Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F

Walz, Andreas; Feinstein, Paul; Khan, Mona; Mombaerts, Peter

doi:10.1242/dev.008722

Cited by 62 publications

(56 citation statements)

References 56 publications

(100 reference statements)

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“…The MFC-CS group showed increased 2-DG uptake located in the isolated areas of the glomerular layer (c-MOB-iGl) forming a characteristic ring encircling the c-MOB. This pattern of neural activity resembles the location of the necklace glomeruli (NG), which more rostrally form a ring around the anterior portion of the accessory olfactory bulb (AOB) and moving posteriorly, encircle the entire trunk of the c-MOB (23). Interestingly, we observed the highest activity in the ventral aspect of the c-MOB (Fig.…”

Section: Amygdala and Olfactory Autoradiography Of Mother-to-infantsupporting

confidence: 55%

“…Interestingly, we observed the highest activity in the ventral aspect of the c-MOB (Fig. 3D), which has been shown to contain the largest NG (23). The robust activity in the c-MOB-iGl suggests that this area is involved in the transfer of fear, possibly through the Grueneberg ganglion (GG)-NG olfactory subsystem, which was recently shown to be involved in alarm odor processing (21) and which was further explored below.…”

Section: Amygdala and Olfactory Autoradiography Of Mother-to-infantmentioning

confidence: 67%

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Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Dębiec

Sullivan

2014

Proc. Natl. Acad. Sci. U.S.A.

146

119

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Emotional trauma is transmitted across generations. For example, children witnessing their parent expressing fear to specific sounds or images begin to express fear to those cues. Within normal range, this is adaptive, although pathological fear, such as occurs in posttraumatic stress disorder or specific phobias, is also socially transmitted to children and is thus of clinical concern. Here, using a rodent model, we report a mother-to-infant transfer of fear to a novel peppermint odor, which is dependent on the mother expressing fear to that smell in pups' presence. Examination of pups' neural activity using c-Fos early gene expression and 14 C 2-deoxyglucose autoradiography during mother-to-infant fear transmission revealed lateral and basal amygdala nuclei activity, with a causal role highlighted by pharmacological inactivation of pups' amygdala preventing the fear transmission. Maternal presence was not needed for fear transmission, because an elevation of pups' corticosterone induced by the odor of the frightened mother along with a novel peppermint odor was sufficient to produce pups' subsequent aversion to that odor. Disruption of axonal tracts from the Grueneberg ganglion, a structure implicated in alarm chemosignaling, or blockade of pups' alarm odor-induced corticosterone increase prevented transfer of fear. These memories are acquired at younger ages compared with amygdala-dependent odorshock conditioning and are more enduring following minimal conditioning. Our results provide clues to understanding transmission of specific fears across generations and its dependence upon maternal induction of pups' stress response paired with the cue to induce amygdala-dependent learning plasticity. Results are discussed within the context of caregiver emotional responses and adaptive vs. pathological fears social transmission.necklace glomeruli | pheromone | olfaction | PTSD | social referencing

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Section: Amygdala and Olfactory Autoradiography Of Mother-to-infantsupporting

confidence: 55%

Section: Amygdala and Olfactory Autoradiography Of Mother-to-infantmentioning

confidence: 67%

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Dębiec

Sullivan

2014

Proc. Natl. Acad. Sci. U.S.A.

146

119

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“…Swatches of olfactory epithelium were peeled off and placed in oxygenated Hepes based Ringer solution (140 mM NaCl/1.5 mM KCl/1 mM MgCl2/2.5 mM CaCl2/11 mM glucose/10 mM Hepes, pH 7.4). In these mice, GFP is coexpressed with GC-D by bicistronic strategy that leaves the coding region of GC-D intact (8). For cell-attached patch recording, intracellular pipette solution contained (in mM) 130 K-gluconate, 5 KCl, 10 Hepes, 13 Na-phosphocreatine, and 4 MgCl 2 and 0.6 EGTA.…”

Section: Methodsmentioning

confidence: 99%

“…Guanylyl cyclase-D (GC-D) is expressed exclusively in the CO 2 -responsive neurons, which are thus named GC-D ϩ neurons (6)(7)(8). GC-D ϩ neurons also express other components of signaling pathway that implicate cGMP as the second messenger, including cGMP-stimulated phosphodiesterase 2A (PDE2A) and cGMPsensitive cyclic nucleotide-gated (CNG) channels (7,9).…”

mentioning

confidence: 99%

Guanylyl cyclase-D in the olfactory CO ₂ neurons is activated by bicarbonate

Sun

Wang

Jian

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

115

110

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Atmospheric CO2 is an important environmental cue that regulates several types of animal behavior. In mice, CO 2 responses of the olfactory sensory neurons (OSNs) require the activity of carbonic anhydrase to catalyze the conversion of CO 2 to bicarbonate and the opening of cGMP-sensitive ion channels. However, it remains unknown how the enhancement of bicarbonate levels results in cGMP production. Here, we show that bicarbonate activates cGMP-producing ability of guanylyl cyclase-D (GC-D), a membrane GC exclusively expressed in the CO 2-responsive OSNs, by directly acting on the intracellular cyclase domain of GC-D. Also, the molecular mechanism for GC-D activation is distinct from the commonly believed model of ''release from repression'' for other membrane GCs. Our results contribute to our understanding of the molecular mechanisms of CO 2 sensing and suggest diverse mechanisms of molecular activation among membrane GCs.carbonic anhydrase ͉ CNG channels ͉ necklace glomeruli ͉ transduction

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“…It consists of a cluster of neurons-henceforward referred to as Grueneberg ganglion neurons (GGNs)-that express olfactory marker protein (OMP) and project their axons to a small number of glomeruli in the caudal main olfactory bulb (Fuss et al, 2005;Koos and Fraser, 2005;Fleischer et al, 2006;Roppolo et al, 2006;Storan and Key, 2006). Interestingly, these glomeruli are near the necklace glomeruli innervated by olfactory sensory neurons expressing the receptor guanylyl cyclase GC-D (Fülle et al, 1995;Juilfs et al, 1997;Leinders-Zufall et al, 2007;Walz et al, 2007; for review, see Munger et al, 2009), and both GC-D-expressing neurons and GGNs express elements of a cGMP second messenger pathway, including the cGMP-specific cyclic nucleotide-gated channel CNGA3 and the cGMP-stimulated phosphodiesterase PDE2 (Juilfs et al, 1997;Meyer et al, 2000;Leinders-Zufall et al, 2007;Fleischer et al, 2009;Liu et al, 2009). They differ, however, in the membrane-bound guanylyl cyclases they express; GGNs express guanylyl cyclase type G but not GC-D (Fleischer et al, 2009;Liu et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Grueneberg Ganglion Neurons Are Finely Tuned Cold Sensors

Schmid¹,

Pyrski²,

Biel³

et al. 2010

J. Neurosci.

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The Grueneberg ganglion is a newly appreciated nasal subsystem with neural connections to the olfactory forebrain, but its functional role has not been well defined. Here, we assess whether Grueneberg ganglion neurons (GGNs) function as thermosensors. By investigating the effect of acute temperature changes on the cytosolic Ca 2ϩ concentration of genetically labeled mouse GGNs (either gender), we demonstrate that GGNs are thermosensory neurons specialized to detect a temperature decline within a given temperature window. Furthermore, GGNs comprise a relatively homogeneous cell population with respect to temperature sensitivity. GGNs do not respond to ligands of the temperature-sensitive TRP channels TRPM8 and TRPA1, suggesting a novel mechanism for temperature sensing. One possibility is a cGMP-mediated mechanism, as GGNs express the receptor guanylyl cyclase GC-G, the cGMP-sensitive phosphodiesterase PDE2 and the cGMP-sensitive channel CNGA3. Surprisingly, Cnga3-null mice show normal cooling-induced Ca 2ϩ responses although cGMP-dependent Ca 2ϩ increases are absent in these mice. Rather, the cooling-induced Ca 2ϩ response of GGNs depends critically on the activity of a tetrodotoxin-sensitive voltage-gated sodium channel whereas the cGMP-dependent Ca 2ϩ signal does not. These findings establish the Grueneberg ganglion as a sensory organ mediating cold-evoked neural responses, possibly in conjunction with the sensing of other stress-or fear-related chemical social cues.

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Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F

Cited by 62 publications

References 56 publications

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Guanylyl cyclase-D in the olfactory CO ₂ neurons is activated by bicarbonate

Grueneberg Ganglion Neurons Are Finely Tuned Cold Sensors

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Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F

Cited by 62 publications

References 56 publications

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Guanylyl cyclase-D in the olfactory CO 2 neurons is activated by bicarbonate

Grueneberg Ganglion Neurons Are Finely Tuned Cold Sensors

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Guanylyl cyclase-D in the olfactory CO ₂ neurons is activated by bicarbonate