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Volume 17, Number 8,
Issue of April 15, 1997
pp. 2703-2712
Copyright ©1997 Society for Neuroscience
Identification of a Long-Lasting Form of Odor Adaptation that
Depends on the Carbon Monoxide/cGMP SecondMessenger System
Received Dec. 2, 1996; revised Jan. 21, 1997; accepted Jan. 31, 1997.
Frank Zufall, and
Trese Leinders-Zufall
Section of Neurobiology, Yale University School of Medicine, New
Haven, Connecticut 06510
The diffusible messenger carbon monoxide (CO) has been proposed to
mediate endogenous cyclic guanosine 3 ,5-monophosphate (cGMP)
formation and sensory adaptation in vertebrate olfactory receptor
neurons (ORNs). We have identified and characterized a long-lasting
form of odor response adaptation (LLA) that operates at the level of
isolated salamander ORNs and does not require any interactions from
other cells. Manifestations of LLA are seen in reduced amplitude and
prolonged kinetics of the cAMP-mediated excitatory odor response and
the generation of a persistent current component that lasts for several
minutes and is attributable to cyclic nucleotide-gated (CNG) channel
activation by cGMP. Because these effects can be mimicked by micromolar
amounts of exogenous cGMP or CO, we applied various inhibitors of cGMP
formation. LLA is abolished selectively by heme oxygenase inhibitors
known to prevent CO release and cGMP formation in ORNs, whereas odor
excitation remains unaffected. In contrast, blockers of nitric oxide
synthase are unable to eliminate LLA. Several controls rule out a
contribution of nonspecific actions to the effects of CO inhibitors.
The results indicate that endogenous CO/cGMP signals contribute to
olfactory adaptation and underlie the control of gain and sensitivity
of odor transduction. The findings offer a mechanism by which a single, brief odor stimulus can be translated into long-lasting intracellular changes that could play an important role in the perceptual adaptation to odors, and explain the longstanding puzzle that the olfactory CNG
channels can be gated by both cAMP and cGMP.
Key words:
olfactory receptor neuron;
cyclic nucleotide-gated
channel;
carbon monoxide;
nitric oxide;
cAMP;
cGMP;
salamander;
sensory
adaptation;
heme oxygenase inhibitors
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