Differential Requirements for Semaphorin 3F and Slit-1 in Axonal Targeting, Fasciculation, and Segregation of Olfactory Sensory Neuron Projections

Cloutier, Jasmin; Sahay, Amar; Chang, Ernie; Tessier‐Lavigne, Marc; Dulac, Catherine; Kolodkin, Alex L.; Ginty, David D.

doi:10.1523/jneurosci.2786-04.2004

Cited by 106 publications

(114 citation statements)

References 40 publications

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“…The perinatal lethality of robo-2 Ϫ/Ϫ mice precluded us from evaluating the requirement for Robo-2 in the development of accurate NQO-1-expressing axonal projections in the adult olfactory glomerular map. We therefore selectively ablated expression of Robo-2 in neurons by generating robo-2 conditional null mice that express the Cre (bacterio phage P1 cyclization recombinase) recombinase under the control of the pan-neuronal synapsin-1 (syn-1) promoter (Hoesche et al, 1993(Hoesche et al, , 1995Cloutier et al, 2004;Lu et al, 2007). robo-2 C/C ; syn-1 Cre/ϩ mice survive until adulthood, and their OBs are fully innervated by NQO-1-and OCAM-expressing axons.…”

Section: F G I J L M O) and Anti-ocam (B C E F H I Kmentioning

confidence: 99%

“…Moreover, we demonstrated previously that the Slit and Robo families of axon guidance cues can promote zonal segregation of vomeronasal axons in the accessory olfactory system in mice (Cloutier et al, 2004). We therefore evaluated whether SlitRobo signaling controls zonal segregation of OSNs in the main olfactory bulb.…”

Section: Introductionmentioning

confidence: 97%

“…Members of the secreted semaphorin (Sema) family and their receptors, the neuropilins, have been implicated in the development of OSN projections. (de Castro et al, 1999;Pasterkamp et al, 1999;Renzi et al, 2000;Schwarting et al, 2000;Walz et al, 2002;Cloutier et al, 2004;Schwarting et al, 2004). Indeed, Sema3A is required for appropriate medial to lateral targeting of OSN axons (Schwarting et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

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Requirement for Slit-1 and Robo-2 in Zonal Segregation of Olfactory Sensory Neuron Axons in the Main Olfactory Bulb

Cho¹,

Lépine²,

Andrews³

et al. 2007

J. Neurosci.

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112

125

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The formation of precise stereotypic connections in sensory systems is critical for the ability to detect and process signals from the environment. In the olfactory system, olfactory sensory neurons (OSNs) project axons to spatially defined glomeruli within the olfactory bulb (OB). A spatial relationship exists between the location of OSNs within the olfactory epithelium (OE) and their glomerular targets along the dorsoventral axis in the OB. The molecular mechanisms underlying the zonal segregation of OSN axons along the dorsoventral axis of the OB are poorly understood. Using robo-2 Ϫ/Ϫ (roundabout) and slit-1 Ϫ/Ϫ mice, we examined the role of the Slit family of axon guidance cues in the targeting of OSN axons during development. We show that a subset of OSN axons that normally project to the dorsal region of the OB mistarget and form glomeruli in the ventral region in robo-2 Ϫ/Ϫ and slit-1 Ϫ/Ϫ mice. In addition, we show that the Slit receptor, Robo-2, is expressed in OSNs in a high dorsomedial to low ventrolateral gradient across the OE and that Slit-1 and Slit-3 are expressed in the ventral region of the OB. These results indicate that the dorsal-to-ventral segregation of OSN axons are not solely defined by the location of OSNs within the OE but also relies on axon guidance cues.

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Section: F G I J L M O) and Anti-ocam (B C E F H I Kmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

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Requirement for Slit-1 and Robo-2 in Zonal Segregation of Olfactory Sensory Neuron Axons in the Main Olfactory Bulb

Cho¹,

Lépine²,

Andrews³

et al. 2007

J. Neurosci.

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112

125

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“…Concomitantly, members of the plexin-A subfamily are expressed in the olfactory system, with robust expression of plexin-A1 (Plxna1) in the VNO and vomeronasal nerves (VNNs) (Murakami et al, 2001). Loss of Sema3A results in guidance errors in subsets of olfactory axons (Schwarting et al, 2000;Taniguchi et al, 2003), whereas loss of Sema3F or Npn-2 functions results in defasciculation of the VNNs along the medial surface of the olfactory bulb (Cloutier et al, 2002(Cloutier et al, , 2004Walz et al, 2002). Moreover, it has been reported that Npn-2 Ϫ/Ϫ mice are often infertile (Giger et al, 2000;Walz et al, 2002), prompting us to investigate the role of Npn-2 in the development and migration of GnRH neurons.…”

Section: Introductionmentioning

confidence: 99%

Neuropilins and Their Ligands Are Important in the Migration of Gonadotropin-Releasing Hormone Neurons

Cariboni¹,

Hickok²,

Rakić³

et al. 2007

J. Neurosci.

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Gonadotropin-releasing hormone (GnRH) neurons in the hypothalamus play an important role in reproductive function. These cells originate in the nasal compartment and migrate into the basal forebrain in association with olfactory/vomeronasal nerves in embryonic life in rodents. Here, we studied the role of neuropilins and their ligands, semaphorins, in the development of the olfactory-GnRH system. We focused on Neuropilin-2 knock-out (Npn-2 ؊/؊ ) mice, because they are known to display defasciculation of olfactory nerves and reduced fertility. We found a significant decrease in the number of GnRH neurons in the hypothalamus and a marked reduction in their gonadal size. We then observed an abnormal increase of GnRH neurons in the noses of Npn-2 ؊/؊ mice, indicating that these cells failed to migrate into the forebrain. However, because neuropilins and semaphorins are involved in events of neuronal migration in the brain, we asked whether the observed reduction in GnRH neurons was directly attributable to the action of these molecules. Using fluorescenceactivated cell sorting and reverse transcription-PCR on mRNA derived from embryonic green fluorescent protein (GFP)-GnRH transgenic mice, we found expression of class 3 semaphorins and their receptors (neuropilin-1/2 and plexin-A1) in GnRH neurons. Furthermore, double-immunofluorescence experiments showed that migrating GnRH neurons, as well as associated olfactory fibers, express Npn-2 in the nasal region. We then used a line of immortalized GnRH neurons (GN11 cells) that display the same expression patterns for semaphorins and their receptors as GFP-GnRH cells and found that class 3 semaphorins and vascular endothelial growth factors modulate their migratory activity. These studies provide support for the direct involvement of neuropilins and their ligands in the establishment of the GnRH neuroendocrine system.

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“…Of particular interest to olfactory behavior is the implication that class 3 soluble semaphorins and their receptors play a role in axon guidance in the mouse olfactory system (Renzi et al 2000;Schwarting et al 2000;Walz et al 2002;Taniguchi et al 2003;Cloutier et al 2004). A null mutation in Sema3F resulted in defasciculation of the vomeronasal nerve and rerouting of axons from vomeronasal sensory neurons into the main olfactory bulb.…”

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confidence: 99%

The Early Developmental Gene Semaphorin 5c Contributes to Olfactory Behavior in Adult Drosophila

et al. 2007

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Behaviors are complex traits influenced by multiple pleiotropic genes. Understanding the mechanisms that give rise to complex behaviors requires an understanding of how variation in transcriptional regulation shapes nervous system development and how variation in brain structure influences an organism's ability to respond to its environment. To begin to address this problem, we used olfactory behavior in Drosophila melanogaster as a model and showed that a hypomorphic transposon-mediated mutation of the early developmental gene Semaphorin-5c (Sema-5c) results in aberrant behavioral responses to the repellant odorant benzaldehyde. We fine mapped this effect to the Sema-5c locus using deficiency mapping, phenotypic reversion through P-element excision, and transgenic rescue. Morphometric analysis of this Sema5c allele reveals subtle neuroanatomical changes in the brain with a reduction in the size of the ellipsoid body. High-density oligonucleotide expression microarrays identified 50 probe sets with altered transcriptional regulation in the Sema-5c background and quantitative complementation tests identified epistatic interactions between nine of these coregulated genes and the transposon-disrupted Sema-5c gene. Our results demonstrate how hypomorphic mutation of an early developmental gene results in genomewide transcriptional consequences and alterations in brain structure accompanied by profound impairment of adult behavior.

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Differential Requirements for Semaphorin 3F and Slit-1 in Axonal Targeting, Fasciculation, and Segregation of Olfactory Sensory Neuron Projections

Cited by 106 publications

References 40 publications

Requirement for Slit-1 and Robo-2 in Zonal Segregation of Olfactory Sensory Neuron Axons in the Main Olfactory Bulb

Requirement for Slit-1 and Robo-2 in Zonal Segregation of Olfactory Sensory Neuron Axons in the Main Olfactory Bulb

Neuropilins and Their Ligands Are Important in the Migration of Gonadotropin-Releasing Hormone Neurons

The Early Developmental Gene Semaphorin 5c Contributes to Olfactory Behavior in Adult Drosophila

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