Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation

Nosrat, Christopher A.; Ebendal, Ted; Olson, Lar̀s

doi:10.1002/(sici)1096-9861(19961223)376:4<587::aid-cne7>3.0.co;2-y

Cited by 117 publications

(92 citation statements)

References 69 publications

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“…BDNF is produced in developing gustatory epithelia and taste buds, while NT3 is produced by epithelia surrounding the taste buds (Nosrat andOlson, 1995, 1998;Nosrat et al, 1996Nosrat et al, , 2001Nosrat, 1998). It is possible that neurotrophins produced in or around taste buds bind directly to p75 receptors and influence taste buds via autocrine or paracrine mechanisms.…”

Section: Discussionmentioning

confidence: 99%

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

Krimm

2006

Anat. Rec.

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Brain-derived neurotrophic factor and neurotrophin-4 are required for normal taste bud development. Although these neurotrophins normally function via the tyrosine kinase receptor, trkB, they also bind to the panneurotrophin receptor, p75. The goal of the present study was to determine whether the p75 receptor is required for the development or maintenance of a full complement of adult taste buds. Mice with p75 null mutations lose 34% of their circumvallate taste buds, 36% of their fungiform papillae, and 26% of their fungiform taste buds by adulthood. The reduction of taste buds in the adult circumvallate papilla was similar to that observed previously at postnatal day 7 (Fan et al. Brain Res Dev Brain Res 2004;150:23-39). Taken together, these findings indicate that the p75 receptor is critical for the development of a full complement of taste buds, but is not required for maintenance of circumvallate taste buds in adulthood. Immunolabeling for p75 was not observed in taste buds, indicating that p75 signaling influences taste bud number indirectly. Geniculate ganglion neurons, which provides innervation to fungiform taste buds, express the p75 receptor. Mice with p75 null mutations also have fewer neurons in the geniculate ganglion. Together, these results suggest that the p75 receptor is important for the survival of geniculate neurons and geniculate neuron survival is required for the development of a full complement of taste buds by adulthood.

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Section: Discussionmentioning

confidence: 99%

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

Krimm

2006

Anat. Rec.

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“…BDNF mRNA is expressed in the epithelium of the developing gustatory papillae prior to the formation of taste buds and continues to be expressed throughout adulthood (Nosrat et al, 1996;Nosrat and Olson, 1995). NT3 mRNA is located in those areas were BDNF is not expressed, such as the superior surface and the lateral epithelium of the fungiform papillae (Nosrat et al, 1996) (Fig.…”

Section: The Nt3/nt3 Alleles Supports Neither Survival Of Taste Neuromentioning

confidence: 99%

BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development

et al. 2003

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Neurotrophins have multiple functions during peripheral nervous system development such as controlling neuronal survival, target innervation and synaptogenesis. Neurotrophin specificity has been attributed to the selective expression of the Trk tyrosine kinase receptors in different neuronal subpopulations. However, despite overlapping expression of TrkB and TrkC in many sensory ganglia, brain-derived neurotrophic factor (BDNF) and neurotrophin 3 (NT3) null mutant mice display selective losses in neuronal subpopulations. In the present study we have replaced the coding part of theBDNF gene in mice with that of NT3 (BDNFNT3/NT3)to analyse the specificity and selective roles of BDNF and NT3 during development. Analysis of BDNFNT3/NT3 mice showed striking differences in the ability of NT3 to promote survival, short-range innervation and synaptogenesis in different sensory systems. In the cochlea, specificity is achieved by a tightly controlled spatial and temporal ligand expression. In the vestibular system TrkB or TrkC activation is sufficient to promote vestibular ganglion neuron survival, while TrkB activation is required to promote proper innervation and synaptogenesis. In the gustatory system, NT3 is unable to replace the actions of BDNF possibly because of a temporally selective expression of TrkB in taste neurons. We conclude that there is no general mechanism by which neurotrophin specificity is attained and that specificity is achieved by (i) a tightly controlled spatial and temporal expression of ligands, (ii) different Trk receptors playing distinct roles within the same neuronal subpopulation, or (iii) selective receptor expression in sensory neuron subpopulations.

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“…8 D), where the highest number of fungiform papillae is normally observed. Fungiform papillae in the posterior part of the tongue are generally larger than those located anteriorly in wild-type mice (Nosrat et al, 1996(Nosrat et al, , 1997a. Fungiform papillae in BDN F-transgenic mice (Fig.…”

Section: Abnormal Tongue Surface Morphologymentioning

confidence: 99%

Role of Brain-Derived Neurotrophic Factor in Target Invasion in the Gustatory System

1999

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Brain-derived neurotrophic factor (BDNF) is a survival factor for different classes of neurons, including gustatory neurons. We have studied innervation and development of the gustatory system in transgenic mice overexpressing BDNF under the control of regulatory sequences from the nestin gene, an intermediate filament gene expressed in precursor cells of the developing nervous system and muscle. In transgenic mice, the number and size of gustatory papillae were decreased, circumvallate papillae had a deranged morphology, and there was also a severe loss of lingual taste buds. Paradoxically, similar deficits have been found in BDNF knock-out mice, which lack gustatory neurons. However, the number of neurons in gustatory ganglia was increased in BDNF-overproducing mice. Although gustatory fibers reached the tongue in normal numbers, the amount and density of nerve fibers in gustatory papillae were reduced in transgenic mice compared with wild-type littermates. Gustatory fibers appeared stalled at the base of the tongue, a site of ectopic BDNF expression, where they formed abnormal branches and sprouts. Interestingly, palatal taste buds, which are innervated by gustatory neurons whose afferents do not traverse sites of ectopic BDNF expression, appeared unaffected. We suggest that lingual gustatory deficits in BDNF overexpressing mice are a consequence of the failure of their BDNF-dependent afferents to reach their targets because of the effects of ectopically expressed BDNF on fiber growth. Our findings suggest that mammalian taste buds and gustatory papillae require proper BDNF-dependent gustatory innervation for development and that the correct spatial expression of BDNF in the tongue epithelium is crucial for appropriate target invasion and innervation. Key words: taste buds; gustatory; neurotrophins; gustation; transgenic; innervationThe peripheral gustatory system offers an interesting model for the study of target innervation and interaction between ingrowing nerves and neurotrophins. Developmental and experimental studies of gustatory papillae and taste buds have also offered information about the mechanisms underlying sensory organ development and maintenance in the tongue. Lingual papillae cover the dorsal surface of the tongue in mammals. Lingual gustatory papillae, namely f ungiform, circumvallate, and foliate papillae contain taste buds that are specialized peripheral sensory organs involved in perceiving chemical stimuli and in taste transduction. Fungiform papillae are located on the anterior dorsal surface of the tongue, and a single circumvallate papilla is located in the midline at the posterior part of the tongue in rodents. Lingual taste buds are innervated by nerve cells residing in the geniculate and petrosal ganglia. The somatosensory innervation of the posterior part of the tongue is derived from the petrosal ganglion, whereas trigeminal neurons provide somatosensory innervation to the anterior part of the tongue. Gustatory nerves innervate taste receptor cells in taste buds, whereas the sur...

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Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation

Cited by 117 publications

References 69 publications

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development

Role of Brain-Derived Neurotrophic Factor in Target Invasion in the Gustatory System

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