Temporal regulation of neuropilin‐1 expression and sensitivity to semaphorin 3A in NGF‐ and NT3‐responsive chick sensory neurons

Pond, Ausra; Roche, Florence K.; Letourneau, Paul C.

doi:10.1002/neu.10041

Cited by 35 publications

(43 citation statements)

References 31 publications

(44 reference statements)

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“…2a-c). These results closely resemble the B48% reduction that was reported for the chick 41 . Importantly, only a mild decrease was observed for cutaneous axons at E14 and E15 (7 and 5%, respectively), consistent with the continual Sema3A sensitivity of this axonal subtype (Fig.…”

Section: Resultssupporting

confidence: 90%

“…Proprioceptive axons' loss of responsiveness to Sema3A is a conserved developmental process, which has been demonstrated for mouse and chick 37,41 . In rat, proprioceptive axons are already insensitive to Sema3A at embryonic day 14 (E14) 36 .…”

Section: Resultsmentioning

confidence: 91%

“…In chick, loss of responsiveness to Sema3A correlates with a sharp decrease in Nrp1 levels 41 . To test the relevance of these observations to mammals, we examined Nrp1's expression in rat embryonic DRG neurons.…”

Section: Resultsmentioning

confidence: 99%

“…In early stages of development, proprioceptive axons are also repelled by Sema3A. However, as they penetrate the spinal cord and progress towards their ventral targets, these axons lose sensitivity to the repellant by downregulating its receptor, Nrp1 40,41 . Here we show that downregulation of Nrp1 is facilitated by ADAM MPs, which cleave the receptor from the surface of growth cones at a precise developmental time point.…”

Section: Resultsmentioning

confidence: 99%

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ADAM metalloproteases promote a developmental switch in responsiveness to the axonal repellant Sema3A

et al. 2014

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During embryonic development, axons can gain and lose sensitivity to guidance cues, and this flexibility is essential for the correct wiring of the nervous system. Yet, the underlying molecular mechanisms are largely unknown. Here we show that receptor cleavage by ADAM (A Disintegrin And Metalloprotease) metalloproteases promotes murine sensory axons loss of responsiveness to the chemorepellant Sema3A. Genetic ablation of ADAM10 and ADAM17 disrupts the developmental downregulation of Neuropilin-1 (Nrp1), the receptor for Sema3A, in sensory axons. Moreover, this is correlated with gain of repulsive response to Sema3A. Overexpression of Nrp1 in neurons reverses axonal desensitization to Sema3A, but this is hampered in a mutant Nrp1 with high susceptibility to cleavage. Lastly, we detect guidance errors of proprioceptive axons in ADAM knockouts that are consistent with enhanced response to Sema3A. Our results provide the first evidence for involvement of ADAMs in regulating developmental switch in responsiveness to axonal guidance cues.

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Section: Resultssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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ADAM metalloproteases promote a developmental switch in responsiveness to the axonal repellant Sema3A

et al. 2014

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“…In neuropilin or Sema3A knockout mice both peripheral and central TG axons expand out and invade territories they normally would not [21,42]. Studies in the chick also show spatiotemporal regulation of Sema 3A and neuropilin expression in the spinal cord and DRG [35]. In vitro assays indicate that neurotrophins can differentially modify growth cone responses to Sema 3A [40].…”

Section: Neurotrophins and Axon Guidance Molecules In Construction Ofmentioning

confidence: 96%

Local neurotrophin effects on central trigeminal axon growth patterns

Özdinler

Ulupinar

Erzurumlu

2004

Developmental Brain Research

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In dissociated cell and wholemount explant cultures of the embryonic trigeminal pathway NGF promotes exuberant elongation of trigeminal ganglion (TG) axons, whereas NT-3 leads to precocious arborization [J. Comp. Neurol. 425 (2000) 202]. In the present study, we investigated the axonal effects of local applications of NGF and NT-3. We placed small sepharose beads loaded with either NGF or NT-3 along the lateral edge of the central trigeminal tract in TGbrainstem intact wholemount explant cultures prepared from embryonic day 15 rats. Labeling of the TG with carbocyanine dye, DiI, revealed that NGF induces local defasciculation and diversion of trigeminal axons. Numerous axons leave the tract, grow towards the bead and engulf it, while some axons grow away from the neurotrophin source. NT-3, on the other hand, induced localized interstitial branching and formation of neuritic tangles in the vicinity of the neurotrophin source. Double immunocytochemistry showed that axons responding to NGF were predominantly TrkApositive, whereas both TrkA and TrkC-positive axons responded to NT-3. Our results indicate that localized neurotrophin sources along the routes of embryonic sensory axons in the central nervous system, far away from their parent cell bodies, can alter restricted axonal pathways and induce elongation, arborization responses. D

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Molecular determinants of the face map development in the trigeminal brainstem

2006

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The perception of external sensory information by the brain requires highly ordered synaptic connectivity between peripheral sensory neurons and their targets in the central nervous system. Since the discovery of the whisker-related barrel patterns in the mouse cortex, the trigeminal system has become a favorite model for study of how its connectivity and somatotopic maps are established during development. The trigeminal brainstem nuclei are the first CNS regions where whisker-specific neural patterns are set up by the trigeminal afferents that innervate the whiskers. In particular, barrelette patterns in the principal sensory nucleus of the trigeminal nerve provide the template for similar patterns in the face representation areas of the thalamus and subsequently in the primary somatosensory cortex. Here, we describe and review studies of neurotrophins, multiple axon guidance molecules, transcription factors, and glutamate receptors during early development of trigeminal connections between the whiskers and the brainstem that lead to emergence of patterned face maps. Studies from our laboratories and others' showed that developing trigeminal ganglion cells and their axons depend on a variety of molecular signals that cooperatively direct them to proper peripheral and central targets and sculpt their synaptic terminal fields into patterns that replicate the organization of the whiskers on the muzzle. Similar mechanisms may also be used by trigeminothalamic and thalamocortical projections in establishing patterned neural modules upstream from the trigeminal brainstem. The somatotopic map forms sequentially, beginning at the periphery and ending in the primary somatosensory cortex. In some species, such as rodents, neural modules form within the CNS body maps that correspond to patterned distribution of the sensory receptors in the periphery. In the mouse and rat muzzle, whiskers and sinus hairs are patterned in discrete arrays with constant numbers in each row of follicles (Yamakado and Yohro, 1979;Dörfl, 1985;Rice et al., 1986Rice et al., , 1993Brecht et al., 1997). The infraobital nerve (ION) of the trigeminal ganglion (TG) innervates the whisker pad and relays the whiskerrelated information to the principal sensory nucleus (PrV) in the brainstem, which in turn conveys the signals to the thalamus and the cortex via ascending afferents. The trigeminal brainstem complex also contains the spinal trigeminal nucleus, including subnuclei oralis (SpVo), inter-*Correspondence to: Reha S. Erzurumlu,

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Temporal regulation of neuropilin‐1 expression and sensitivity to semaphorin 3A in NGF‐ and NT3‐responsive chick sensory neurons

Cited by 35 publications

References 31 publications

ADAM metalloproteases promote a developmental switch in responsiveness to the axonal repellant Sema3A

ADAM metalloproteases promote a developmental switch in responsiveness to the axonal repellant Sema3A

Local neurotrophin effects on central trigeminal axon growth patterns

Molecular determinants of the face map development in the trigeminal brainstem

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