Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb

Tsuboi, Akito; Yoshihara, Shingo; Yamazaki, Nika; Kasai, Hiroaki; Asai-Tsuboi, Hisae; Komatsu, Madoka; Serizawa, Shou; Ishii, Takeshi; Matsuda, Yoichi; Nagawa, Fumikiyo; Sakano, Hitoshi

doi:10.1523/jneurosci.19-19-08409.1999

Cited by 150 publications

(132 citation statements)

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(50 reference statements)

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“…Ultimately, axons of like specificity converge on four glomeruli, one on each side of each bulb (Yoshihara and Mori, 1997). Axons with closely related specificities are targeted to glomeruli that are in close proximity to one another (Tsuboi et al, 1999). Thus, initially in its course, an olfactory axon is surrounded by axons of different specificities from its own; late in its course it is surrounded by axons of related specificities, and at the very end of its course it is surrounded by axons of identical specificity.…”

Section: Discussionmentioning

confidence: 99%

Intercellular interactions in the mammalian olfactory nerve

Blinder

Pumplin

Paul

et al. 2003

J of Comparative Neurology

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The small, unmyelinated axons of olfactory sensory neurons project to the olfactory bulb in densely packed fascicles, an arrangement conducive to axo-axonal interactions. We recently demonstrated ephaptic interactions between these axons in the olfactory nerve layer, the layer of the olfactory bulb in which the axon fascicles interweave and rearrange extensively. In the present study, we hypothesized that the axons, which express connexins, may have another mode of communication: gap junctions. Previous transmission electron microscopy (TEM) studies have failed to demonstrate such junctions. However, the definitive method for detecting gap junctions, freeze fracture, has not been used to examine the interaxonal connections of the olfactory nerve layer. Here, we apply a combined approach of TEM and freeze fracture to determine if gap junctions are present between the olfactory axons. Gap junctions involving olfactory axons were not found. However, by freeze fracture, P faces of both the axons and ensheathing cells (glia that surround the axon fascicles) contained distinctive linear arrays of particles, aligned along the small columns of extracellular space. In axons, few intramembranous particles were present outside of these arrays. Multi-helix proteins, including ion channels and connexin hemichannels, have been shown to be visible as particles by freeze fracture. This suggests that the proteins important for signal transmission are confined to the linear arrays. Such an arrangement would facilitate ephaptic transmission, calcium waves, current oscillations, and paracrine communication and may be important for olfactory neural code processing.Keywords freeze fracture; ultrastructure; olfactory bulb; ephaptic; connexins; hemichannels Olfactory receptor neurons project from the olfactory epithelium to the olfactory bulb by dense bundles of thin, unmyelinated olfactory axons (Marin-Padilla and Amieva, 1989;Daston et al., 1990;Mori, 1993). The high packing density of these axons and the absence of intervening glia suggest that olfactory coding may be affected by axoaxonal interactions.We recently demonstrated (Bokil et al., 2001) that neighboring axons are able to influence each other by ephaptic interactions-current spread through the small extracellular space. We have argued (Bokil et al., 2001) that ephaptic interactions, as well as interneuronal interactions mediated by extruded potassium ions (Bliss and Rosenberg, 1979) First, olfactory receptors of mature mammals are constantly regenerated (Graziadei and Graziadei, 1979;Graziadei and Monti Graziadei, 1983), and developing neurons of the central nervous system are often extensively coupled by gap junctions (reviewed in Kandler and Katz, 1995;Naus and Bani-Yaghoub, 1998;Chang and Balice-Gordon, 2000). Second, olfactory receptor neurons express connexins, the proteins that form gap junctions. Olfactory receptor neurons express mRNA for connexins 43 (Zhang et al., 2000), 45 (Zhang andRestrepo, 2002), and 36 (Zhang andRestrepo, 2003). Furthermore, in immun...

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Section: Discussionmentioning

confidence: 99%

Intercellular interactions in the mammalian olfactory nerve

Blinder

Pumplin

Paul

et al. 2003

J of Comparative Neurology

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“…Digoxigenine (DIG)-labeled T7 cRNA probes were synthesized from 50 ng of dsDNA template by a DIG RNA Labeling Kit (175025, Roche, Basel, Switzerland). The procedures used for section treatment and hybridization were based on those used by Tsuboi et al (1999) with a minor modification described as follows [41]. Frozen sections were covered with 10 μl in situ hybridization solution containing 5 ng/μl cRNA probe.…”

Section: Methodsmentioning

confidence: 99%

Localization of eNOS in the Olfactory Epithelium of the Rat

Endo

Yamamoto

Yamaguchi-Yamada

et al. 2011

The Journal of Veterinary Medical Science

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ABSTRACT. Nitric oxide (NO) is a free radical and produced from L-arginine by nitric oxide synthase (NOS). Since NO is recently suggested to be involved in olfactory perception, the expression of eNOS, an isoform of NOS, was examined in the rat olfactory epithelium. The activity of NADPH-diaphorase was also examined as a marker of NOS. In the dorsomedial region of the nasal cavity, intensely positive reactions for NADPH-diaphorase were observed in the entire cytoplasm of sensory cells (olfactory cells). By immunohistochemistry, intensely positive reactions for eNOS were also found in the dorsomedial region of the nasal cavity. These reactions were observed on the free border of the olfactory epithelium. By immunoelectron microscopy, positive reactions for eNOS were found in the cilia of olfactory cells. In addition, in situ hybridization analysis of the olfactory epithelium revealed the expression of eNOS mRNA in the olfactory cells. These results indicate the presence of eNOS in the olfactory cells of the rat, and differential expression of eNOS in the olfactory epithelium depending on the regions of the nasal cavity. In addition, NO produced by eNOS may be involved in olfactory perception in the cilia of olfactory cells.KEY WORDS: eNOS, NADPH-diaphorase, nitric oxide, olfactory epithelium, rat.J. Vet. Med. Sci. 73(4): 423-430, 2011 Nitric oxide (NO) is a free radical with many functions in the cardiovascular, nervous, and immune systems [2]. Biologically, NO is produced from L-arginine by nitric oxide synthase (NOS). NOS is divided into 3 types of major isoforms, i.e., neuronal NOS (nNOS), endothelial NOS (eNOS), and inducible NOS (iNOS). The nNOS and eNOS are constitutive forms of NOS and mainly expressed in the neuronal and endothelial cells, respectively. The iNOS is an inducible form of NOS and mainly expressed in macrophages [15].Primary function of NO is the activation of soluble guanylyl cyclase (sGC) to increase cGMP levels [1]. In the cilia of the rat sensory cells (olfactory cells), it is reported that odorant-stimulus induces the increase of cGMP levels and that specific NOS inhibitor L-N G -nitro arginine or NO scavenger hemoglobin inhibits this increase [4]. These findings indicate that odorant-stimulus induces NO production in the rat olfactory cells. Schmachtenberg et al. (2000Schmachtenberg et al. ( , 2003 reported that NO-stimulus induces outward potassium currents in 30 out of 72 olfactory cells and inward potassium currents in 3 out of 54 cells by physiological study [36,37]. In the cilia of rat olfactory cells, moreover, NO-stimulus is reported to activate or inhibit olfactory cyclic nucleotidegated (CNG) channels [5,6,28,36,37]. These reports suggest that NO is produced by the olfactory cells in response to odorant-stimulus, and has inhibitory and/or weakly excitatory effects to the olfactory cells by gating of CNG channel. However, it is still unclear which type of NOS isoforms generates NO in the olfactory cells of the rat. Because it has been reported that iNOS and eNOS are expressed...

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“…MOR236-1 and MOR235-1, the closest counterparts in the mouse genome, are encoded by two genes located next to each other on Chromosome 2, sharing 91% similarity in the amino acid sequence (Tsuboi et al, 1999). Although their expression patterns are comparable in adults (Table 1 and Fig.…”

Section: Asynchronous Onsets Of Osns Expressing Different Orsmentioning

confidence: 99%

Differential development of odorant receptor expression patterns in the olfactory epithelium: A quantitative analysis in the mouse septal organ

Tian

2008

Developmental Neurobiology

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The rodent olfactory epithelium expresses more than 1000 odorant receptors (ORs) with distinct patterns, yet it is unclear how such patterns are established during development. In the current study, we investigated development of the expression patterns of different ORs in the septal organ, a small patch of olfactory epithelium predominantly expressing nine identified ORs. The presumptive septal organ first appears at about embryonic day 16 (E16) and it completely separates from the main olfactory epithelium (MOE) at about postnatal day 7 (P7). Using in situ hybridization, we quantified the densities of the septal organ neurons labeled by specific RNA probes of the nine abundant OR genes from E16 to postnatal 3 months. The results indicate that olfactory sensory neurons (OSNs) expressing different ORs have asynchronous temporal onsets. For instance, MOR256-17 and MOR236-1 cells are present in the septal organ at E16; however, MOR0-2 cells do not appear until P0. In addition, OSNs expressing different ORs show distinct developmental courses and reach their maximum densities at different stages ranging from E16 (e.g. MOR256-17) to 1 month (e.g. MOR256-3 and MOR235-1). Furthermore, early onset does not correlate with high abundance in adult. This study reveals a dynamic composition of the OSNs expressing different ORs in the developing olfactory epithelium.

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Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb

Cited by 150 publications

References 37 publications

Intercellular interactions in the mammalian olfactory nerve

Intercellular interactions in the mammalian olfactory nerve

Localization of eNOS in the Olfactory Epithelium of the Rat

Differential development of odorant receptor expression patterns in the olfactory epithelium: A quantitative analysis in the mouse septal organ

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