Effects of cGMP and sodium nitroprusside on odor responses in
turtle olfactory sensory neurons
Kouhei
Inamura,
Makoto
Kashiwayanagi, and
Kenzo
Kurihara
Graduate School of Pharmaceutical Sciences, Hokkaido University,
Sapporo 060-0812, Japan
 |
ABSTRACT |
The effects of
cGMP and sodium nitroprusside (SNP) on odor responses in isolated
turtle olfactory neurons were examined. The inward current induced by
dialysis of a mixture of 1 mM cAMP and 1 mM cGMP was similar to that
induced by dialysis of 1 mM cAMP or 1 mM cGMP alone. After the neurons
were desensitized by the application of 1 mM cGMP, 3 mM
8-(4-chlorophenylthio)-cAMP, a membrane-permeable cAMP analog, did not
elicit any current, indicating that both cAMP and cGMP activated the
same channel. Extracellular application of SNP, a nitric oxide (NO)
donor, evoked inward currents in a dose-dependent manner. However,
application of SNP did not induce any currents after desensitization of
the cGMP-induced currents, suggesting that SNP-induced currents are
mediated via the cGMP-dependent pathway. Application of the
cAMP-producing odorants to the neurons induced a large inward current
even after neurons were desensitized to a high concentration of cGMP or
SNP. These results suggest that the transduction pathway independent of
cAMP, cGMP, and NO also contributes to the generation of odor responses
in addition to the cAMP-dependent pathway.
guanosine 3',5'-cyclic monophosphate; nitric oxide; olfactory transduction
 |
INTRODUCTION |
THE VERTEBRATE OLFACTORY system is able to distinguish
among a large number of odorants with diverse molecular structures and
to discriminate them. Olfactory responses are generally thought to be
generated via the cAMP- or inositol 1,4,5-trisphosphate (IP3)-mediated cascades; an
increase in second messenger concentration in olfactory cilia (2, 17)
causes opening of cyclic nucleotide-gated (CNG) channels (13) or
IP3-gated cation channels (15),
resulting in cell depolarization and the generation of action
potentials.
Stimulation of isolated rat olfactory cilia with relatively large
concentrations of odorants causes not only rapid and transient increases in cAMP or IP3
concentrations but also delayed and sustained increases in the
concentration of cGMP (3). The concentration of cGMP in the olfactory
cilia preparation is about 1/30th that of cAMP, but, in olfactory
sensory neurons, cGMP also activates the CNG channel. Because cGMP has
a higher affinity for the CNG channel than cAMP, the potential of cGMP
to act as an activator may equal that of cAMP. Application of sodium
nitroprusside (SNP), a nitric oxide (NO)-generating agent, to the rat
cilia preparation (3) also increases cGMP concentration by activation
of soluble guanylyl cyclase. Application of NO donors to
Xenopus laevis (12) and salamander
olfactory sensory neurons (5) evoked an inward current. These
observations suggest that, in addition to cAMP and
IP3, cGMP and NO play a functional
role in olfactory transduction (4).
The goal of this study is to ascertain whether cGMP and/or NO
function as second messengers in odor reception in turtle olfactory neurons. The results obtained suggest that both cGMP and SNP induce the
responses via a cAMP-dependent pathway.
 |
MATERIALS AND METHODS |
Isolation of olfactory cells.
Turtles, Geoclemys reevesii, weighing
150-300 g, were obtained from commercial suppliers. Isolated
olfactory neurons were prepared as described previously (9). Briefly,
the turtles were cooled to 0°C and decapitated. The epithelia were
quickly removed and, while in normal Ringer solution at 0°C, cut
into slices ~300 µm thick and then incubated for 0.5-2 h at
37°C in Ca2+-free Ringer
solution. Immediately before recordings were made, one slice of the
epithelium was placed in 500 µl of normal Ringer solution in the
recording chamber and shaken. No enzymes were added. Olfactory neurons
with motile cilia were used for this study.
Whole cell recordings.
Recordings were made with an Axopatch 1D amplifier (Axon Instruments,
Foster City, CA) using patch electrodes with resistance of 5-10
M
. Gigaohm seals were obtained by applying negative pressure (
30 to
100 cmH2O),
and the whole cell configuration was attained by application of
additional negative pressure. Holding potential was
70 mV. All
recordings were performed at room temperature. Analysis was carried out
on a personal computer using pCLAMP software (Axon Instruments). All
values are given as means ± SE. No corrections were made for
junction potentials at the pipette tip; junction potentials between the
solutions used in this paper never exceeded 7 mV. Three electrically
actuated valves were used to switch adapting Ringer solution and
odorant cocktail solutions, which were delivered from the stimulating
tube placed within ~500 µm from the cell.
Preparation of solutions and chemicals.
Normal Ringer solution contained (in mM) 116 NaCl, 4 KCl, 2 CaCl2, 2 MgCl2, 15 glucose, 5 sodium
pyruvate, and 10 HEPES-NaOH (pH 7.4). Patch pipettes were filled with
an internal solution consisting of (in mM) 115 KCl, 5 NaCl, 2 MgCl2, and 10 HEPES-KOH (pH 7.4).
Stocked IBMX solution was prepared by dissolution of IBMX in DMSO at
100 mM, and appropriate volumes were added to 1 mM cGMP solution. The
final concentration of DMSO never exceeded 0.4%. This concentration of
DMSO alone had no measurable effect on the electrical properties of the
neurons. SNP solutions were used within 2 h after mixing. The
cAMP-producing odorant cocktail consisted of 200 µM each of citralva,
hedione, eugenol, l-carvone, and
cineole, which increased cAMP concentration in the membrane preparation
of the turtle olfactory epithelium (14), without affecting
IP3 concentration in the rat cilia
preparation (2). All odorants were supplied by Takasago International
(Tokyo, Japan). SNP, cAMP, NaCN, and IBMX were obtained from Wako Pure
Chemical Industries (Osaka, Japan), and 8-(4-chlorophenylthio)
(CPT)-cAMP was obtained from Boehringer Mannheim (Mannheim, Germany).
 |
RESULTS |
Whole cell current induced by intracellular dialysis of cGMP.
First, the current induced by cGMP of varying concentrations dialyzed
into freshly isolated olfactory sensory neurons was recorded using the
whole cell voltage-clamped technique. When the pipette was filled with
a cGMP-free internal solution, the neurons held a steady baseline over
the test interval for ~5 min after membrane rupture. Intracellular
dialysis of cGMP into the cells immediately evoked inward currents
after membrane rupture in all cells examined (Fig.
1A).
The magnitude of inward current induced by cGMP increased with
increases in cGMP concentrations. Figure
1B shows the magnitude of the
responses induced by cGMP plotted as a function of cGMP concentration.
Data points were fitted by the Hill equation, giving concentration for
half-maximal activation
(K1/2) = 215 µM and a Hill coefficient
(n) of 1.3. The value of
K1/2 is different
from that obtained from excised inside-out patches (13) but is close to
that obtained from whole cell recordings (11). The currents appeared
between 0 and 0.1 mM, increased with an increase in cGMP
concentrations, and plateaued at 1 mM. The threshold concentration of
cGMP and the magnitude of current were similar to those reported with
isolated olfactory neurons of the newt (11).

View larger version (26K):
[in this window]
[in a new window]
|
Fig. 1.
Responses to cGMP dialyzed into turtle olfactory sensory neurons.
A: response induced by intracellular
dialysis of cGMP from the patch pipette to a turtle olfactory sensory
neuron. Concentrations of cGMP contained in the pipette are shown at
the top of each trace. Holding potential was 70 mV.
B: dose dependence of response induced
by intracellular application of cGMP into turtle olfactory sensory
neurons. Data were fitted by the Hill equation with
n = 1.3, concentration for
half-maximal activation
(K1/2) = 215 µM, and maximal current
(Imax) = 412 pA. Each point is mean ± SE of data obtained from
n preparations indicated in
parentheses. C: whole cell
current-voltage relationships for the current evoked by intracellular
application of 1 mM cGMP. Current was measured by applying a voltage
ramp (500 mV/s) from 120 to 80 mV during
(a) and after
(b) response induced by 1 mM cGMP.
Inset: record of the cGMP-induced
response of this cell under whole cell voltage-clamp condition at
70 mV. D: cGMP-induced
current was obtained by subtracting current after the response from
that obtained during the response in
C. Reversal potential was estimated to
be 2 mV.
|
|
As shown in Fig. 1C, the
current-voltage
(I-V)
relationship was examined by applying a voltage ramp from
120 to
+80 mV (500 mV/s) to voltage-clamped olfactory sensory neurons during
and after the response induced by 1 mM cGMP. The slope of the
I-V curve measured during the response was steeper than that measured after
the response, indicating that dialysis of cGMP increases the membrane
conductance. Figure 1D shows a
subtracted current before the response from that during the response.
The reversal potential for the response to cGMP was estimated to be
2 mV from the intersection of the line at 0 pA and the line
extrapolated in which no voltage-sensitive currents were activated. The
mean reversal potential was estimated to be 6.8 ± 1.7 mV
(n = 67), which was similar to the
potential for the response to cAMP in isolated turtle olfactory neurons
(17.0 ± 9.5 mV, n = 9;
Kashiwayanagi and Kurihara, unpublished observations) and isolated newt
olfactory neurons (11), as well as the potentials for the responses to cAMP and cGMP observed with patch membranes excised from the cilia of
the frog (13) and the olfactory knob of the frog and rat (7).
Characterization of cGMP and cAMP responses.
As shown above, the reversal potential of the response to cGMP is
closely similar to the response to cAMP. To confirm whether cAMP and
cGMP activate the same conductance, measurements were made of the
inward current induced by 3 mM CPT-cAMP, a membrane-permeable cAMP
analog, after the desensitization of the response to cGMP. That is,
after the response to 1 mM cGMP had decayed, 3 mM CPT-cAMP was applied
extracellularly, but no inward current was induced in any of the seven
neurons examined (Fig.
2B).
Figure 2A shows an inward current
induced by 3 mM CPT-cAMP applied extracellularly alone. Figure
2C plots the mean magnitudes of inward
currents induced by 3 mM CPT-cAMP after the decay of cGMP-induced
current as a function of cGMP concentration. The magnitude of the
response to CPT-cAMP after intracellular application of cGMP decreased with increasing cGMP concentration and reached zero after 1 mM cGMP. It
is possible that high phosphodiesterase activity in the cilia might
result in a concentration gradient along the cilia. To confirm whether
the CNG channels completely desensitized under dialysis of cGMP, we
added 0.5 mM IBMX, a nonspecific inhibitor of phosphodiesterase, to 1 mM cGMP to inhibit phosphodiesterase activity. The mean amplitude of
response was unchanged (395 ± 77 pA,
n = 10), indicating that the dialysis
of saturated concentration of cGMP alone was sufficient to fully
desensitize the CNG channels. These results are similar to those found
in a previous study on the effects of cAMP and CPT-cAMP on the CNG
channel in the turtle (10).

View larger version (26K):
[in this window]
[in a new window]
|
Fig. 2.
Characterization of cGMP and cAMP response.
A: inward current induced by 3 mM
8-(4-chlorophenylthio) (CPT)-cAMP applied extracellularly.
B: 1 mM cGMP was applied first from
the patch pipette and then 3 mM CPT-cAMP was applied extracellularly
after adaptation to cGMP. C: mean
amplitude of inward currents to 3 mM CPT-cAMP applied extracellularly
after the responses to varying concentrations of cGMP were desensitized
as a function of cGMP concentration. Data were fitted by the equation,
I = Imax + (Imin Imax) × [cGMP]n/([cGMP]n + Kn1/2)
with n = 3.7, K1/2 = 222 µM,
minimal current
(Imin) = 0 pA,
and Imax = 178 pA, where [cGMP] is cGMP concentration. Numbers in
parentheses are no. of tested cells.
D: mean amplitude of inward currents
induced by 1 mM cAMP, 1 mM cGMP, and a mixture of 1 mM cAMP and 1 mM
cGMP. Numbers in parentheses are no. of tested cells.
|
|
Saturation was observed when the concentration of either cGMP (Fig.
1B) or cAMP (10) was 1 mM. If the
responses to cAMP and cGMP are mediated via different CNG channels
and/or the Ca2+-activated
Cl
channel contributes to
the response to cAMP in a different way from that to cGMP, the response
to simultaneous application of cAMP and cGMP should increase
additively. Figure 2D shows the response obtained when an internal solution containing both 1 mM cAMP
and 1 mM cGMP was dialyzed into the neurons. The mean amplitude of the
response was 362 ± 33 pA (n = 16),
which was similar to that induced by intracellular dialysis of 1 mM
cAMP or 1 mM cGMP alone. These results suggest that both cAMP and cGMP activate the same channel in turtle olfactory sensory neurons.
Large odor responses after complete desensitization of the
cGMP-mediated cascade.
As in a previous study, in which the responses to odorants occurred
even after desensitization of the cAMP-dependent transduction pathway
in the turtle olfactory system (8, 10), here the application of an
odorant cocktail elicited an inward current after the complete
desensitization of cGMP-induced response by intracellular dialysis of 1 mM cGMP (Fig.
3A). The
mean amplitudes of inward currents in response to the odorant cocktail
when the patch pipette contained no cGMP, 1 mM cGMP, and 2 mM cGMP were 30.4 ± 14.7 pA (n = 32), 20.0 ± 10.3 pA (n = 14), and 14.7 ± 8.9 pA (n = 9), respectively (Fig.
3B). In addition, the odor response was evoked after the desensitization of the response to 1 mM cGMP + 0.5 mM IBMX (48.0 ± 33.4 pA, n = 6).
These results together with the previous ones suggest that odorants
induced large responses even after complete desensitization of cGMP-
and/or cAMP-mediated cascade in turtle olfactory sensory
neurons.

View larger version (14K):
[in this window]
[in a new window]
|
Fig. 3.
Odor response evoked after desensitization of cGMP-dependent pathway.
A: inward current in response to
odorant cocktail after desensitization of the response to 1 mM cGMP.
B: mean amplitude of odor responses
when the patch pipettes contained no cGMP (control), 1 mM cGMP, and 2 mM cGMP. Test stimuli are not significantly different from control
level when data were analyzed by
t-test
(P > 0.2). Numbers in parentheses
are no. of tested cells.
|
|
SNP-evoked inward currents.
Extracellular application of 10 mM SNP induced an inward current that
was observed in 20 of 27 neurons (Fig.
4A). The
amplitude of the inward current varied from 0 to 276 pA with a mean
magnitude of 50.2 ± 12.2 pA (n = 27), and the inward currents were desensitized to spontaneous levels.
The time-to-peak for the response to 10 mM SNP was 43.1 ± 4.5 s
(n = 20). This time was slower than
that for 1 mM cGMP-induced response (3.4 ± 0.3 s,
n = 52) but similar to that for the
response to 3 mM CPT-cAMP (60.8 ± 8.3 s,
n = 8). Long-lasting response to SNP
and CPT-cAMP may be due to extracellular application. Ten millimolar
SNP, which had been voided by exposure to light for 2 days, showed only
a small inward current in any of the seven neurons tested (6.3 ± 3.2 pA). SNP often generates an active by-product, cyanide. However, 10 mM cyanide solution did not elicit a large inward current (1.5 ± 0.6 pA, n = 8). These results suggest
that the response to SNP was not generated by cyanide. Figure
4B shows a dose-response relation of
SNP-stimulated inward currents. The response appeared at 10 µM and
increased with increasing SNP concentration. The maximal current
induced by SNP when saturation occurred was ~50 pA. To characterize
further the SNP-stimulated currents, the voltage-dependence of 10 mM
SNP-induced currents was examined by applying a voltage ramp to
voltage-clamped neurons before, during, and after the response (Fig.
4C). Figure 4D shows subtraction of current before
the response from one at the peak of the response. The mean reversal
potential was estimated to be 31.9 ± 6.6 mV
(n = 17), which was more positive than
the potential observed with cGMP (6.8 ± 1.7 mV) and that with cAMP (17.0 ± 9.5 mV; Kashiwayanagi and Kurihara, unpublished
observations) but not statistically significant
(P > 0.2;
t-test).

View larger version (26K):
[in this window]
[in a new window]
|
Fig. 4.
Responses to sodium nitroprusside (SNP) applied to turtle olfactory
sensory neurons. A: response induced
by extracellular application of 10 mM SNP to a turtle olfactory sensory
neuron. Holding potential was 70 mV.
B: dose dependence of response induced
by SNP. Data were fitted by the Hill equation with
n = 2.0, K1/2 = 30.3 µM,
and Imax = 51.7 pA. Each point is mean ± SE of data obtained from
n preparations indicated in
parentheses. C: whole cell
current-voltage relationships for current evoked by extracellular
application of 10 mM SNP in A. Current
was measured by applying a voltage ramp (500 mV/s) from 120 to
80 mV before (a), during
(b), and after
(c) the response induced by 10 mM
SNP. D: SNP-induced current was
obtained by subtracting current before the response from that obtained
during the response in C. Reversal
potential was estimated to be 26 mV.
|
|
After the cGMP-dependent pathway was desensitized by
intracellular dialysis of 1 mM cGMP, the response to 10 mM SNP was
measured (Fig.
5A).
Application of 10 mM SNP induced only a small response, 2.8 ± 1.5 pA (n = 14) (Fig.
5B), suggesting that the SNP-induced response was mediated via the CNG channel.

View larger version (12K):
[in this window]
[in a new window]
|
Fig. 5.
Effects of SNP on cGMP-dependent pathway.
A: inward current in response to 10 mM
SNP after desensitization of the response to 1 mM cGMP.
B: mean amplitude of SNP-induced
responses when patch pipettes contained no cGMP (control) and 1 mM
cGMP. Test stimulation is significantly different from control level
when data were analyzed by the t-test
(*** P < 0.001). Numbers in
parentheses are no. of tested cells.
|
|
Effects of SNP on odor response.
Finally, we examined whether NO contributes to the generation of odor
response. Even after the neurons were desensitized by the extracellular
application of 1 mM SNP, the odorant cocktail elicited a large odor
response (Fig. 6,
A and
B). The mean magnitude of inward
currents evoked by the odorant cocktail after desensitization to SNP
was 47.7 ± 16.6 pA (n = 14). This value was not statistically different from that of the
control response, 30.4 ± 14.7 pA
(P > 0.2). These results suggest
that the NO-dependent pathway did not significantly contribute to odor
responses in turtle olfactory sensory neurons.

View larger version (12K):
[in this window]
[in a new window]
|
Fig. 6.
Odor response evoked after desensitization of nitric oxide-dependent
pathway. A: inward current in response
to the odorant cocktail after desensitization of the response to 1 mM
SNP. B: mean amplitude of odor
responses after complete desensitization of the response to 1 mM SNP
and before application of 1 mM SNP (control). Test stimulation is not
significantly different from control level when data were analyzed by
the t-test
(P > 0.2). Numbers in parentheses
are no. of tested cells.
|
|
 |
DISCUSSION |
It is generally thought that the olfactory response is generated by the
cascade reactions in which cAMP is a second messenger for most of the
odorants. We previously found that a cAMP-independent pathway also
existed in turtle olfactory sensory neurons; odor responses occurred
even after the complete desensitization of the cAMP-dependent pathway
caused by intracellular dialysis of high concentrations of cAMP into
the turtle olfactory sensory neurons (10).
It is possible that an NO/cGMP-cascade is responsible for the
cAMP-independent pathways in the odor reception. Stimulation of
isolated rat olfactory cilia with relatively large concentrations of
odorants caused an increase in cGMP concentration as well as an
increase in cAMP concentration (3). Although immunoreactivity with
neuronal NO synthase antibody was not found in mature rat olfactory
neurons (1, 16), specific staining for NADPH diaphorase in mature
olfactory neurons in rat and catfish olfactory epithelia (6) suggests
the presence of NO synthase in the neurons. Although the existence of
NO synthase in mature olfactory neurons remained unclear, Breer et al.
(3) showed that application of odorants increased cGMP concentration
mediated via NO in the rat cilia preparation. As shown in the present
study, application of SNP to the turtle olfactory sensory neurons
induced inward currents, which in turn were caused by an increase in
cGMP concentration. These data suggest the possibility of
NO/cGMP-cascade present in the cAMP-independent pathways.
The following results, however, suggested that SNP-induced currents are
generated via the cyclic nucleotide-dependent pathway. After the
response to intracellular dialysis of cGMP was desensitized, the
response to CPT-cAMP applied extracellularly decreased with increasing
cGMP concentration in the pipette, and no response to CPT-cAMP appeared
when the cGMP response reached the saturated level. The mean amplitude
of the response induced by simultaneous dialysis of cAMP and cGMP at 1 mM each was similar to that induced by dialysis of 1 mM cAMP or cGMP
alone. The reversal potential of the cGMP response was similar to that
of the cAMP response. These results suggest that both cAMP and cGMP
activate the same channel in turtle olfactory sensory neurons. On the
other hand, it is reported that NO directly activated the CNG channels
by modification of sulfhydryl groups and elicited an inward current (5). Hence, NO may activate the CNG channels by modification of
channels in the turtle olfactory neurons, or NO may indirectly activate
the CNG channels via cGMP production. The response to 10 mM SNP after
the desensitization of the response to 1 mM cGMP was very small,
suggesting that SNP-induced inward currents are mediated via the CNG
channel. Thus it appears that the NO/cGMP-cascade is mediated via
activation of the CNG channel.
The present studies demonstrate that large odor responses are elicited
even after complete desensitization of the NO- and/or cGMP-dependent pathways achieved by application of high concentrations of cGMP or SNP. As described above, odorants induced the responses after the complete desensitization of the cAMP-dependent pathway. These
results suggest that cAMP-, cGMP-, and NO-independent pathways also
contribute to the generation of odor response in the turtle in addition
to the cAMP-dependent pathway.
 |
ACKNOWLEDGEMENTS |
We express our gratitude to Takasago International for supplying highly
pure odorants. This work was supported by a Grant-in-Aid for Scientific
Research from the Ministry of Education, Science, and Culture, Japan,
and by a grant from the Human Frontier Science Program.
 |
FOOTNOTES |
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address reprint requests to M. Kashiwayanagi.
Received 27 January 1998; accepted in final form 10 July 1998.
 |
REFERENCES |
1.
Bredt, D. S.,
and
S. H. Snyder.
Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium.
Neuron
13:
301-313,
1994[Medline].
2.
Breer, H.,
and
I. Boekhoff.
Odorants of the same odor class activate different second messenger pathways.
Chem. Senses
16:
19-29,
1991.
3.
Breer, H.,
T. Klemm,
and
I. Boekhoff.
Nitric oxide mediated formation of cyclic GMP in the olfactory system.
Neuroreport
3:
1030-1032,
1992[Medline].
4.
Breer, H.,
and
G. M. Shepherd.
Implications of the NO/cGMP system for olfaction.
Trends Neurosci.
16:
5-9,
1993[Medline].
5.
Broillet, M. C.,
and
S. Firestein.
Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds.
Neuron
16:
377-385,
1996[Medline].
6.
Dellacorte, C.,
D. L. Kalinoski,
T. Huque,
L. Wysocki,
and
D. Restrepo.
NADPH diaphorase staining suggests localization of nitric oxide synthase within mature vertebrate olfactory neurons.
Neuroscience
66:
215-225,
1995[Medline].
7.
Frings, S.,
J. W. Lynch,
and
B. Lindemann.
Properties of cyclic nucleotide-gated channels mediating olfactory transduction: activation, selectivity, and blockage.
J. Gen. Physiol.
100:
45-67,
1992[Abstract].
8.
Kashiwayanagi, M.,
H. Kawahara,
T. Hanada,
and
K. Kurihara.
A large contribution of a cyclic AMP-independent pathway to turtle olfactory transduction.
J. Gen. Physiol.
103:
957-974,
1994[Abstract].
9.
Kashiwayanagi, M.,
and
K. Kurihara.
Odor discrimination in single turtle olfactory receptor neuron.
Neurosci. Lett.
170:
233-236,
1994[Medline].
10.
Kashiwayanagi, M.,
and
K. Kurihara.
Odor responses after complete desensitization of the cAMP-dependent pathway in turtle olfactory cells.
Neurosci. Lett.
193:
61-64,
1995[Medline].
11.
Kurahashi, T.
The response induced by intracellular cyclic AMP in isolated olfactory receptor cells of the newt.
J. Physiol. (Lond.)
430:
355-371,
1990[Abstract].
12.
Lischka, F. W.,
and
D. Schild.
Effects of nitric oxide upon olfactory receptor neurons in Xenopus laevis.
Neuroreport
4:
582-584,
1993[Medline].
13.
Nakamura, T.,
and
G. H. Gold.
A cyclic nucleotide-gated conductance in olfactory receptor cilia.
Nature
325:
442-444,
1987[Medline].
14.
Okamoto, K.,
Y. Tokumitsu,
and
M. Kashiwayanagi.
Adenylyl cyclase activity in turtle vomeronasal and olfactory epithelium.
Biochem. Biophys. Res. Commun.
220:
98-101,
1996[Medline].
15.
Restrepo, D.,
T. Miyamoto,
B. P. Bryant,
and
J. H. Teeter.
Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish.
Science
249:
1166-1168,
1990[Medline].
16.
Roskams, A. J.,
D. S. Bredt,
T. M. Dawson,
and
G. V. Ronnett.
Nitric oxide mediates the formation of synaptic connections in developing and regenerating olfactory receptor neurons.
Neuron
13:
289-299,
1994[Medline].
17.
Sklar, P. B.,
R. R. H. Anholt,
and
S. H. Snyder.
The odorant-sensitive adenylate cyclase of olfactory receptor cells: differential stimulation by distinct classes of odorants.
J. Biol. Chem.
261:
15538-15543,
1986[Abstract/Free Full Text].
Am J Physiol Cell Physiol 275(5):C1201-C1206
0002-9513/98 $5.00
Copyright © 1998 the American Physiological Society