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Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status.

ABSTRACT: Olfaction is a fundamental sense through which most animals perceive the external world. The olfactory system detects odors via specialized sensory organs such as the main olfactory epithelium and the vomeronasal organ. Sensory neurons in these organs use G-protein coupled receptors to detect chemosensory stimuli. The odorant receptor (OR) family is expressed in sensory neurons of the main olfactory epithelium, while the adult vomeronasal organ is thought to express other types of receptors.Here, we describe Olfr692, a member of the OR gene family identified by next-generation RNA sequencing, which is highly upregulated and non-canonically expressed in the vomeronasal organ. We show that neurons expressing this gene are activated by odors emanating from pups. Surprisingly, activity in Olfr692-positive cells is sexually dimorphic, being very low in females. Our results also show that juvenile odors activate a large number of Olfr692 vomeronasal neurons in virgin males, which is correlated with the display of infanticide behavior. . In contrast, activity substantially decreases in parenting males (fathers), where infanticidal aggressive behavior is not frequently observed.Our results describe, for the first time, a sensory neural population with a specific molecular identity involved in the detection of pup odors. Moreover, it is one of the first reports of a group of sensory neurons the activity of which is sexually dimorphic and depends on social status. Our data suggest that the Olfr692 population is involved in mediating pup-oriented behaviors in mice.

SUBMITTER: Nakahara TS

PROVIDER: S-EPMC4753656 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status.

Nakahara Thiago S TS Cardozo Leonardo M LM Ibarra-Soria Ximena X Bard Andrew D AD Carvalho Vinicius M A VM Trintinalia Guilherme Z GZ Logan Darren W DW Papes Fabio F

BMC biology 20160215

<h4>Background</h4>Olfaction is a fundamental sense through which most animals perceive the external world. The olfactory system detects odors via specialized sensory organs such as the main olfactory epithelium and the vomeronasal organ. Sensory neurons in these organs use G-protein coupled receptors to detect chemosensory stimuli. The odorant receptor (OR) family is expressed in sensory neurons of the main olfactory epithelium, while the adult vomeronasal organ is thought to express other type ...[more]

PMID: 26878847

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Project description:BackgroundIn teleost fishes that lack a vomeronasal organ, both main odorant receptors (ORs) and vomeronasal receptors family 2 (V2Rs) are expressed in the olfactory epithelium, and used for perception of water-soluble chemicals. In zebrafish, it is known that both ORs and V2Rs formed multigene families of about a hundred copies. Whereas the contribution of V2Rs in zebrafish to olfaction has been found to be substantially large, the composition and structure of the V2R gene family in other fishes are poorly known, compared with the OR gene family.ResultsTo understand the evolutionary dynamics of V2R genes in fishes, V2R sequences in zebrafish, medaka, fugu, and spotted green pufferfish were identified from their draft genome sequences. There were remarkable differences in the number of intact V2R genes in different species. Most V2R genes in these fishes were tightly clustered in one or two specific chromosomal regions. Phylogenetic analysis revealed that the fish V2R family could be subdivided into 16 subfamilies that had diverged before the separation of the four fishes. Genes in two subfamilies in zebrafish and another subfamily in medaka increased in their number independently, suggesting species-specific evolution in olfaction. Interestingly, the arrangements of V2R genes in the gene clusters were highly conserved among species in the subfamily level. A genomic region of tetrapods corresponding to the region in fishes that contains the V2R cluster was found to have no V2R gene in any species.ConclusionOur results have indicated that the evolutionary dynamics of fish V2Rs are characterized by rapid gene turnover and lineage-specific phylogenetic clustering. In addition, the present phylogenetic and comparative genome analyses have shown that the fish V2Rs have expanded after the divergence between teleost and tetrapod lineages. The present identification of the entire V2R repertoire in fishes would provide useful foundation to the future functional and evolutionary studies of fish V2R gene family.

Dataset Information

Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status.

Publications

Detection of pup odors by non-canonical adult vomeronasal neurons expressing an odorant receptor gene is influenced by sex and parenting status.

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