNER, R. Store depletion and calcium influx. Physiol. Rev. 77: 901-930, 1997.
41. POZZAN, T., RIZZUTO, R., VOLPE, P., AND MELDOLESI, J. Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74: 595-636, 1994.
42. PUTNEY, J. W. A model for receptor-regulated calcium entry. Cell Calcium 7: 1-12, 1986.
43. RAWSON, N. E., GOMEZ, G., COWART, B., BRAND, J. G., LOWRY, L. D., PRIBITKIN, E. A., AND RESTREPO, D. Selectivity and response characteristics of human olfactory neurons. J. Neurophysiol. 77: 1606-1613, 1997.
44. REED, R. R. Signaling pathways in odorant detection. Neuron 8: 205-209, 1992.
45. 2+ extrusion governs response recovery in frog olfactory receptor cells. J. Gen. Physiol. 112: 529-535, 1998.
46. RESTREPO, D., TEETER, J. H., AND SCHILD, D. Second messenger signaling in olfactory transduction. J. Neurobiol. 30: 37-48, 1996.
47. REUTER, D., ZIEROLD, K., SCHRÖDER, W. H., AND FRINGS, S. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ. J. Neurosci. 18: 6623-6630, 1998.
48. RONNETT, G. V., CHO, H., HESTER, L. D., WOOD, S. F., AND SNYDER, S. H. Odorants differentially enhance phosphoinositide turnover and adenylyl cyclase in olfactory receptor neuronal cultures. J. Neurosci. 13: 1751-1758, 1993.
49. ROSSIER, M. F., PYTHON, C. P., BURNAY, M. M., SCHLEGEL, W., VALLOTTON, M. B., AND CAPPONI, A. M. Thapsigargin inhibits voltage-activated calcium channels in adrenal glomerulosa cells. Biochem. J. 296: 369-312, 1993.
50. SATO, T., HIRONO, J., TONOIKE, M., AND TAKEBAYSHI, M. Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. J. Neurophysiol. 72: 2980-2989, 1994.
51. i by activating two distinct current components in vertebrate olfactory cells. J. Neurophysiol. 73: 862-866, 1995.
52. 2+ channels. Neuroscience 65: 1109-1118, 1995.
53. SIMMONS, P. A., RAFOLS, J. A., AND GETCHELL, T. V. Ultrastructural changes in olfactory receptor neurons following olfactory nerve section. J. Comp. Neurol. 197: 237-257, 1981.
54. 2+ stores: activation and function. Trends Neurosci. 18: 299-306, 1995.
55. TAKECHI, H., EILERS, J., AND KONNERTH, A. A new class of synaptic responses involving calcium release in dendritic spines. Nature 396: 757-760, 1998.
56. TAREILUS, E., NOÉ, J., AND BREER, H. Calcium signals in olfactory neurons. Biochim. Biophys. Acta 1269: 129-138, 1995.
57. 2+ signalling: problems and pitfalls. Trends Pharmacol. Sci. 19: 370-375, 1998.
58. 2+-ATPase. Proc. Natl. Acad. Sci. USA 87: 2466-2470, 1990.
59. THOMAS, D. AND HANLEY, M. R. Pharmacological tools for pertubing intracellular calcium storage. Methods Cell Biol. 40: 65-89, 1994.
60. THOMAS, M. V. Voltage-clamp analysis of a calcium-mediated potassium conductance in cockroach (Periplaneta americana) central neurons. J. Physiol. (Lond.) 350: 159-178, 1984.
61. TOUHARA, K., SENGOKU, S., INAKI, K., TSUBOI, A., HIRONO, J., SATO, T., SAKANO, H., AND HAGA, T. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA 96: 4040-4045, 1999.
62. 2+-ATPase. Trends Pharmacol. Sci. 19: 131-135, 1998.
63. WEI, J., ZHAO, A. Z., CHAN, G.C.K., BAKER, L. P., IMPEY, S., BEAVO, J. A., AND STORM, D. R. Phosphorylation and inhibition of olfactory adenylyl cyclase by CaM kinase II in neurons: a mechanism for attenuation of olfactory signals. Neuron 21: 495-504, 1998.