Axonal transport of neurotrophins by visceral afferent and efferent neurons of the vagus nerve of the rat

Abstract

The receptor-mediated axonal transport of [125I]-labeled neurotrophins by afferent and efferent neurons of the vagus nerve was determined to predict the responsiveness of these neurons to neurotrophins in vivo. [125I]-labeled neurotrophins were administered to the proximal stump of the transected cervical vagus nerve of adult rats. Vagal afferent neurons retrogradely transported [125I]neurotrophin-3 (NT-3), [125I]nerve growth factor (NGF), and [125I]neurotrophin-4 (NT-4) to perikarya in the ipsilateral nodose ganglion, and transganglionically transported [125I]NT-3, [125I]NGF, and [125I]NT-4 to the central terminal field, the nucleus tractus solitarius (NTS). Vagal afferent neurons showed minimal accumulation of [125I]brain-derived neurotrophic factor (BDNF). In contrast, efferent (parasympathetic and motor) neurons located in the dorsal motor nucleus of the vagus and nucleus ambiguus retrogradely transported [125I]BDNF, [125I]NT-3, and [125I]NT-4, but not [125I]NGF. The receptor specificity of neurotrophin transport was examined by applying [125I]-labeled neurotrophins with an excess of unlabeled neurotrophins. The retrograde transport of [125I]NT-3 to the nodose ganglion was reduced by NT-3 and by NGF, and the transport of [125I]NGF was reduced only by NGF, whereas the transport of [125I]NT-4 was significantly reduced by each of the neurotrophins. The competition profiles for the transport of NT-3 and NGF are consistent with the presence of TrkA and TrkC and the absence of TrkB in the nodose ganglion, whereas the profile for NT-4 suggests a p75 receptor-mediated transport mechanism. The transport profiles of neurotrophins by efferent vagal neurons in the dorsal motor nucleus of the vagus and nucleus ambiguus are consistent with the presence of TrkB and TrkC, but not TrkA, in these nuclei. These observations describe the unique receptor-mediated axonal transport of neurotrophins in adult vagal afferent and efferent neurons and thus serve as a template to discern the role of specific neurotrophins in the functions of these visceral sensory and motor neurons in vivo.

BDNF-TrkB signaling interacts with the GABAergic system to inhibit rhythmic swallowing in the rat

“…It seems unlikely that the observed variations in BDNF content could originate from SLN or vagal afferent fibers. Indeed, there are no available data supporting the view that SLN afferent neurons express BDNF mRNA or protein, and vagal afferent fibers do not transport BDNF in an anterograde manner but only in a retrograde manner in adult rats (16). High quantities of BDNF are also expressed within viscera (26).…”

Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

“…In other parts of the embryo, it is known that axons recruit crest cells to the Schwann cell lineage (Noden, 1975). Additionally, the vagus is known to produce a variety of neurotrophic factors (Helke et al, 1998), providing evidence that the extrinsic fibers may trigger the appearance of neurons in these instances, although clearly throughout most of the gut, neurons differentiate in the absence of extrinsic innervation. This finding suggests the possibility of different sets of cues for neuron differentiation within the gut.…”

Inflammation-Induced Plasticity of the Afferent Innervation of the Airways

“…Potential cellular sources for this increase in airway neurotrophins include the respiratory epithelium, T lymphocytes, alveolar macrophages, and mast cells (60)(61)(62). Neurotrophins initiate their effects in vagal afferent neurons, in part, by binding to highaffinity receptors of the tyrosine kinase family, followed by uptake and retrograde transport to the cell body in the vagal ganglia (63). Among the family of neurotrophins most attention has been given to NGF as a potential mediator in afferent plasticity in inflamed airways.…”