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| Open AccessAsymmetric ephaptic inhibition between compartmentalized olfactory receptor neurons
In Drosophila antenna, an unusual non-synaptic form of lateral inhibition occurs between subtypes of compartmentalized olfactory receptor neurons (ORNs). Here, authors show that direct electrical (ephaptic) interactions mediate lateral inhibition between ORNs, with physically larger ORNs dominating ephaptic interactions.
- Ye Zhang
- , Tin Ki Tsang
- & Chih-Ying Su
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Article
| Open AccessOdor mixtures of opposing valence unveil inter-glomerular crosstalk in the Drosophila antennal lobe
Fruit flies need to appropriately respond to mixtures of attractive and repellent odors in their natural environment. Here, the authors propose that lateral inhibition between glomeruli activated by attractants or repulsive odors mediates the appropriate response.
- Ahmed A. M. Mohamed
- , Tom Retzke
- & Silke Sachse
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Article
| Open AccessHuman olfactory-auditory integration requires phase synchrony between sensory cortices
Humans integrate sensory cues across multiple modalities to guide behaviour. Here, the authors report long-range phase synchronization between auditory and olfactory cortices prior to odor arrival, in a task where sound cues predict odors.
- Guangyu Zhou
- , Gregory Lane
- & Christina Zelano
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Article
| Open AccessInverse resource allocation between vision and olfaction across the genus Drosophila
Neural architecture may be shaped by selection, but is likely also constrained by development. Here, Keesey and colleagues find an inverse relationship between allocation towards visual and olfactory sensory systems across the genus Drosophila, which may reflect a developmental trade-off.
- Ian W. Keesey
- , Veit Grabe
- & Bill S. Hansson
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Article
| Open AccessMesoscopic and microscopic imaging of sensory responses in the same animal
Neuronal activity leads to a local increase in blood flow and volume, a process termed hyperaemia. Here, the authors employ multiple imaging approaches of neuronal and vascular activity at varying resolution to delineate the spatiotemporal dynamics of neurovascular coupling evoked by odours in the olfactory bulb.
- Davide Boido
- , Ravi L. Rungta
- & Serge Charpak
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Article
| Open AccessContribution of individual olfactory receptors to odor-induced attractive or aversive behavior in mice
Recent evidence suggests that some olfactory receptor types (OR) may be indispensable to elicit certain innate odor-evoked behaviors. Here, the authors report that eliminating a single OR from the odor-activated ensemble leads to significant changes in odor perception and the evoked behavioral response.
- Nao Horio
- , Ken Murata
- & Kazushige Touhara
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Article
| Open AccessSex separation induces differences in the olfactory sensory receptor repertoires of male and female mice
Olfactory experience can alter the relative abundance of neurons expressing specific chemoreceptors. Here, the authors demonstrate that the distinct odor experiences of sex-separated male and female mice induce sex-specific differences in the abundance of neurons that detect sexually dimorphic odors.
- Carl van der Linden
- , Susanne Jakob
- & Stephen W. Santoro
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Article
| Open AccessOlfactory marker protein (OMP) regulates formation and refinement of the olfactory glomerular map
Olfactory marker protein (OMP) expressed in all olfactory sensory neurons (OSN) is required for proper signal transduction and odor discrimination. Here, the authors report that OMP deletion leads to formation of glomeruli with axons from heterogeneous OSNs due to local axonal mistargeting.
- Dinu F. Albeanu
- , Allison C. Provost
- & Venkatesh N. Murthy
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Article
| Open AccessPredicting natural language descriptions of mono-molecular odorants
It is now possible to predict what a chemical smells like based on its chemical structure, however to date, this has only been done for a small number of odor descriptors. Here, using natural-language semantic representations, the authors demonstrate prediction of a much wider range of descriptors.
- E. Darío Gutiérrez
- , Amit Dhurandhar
- & Guillermo A. Cecchi
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Article
| Open AccessHigh-resolution ultramicroscopy of the developing and adult nervous system in optically cleared Drosophila melanogaster
Optical aberrations due to pigments in the eye and cuticle have undermined the ability for high-resolution imaging of the intact Drosophila. Here, the authors report an improved tissue-clearing agent, light-sheet optics and a multi-view combining algorithm to overcome these limitations.
- Marko Pende
- , Klaus Becker
- & Hans-Ulrich Dodt
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Article
| Open AccessAn intrinsic association between olfactory identification and spatial memory in humans
Olfaction, the sense of smell, may have originally evolved to aid navigation in space, but there is no direct evidence of a link between olfaction and navigation in humans. Here the authors show that olfaction and spatial memory abilities are correlated and rely on similar brain regions in humans.
- Louisa Dahmani
- , Raihaan M. Patel
- & Véronique D. Bohbot
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Article
| Open AccessOlfactory receptor OR2AT4 regulates human hair growth
Increasing evidence suggest that olfactory receptors can carry additional functions besides olfaction. Here, Chéret et al. show that stimulation of the olfactory receptor ORT2A4 by the odorant Sandalore® stimulates growth of human scalp hair follicles ex vivo, suggesting the use of ORT2A4-targeting odorants as hair growth-promoting agents.
- Jérémy Chéret
- , Marta Bertolini
- & Ralf Paus
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| Open AccessDynamic contrast enhancement and flexible odor codes
Sensory stimuli are encountered in multiple ways necessitating a flexible and adaptive neural population code for identification. Here, the authors show that the dynamics of odor coding in the locust antennal lobe varies with stimulus context so as to enhance the target stimulus representation.
- Srinath Nizampatnam
- , Debajit Saha
- & Baranidharan Raman
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Article
| Open AccessSingle olfactory receptors set odor detection thresholds
Odorous chemicals broadly activate subsets of olfactory receptors in the nose, but how individual receptors contribute to behavioral sensitivity is not clear. Here, the authors demonstrate that detection thresholds in mice are set solely by the highest affinity receptor for a given odorant.
- Adam Dewan
- , Annika Cichy
- & Thomas Bozza
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Article
| Open AccessHippocampal projections to the anterior olfactory nucleus differentially convey spatiotemporal information during episodic odour memory
Hippocampus is necessary for integrating the context with sensory cues to retrieve memory for unique episodes. Here, the authors show that inhibiting topographically organized projections from hippocampus to the anterior olfactory nucleus independently impairs spatial and temporal odour memory recall.
- Afif J. Aqrabawi
- & Jun Chul Kim
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Article
| Open AccessOlfactory bulb acetylcholine release dishabituates odor responses and reinstates odor investigation
Habituation reduces neural responsiveness to prolonged irrelevant stimuli and dishabituation reverses these effects when a salient stimulus is encountered. Here the authors demonstrate that acetylcholine is involved in dishabituating odor responses in the mouse olfactory bulb.
- M. Cameron Ogg
- , Jordan M. Ross
- & Max L. Fletcher
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Article
| Open AccessSema7A/PlxnCl signaling triggers activity-dependent olfactory synapse formation
The molecular mechanisms underlying synapse formation in the olfactory bulb are not fully understood. Here the authors demonstrate that semaphorin 7A on olfactory sensory neurons, and its receptor plexin C1 expressed on mitral and tufted cells, is required for correct synapse formation.
- Nobuko Inoue
- , Hirofumi Nishizumi
- & Hitoshi Sakano
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Article
| Open AccessOlfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior
Nasal airflow and olfactory bulb activity are linked to oscillations in cortical areas. This study shows olfactory input and respiration are correlated with oscillation in the prefrontal cortex during freezing behavior in mice, and attenuation of olfactory inputs can increase behavioral freezing.
- Andrew H. Moberly
- , Mary Schreck
- & Minghong Ma
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Article
| Open AccessStimulus dependent diversity and stereotypy in the output of an olfactory functional unit
Mitral/tufted (MT) cells connect to a single glomerulus and receive inputs from sensory neurons expressing the same odorant receptor. Here the authors report that sister MT cells connected to the M72 glomerulus exhibit variable responses to most M72 ligands but respond in a reproducible and stereotyped way to a high-affinity M72 ligand.
- Ezequiel M. Arneodo
- , Kristina B. Penikis
- & Dmitry Rinberg
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| Open AccessLong-term optical brain imaging in live adult fruit flies
Time-lapse imaging studies of more than a day in the fly brain have been infeasible until now. Here the authors present a laser microsurgery approach to create a permanent window in the fly cuticle to enable time-lapse imaging of neural architecture and dynamics for up to 10–50 days.
- Cheng Huang
- , Jessica R. Maxey
- & Mark J. Schnitzer
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Article
| Open AccessAn olfactory virtual reality system for mice
Odor-guided spatial behaviours are difficult to study due to the challenge of controlling chemical concentrations in space and time. Here the authors present a precise odor delivery system to generate a olfactory virtual landscape that engages hippocampal place cells in mice.
- Brad A. Radvansky
- & Daniel A. Dombeck
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Article
| Open AccessArchitecture of a mammalian glomerular domain revealed by novel volume electroporation using nanoengineered microelectrodes
Microcircuit tracing reconstructions often rely on statistical labeling that may not detect all inputs and outputs of a microcircuit. Here the authors employ a novel electroporation approach to densely label neurons and demonstrate its ability to identify sparse anatomical features in the olfactory glomerulus.
- D. Schwarz
- , M. Kollo
- & A. T. Schaefer
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Article
| Open AccessA primacy code for odor identity
Odor identity remains stable despite changes in concentration yet the neural mechanisms are relatively unknown. Here the authors test a primacy coding model using an optogenetic masking paradigm in mice to show that a set of earliest activated receptors are sufficient to make decisions about odor identity across concentrations.
- Christopher D. Wilson
- , Gabriela O. Serrano
- & Dmitry Rinberg
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Article
| Open AccessOdor-evoked inhibition of olfactory sensory neurons drives olfactory perception in Drosophila
It is well established that odor-evoked excitation in olfactory sensory neurons (OSNs) encodes odor information. Here the authors report that odor-evoked inhibition in OSNs of Drosophila also encodes odor identity, and can in itself drive both attraction and avoidance behaviors.
- Li-Hui Cao
- , Dong Yang
- & Dong-Gen Luo
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Article
| Open AccessA long-range cis-regulatory element for class I odorant receptor genes
“Each olfactory sensory neuron expresses a single odorant receptor gene from either class I or class II genes. Here, the authors identify an enhancer for mouse class I genes, that is highly conserved, and regulates most class I genes expression by acting over ~ 3 megabases within the whole cluster.”
- Tetsuo Iwata
- , Yoshihito Niimura
- & Junji Hirota
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Article
| Open AccessLayer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb
Cholinergic neurons innervate multiple layers in the main olfactory bulb but the precise circuitry of this input is not known. Here the authors show that VGLUT3+ cholinergic neurons selectively innervate deep short axon cells in specific layers and elicit robust monosynaptic GABAergic and nicotinic postsynaptic currents.
- Daniel T. Case
- , Shawn D. Burton
- & Rebecca P. Seal
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Article
| Open AccessExtrinsic mechanical forces mediate retrograde axon extension in a developing neuronal circuit
How neuronal migration and axon growth coordinate during development is only partially understood. Here the authors use quantitative imaging to characterise the morphogenesis of the zebrafish olfactory placode and report an unexpected phenomenon, whereby axons extend through the passive movement of neuron cell bodies away from tethered axon tips.
- M. A. Breau
- , I. Bonnet
- & S. Schneider-Maunoury
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Article
| Open AccessSpecialized odorant receptors in social insects that detect cuticular hydrocarbon cues and candidate pheromones
Cuticular hydrocarbons (CHC) mediate the interactions between individuals in eusocial insects, but the sensory receptors for CHCs are unclear. Here the authors show that in ants such as H. saltator, the 9-exon subfamily of odorant receptors (HsOrs) responds to CHCs, and ectopic expression of HsOrs in Drosophila neurons imparts responsiveness to CHCs.
- Gregory M. Pask
- , Jesse D. Slone
- & Anandasankar Ray
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Article
| Open AccessNrp2 is sufficient to instruct circuit formation of mitral-cells to mediate odour-induced attractive social responses
Neuropilin 2 (Nrp2) is expressed by a subset of mitral cells in the postero-ventral olfactory bulb in mice. Here the authors show that Nrp2 is sufficient to instruct mitral cell targeting to the anterior part of medial amygdala that modulates olfactory-driven attractive social behaviour.
- Kasumi Inokuchi
- , Fumiaki Imamura
- & Hitoshi Sakano
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Article
| Open AccessMeasuring the olfactory bulb input-output transformation reveals a contribution to the perception of odorant concentration invariance
Humans and animals recognize an odorant across a range of odorant concentrations, but where in the olfactory processing pathway this invariance is generated is unclear. By measuring and comparing olfactory bulb outputs to inputs, the authors show that the olfactory bulb participates in generating the perception of odorant concentration invariance.
- Douglas A. Storace
- & Lawrence B. Cohen
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Article
| Open AccessImmobility responses are induced by photoactivation of single glomerular species responsive to fox odour TMT
The olfactory bulb is arranged in glomeruli defined by their olfactory receptor expression. The authors identify an olfactory receptor for fox odour, TMT, and show that activation of the glomerulus expressing that receptor in mice leads to immobility, but does not lead to other fear behaviours.
- Harumi Saito
- , Hirofumi Nishizumi
- & Hitoshi Sakano
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Article
| Open AccessFunctional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire
The range of odours that an insect can detect depends on its olfactory receptors. Here, the authors functionally characterize the olfactory receptor repertoire of the mothSpodoptera littoralis using the Drosophilaempty neuron system and reconstruct the evolution of these receptors in the Lepidoptera.
- Arthur de Fouchier
- , William B. Walker III
- & Emmanuelle Jacquin-Joly
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Article
| Open AccessEngaging and disengaging recurrent inhibition coincides with sensing and unsensing of a sensory stimulus
Sensory stimuli evoke temporally dynamic responses. Here the authors report that responses to odour onset and offset are orthogonally represented in the locust antennal lobe, differentially entrain oscillations, and propose a model in which they are necessary for initiation and termination of behaviour.
- Debajit Saha
- , Wensheng Sun
- & Baranidharan Raman
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Article
| Open AccessLamin B1 is required for mature neuron-specific gene expression during olfactory sensory neuron differentiation
Emerging evidence suggests that lamins regulate gene expression during cellular differentiation. Giganteet al. show that lamin B1 is necessary for the upregulation of mature neuron-specific genes during olfactory neuron differentiation, and its deficiency leads to attenuated olfactory neuron response to odour in mice.
- Crystal M. Gigante
- , Michele Dibattista
- & Haiqing Zhao
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Article
| Open AccessTop-down modulation of olfactory-guided behaviours by the anterior olfactory nucleus pars medialis and ventral hippocampus
The anterior olfactory nucleus pars medialis (mAON) provides cortical feedback to the olfactory bulb, but the behavioural relevance of these projections is unknown. Here, using opto- and chemogenetic approaches, the authors find the mAON bidirectionally modulates olfactory sensitivity and olfaction-dependent behaviours.
- Afif J. Aqrabawi
- , Caleb J. Browne
- & Jun Chul Kim
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| Open AccessOrganization of olfactory centres in the malaria mosquito Anopheles gambiae
Mosquitoes use olfactory cues to locate their host. Here, Riabinina et al. use genetic labelling of olfactory receptor neurons in the malaria vector Anopheles gambiaeto show that these neurons project to the antennal lobe, a known insect olfactory centre, and the subesophageal zone, a region previously linked to gustatory processing.
- Olena Riabinina
- , Darya Task
- & Christopher J. Potter
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Article
| Open AccessPrincipal cell activity induces spine relocation of adult-born interneurons in the olfactory bulb
The mechanism by which adult-born neurons quickly adjust olfactory bulb network functioning is not understood. Here the authors describe a novel form of structural plasticity in which mature spines relocate toward active mitral cell dendrite along spine head filopodia via AMPA and BDNF mediated signalling.
- Vincent Breton-Provencher
- , Karen Bakhshetyan
- & Armen Saghatelyan
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Article
| Open AccessMolecular signatures of neural connectivity in the olfactory cortex
The piriform cortex projects to multiple brain regions involved in diverse aspects of olfactory behavior but information about the organization of these outputs is lacking. Here the authors show that piriform neurons exhibit layer specific gene expression patterns that also define distinct projection targets.
- Assunta Diodato
- , Marion Ruinart de Brimont
- & Alexander Fleischmann
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Article
| Open AccessDisruption of Kcc2-dependent inhibition of olfactory bulb output neurons suggests its importance in odour discrimination
Synaptic inhibition in the olfactory bulb (OB) is believed to play a role in odour processing. Here, the authors use a Pcdh21-driven Cre-line to disrupt KCC2 expression in OB mitral cells and find altered synaptic connectivity along with disrupted separation of odour-induced activity patterns.
- Kathrin Gödde
- , Olivier Gschwend
- & Thomas J. Jentsch
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Article
| Open AccessFaecal bile acids are natural ligands of the mouse accessory olfactory system
The accessory olfactory system (AOS) processes social chemosensory information and guides behaviors that are important for survival and reproduction in mammals. Here the authors report that mouse feces are a source of AOS neuronal activity and identify unconjugated bile acids in feces as a class of natural AOS ligands.
- Wayne I. Doyle
- , Jordan A. Dinser
- & Julian P. Meeks
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Article
| Open AccessApplying medicinal chemistry strategies to understand odorant discrimination
Understanding the basis of odour perception and discrimination is a challenging task, due to the inherent complexity of the olfactory system. Here, the authors use a medicinal chemistry approach to derive biologically relevant rules for odorant classification.
- Erwan Poivet
- , Zita Peterlin
- & Stuart Firestein
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Article
| Open AccessRapid and continuous activity-dependent plasticity of olfactory sensory input
New olfactory sensory neurons (OSNs) wire into olfactory bulb circuits throughout life. Here, the authors show that newly generated OSNs form highly dynamics synapses and can elicit functional responses in OB neurons, while mature OSNs retain a high level of activity-dependent synaptic reorganisation.
- Claire E. J. Cheetham
- , Una Park
- & Leonardo Belluscio
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Article
| Open AccessDisinhibition of olfactory bulb granule cells accelerates odour discrimination in mice
How odour discrimination is influenced by granule cells in the olfactory bulb is poorly understood. Here, the authors show that disinhibition of granule cells in mice increases mitral cell inhibition and accelerates odour discrimination time, independent of odour similarity.
- Daniel Nunes
- & Thomas Kuner
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Article
| Open AccessCerebral complexity preceded enlarged brain size and reduced olfactory bulbs in Old World monkeys
The evolution of the brain in Old World monkeys (cercopithecoids) is poorly understood. Here the authors describe a complete endocast of Victoriapithecus, a 15 Myr old cercopithecoid, which shows that the brain size was much smaller and the olfactory bulbs much larger than in any extant catarrhine primate.
- Lauren A. Gonzales
- , Brenda R. Benefit
- & Fred Spoor
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Article
| Open AccessBehavioural correlates of combinatorial versus temporal features of odour codes
In the olfactory system, odourants typically evoke spiking responses in neurons that are both spatially and temporally structured. Here, the authors demonstrate that odour identity is encoded purely by the combinations of neurons activated and is insensitive to changes in temporal structure.
- Debajit Saha
- , Chao Li
- & Baranidharan Raman
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Muscarinic acetylcholine receptor M3 modulates odorant receptor activity via inhibition of β-arrestin-2 recruitment
Type three muscarinic acetylcholine receptors (M3-Rs) physically interact with olfactory receptors to potentiate odour-induced responses. Here, the authors demonstrate that acetylcholine potentiates odour-induced responses in olfactory sensory neurons via M3-R-mediated inhibition of β-arrestin-2 recruitment.
- Yue Jiang
- , Yun Rose Li
- & Hiroaki Matsunami
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In vivo odourant response properties of migrating adult-born neurons in the mouse olfactory bulb
Juxtaglomerular neurons (JGNs) of the mammalian olfactory bulb are generated throughout life, but when and how these adult-born cells acquire responsiveness to sensory stimuli remains unknown. Here, the authors use in vivotwo-photon imaging to monitor the migration and integration of adult-born JGNs and their sensory response properties.
- Yury Kovalchuk
- , Ryota Homma
- & Olga Garaschuk
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Article |
Amino acid coevolution reveals three-dimensional structure and functional domains of insect odorant receptors
The structure of insect odorant receptors (ORs) has remained elusive due to their lack of homology to other proteins and the inability to obtain OR crystals. Here, the authors use amino acid evolutionary covariation patterns to fold these proteins de novoand generate the first three-dimensional models of insect ORs.
- Thomas A. Hopf
- , Satoshi Morinaga
- & Richard Benton
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Article
| Open AccessDirect evidence for BBSome-associated intraflagellar transport reveals distinct properties of native mammalian cilia
Loss of olfactory function is one of the many symptoms of the ciliopathy Bardet–Biedl syndrome. Williams et al. show that Bardet–Biedl proteins are components of intraflagellar transport particles within cilia, and directly visualize their trafficking in native mammalian olfactory neurons.
- Corey L. Williams
- , Jeremy C. McIntyre
- & Jeffrey R. Martens