Support of trigeminal sensory neurons by nonneuronal p75 neurotrophin receptors

• Published in: Brain research. Developmental brain research Vol. 150; no. 1; pp. 23 - 39
• Main Authors: Fan, Lixin, Girnius, Saulius, Oakley, Bruce
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 19-05-2004
• Subjects: Animals; Brain-derived neurotrophic factor; Cell Communication - physiology; Cell Differentiation - physiology; Cells, Cultured; Coculture Techniques; Down-Regulation - physiology; Epithelial Cells - cytology; Epithelial Cells - metabolism; Female; Fibroblasts - metabolism; Geniculate ganglion; Geniculate Ganglion - cytology; Geniculate Ganglion - growth & development; Geniculate Ganglion - metabolism; Lac Operon - genetics; Lingual somatosensory receptor; Male; Mice; Mice, Knockout; Neurites - metabolism; Neurons, Afferent - cytology; Neurons, Afferent - metabolism; Neurotrophin 3 - deficiency; Neurotrophin-3; Receptor, Nerve Growth Factor; Receptors, Nerve Growth Factor - metabolism; Taste bud; Taste Buds - cytology; Taste Buds - growth & development; Taste Buds - metabolism; Tongue - innervation; Trigeminal Ganglion - cytology; Trigeminal Ganglion - growth & development; Trigeminal Ganglion - metabolism; Trigeminal neuron; TrkC; Geniculate ganglion; TrkC; Brain-derived neurotrophic factor; Neurotrophin-3; Trigeminal neuron; Development and regeneration; Lingual somatosensory receptor; Taste bud
• ISSN: 0165-3806
• DOI: 10.1016/j.devbrainres.2004.02.008

The p75 neurotrophin receptor (p75NTR) binds all four mammalian neurotrophins, including neurotrophin-3 (NT-3) required for the development of select sensory neurons. This study demonstrated that many gustatory and somatosensory neurons of the tongue depend upon p75NTR. Each of thousands of filiform papillae at the front of the tongue as well as each somatosensory prominence at the back of the tongue has a small cluster of p75NTR-positive epithelial cells that is targeted by somatosensory innervation. This expression of p75NTR by epithelial target cells required NT-3 but not adult innervation. NT-3-secreting cells were adjacent to the p75NTR-positive target cells of each somatosensory organ, as demonstrated in
NT-3(lacZneo) transgenic mice. In
NT-3 null mutant mice, there were few lingual somatosensory neurons. In
p75NTR null mutant mice, the lingual somatosensory axons were likewise absent or had deficient terminal arborizations. Cell culture indicated that substrate p75NTR can influence neuronal outgrowth. Specifically, dissociated trigeminal sensory neurons more than doubled their neurite lengths when grown on a lawn of p75NTR-overexpressing fibroblasts. This enhancement of neurite outgrowth by fibroblast p75NTR raises the possibility that epithelial target cell p75NTR may help to promote axonal arborization in vivo. The co-occurrence in
p75NTR null mice of a 35% reduction in geniculate ganglion taste neurons and a shortfall of taste buds is consistent with the established role of gustatory innervation in prompting mammalian taste receptor cell differentiation.