Odorant Receptor Map in the Mouse Olfactory Bulb: In Vivo Sensitivity and Specificity of Receptor-Defined Glomeruli

Oka, Yuki; Katada, Sayako; Omura, Masayo; Suwa, Makiko; Yoshihara, Yoshihiro; Touhara, Kazushige

doi:10.1016/j.neuron.2006.10.019

Cited by 173 publications

(207 citation statements)

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“…Receptor affinities can be much lower in heterologous systems than in vivo (28)(29)(30), where expression of receptors and signaling components are presumably optimized. Nevertheless, the threshold of cadaverine detection by TAAR13c of 3 μM is very similar to in vivo thresholds observed for the intact olfactory system (6,31) and to thresholds measured for isolated olfactory sensory neurons (2).…”

Section: Discussionmentioning

confidence: 99%

High-affinity olfactory receptor for the death-associated odor cadaverine

Hussain

Saraiva

Ferrero

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

172

234

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Carrion smell is strongly repugnant to humans and triggers distinct innate behaviors in many other species. This smell is mainly carried by two small aliphatic diamines, putrescine and cadaverine, which are generated by bacterial decarboxylation of the basic amino acids ornithine and lysine. Depending on the species, these diamines may also serve as feeding attractants, oviposition attractants, or social cues. Behavioral responses to diamines have not been investigated in zebrafish, a powerful model system for studying vertebrate olfaction. Furthermore, olfactory receptors that detect cadaverine and putrescine have not been identified in any species so far. Here, we show robust olfactory-mediated avoidance behavior of zebrafish to cadaverine and related diamines, and concomitant activation of sparse olfactory sensory neurons by these diamines. The large majority of neurons activated by low concentrations of cadaverine expresses a particular olfactory receptor, trace amineassociated receptor 13c (TAAR13c). Structure-activity analysis indicates TAAR13c to be a general diamine sensor, with pronounced selectivity for odd chains of medium length. This receptor can also be activated by decaying fish extracts, a physiologically relevant source of diamines. The identification of a sensitive zebrafish olfactory receptor for these diamines provides a molecular basis for studying neural circuits connecting sensation, perception, and innate behavior.Danio rerio | aversion | heterologous expression | polyamines C adaverine, putrescine, and other biogenic diamines are strongly repulsive odors to humans, for whom these odors presumably signal bacterial contamination. It may be expected that animal species feeding on carcasses attribute a more positive valence to diamines, and indeed both putrescine and cadaverine have been reported to be feeding attractants for rats (1) as well as goldfish (2). Similarly, insects depositing their eggs in carcasses or other proteineacous materials are attracted by these diamines (3). Beyond signaling danger or food, putrescine and cadaverine also serve as social cues in several vertebrate species, both for marking of territories-for example, in feline species (4)-and for burial of conspecifics (5).Very little is known about the molecular and cellular basis of cadaverine-driven behaviors. Cadaverine and putrescine evoke electrophysiological responses in the olfactory epithelium of two fish species (2, 6) and cadaverine-responsive olfactory sensory neurons and glomeruli have been identified in the mouse (7,8). However, chemosensory receptors that detect cadaverine or related diamines are unknown in any species, and could provide valuable tools to study how the olfactory system mediates innate aversion or attraction.Here, we show that cadaverine is a major product of zebrafish tissue decay, activates a zebrafish olfactory receptor (trace amineassociated receptor 13c, TAAR13c) with high affinity, and elicits a strong, low-threshold, and olfactory-mediated avoidance response in zebrafish. In vivo me...

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Section: Discussionmentioning

confidence: 99%

High-affinity olfactory receptor for the death-associated odor cadaverine

Hussain

Saraiva

Ferrero

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

172

234

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“…Recent studies, particularly at the receptor level, have included olfactory concentrationresponse relationships (Abaffy T et al, 2006;Jacquier V et al, 2006;Kajiya K et al, 2001;Katada S et al, 2005;Oka Y et al, 2006;Pelz D et al, 2006;Shirokova E et al, 2005). Table 3 summarizes their characteristics and those of the present work.…”

Section: Vapor Concentration Range Issuesmentioning

confidence: 99%

“…(Studies where the odorant is presented indirectly in the liquid phase -and, often, quantified only in such phase -but where the tested species actually samples the vapor above the liquid do not constitute liquid phase presentations.) Notably, experiments within the same study (Oka Y et al, 2006) have shown that whereas delivery of the odorant as a vapor still needs to reach μM concentrations when the response is measured at the cell level (e.g., HEK293 or isolated olfactory sensory neurons: OSNs), it only needs to reach nM concentrations when the response is measured at the glomerular level. Thus, responses measured beyond the individual cell level, be it at the olfactory bulb (mouse) (Oka Y et al, 2006), the antennal lobe (fly) (Pelz D et al, 2006), or the integrated olfactory system (human) (this study; Cain WS et al, 2007b;Cometto-Muñiz JE et al, 2004;Wise PM et al, 2007), produce EC 50 s at or below the nM range.…”

Section: Vapor Concentration Range Issuesmentioning

confidence: 99%

“…Notably, experiments within the same study (Oka Y et al, 2006) have shown that whereas delivery of the odorant as a vapor still needs to reach μM concentrations when the response is measured at the cell level (e.g., HEK293 or isolated olfactory sensory neurons: OSNs), it only needs to reach nM concentrations when the response is measured at the glomerular level. Thus, responses measured beyond the individual cell level, be it at the olfactory bulb (mouse) (Oka Y et al, 2006), the antennal lobe (fly) (Pelz D et al, 2006), or the integrated olfactory system (human) (this study; Cain WS et al, 2007b;Cometto-Muñiz JE et al, 2004;Wise PM et al, 2007), produce EC 50 s at or below the nM range. In terms of concentration span, the odorant response often rises from background to maximum within approximately two log units of concentration but this span can vary from one {e.g., (Kajiya K et al, 2001)} to three {e.g., (Abaffy T et al, 2006)} log units, irrespective of stimulus phase (liquid or vapor) or level at which the olfactory path is probed.…”

Section: Vapor Concentration Range Issuesmentioning

confidence: 99%

“…A main aim of these functions is to understand the physicochemical basis for the olfactory activity of vapors, and to define the chemical tuning characteristics of the sense of smell within various parts or as a whole. Recent examples of structure-activity studies exploring dose-response functions have included testing human Wise PM et al, 2007), mouse (Katada S et al, 2005;Oka Y et al, 2006), and fly (Pelz D et al, 2006;Stensmyr MC et al, 2003) olfactory responses at the receptor, cell, olfactory bulb or antennal/antennal lobe, and behavioral levels.…”

Section: Introductionmentioning

confidence: 99%

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Human olfactory detection of homologous n-alcohols measured via concentration–response functions

Cometto‐Muñiz

Abraham

2008

Pharmacology Biochemistry and Behavior

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We explored in humans concentration-detection functions for the odor of the homologous n-alcohols ethanol, 1-butanol, 1-hexanol, and 1-octanol. These functions serve to establish structure-activity relationships, and reflect the pharmacology of the olfactory sense at the behavioral level. We tested groups of 14 to 17 subjects (half of them females), averaging 31 to 35 years old. An 8-station vapor delivery device (VDD8) presented the stimulus under a three-alternative forced-choice procedure against carbon-filtered air. The VDD8 was built to meet the demands of typical human sniffs in a short-term (<5 sec) olfactory detection task, and to accurately control odorant generation, delivery, and stability. Actual stimulus concentration was quantified by gas chromatography before and during testing. The functions obtained were log normally distributed and were accurately modeled by a sigmoid (logistic) function, both at the group and at the individual level. Sensitivity to ethanol was the lowest and to 1-octanol the highest. Functions became steeper with increasing carbon chain length. For all alcohols the concentration detected halfway between chance and perfect detection (threshold) was at the ppb (or nM) level. Females were slightly more sensitive than males. Intersubject variability across participants was between one and two orders of magnitude. The present odor thresholds were lower than many reported in the past but their relative pattern across alcohols paralleled that in our earlier data and in compilation studies. A previously described quantitative structure-activity relationship for odor potency holds promise to model thresholds that, like those obtained here, best reflect the intrinsic sensitivity of human olfaction.

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The Mechanism of Olfaction

Sell¹

2014

Chemistry and the Sense of Smell

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Odorant Receptor Map in the Mouse Olfactory Bulb: In Vivo Sensitivity and Specificity of Receptor-Defined Glomeruli

Cited by 173 publications

References 51 publications

High-affinity olfactory receptor for the death-associated odor cadaverine

High-affinity olfactory receptor for the death-associated odor cadaverine

Human olfactory detection of homologous n-alcohols measured via concentration–response functions

The Mechanism of Olfaction

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