Taste buds are not derived from neural crest in mouse, chicken, and zebrafish

Wenxin Yu, Zhonghou Wang, Brett Marshall, Yuta Yoshida, Renita Patel, Xiaogang Cui, Rebecca Ball, Linlin Yin, Fuminori Kawabata, Shoji Tabata, Wenbiao Chen, Robert N. Kelsh, James D. Lauderdale, Hong Xiang Liu

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Abstract

Our lineage tracing studies using multiple Cre mouse lines showed a concurrent labeling of abundant taste bud cells and the underlying connective tissue with a neural crest (NC) origin, warranting a further examination on the issue of whether there is an NC derivation of taste bud cells. In this study, we mapped NC cell lineages in three different models, Sox10-iCreERT2/tdT mouse, GFP+ neural fold transplantation to GFP chickens, and Sox10-Cre/GFP-RFP zebrafish model. We found that in mice, Sox10-iCreERT2 specifically labels NC cell lineages with a single dose of tamoxifen at E7.5 and that the labeled cells were widely distributed in the connective tissue of the tongue. No labeled cells were found in taste buds or the surrounding epithelium in the postnatal mice. In the GFP+/GFP chicken chimera model, GFP+ cells migrated extensively to the cranial region of chicken embryos ipsilateral to the surgery side but were absent in taste buds in the base of oral cavity and palate. In zebrafish, Sox10-Cre/GFP-RFP faithfully labeled known NC-derived tissues but did not label taste buds in lower jaw or the barbel. Our data, together with previous findings in axolotl, indicate that taste buds are not derived from NC cells in rodents, birds, amphibians or teleost fish.

Original languageEnglish
Pages (from-to)76-88
Number of pages13
JournalDevelopmental Biology
Volume471
Early online date14 Dec 2020
DOIs
Publication statusPublished - 31 Mar 2021

Bibliographical note

Funding Information:
The authors give thanks to Shi-You Chen, Luke Mortensen, Steven Stice, and Franklin West, (Regenerative Bioscience Center, The University of Georgia, Athen, Georgia) for the discussion and feedbacks; to Mary Redmond Hutson (Duke University, Durham, NC) and Richard Schneider (University of California at San Francisco, San Francisco, CA) as consultants for chicken chimera surgery; to Paul Trainor (Stowers Institute for Medical Research), Prasangi Rajapaksha (University of Kentucky, Lexington, KY), Jason Payne and Robert Beckstead (University of Georgia, Athens, GA) for technical assistance of labeling NC cells in chicken model, and The Jackson Laboratory for transgenic mouse lines. This study was supported by the National Institutes of Health , grant number R01DC012308 and R21DC018089 to HXL; R01NS090645 to JDL.

Publisher Copyright:
© 2020 Elsevier Inc.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Funding

The authors give thanks to Shi-You Chen, Luke Mortensen, Steven Stice, and Franklin West, (Regenerative Bioscience Center, The University of Georgia, Athen, Georgia) for the discussion and feedbacks; to Mary Redmond Hutson (Duke University, Durham, NC) and Richard Schneider (University of California at San Francisco, San Francisco, CA) as consultants for chicken chimera surgery; to Paul Trainor (Stowers Institute for Medical Research), Prasangi Rajapaksha (University of Kentucky, Lexington, KY), Jason Payne and Robert Beckstead (University of Georgia, Athens, GA) for technical assistance of labeling NC cells in chicken model, and The Jackson Laboratory for transgenic mouse lines. This study was supported by the National Institutes of Health, grant number R01DC012308 and R21DC018089 to HXL; R01NS090645 to JDL. The authors give thanks to Shi-You Chen, Luke Mortensen, Steven Stice, and Franklin West, (Regenerative Bioscience Center, The University of Georgia, Athen, Georgia) for the discussion and feedbacks; to Mary Redmond Hutson (Duke University, Durham, NC) and Richard Schneider (University of California at San Francisco, San Francisco, CA) as consultants for chicken chimera surgery; to Paul Trainor (Stowers Institute for Medical Research), Prasangi Rajapaksha (University of Kentucky, Lexington, KY), Jason Payne and Robert Beckstead (University of Georgia, Athens, GA) for technical assistance of labeling NC cells in chicken model, and The Jackson Laboratory for transgenic mouse lines. This study was supported by the National Institutes of Health , grant number R01DC012308 and R21DC018089 to HXL; R01NS090645 to JDL.

FundersFunder number
Jackson Laboratory for transgenic mouse lines
Regenerative Bioscience Center
National Institutes of HealthR21DC018089, R01NS090645, R01DC012308
University of Georgia

    Keywords

    • Chicken
    • Mouse
    • Neural crest
    • Progenitors
    • Taste buds
    • Zebrafish

    ASJC Scopus subject areas

    • Molecular Biology
    • Developmental Biology
    • Cell Biology

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