Mammalian odorant receptors: functional evolution and variation

Jiang, Yue; Matsunami, Hiroaki

doi:10.1016/j.conb.2015.01.014

Cited by 34 publications

(25 citation statements)

References 54 publications

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“…2001; Zhang and Firestein 2002; Niimura et al. 2014; Jiang and Matsunami 2015). For T. urticae GRs, these dynamics may have been facilitated by their compact structure, i.e., few introns of small size, which may have facilitated pairing and nonallelic homologous recombination between duplicates to produce copy number variation (Hastings et al.…”

Section: Discussionmentioning

confidence: 99%

“…2013; Freeman et al. 2014; Benton 2015; Jiang and Matsunami 2015). In the well-studied vertebrate olfactory system, compounds are perceived by seven transmembrane (TM) domain metabotropic G-protein coupled receptors (GPCRs), with ligand binding initiating an intracellular signaling cascade that leads to the opening of ion channels (Nei et al.…”

Section: Introductionmentioning

confidence: 99%

“…In both vertebrates and insects CR evolution is highly dynamic (Tribolium Genome Sequencing Consortium et al. 2008; Jiang and Matsunami 2015; Zhou et al. 2015).…”

Section: Introductionmentioning

confidence: 99%

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Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore

Ngoc¹,

Greenhalgh²,

Dermauw³

et al. 2016

Genome Biol Evol

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While mechanisms to detoxify plant produced, anti-herbivore compounds have been associated with plant host use by herbivores, less is known about the role of chemosensory perception in their life histories. This is especially true for generalists, including chelicerate herbivores that evolved herbivory independently from the more studied insect lineages. To shed light on chemosensory perception in a generalist herbivore, we characterized the chemosensory receptors (CRs) of the chelicerate two-spotted spider mite, Tetranychus urticae, an extreme generalist. Strikingly, T. urticae has more CRs than reported in any other arthropod to date. Including pseudogenes, 689 gustatory receptors were identified, as were 136 degenerin/Epithelial Na+ Channels (ENaCs) that have also been implicated as CRs in insects. The genomic distribution of T. urticae gustatory receptors indicates recurring bursts of lineage-specific proliferations, with the extent of receptor clusters reminiscent of those observed in the CR-rich genomes of vertebrates or C. elegans. Although pseudogenization of many gustatory receptors within clusters suggests relaxed selection, a subset of receptors is expressed. Consistent with functions as CRs, the genomic distribution and expression of ENaCs in lineage-specific T. urticae expansions mirrors that observed for gustatory receptors. The expansion of ENaCs in T. urticae to > 3-fold that reported in other animals was unexpected, raising the possibility that ENaCs in T. urticae have been co-opted to fulfill a major role performed by unrelated CRs in other animals. More broadly, our findings suggest an elaborate role for chemosensory perception in generalist herbivores that are of key ecological and agricultural importance.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore

Ngoc¹,

Greenhalgh²,

Dermauw³

et al. 2016

Genome Biol Evol

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“…Identification of the odorant as the ligand leads us to hypothesize that CD36 could play a role in the control of actions for survival in mammals (e.g., food selection and territory defense) through its ability to detect specific odorants in the environment. In mammals, odorants are perceived via mechanisms mediated through G-protein-coupled receptors expressed by olfactory sensory neurons (i.e., olfactory receptors) (10), possibly in coordination with several species of lipocalin-like soluble proteins called odorant-binding proteins (25). We postulate that, like odorant-binding proteins (25), CD36 in the nasal cavity may have a role to play in capturing parisons of the inhibitory activities between Z,Z-TDD and E,Z,Z-TDT and between (Z,Z)-4,7-tridecadienoic and (E,Z,Z)-2,4,7-tridecatrienoic acids revealed a negative influence of C2-C3 double bonds or the E configuration at the bond on interactions with CD36.…”

Section: Investigation Of the Cd36 Ligand Activity Of Ezz-tdt Ezzmentioning

confidence: 99%

Identification of the odor-active volatile compound (Z,Z)-4,7-tridecadienal as a potential ligand for the transmembrane receptor CD36

et al. 2016

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Cluster of differentiation 36 (CD36) is a broadly expressed transmembrane protein that has multiple ligands, including oxidized low-density lipoproteins. We found recently that CD36 is expressed in olfactory sensory neurons and postulated that it plays a role in the detection of distinct odorants in the nasal cavity. To date, however, there have been few examples of attempts to identify CD36-recognizable odorants. In this study, by an in vitro assay using a peptide mimic of the receptor, we provided evidence that CD36 recognizes (Z,Z)-4,7-tridecadienal, an odor-active volatile compound that is known to occur in Katsuobushi (dried, fermented, and smoked skipjack tuna commonly used in Japanese cuisine as a seasoning) and in the preorbital secretion of male oribi. In addition, by comparing the data with those of its related compounds, we provided information on the structural requirements of (Z,Z)-4,7-tridecadienal for recognition by CD36. For instance, we showed that flexible rotation around the C2-C3 bond of the volatile may be of importance in gaining access to CD36. Identification of (Z,Z)-4,7-tridecadienal as the ligand prompts us to hypothesize that CD36 could participate in the control of distinct mammalian behaviors (e.g., food selection) through its ability to recognize specific odorants in the environment.

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“…These accidents can trigger a variety of changes, of innovations ranging from the alteration of protein identity to the modulation of transcriptional activity. In mammals, genes expressed in the olfactory system (more precisely, those coding for olfactory chemosensors) evolve very quickly, because unusual selective pressures act on this system (1)(2)(3). Thus, studying the dynamics of olfactory chemoreceptor diversity offers a unique opportunity to identify the molecular events at the origin of the genetic novelties that underlie evolutionary processes.…”

mentioning

confidence: 99%

Evolution of immune chemoreceptors into sensors of the outside world

Dietschi

Tuberosa

Rösingh

et al. 2017

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

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Changes in gene expression patterns represent an essential source of evolutionary innovation. A striking case of neofunctionalization is the acquisition of neuronal specificity by immune formyl peptide receptors (Fprs). In mammals, Fprs are expressed by immune cells, where they detect pathogenic and inflammatory chemical cues. In rodents, these receptors are also expressed by sensory neurons of the vomeronasal organ, an olfactory structure mediating innate avoidance behaviors. Here we show that two gene shuffling events led to two independent acquisitions of neuronal specificity by Fprs. The first event targeted the promoter of a V1R receptor gene. This was followed some 30 million years later by a second genomic accident targeting the promoter of a V2R gene. Finally, we show that expression of a vomeronasal Fpr can reverse back to the immune system under inflammatory conditions via the production of an intergenic transcript linking neuronal and immune Fpr genes. Thus, three hijackings of regulatory elements are sufficient to explain all aspects of the complex expression patterns acquired by a receptor family that switched from sensing pathogens inside the organism to sensing the outside world through the nose.olfaction | vomeronasal organ | olfactory receptor | gene evolution | neofunctionalization

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Mammalian odorant receptors: functional evolution and variation

Cited by 34 publications

References 54 publications

Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore

Complex Evolutionary Dynamics of Massively Expanded Chemosensory Receptor Families in an Extreme Generalist Chelicerate Herbivore

<b>Identification of the odor-active volatile compound (</b><i><b>Z</b></i><b>,</b><i><b>Z</b></i><b>)-4,7-tridecadienal as a potential ligand for the transmembrane receptor </b><b>CD36 </b>

Evolution of immune chemoreceptors into sensors of the outside world

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