Exuberant neuronal convergence onto reduced taste bud targets with preservation of neural specificity in mice overexpressing neurotrophin in the tongue epithelium.
A mouse fungiform taste bud is innervated by only four to five geniculate ganglion neurons; their peripheral fibers do not branch to other buds. We examined whether the degree or specificity of this exclusive innervation pattern is influenced by brain-derived neurotrophic factor (BDNF), a prominent lingual neurotrophin implicated in taste receptoneural development. Labeled ganglion cells were counted after injecting single buds with different color markers in BDNF-lingual-overexpressing (OE) mice. To evaluate the end-organs, taste buds and a class of putative taste receptor cells were counted from progeny of BDNF-OE mice crossbred with green fluorescent protein (GFP) (gustducin) transgenic mice. Fungiform bud numbers in BDNF-OE mice are 35%, yet geniculate neuron numbers are 195%, of wild-type mice. Neurons labeled by single-bud injections in BDNF-OE animals were increased fourfold versus controls. Injecting three buds, each with different color markers, resulted in predominantly single-labeled ganglion cells, a discrete innervation pattern similar to controls. Thus, hyper-innervation of BDNF-OE buds involves many neurons innervating single buds, not increased fiber branching. Therefore, both wild-type and BDNF-OE mice exhibit, in fungiform buds, the same, "discrete" receptoneural pattern, this despite dramatic neurotrophin overexpression-related decreases in bud numbers and increases in innervation density. Hyperinnervation did not affect GFP positive cell numbers; proportions of GFP cells in BDNF-OE buds were the same as in wild-type mice. Total numbers of ganglion cells innervating buds in transgenic mice are similar to controls; the density of taste input to the brain appears maintained despite dramatically reduced receptor organs and increased ganglion cells.
Zaidi
Faisal N
FN
Howard Hughes Medical Institute and Department of Neurobiology, University of California, San Diego, La Jolla, California 92093, USA.
Krimm
Robin F
RF
Whitehead
Mark C
MC
D000818:Animals; D002452:Cell Count; D003433:Crosses, Genetic; D004847:Epithelial Cells / Q000378:metabolism*; D005456:Fluorescent Dyes / Q000493:pharmacokinetics; D005830:Geniculate Ganglion / Q000002:abnormalities / Q000473:pathology; D049452:Green Fluorescent Proteins / Q000096:biosynthesis / Q000235:genetics; D007478:Iontophoresis; D051379:Mice; D008822:Mice, Transgenic; D009414:Nerve Growth Factors / Q000096:biosynthesis* / Q000235:genetics; D009475:Neurons, Afferent / Q000378:metabolism* / Q000473:pathology; D013650:Taste Buds / Q000002:abnormalities* / Q000378:metabolism* / Q000473:pathology; D014059:Tongue / Q000294:innervation*
D005456:Fluorescent Dyes; D009414:Nerve Growth Factors; D049452:Green Fluorescent Proteins