Phyletic Distribution of Crypt-Type Olfactory Receptor Neurons in Fishes

Hansen, Anne; Finger, Thomas E.

doi:10.1159/000006645

Cited by 127 publications

(109 citation statements)

References 18 publications

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“…In the present study, we revealed that CCs of barfin flounder have similar ultrastructure to those of the ordinary teleost [8]. The most striking feature of CCs is the apical invagination equipped with both cilia and microvilli.…”

supporting

confidence: 58%

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Ultrastructure of the Olfactory Epithelium in a Flatfish, Barfin Flounder (Verasper moseri)

Nakamuta

Taniguchi

2010

J. Vet. Med. Sci.

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ABSTRACT. In this study, we examined the olfactory epithelium (OE) of the barfin flounder by transmission electron microscopy. As in the case of the ordinary teleost, the OE of the barfin flounder had 3 types of olfactory receptor cells (ciliated olfactory receptor cell, microvillous olfactory receptor cell and crypt cell), 3 types of supporting cells (ciliated, microvillous and crypt supporting cells) and basal cells. Each type of OE cells in the barfin flounder had similar ultrastructure to that of the ordinary teleost. Crypt cell is the third type of olfactory receptor cell unique to fish, whose function is unclear. The barfin flounder may be a suitable material to study crypt cells because it has relatively abundant crypt cells in the OE.KEY WORDS: fish, olfactory epithelium, ultrastructure.J. Vet. Med. Sci. 72(6): 801-804, 2010 Many vertebrates have anatomically separated two olfactory organs: the olfactory epithelium (OE) and the vomeronasal organ (VNO). They detect general odorants and pheromones, respectively [1,3]. Although the OE is observed in all vertebrates, the VNO first appeared in amphibians during phylogeny. Since fish do not possess VNO, the OE of fish has been supposed to detect both general odorants and pheromones [9]. As in the case of other vertebrates, the OE of fish consists of the olfactory receptor cells (ORCs), supporting cells (SCs) and basal cells (BCs). In fish, there are three types of ORCs: the ciliated ORCs (cORCs), microvillous ORCs (mORCs) and crypt cells (CCs) [9]. In goldfish, the cORCs and mORCs have been shown to express genes homologous to the mammalian odorant receptors and vomeronasal receptors, respectively [2,10,11]. They are bipolar ORCs. On the other hand, CCs are the third type of ORCs unique to fish. Although CCs have been found in the OE of various kind of fish [4,8], their function in the olfaction is still unclear. In addition, SCs have been supposed to help ORCs in their olfactory function and BCs have been supposed to be the precursor cells of ORCs [9].The barfin flounder is a suitable material to study fish olfaction, because it is one of the macrosmatic fish, depends mainly on the olfaction for feeding, and is convenient to obtain as it is cultivated in a local research institute. Previously using the barfin flounder, we investigated the morphology of olfactory system by scanning electron microscopy, lectin histochemistry and immunohistochemistry [12][13][14]. In the present study, we examined the OE of the barfin flounder by transmission electron microscopy (TEM) to reveal the possible relationship between their ultrastructure and function.Three adult barfin flounders, about 30 cm in length, were obtained from the Iwate Fisheries Technology Center (Kamaishi, Japan). After euthanasia by decapitation, the olfactory epithelium was dissected out and fixed in 2% glutaraldehyde and 2.5% paraformaldehyde in 0.1 M cacodylate buffer (pH 7.4) overnight at 4C. Subsequently, it was postfixed in 1% osmium tetroxide for 2 hr at 4C, dehydrated in a graded series of e...

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supporting

confidence: 58%

“…On the other hand, CCs are the third type of ORCs unique to fish. Although CCs have been found in the OE of various kind of fish [4,8], their function in the olfaction is still unclear. In addition, SCs have been supposed to help ORCs in their olfactory function and BCs have been supposed to be the precursor cells of ORCs [9].…”

mentioning

confidence: 99%

Ultrastructure of the Olfactory Epithelium in a Flatfish, Barfin Flounder (Verasper moseri)

Nakamuta

Taniguchi

2010

J. Vet. Med. Sci.

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“…In contrast to those found in teleost, the CNs found in S. canicula did not show Ga o -like ir. CNs are RNs present in both cartilaginous and bony fishes (Hansen and Finger, 2000;Ferrando et al, 2006a) but their role in olfaction, their odorant specificity, and the family of receptors they express, are still unknown. Despite an involvement in reproductive behaviour which has been suggested for this kind of RNs (Hamdani and Døving, 2006;Hamdani et al, 2008), studies on their electrophysiological properties in teleost suggest their response to amino acids, generally thought to mediate feeding behaviour (Schmachtenberg, 2006;Vielma et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Immunolocalization of G‐Protein Alpha Subunits in the Olfactory System of the Cartilaginous Fish Scyliorhinus Canicula

Ferrando

Gambardella

Ravera

et al. 2009

The Anatomical Record

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In the olfactory and vomeronasal systems of vertebrates, the morphology of the receptor neurons, the receptor gene family they express, the G-protein coupled with the receptor (in particular the G-protein alpha subunit), and their projection to the olfactory bulb are correlated. Much information about this complicated system have been collected in different groups, but nothing is known about Chondrichthyes. In this work, the presence and distribution of immunoreactivity for different types of G-protein alpha subunit (Ga o , Ga q and Ga s/olf ) were investigated in the olfactory mucosa and olfactory bulb of the shark Scyliorhinus canicula. Only Ga olike immunoreactivity was detected in the olfactory mucosa and bulb, both in tissues and homogenates. Its distribution was partially similar to that found in other vertebrates: it was localized in the microvillous receptor neurons, in numerous axon bundles of the fila olfactoria, in the stratum nervosum and in the most of glomeruli in the stratum glomerulosum. No immunoreactivity was instead observed in the crypt neurons, the second type of olfactory neurons present in cartilaginous fish. The projections of crypt neurons to olfactory bulb probably correspond to the few ventrallylocated glomeruli which were negative to the antiserum against Ga o . These data suggest, in S. canicula, different olfactory neuron types send projections to the olfactory bulb with a segregated distribution, as observed in other vertebrates. Anat Rec, 292:1771Rec, 292: -1779Rec, 292: , 2009. V V C 2009 Wiley-Liss, Inc.

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“…The crypt OSNs are located in the superficial layer of the OE and have unique characters such as typical ovoid-shaped cell bodies and strong S100 protein-like immunoreactivity (Hansen and Finger, 2000;Hansen et al, 2003Hansen et al, , 2004Germanà et al, 2004). We examined whether crypt OSNs are labeled with fluorescent proteins in the OMP:YFP and TRPC2:Venus transgenic fish.…”

Section: Transgenic Zebrafish Lines Expressing Fluorescent Proteins Imentioning

confidence: 99%

Mutually Exclusive Glomerular Innervation by Two Distinct Types of Olfactory Sensory Neurons Revealed in Transgenic Zebrafish

Sato¹,

Miyasaka²,

Yoshihara³

2005

J. Neurosci.

249

323

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The olfactory epithelium of fish contains two major types of olfactory sensory neurons (OSNs) that are distinct morphologically (ciliated vs microvillous) and possibly functionally. Here, we found that these OSNs express different sets of signal transduction machineries: the ciliated OSNs express OR-type odorant receptors, cyclic nucleotide-gated channel A2 subunit, and olfactory marker protein (OMP), whereas the microvillous OSNs express V2R-type receptors and transient receptor potential channel C2 (TRPC2). To visualize patterns of axonal projection from the two types of OSNs to the olfactory bulb (OB), we generated transgenic zebrafish in which spectrally distinct fluorescent proteins are expressed in the ciliated and microvillous OSNs under the control of OMP and TRPC2 gene promoters, respectively. An observation of whole-mount OB in adult double-transgenic zebrafish revealed that the ciliated OSNs project axons mostly to the dorsal and medial regions of the OB, whereas the microvillous OSNs project axons to the lateral region of the OB. A careful histological examination of OB sections clarified that the axons from the two distinct types of OSNs target different glomeruli in a mutually exclusive manner. This segregation is already established at very early developmental stages in zebrafish embryos. These findings clearly demonstrate the relationships among cell morphology, molecular signatures, and axonal terminations of the two distinct types of OSNs and suggest that the two segregated neural pathways are responsible for coding and processing of different types of odor information in the zebrafish olfactory system.

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Phyletic Distribution of Crypt-Type Olfactory Receptor Neurons in Fishes

Cited by 127 publications

References 18 publications

Ultrastructure of the Olfactory Epithelium in a Flatfish, Barfin Flounder (Verasper moseri)

Ultrastructure of the Olfactory Epithelium in a Flatfish, Barfin Flounder (Verasper moseri)

Immunolocalization of G‐Protein Alpha Subunits in the Olfactory System of the Cartilaginous Fish Scyliorhinus Canicula

Mutually Exclusive Glomerular Innervation by Two Distinct Types of Olfactory Sensory Neurons Revealed in Transgenic Zebrafish

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