Expanded Terminal Fields of Gustatory Nerves Accompany Embryonic BDNF Overexpression in Mouse Oral Epithelia

Sun, Chengsan; Dayal, Arjun; Hill, David L.

doi:10.1523/jneurosci.2381-14.2015

Cited by 17 publications

(25 citation statements)

References 86 publications

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“…A previous study has observed that the overexpression of BDNF in the precursor/progenitor subpopulation increases the number of gustatory neurons that innervate multiple taste buds (Zaidi et al, 2007). Because the same number of chorda tympani neurons innervate the tongue in wild-type and K14-Bdnf -OE mice (Sun et al, 2015), the increased in innervation to taste buds must be due to increased branching. Since innervation density is similar in the taste buds of P5 wild-type and K14-Bdnf -OE mice, the increased branching in adult K14-Bdnf -OE mice (Zaidi et al, 2007) could be due to a blockade of normal refinement between P5 and P10.…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, the overexpression of BDNF in this location may also prevent the postnatal refinement of innervation within the taste bud. The functional consequences of BDNF overexpression in the precursor/progenitor subpopulation are increased sucrose responses relative to other taste stimuli (Sun et al, 2015). One potential explanation for this finding is that these sweet-transducing taste cells are innervated by nerve fibers whose innervation would normally be eliminated if BDNF had not been overexpressed.…”

Section: Discussionmentioning

confidence: 99%

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Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Huang

Krimm

2015

Developmental Biology

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The refinement of innervation is a common developmental mechanism that serves to increase the specificity of connections following initial innervation. In the peripheral gustatory system, the extent to which innervation is refined and how refinement might be regulated is unclear. The initial innervation of taste buds is controlled by brain-derived neurotrophic factor (BDNF). Following initial innervation, taste receptor cells are added and become newly innervated. The connections between the taste receptor cells and nerve fibers are likely to be specific in order to retain peripheral coding mechanisms. Here, we explored the possibility that the down-regulation of BDNF regulates the refinement of taste bud innervation during postnatal development. An analysis of BDNF expression in BdnflacZ/+ mice and real-time reverse transcription polymerase chain reaction (RT-PCR) revealed that BDNF was down-regulated between postnatal day (P) 5 and P10. This reduction in BDNF expression was due to a loss of precursor/progenitor cells that express BDNF, while the expression of BDNF in the subpopulations of taste receptor cells did not change. Gustatory innervation, which was identified by P2X3 immunohistochemistry, was lost around the perimeter where most progenitor/precursor cells are located. In addition, the density of innervation in the taste bud was reduced between P5 and P10, because taste buds increase in size without increasing innervation. This reduction of innervation density was blocked by the overexpression of BDNF in the precursor/progenitor population of taste bud cells. Together these findings indicate that the process of BDNF restriction to a subpopulation of taste receptor cells between P5 and P10, results in a refinement of gustatory innervation. We speculate that this refinement results in an increased specificity of connections between neurons and taste receptor cells during development.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Huang

Krimm

2015

Developmental Biology

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“…Procedures used to label the chorda tympani and greater superficial nerves with fluorescent tracers were previously described (Sun, Dayal, & Hill, 2015;Sun, Hummler, & Hill, 2017). Adult Phox2b-Cre:tdTomato mice were anesthetized in the same manner as with CT-nerve section.…”

Section: Fluorescent Anterograde Nerve Labelingmentioning

confidence: 99%

The transcription factor Phox2b distinguishes between oral and non‐oral sensory neurons in the geniculate ganglion

Ohman-Gault

Huang

Krimm

2017

J of Comparative Neurology

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Many basic characteristics of gustatory neurons remain unknown, partly due to the absence of specific markers. Some neurons in the geniculate ganglion project to taste regions in the oral cavity, whereas others innervate the outer ear. We hypothesized that the transcription factor Phox2b would identify oral cavity-projecting neurons in the geniculate ganglion. To test this possibility, we characterized mice in which Phox2b-Cre mediated gene recombination labeled neurons with tdTomato. Nerve labeling revealed that all taste neurons projecting through the chorda tympani (27%) and greater superficial petrosal nerves (15%) expressed Phox2b during development, whereas non-oral somatosensory neurons (58%) in the geniculate ganglion did not. We found tdTomato-positive innervation within all taste buds. Most (57%) of the fungiform papillae had labeled innervation only in taste buds, whereas 43% of the fungiform papillae also had additional labeled innervation to the papilla epithelium. Chorda tympani nerve transection eliminated all labeled innervation to taste buds, but most of the additional innervation in the fungiform papillae remained. Some of these additional fibers also expressed tyrosine hydroxylase, suggesting a sympathetic origin. Consistent with this, both sympathetic and parasympathetic fibers innervating blood vessels and salivary glands contained tdTomato labeling. Phox2b-tdTomato labels nerve fascicles in the tongue of the developing embryo and demonstrates a similar stereotyped branching pattern DiI-labeling.

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“…The CT, glossopharyngeal (GL; the nerve that innervates taste buds in circumvallate and posterior foliate papillae), and greater superficial petrosal (GSP; which innervates taste buds in the soft palate, nasoincisor duct, and geschmacksstreifen) terminal fields normally prune in volume by roughly one-third between P15 and adulthood (Sollars et al, 2006;Mangold and Hill, 2008). The size of gustatory terminal fields is influenced by diet (Pittman and Contreras, 2002;May and Hill, 2006;Sollars et al, 2006;Thomas and Hill, 2008), taste receptor protein expression (Skyberg et al, 2017;Sun et al, 2017), and neurotrophic factors (Sun et al, 2015;.…”

Section: Glossarymentioning

confidence: 99%

Regenerative Failure Following Rat Neonatal Chorda Tympani Transection is Associated with Geniculate Ganglion Cell Loss and Terminal Field Plasticity in the Nucleus of the Solitary Tract

Martin

Lane

Samson

et al. 2018

Preprint

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Neural insult during development results in recovery outcomes that vary dependent upon the system under investigation. Nerve regeneration does not occur if the rat gustatory chorda tympani nerve is sectioned (CTX) during neonatal (≤ P10) development. It is unclear how chorda tympani soma and terminal fields are affected after neonatal CTX. The current study determined the impact of neonatal CTX on chorda tympani neurons and brainstem gustatory terminal fields.To assess terminal field volume in the nucleus of the solitary tract (NTS), rats received CTX at P5 or P10 followed by chorda tympani label, or glossopharyngeal (GL) and greater superficial petrosal (GSP) label as adults. In another group of animals, terminal field volumes and numbers of chorda tympani neurons in the geniculate ganglion (GG) were determined by labeling the chorda tympani with DiI at the time of CTX in neonatal (P5) and adult (P50) rats. There was a greater loss of chorda tympani neurons following P5 CTX compared to adult denervation.Chorda tympani terminal field volume was dramatically reduced 50 days after P5 or P10 CTX.Lack of nerve regeneration after neonatal CTX is not caused by ganglion cell death alone, as approximately 30% of chorda tympani neurons survived into adulthood. Although the total field volume of intact gustatory nerves was not altered, the GSP volume and GSP-GL overlap increased in the dorsal NTS after CTX at P5, but not P10, demonstrating age-dependent plasticity. Our findings indicate that the developing gustatory system is highly plastic and simultaneously vulnerable to injury. Highlights• The volume of chorda tympani central processes is severely diminished after the nerve is sectioned in 5-or 10-day-old rats.• Compared to adult injury, neonatal denervation produced greater loss of terminal field and ganglion cell bodies.• About 30% of chorda tympani neurons survive early section, suggesting lack of regeneration is not caused by cell loss alone.• The organization of intact gustatory terminal fields is altered by early chorda tympani nerve section.2004; Reddaway et al., 2012), but it is not clear how the CT itself is impacted by neonatal CTX.The present study was designed to determine the effects of neonatal CTX on CT neurons and intact nerve terminal fields of the GL and GSP. To examine this, gustatory nerve terminal fields were labeled following neonatal CTX, and CT neurons in the GG were examined after neonatal or adult CT denervation. We found that neonatal CTX caused a profound loss of CT terminal field and ganglion cells and altered the organization of intact gustatory terminal fields. Experimental Procedures SubjectsFemale Sprague-Dawley rats (n = 47) were used for these experiments. Rats were bred in the University of Nebraska at Omaha vivarium. The day of birth was designated P0, and animals were weaned at P25. Rats were socially housed in clear Plexiglas cages where they had free access to food pellets (Teklad or Labdiet) and tap water. Animals were kept on a 12:12 light-dark cycle. All procedures were approve...

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Expanded Terminal Fields of Gustatory Nerves Accompany Embryonic BDNF Overexpression in Mouse Oral Epithelia

Cited by 17 publications

References 86 publications

Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

Postnatal reduction of BDNF regulates the developmental remodeling of taste bud innervation

The transcription factor Phox2b distinguishes between oral and non‐oral sensory neurons in the geniculate ganglion

Regenerative Failure Following Rat Neonatal Chorda Tympani Transection is Associated with Geniculate Ganglion Cell Loss and Terminal Field Plasticity in the Nucleus of the Solitary Tract

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