Abstract
1. Flash photolysis of caged cyclic nucleotides was used to examine the contribution of the ciliary cyclic nucleotide-gated conductance to olfactory transduction in the tiger salamander. Brief illumination of solitary olfactory receptor cells loaded with 100 microM caged cyclic AMP caused a large inward current (peak amplitude 355 +/- 200 pA; mean +/- S.D. for eleven cells) under whole-cell voltage clamp at -50 mV. 2. The photolysis response was initiated after a latency of 4-12 ms, whereas an odorant response of identical amplitude had a latency of several hundred milliseconds. The amplitudes of both responses exhibited almost identical voltage dependence between -50 and +25 mV, with both reversing near 0 mV. The time courses of the falling phases of odorant and photolysis responses also exhibited similar voltage dependence, both being prolonged at positive voltages. 3. Photolysis of caged cyclic GMP activated a current similar in amplitude and time course to that produced by photolysis of caged cyclic AMP. 4. When the flash was spatially limited to the cilia, the amplitude and duration of the photolysis response increased linearly with the length of the cilia illuminated (for cilia not longer than 30-40 microns) while the latency remained constant at 4-12 ms. The increase in duration was described semi-quantitatively by a model which incorporated diffusion and saturable hydrolysis of cyclic AMP. When the flash was limited to the soma or proximal dendrite, the response latency was proportional to the square of the distance between the illuminated region and the cilia. 5. Dialysis of cells with 500 microM cyclic AMP from a whole-cell electrode under voltage clamp activated a large transient inward current. Simultaneous suction electrode recording showed that this current originated almost entirely from the ciliary membrane. The density of cyclic nucleotide-gated channels was estimated to be 800-fold higher in the cilia than in the soma. 6. Summation of simultaneous odorant and photolysis responses was non-linear, the flash-induced current being enhanced during a small odorant response and attenuated during a large odorant response. Summation of two photolysis responses was similarly non-linear. The data were consistent with odorant stimuli and cyclic AMP both activating a common cyclic nucleotide-gated conductance with a Hill coefficient, n, of 2.0-4.4. For n = 2.5, the basal cyclic AMP concentration was estimated to be less than 20% of the K 1/2, which predicts a basal current of 5.8 pA, less than 2% of the maximum.(ABSTRACT TRUNCATED AT 400 WORDS)
Full text
PDF





















Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bakalyar H. A., Reed R. R. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science. 1990 Dec 7;250(4986):1403–1406. doi: 10.1126/science.2255909. [DOI] [PubMed] [Google Scholar]
- Boekhoff I., Tareilus E., Strotmann J., Breer H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 1990 Aug;9(8):2453–2458. doi: 10.1002/j.1460-2075.1990.tb07422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borisy F. F., Ronnett G. V., Cunningham A. M., Juilfs D., Beavo J., Snyder S. H. Calcium/calmodulin-activated phosphodiesterase expressed in olfactory receptor neurons. J Neurosci. 1992 Mar;12(3):915–923. doi: 10.1523/JNEUROSCI.12-03-00915.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boyle A. G., Park Y. S., Huque T., Bruch R. C. Properties of phospholipase C in isolated olfactory cilia from the channel catfish (Ictalurus punctatus). Comp Biochem Physiol B. 1987;88(3):767–775. doi: 10.1016/0305-0491(87)90242-2. [DOI] [PubMed] [Google Scholar]
- Firestein S., Darrow B., Shepherd G. M. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 1991 May;6(5):825–835. doi: 10.1016/0896-6273(91)90178-3. [DOI] [PubMed] [Google Scholar]
- Firestein S., Shepherd G. M., Werblin F. S. Time course of the membrane current underlying sensory transduction in salamander olfactory receptor neurones. J Physiol. 1990 Nov;430:135–158. doi: 10.1113/jphysiol.1990.sp018286. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Firestein S., Werblin F. Odor-induced membrane currents in vertebrate-olfactory receptor neurons. Science. 1989 Apr 7;244(4900):79–82. doi: 10.1126/science.2704991. [DOI] [PubMed] [Google Scholar]
- Firestein S., Zufall F., Shepherd G. M. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J Neurosci. 1991 Nov;11(11):3565–3572. doi: 10.1523/JNEUROSCI.11-11-03565.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frings S., Lindemann B. Current recording from sensory cilia of olfactory receptor cells in situ. I. The neuronal response to cyclic nucleotides. J Gen Physiol. 1991 Jan;97(1):1–16. doi: 10.1085/jgp.97.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones D. T., Reed R. R. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science. 1989 May 19;244(4906):790–795. doi: 10.1126/science.2499043. [DOI] [PubMed] [Google Scholar]
- Karpen J. W., Loney D. A., Baylor D. A. Cyclic GMP-activated channels of salamander retinal rods: spatial distribution and variation of responsiveness. J Physiol. 1992 Mar;448:257–274. doi: 10.1113/jphysiol.1992.sp019040. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karpen J. W., Zimmerman A. L., Stryer L., Baylor D. A. Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1287–1291. doi: 10.1073/pnas.85.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kolesnikov S. S., Zhainazarov A. B., Kosolapov A. V. Cyclic nucleotide-activated channels in the frog olfactory receptor plasma membrane. FEBS Lett. 1990 Jun 18;266(1-2):96–98. doi: 10.1016/0014-5793(90)81515-p. [DOI] [PubMed] [Google Scholar]
- Kurahashi T. Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt. J Physiol. 1989 Dec;419:177–192. doi: 10.1113/jphysiol.1989.sp017868. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kurahashi T., Kaneko A. High density cAMP-gated channels at the ciliary membrane in the olfactory receptor cell. Neuroreport. 1991 Jan;2(1):5–8. doi: 10.1097/00001756-199101000-00001. [DOI] [PubMed] [Google Scholar]
- Kurahashi T., Shibuya T. Ca2(+)-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res. 1990 May 7;515(1-2):261–268. doi: 10.1016/0006-8993(90)90605-b. [DOI] [PubMed] [Google Scholar]
- Kurahashi T. The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt. J Physiol. 1990 Nov;430:355–371. doi: 10.1113/jphysiol.1990.sp018295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowe G., Gold G. H. The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J Physiol. 1991 Oct;442:147–168. doi: 10.1113/jphysiol.1991.sp018787. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowe G., Nakamura T., Gold G. H. Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5641–5645. doi: 10.1073/pnas.86.14.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miyamoto T., Restrepo D., Cragoe E. J., Jr, Teeter J. H. IP3- and cAMP-induced responses in isolated olfactory receptor neurons from the channel catfish. J Membr Biol. 1992 May;127(3):173–183. doi: 10.1007/BF00231505. [DOI] [PubMed] [Google Scholar]
- Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
- Nerbonne J. M., Richard S., Nargeot J., Lester H. A. New photoactivatable cyclic nucleotides produce intracellular jumps in cyclic AMP and cyclic GMP concentrations. Nature. 1984 Jul 5;310(5972):74–76. doi: 10.1038/310074a0. [DOI] [PubMed] [Google Scholar]
- Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 1985 Jul 18;316(6025):255–258. doi: 10.1038/316255a0. [DOI] [PubMed] [Google Scholar]
- Restrepo D., Miyamoto T., Bryant B. P., Teeter J. H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science. 1990 Sep 7;249(4973):1166–1168. doi: 10.1126/science.2168580. [DOI] [PubMed] [Google Scholar]
- Shirley S. G., Robinson C. J., Dickinson K., Aujla R., Dodd G. H. Olfactory adenylate cyclase of the rat. Stimulation by odorants and inhibition by Ca2+. Biochem J. 1986 Dec 1;240(2):605–607. doi: 10.1042/bj2400605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sklar P. B., Anholt R. R., Snyder S. H. The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J Biol Chem. 1986 Nov 25;261(33):15538–15543. [PubMed] [Google Scholar]
- Tang J. M., Wang J., Quandt F. N., Eisenberg R. S. Perfusing pipettes. Pflugers Arch. 1990 May;416(3):347–350. doi: 10.1007/BF00392072. [DOI] [PubMed] [Google Scholar]
- Trotier D. A patch-clamp analysis of membrane currents in salamander olfactory receptor cells. Pflugers Arch. 1986 Dec;407(6):589–595. doi: 10.1007/BF00582636. [DOI] [PubMed] [Google Scholar]
- Zufall F., Firestein S., Shepherd G. M. Analysis of single cyclic nucleotide-gated channels in olfactory receptor cells. J Neurosci. 1991 Nov;11(11):3573–3580. doi: 10.1523/JNEUROSCI.11-11-03573.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
