Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms

Elizabeth D. Hutchins, Glenn J. Markov, Walter L. Eckalbar, Rajani M. George, Jesse M. King, Minami A. Tokuyama, Lauren A. Geiger, Nataliya Emmert, Michael J. Ammar, April N. Allen, Ashley L. Siniard, Jason J. Corneveaux, Rebecca E. Fisher, Juli Wade, Dale F. DeNardo, J. Alan Rawls, Matthew J. Huentelman, Jeanne Wilson-Rawls, Kenro Kusumi

Research output: Contribution to journalArticle

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Abstract

Lizards, which are amniote vertebrates like humans, are able to lose and regenerate a functional tail. Understanding the molecular basis of this process would advance regenerative approaches in amniotes, including humans. We have carried out the first transcriptomic analysis of tail regeneration in a lizard, the green anole Anolis carolinensis, which revealed 326 differentially expressed genes activating multiple developmental and repair mechanisms. Specifically, genes involved in wound response, hormonal regulation, musculoskeletal development, and the Wnt and MAPK/FGF pathways were differentially expressed along the regenerating tail axis. Furthermore, we identified 2 microRNA precursor families, 22 unclassified non-coding RNAs, and 3 novel protein-coding genes significantly enriched in the regenerating tail. However, high levels of progenitor/stem cell markers were not observed in any region of the regenerating tail. Furthermore, we observed multiple tissue-type specific clusters of proliferating cells along the regenerating tail, not localized to the tail tip. These findings predict a different mechanism of regeneration in the lizard than the blastema model described in the salamander and the zebrafish, which are anamniote vertebrates. Thus, lizard tail regrowth involves the activation of conserved developmental and wound response pathways, which are potential targets for regenerative medical therapies.

Original languageEnglish (US)
Pages (from-to)e105004
JournalPLoS One
Volume9
Issue number8
DOIs
StatePublished - 2014

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Anolis carolinensis
Lizards
transcriptomics
Vertebrates
lizards
Tail
Regeneration
Repair
tail
Genes
Chemical activation
vertebrates
Untranslated RNA
Stem cells
MicroRNAs
animal injuries
stem cells
Cells
Tissue
Musculoskeletal Development

ASJC Scopus subject areas

  • Medicine(all)

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Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. / Hutchins, Elizabeth D.; Markov, Glenn J.; Eckalbar, Walter L.; George, Rajani M.; King, Jesse M.; Tokuyama, Minami A.; Geiger, Lauren A.; Emmert, Nataliya; Ammar, Michael J.; Allen, April N.; Siniard, Ashley L.; Corneveaux, Jason J.; Fisher, Rebecca E.; Wade, Juli; DeNardo, Dale F.; Rawls, J. Alan; Huentelman, Matthew J.; Wilson-Rawls, Jeanne; Kusumi, Kenro.

In: PLoS One, Vol. 9, No. 8, 2014, p. e105004.

Research output: Contribution to journalArticle

Hutchins, ED, Markov, GJ, Eckalbar, WL, George, RM, King, JM, Tokuyama, MA, Geiger, LA, Emmert, N, Ammar, MJ, Allen, AN, Siniard, AL, Corneveaux, JJ, Fisher, RE, Wade, J, DeNardo, DF, Rawls, JA, Huentelman, MJ, Wilson-Rawls, J & Kusumi, K 2014, 'Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms', PLoS One, vol. 9, no. 8, pp. e105004. https://doi.org/10.1371/journal.pone.0105004
Hutchins, Elizabeth D. ; Markov, Glenn J. ; Eckalbar, Walter L. ; George, Rajani M. ; King, Jesse M. ; Tokuyama, Minami A. ; Geiger, Lauren A. ; Emmert, Nataliya ; Ammar, Michael J. ; Allen, April N. ; Siniard, Ashley L. ; Corneveaux, Jason J. ; Fisher, Rebecca E. ; Wade, Juli ; DeNardo, Dale F. ; Rawls, J. Alan ; Huentelman, Matthew J. ; Wilson-Rawls, Jeanne ; Kusumi, Kenro. / Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. In: PLoS One. 2014 ; Vol. 9, No. 8. pp. e105004.
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AU - King, Jesse M.

AU - Tokuyama, Minami A.

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AU - Fisher, Rebecca E.

AU - Wade, Juli

AU - DeNardo, Dale F.

AU - Rawls, J. Alan

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AU - Kusumi, Kenro

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