Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream

Gliem, Sebastian; Syed, Adnan S.; Sansone, Alfredo; Kludt, E; Tantalaki, Evangelia; Hassenklöver, Thomas; Korsching, Sigrun I.; Manzini, Ivan

doi:10.1007/s00018-012-1226-8

Cited by 50 publications

(169 citation statements)

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“…In larval MOE, amino acid responses have been shown to be mediated primarily by microvillous neurons, but to some extent also by forskolin-responsive (and forskolin-insensitive) ciliated neurons [7,10,16]. A small minority of both forskolin-and amino acid-responsive neurons is also observed in the middle cavity (this study), but not in the postmetamorphotic PC.…”

Section: Discussionmentioning

confidence: 46%

“…The MC contained amino acid-responsive as well as forskolin-responsive cells at all stages examined, similar to the larval MOE [10]. In contrast, the developing PC retains forskolin responses, but gradually loses all amino acid responses (Fig.…”

Section: Metamorphotic Transition Of Amino Acid Odor Sensitivity Frommentioning

confidence: 56%

“…Thus this subpopulation is dying out in the PC, but to some extent replaced during ontogenesis of the MC. Considering that forskolin-responsiveness is a hallmark of the adenylate cyclase signalling pathway characteristic for OR-expressing ciliated neurons and that OMP expression closely parallels forskolin-responsiveness ( [6,10], this study), it may be assumed that the forskolin-responsive neurons of the middle cavity represent ciliated neurons, whose ligands are to be found among water-borne odors, and may also include amino acids.…”

Section: Discussionmentioning

confidence: 99%

“…1 and [12,13]). At the same stages we concomitantly measured forskolin responses to visualize neurons that use a cAMPmediated signal transduction cascade and are presumably ciliated [10]. Amino acid odor-and forskolin-induced responses of ORNs were measured as somatic Ca 2+ transients in acute slice preparations of the epithelia of the MC and PC.…”

Section: Metamorphotic Transition Of Amino Acid Odor Sensitivity Frommentioning

confidence: 99%

“…Remarkably, ORNs activated by amino acids, a major odor group for fish and frogs [8][9][10][11], show a similar spatial distribution as the V2R and TRPC2 expression [6]. It may be expected that amino acid responses and possibly V2R expression do not remain unaltered during metamorphosis, as there appears to be no use for receptors to detect water-borne odorants such as amino acids in the air nose of an adult frog.…”

Section: Introductionmentioning

confidence: 99%

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Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

Syed

Sansone

Hassenklöver

et al. 2016

Cell. Mol. Life Sci.

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All olfactory receptors identified in teleost fish are expressed in a single sensory surface, whereas mammalian olfactory receptor gene families segregate into different olfactory organs, chief among them the main olfactory epithelium expressing ORs and TAARs, and the vomeronasal organ expressing V1Rs and V2Rs. A transitional stage is embodied by amphibians, with their vomeronasal organ expressing more 'modern', later diverging V2Rs, whereas more 'ancient', earlier diverging V2Rs are expressed in the main olfactory epithelium.During metamorphosis the main olfactory epithelium of Xenopus tadpoles transforms into an air-filled cavity (principal cavity, air nose), whereas a newly formed cavity (middle cavity) takes over the function of a water nose. We report here that larval expression of ancient V2Rs is gradually lost from the main olfactory epithelium as it transforms into the air nose.Concomitantly, ancient v2r gene expression begins to appear in the basal layers of the newly forming water nose. We observe the same transition for responses to amino acid odorants, consistent with the hypothesis that amino acid responses may be carried by V2R receptors.3

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Section: Discussionmentioning

confidence: 46%

Section: Metamorphotic Transition Of Amino Acid Odor Sensitivity Frommentioning

confidence: 56%

Section: Discussionmentioning

confidence: 99%

Section: Metamorphotic Transition Of Amino Acid Odor Sensitivity Frommentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

Syed

Sansone

Hassenklöver

et al. 2016

Cell. Mol. Life Sci.

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The Molecular Biology of Vertebrate Olfaction

Hayden

Teeling

2014

The Anatomical Record

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The importance of chemosensation for vertebrates is reflected in the vast and variable nature of their chemosensory tissues, neurons, and genes, which we explore in this review. Immense progress has been made in elucidating the molecular biology of olfaction since the discovery of the olfactory receptor genes by Buck and Axel, which eventually won the authors the Nobel Prize. In particular, research linking odor ligands to olfactory receptors (ORs) is truly revolutionizing our understanding of how a large but limited number of chemosensory receptors can allow us to perceive the massive diversity of odors in our habitat. This research is providing insight into the evolution of genomes and providing the raw data needed to explore links between genotype and phenotype, still a grand challenge in biology. Research into olfaction is still developing and will no doubt continue until we have a clear understanding of how all odors are detected and the evolutionary forces that have molded the chemosensory subgenome in vertebrates. This knowledge will not only be a huge step in elucidating olfactory function, advancing scientific knowledge and techniques, but there are also commercial applications for this research. This review focuses on the molecular basis of chemosensation, particularly olfaction, its evolution across vertebrates and the recent molecular advances linking odors to their cognate receptors. Anat Rec, 297:2216-2226, 2014. V C 2014 Wiley Periodicals, Inc.Key words: chemosensation; olfactory receptor; molecular biology; genomic evolution; odor bindingOlfaction or the "sense of smell" is considered to play an important role in the survival of many animals. It provides an extraordinary sensitivity for the discrimination of environmental and sexual cues and is used to find food, mates, and to avoid predators. Two main classes of molecules; odorants and pheromones, stimulate the olfactory system. It is the sensation of these compounds which is integral for many animals in gathering information from the environment, and the varying complexity of olfactory systems among the vertebrates underlies the way each species depends on their olfactory systems for survival and reproduction.Below we initially describe the chemosensory organs, the different receptors they contain and detail how signal transduction occurs when an odor binds to its receptor. Next, the largest family of the chemosensory receptors, the olfactory receptor subgenome is explored.The diversity and classification of olfactory receptor genes, their evolution, and the research being carried out to uncover which odor binds to which receptor, is

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Metamorphic remodeling of the olfactory organ of the African clawed frog, Xenopus laevis

Dittrich

Kuttler

Hassenklöver

et al. 2015

J of Comparative Neurology

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The amphibian olfactory system undergoes massive remodeling during metamorphosis. The transition from aquatic olfaction in larvae to semiaquatic or airborne olfaction in adults requires anatomical, cellular, and molecular modifications. These changes are particularly pronounced in Pipidae, whose adults have secondarily adapted to an aquatic life style. In the fully aquatic larvae of Xenopus laevis, the main olfactory epithelium specialized for sensing water-borne odorous substances lines the principal olfactory cavity (PC), whereas a separate olfactory epithelium lies in the vomeronasal organ (VNO). During metamorphosis, the epithelium of the PC is rearranged into the adult "air nose," whereas a new olfactory epithelium, the adult "water nose," forms in the emerging middle cavity (MC). Here we performed a stage-by-stage investigation of the anatomical changes of the Xenopus olfactory organ during metamorphosis. We quantified cell death in all olfactory epithelia and found massive cell death in the PC and the VNO, suggesting that the majority of larval sensory neurons is replaced during metamorphosis in both sensory epithelia. The moderate cell death in the MC shows that during the formation of this epithelium some cells are sorted out. Our results show that during MC formation some supporting cells, but not sensory neurons, are relocated from the PC to the MC and that they are eventually eliminated during metamorphosis. Together our findings illustrate the structural and cellular changes of the Xenopus olfactory organ during metamorphosis.

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Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream

Cited by 50 publications

References 69 publications

Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

The Molecular Biology of Vertebrate Olfaction

Metamorphic remodeling of the olfactory organ of the African clawed frog, Xenopus laevis

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