Odorant-Dependent Generation of Nitric Oxide in Mammalian Olfactory Sensory Neurons

Daniela Brunert,Heike Benecke,Stefan Kurtenbach,Günter Gisselmann,Hanns Hatt,Wolfgang Schuhmann,Christian H Wetzel,Sonnur Isik,Huibert D Mansvelder

doi:10.1371/journal.pone.0005499

Daniela Brunert, Heike Benecke + Show 7 more

Open Access

https://doi.org/10.1371/journal.pone.0005499

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Journal: PloS one	Publication Date: May 11, 2009
Citations: 38	License type: CC BY 4.0

Affiliation: Ruhr University Bochum

Abstract

The gaseous signalling molecule nitric oxide (NO) is involved in various physiological processes including regulation of blood pressure, immunocytotoxicity and neurotransmission. In the mammalian olfactory bulb (OB), NO plays a role in the formation of olfactory memory evoked by pheromones as well as conventional odorants. While NO generated by the neuronal isoform of NO synthase (nNOS) regulates neurogenesis in the olfactory epithelium, NO has not been implicated in olfactory signal transduction. We now show the expression and function of the endothelial isoform of NO synthase (eNOS) in mature olfactory sensory neurons (OSNs) of adult mice. Using NO-sensitive micro electrodes, we show that stimulation liberates NO from isolated wild-type OSNs, but not from OSNs of eNOS deficient mice. Integrated electrophysiological recordings (electro-olfactograms or EOGs) from the olfactory epithelium of these mice show that NO plays a significant role in modulating adaptation. Evidence for the presence of eNOS in mature mammalian OSNs and its involvement in odorant adaptation implicates NO as an important new element involved in olfactory signal transduction. As a diffusible messenger, NO could also have additional functions related to cross adaptation, regeneration, and maintenance of MOE homeostasis.

Highlights

Nitric oxide (NO) is a small gaseous molecule that can diffuse through lipid membranes and plays important roles in various intra- and inter-cellular signalling processes [1]
In order to obtain an enriched population of olfactory sensory neurons (OSNs), we dissected the olfactory epithelium of homozygous OMP-GFP mice [10] expressing GFP under control of the promoter of the olfactory marker protein (OMP)
While endothelial NOS (eNOS) is expressed in central neurons of the olfactory system [17], we present the first evidence for its presence, functionality and possible physiological role in the main olfactory neuroepithelium (MOE)

Summary

Introduction

Nitric oxide (NO) is a small gaseous molecule that can diffuse through lipid membranes and plays important roles in various intra- and inter-cellular signalling processes [1]. NNOS functions in the embryonic development of the main olfactory neuroepithelium (MOE) but is down regulated shortly after birth [3]. INOS occurs only in the early embryonic MOE [4]. NOS isoforms, could not be detected in the MOE of mature rodents. Despite this lack of evidence for NO-synthase in mature OSNs several studies suggested that NO potentially modulates one or more elements of olfactory signal transduction [5,6,7,8,9]. We hypothesized that at least one NOS isoform, most likely eNOS, occurs in the MOE and attempted to show the presence, functionality and possible role of eNOS in the OE of adult mice

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