Metamorphic remodeling of the olfactory organ of the African clawed frog, <i>Xenopus laevis</i>

Dittrich, Katarina; Kuttler, Josua; Hassenklöver, Thomas; Manzini, Ivan

doi:10.1002/cne.23887

Cited by 24 publications

(35 citation statements)

References 49 publications

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“…In parallel, the expression of early-derived V2Rs disappears from the larval MOE, as it transforms into the adult principal cavity, and concomitantly appears in the newly generated middle cavity. This is in line with our previous findings that neuronal populations of the olfactory organ change substantially during metamorphosis: larval ORNs undergo apoptotic cell death, do not persist in the long run and are replaced by newly generated neurons [4]. The basal enrichment of V2R-expressing cells within the middle cavity is indistinguishable from that of TRPC2-expressing neurons, very similar to the situation observed in the tadpole MOE [7].…”

Section: Discussionsupporting

confidence: 91%

“…The basal enrichment of V2R-expressing cells within the middle cavity is indistinguishable from that of TRPC2-expressing neurons, very similar to the situation observed in the tadpole MOE [7]. Thus the correlation between V2R and TRPC2 expression is retained in a newly formed organ [4], the middle cavity. In the same vein, the distribution of amino acid-responsive cells between the middle cavity and the principal cavity closely parallels the distribution of V2R-C-expressing cells, consistent with the hypothesis that V2Rs expressed in microvillous neurons mediate the amino acid-responses in amphibians, similar to what has been shown for teleost fish [15].…”

Section: Discussionsupporting

confidence: 69%

“…3, 4). Thus, the middle cavity mimicks the mixed ORN population of the larval main olfactory epithelium, with both ciliated and microvillous receptor neurons, and responses to forskolin as well as amino acids, even though this organ is built de novo during metamorphosis [4].…”

Section: Post-metamorphosis Ancient V2r Genes and A Component Of Theimentioning

confidence: 99%

“…Anurans reconstruct the main olfactory epithelium (MOE) of their aquatic tadpoles into a so-called air nose (principal cavity) during metamorphosis [2]. Secondarily aquatic pipid frogs such as Xenopus laevis have an additional olfactory epithelium, the so-called water nose (middle cavity), that develops newly during metamorphosis [3][4][5], and is responsible for detecting water-borne odors (in terrestrial anurans the middle cavity is non-sensory [2]). …”

Section: Introductionmentioning

confidence: 99%

“…During this metamorphotic reorganization massive apoptotic cell death occurs, former larval olfactory receptor neurons (ORNs) are replaced and newly generated neurons form the middle cavity [4]. Thus one expects massive changes in the molecular and functional response characteristics of olfactory sensory neurons during metamorphosis.…”

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: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 69%

Section: Post-metamorphosis Ancient V2r Genes and A Component Of Theimentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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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Molecular mechanisms of differentiation and class choice of olfactory sensory neurons

Hirota

2024

Genesis

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SummaryThe sense of smell is intricately linked to essential animal behaviors necessary for individual survival and species preservation. During vertebrate evolution, odorant receptors (ORs), responsible for detecting odor molecules, have evolved to adapt to changing environments, transitioning from aquatic to terrestrial habitats and accommodating increasing complex chemical environments. These evolutionary pressures have given rise to the largest gene family in vertebrate genomes. Vertebrate ORs are phylogenetically divided into two major classes; class I and class II. Class I OR genes, initially identified in fish and frog, have persisted across vertebrate species. On the other hand, class II OR genes are unique to terrestrial animals, accounting for ~90% of mammalian OR genes. In mice, each olfactory sensory neuron (OSN) expresses a single functional allele of a single OR gene from either the class I or class II OR repertoire. This one neuron‐one receptor rule is established through two sequential steps: specification of OR class and subsequent exclusive OR expression from the corresponding OR class. Consequently, OSNs acquire diverse neuronal identities during the process of OSN differentiation, enabling animals to detect a wide array of odor molecules. This review provides an overview of the OSN differentiation process through which OSN diversity is achieved, primarily using the mouse as a model animal.

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The ontogeny of the olfactory system in ceratophryid frogs (Anura, Ceratophryidae)

Quinzio

Reiss

2017

Journal of Morphology

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The aquatic-to-terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria.Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental€terrestrial €path-way up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage. K E Y W O R D Sanurans, Lepidobatrachus, nose, recessus olfactorius, secondary aquatic life | I N TR ODU C TI ONWe examine the larval and adult morphology of the peripheral olfactory system in a clade of South American frogs, a clade that includes genera with terrestrial adults (Ceratophrys and Chacophrys) and with secondarily aquatic adults (Lepidobatrachus). The primary question we ask is whether this major difference in lifestyle is correlated with morphological changes in the peripheral olfactory system, and if so, which?We also seek to determine the overall pattern of olfactory ontogeny in the species of the clade, and how it differs among them.Although direct development has evolved at least ten times independently among the anurans (Heinicke et al., 2009), the majority of anuran species are characterized by a biphasic life cycle. In such life cycles, there are larval and adult phases, distinct in their morphology, physiology, and ecology, and united in ontogeny by the set of cellular and systemic changes t...

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

Cited by 24 publications

References 49 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

Molecular mechanisms of differentiation and class choice of olfactory sensory neurons

The ontogeny of the olfactory system in ceratophryid frogs (Anura, Ceratophryidae)

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