Onset of taste bud cell renewal starts at birth and coincides with a shift in SHH function

  1. Erin J Golden
  2. Eric D Larson
  3. Lauren A Shechtman
  4. G Devon Trahan
  5. Dany Gaillard
  6. Timothy J Fellin
  7. Jennifer K Scott
  8. Kenneth L Jones
  9. Linda A Barlow  Is a corresponding author
  1. University of Colorado Anschutz Medical Campus, United States
  2. University of Oklahoma Health Sciences Center, United States

Abstract

Embryonic taste bud primordia are specified as taste placodes on the tongue surface and differentiate into the first taste receptor cells (TRCs) at birth. Throughout adult life, TRCs are continually regenerated from epithelial progenitors. Sonic hedgehog (SHH) signaling regulates TRC development and renewal, repressing taste fate embryonically, but promoting TRC differentiation in adults. Here, using mouse models, we show TRC renewal initiates at birth and coincides with onset of SHHs pro-taste function. Using transcriptional profiling to explore molecular regulators of renewal, we identified Foxa1 and Foxa2 as potential SHH target genes in lingual progenitors at birth, and show SHH overexpression in vivo alters FoxA1 and FoxA2 expression relevant to taste buds. We further bioinformatically identify genes relevant to cell adhesion and cell locomotion likely regulated by FOXA1;FOXA2, and show expression of these candidates is also altered by forced SHH expression. We present a new model where SHH promotes TRC differentiation by regulating changes in epithelial cell adhesion and migration.

Data availability

Sequencing data have been deposited in GEO under accession code GSE159941https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE159941

Article and author information

Author details

  1. Erin J Golden

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Eric D Larson

    Otolaryngology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Lauren A Shechtman

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. G Devon Trahan

    Pediatrics, Section of Hematology, Oncology and Bone Marrow Transplant, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Dany Gaillard

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Timothy J Fellin

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jennifer K Scott

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Kenneth L Jones

    Cell Biology, University of Oklahoma Health Sciences Center, Oklahama City, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Linda A Barlow

    Cell and Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    For correspondence
    LINDA.BARLOW@CUANSCHUTZ.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7998-2219

Funding

National Institute on Deafness and Other Communication Disorders (R01DC012383)

  • Linda A Barlow

National Institute on Deafness and Other Communication Disorders (Postdoc fellowship F32DC015958)

  • Erin J Golden

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Male and female mice were maintained, bred, and embryos and pups at the University of Colorado Anschutz Medical Campus (CU AMC) in accordance with approved protocols #00150 and #52815(02)1C by the Institutional Animal Care and Use Committee at CU AMC. All animals were euthanized via chilling and CO2 prior to tissue harvest to minimize suffering.

Reviewing Editor

  1. Valerie Horsley, Yale University, United States

Publication history

  1. Received: October 14, 2020
  2. Accepted: May 18, 2021
  3. Accepted Manuscript published: May 19, 2021 (version 1)
  4. Version of Record published: June 2, 2021 (version 2)

Copyright

© 2021, Golden et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Erin J Golden
  2. Eric D Larson
  3. Lauren A Shechtman
  4. G Devon Trahan
  5. Dany Gaillard
  6. Timothy J Fellin
  7. Jennifer K Scott
  8. Kenneth L Jones
  9. Linda A Barlow
(2021)
Onset of taste bud cell renewal starts at birth and coincides with a shift in SHH function
eLife 10:e64013.
https://doi.org/10.7554/eLife.64013

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