Developmental plasticity of epithelial stem cells in tooth and taste bud renewal

Ryan F. Bloomquist, Teresa E. Fowler, Zhengwen An, Tian Y. Yu, Kawther Abdilleh, Gareth J. Fraser, Paul T. Sharpe, J. Todd Streelman

Research output: Contribution to journalArticle

Abstract

In Lake Malawi cichlids, each tooth is replaced in one-for-one fashion every ~20 to 50 d, and taste buds (TBs) are continuously renewed as in mammals. These structures are colocalized in the fish mouth and throat, from the point of initiation through adulthood. Here, we found that replacement teeth (RT) share a continuous band of epithelium with adjacent TBs and that both organs coexpress stem cell factors in subsets of label-retaining cells. We used RNA-seq to characterize transcriptomes of RT germs and TBbearing oral epithelium. Analysis revealed differential usage of developmental pathways in RT compared to TB oral epithelia, as well as a repertoire of genome paralogues expressed complimentarily in each organ. Notably, BMP ligands were expressed in RT but excluded from TBs. Morphant fishes bathed in a BMP chemical antagonist exhibited RT with abrogated shh expression in the inner dental epithelium (IDE) and ectopic expression of calb2 (a TB marker) in these very cells. In the mouse, teeth are located on the jaw margin while TBs and other oral papillae are located on the tongue. Previous study reported that tongue intermolar eminence (IE) oral papillae of Follistatin (a BMP antagonist) mouse mutants exhibited dysmorphic invagination.We used these mutants to demonstrate altered transcriptomes and ectopic expression of dental markers in tongue IE. Our results suggest that vertebrate oral epithelium retains inherent plasticity to form tooth and taste-like cell types, mediated by BMP specification of progenitor cells. These findings indicate underappreciated epithelial cell populationswith promising potential in bioengineering and dental therapeutics.

Original languageEnglish (US)
Pages (from-to)17858-17866
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number36
DOIs
StatePublished - Sep 3 2019

Fingerprint

Taste Buds
Tooth
Stem Cells
Epithelial Cells
Epithelium
Tongue
Transcriptome
Fishes
Follistatin
Tooth Germ
Cichlids
Malawi
Bioengineering
Stem Cell Factor
Lakes
Pharynx
Jaw
Mouth
Vertebrates
Mammals

Keywords

  • Regeneration
  • Stem cells
  • Taste buds
  • Teeth

ASJC Scopus subject areas

  • General

Cite this

Developmental plasticity of epithelial stem cells in tooth and taste bud renewal. / Bloomquist, Ryan F.; Fowler, Teresa E.; An, Zhengwen; Yu, Tian Y.; Abdilleh, Kawther; Fraser, Gareth J.; Sharpe, Paul T.; Streelman, J. Todd.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 36, 03.09.2019, p. 17858-17866.

Research output: Contribution to journalArticle

Bloomquist, Ryan F. ; Fowler, Teresa E. ; An, Zhengwen ; Yu, Tian Y. ; Abdilleh, Kawther ; Fraser, Gareth J. ; Sharpe, Paul T. ; Streelman, J. Todd. / Developmental plasticity of epithelial stem cells in tooth and taste bud renewal. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 36. pp. 17858-17866.
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