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 language | English (US) |
|---|---|
| Pages (from-to) | 124-138 |
| Number of pages | 15 |
| Journal | Developmental Neuroscience |
| Volume | 38 |
| Issue number | 2 |
| DOIs | |
| State | Published - Jun 1 2016 |
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Keywords
- Axon guidance
- Ephrin-B2
- Epithelium
- Laminin
- Neurotrophin
- Taste
ASJC Scopus subject areas
- Neurology
- Developmental Neuroscience
Cite this
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 journal › Article
}
TY - JOUR
T1 - Ephrin-B/EphB Signaling Is Required for Normal Innervation of Lingual Gustatory Papillae
AU - Treffy, Randall William
AU - Collins, David
AU - Hoshino, Natalia
AU - Ton, Son
AU - Katsevman, Gennadiy Aleksandrovich
AU - Oleksiak, Michael
AU - Runge, Elizabeth Marie
AU - Cho, David
AU - Russo, Matthew
AU - Spec, Andrej
AU - Gomulka, Jennifer
AU - Henkemeyer, Mark
AU - Rochlin, Michael William
PY - 2016/6/1
Y1 - 2016/6/1
N2 - 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.
AB - 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.
KW - Axon guidance
KW - Ephrin-B2
KW - Epithelium
KW - Laminin
KW - Neurotrophin
KW - Taste
UR - http://www.scopus.com/inward/record.url?scp=84977159873&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84977159873&partnerID=8YFLogxK
U2 - 10.1159/000444748
DO - 10.1159/000444748
M3 - Article
C2 - 27035151
AN - SCOPUS:84977159873
VL - 38
SP - 124
EP - 138
JO - Developmental Neuroscience
JF - Developmental Neuroscience
SN - 0378-5866
IS - 2
ER -