Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae

Randall William Treffy, David Collins, Natalia Hoshino, Son Ton, Gennadiy Aleksandrovich Katsevman, Michael Oleksiak, Elizabeth Marie Runge, David Cho, Matthew Russo, Andrej Spec, Jennifer Gomulka, Mark Henkemeyer, Michael William Rochlin

Research output: Contribution to journalArticle

Abstract

The innervation of taste buds is an excellent model system for studying the guidance of axons during targeting because of their discrete nature and the high fidelity of innervation. The pregustatory epithelium of fungiform papillae is known to secrete diffusible axon guidance cues such as BDNF and Sema3A that attract and repel, respectively, geniculate ganglion axons during targeting, but diffusible factors alone are unlikely to explain how taste axon terminals are restricted to their territories within the taste bud. Nondiffusible cell surface proteins such as Ephs and ephrins can act as receptors and/or ligands for one another and are known to control axon terminal positioning in several parts of the nervous system, but they have not been studied in the gustatory system. We report that ephrin-B2 linked β-galactosidase staining and immunostaining was present along the dorsal epithelium of the mouse tongue as early as embryonic day 15.5 (E15.5), but was not detected at E14.5, when axons first enter the epithelium. Ephrin-B1 immunolabeling was barely detected in the epithelium and found at a somewhat higher concentration in the mesenchyme subjacent to the epithelium. EphB1 and EphB2 were detected in lingual sensory afferents in vivo and geniculate neurites in vitro. Ephrin-B1 and ephrin-B2 were similarly effective in repelling or suppressing outgrowth by geniculate neurites in vitro. These in vitro effects were independent of the neurotrophin used to promote outgrowth, but were reduced by elevated levels of laminin. In vivo, mice null for EphB1 and EphB2 exhibited decreased gustatory innervation of fungiform papillae. These data provide evidence that ephrin-B forward signaling is necessary for normal gustatory innervation of the mammalian tongue.

Original languageEnglish (US)
Pages (from-to)124-138
Number of pages15
JournalDevelopmental Neuroscience
Volume38
Issue number2
DOIs
StatePublished - Jun 1 2016

Fingerprint

Ephrins
Tongue
Epithelium
Ephrin-B1
Ephrin-B2
Taste Buds
Presynaptic Terminals
Axons
Geniculate Ganglion
Semaphorin-3A
Galactosidases
Brain-Derived Neurotrophic Factor
Nerve Growth Factors
Laminin
Mesoderm
Neurites
Nervous System
Cues
Membrane Proteins
Staining and Labeling

Keywords

  • Axon guidance
  • Ephrin-B2
  • Epithelium
  • Laminin
  • Neurotrophin
  • Taste

ASJC Scopus subject areas

  • Neurology
  • Developmental Neuroscience

Cite this

Treffy, R. W., Collins, D., Hoshino, N., Ton, S., Katsevman, G. A., Oleksiak, M., ... Rochlin, M. W. (2016). Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae. Developmental Neuroscience, 38(2), 124-138. https://doi.org/10.1159/000444748

Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae. / Treffy, Randall William; Collins, David; Hoshino, Natalia; Ton, Son; Katsevman, Gennadiy Aleksandrovich; Oleksiak, Michael; Runge, Elizabeth Marie; Cho, David; Russo, Matthew; Spec, Andrej; Gomulka, Jennifer; Henkemeyer, Mark; Rochlin, Michael William.

In: Developmental Neuroscience, Vol. 38, No. 2, 01.06.2016, p. 124-138.

Research output: Contribution to journalArticle

Treffy, RW, Collins, D, Hoshino, N, Ton, S, Katsevman, GA, Oleksiak, M, Runge, EM, Cho, D, Russo, M, Spec, A, Gomulka, J, Henkemeyer, M & Rochlin, MW 2016, 'Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae', Developmental Neuroscience, vol. 38, no. 2, pp. 124-138. https://doi.org/10.1159/000444748
Treffy RW, Collins D, Hoshino N, Ton S, Katsevman GA, Oleksiak M et al. Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae. Developmental Neuroscience. 2016 Jun 1;38(2):124-138. https://doi.org/10.1159/000444748
Treffy, Randall William ; Collins, David ; Hoshino, Natalia ; Ton, Son ; Katsevman, Gennadiy Aleksandrovich ; Oleksiak, Michael ; Runge, Elizabeth Marie ; Cho, David ; Russo, Matthew ; Spec, Andrej ; Gomulka, Jennifer ; Henkemeyer, Mark ; Rochlin, Michael William. / Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae. In: Developmental Neuroscience. 2016 ; Vol. 38, No. 2. pp. 124-138.
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