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Modulation of tissue repair by regeneration enhancer elements

Author

Listed:
  • Junsu Kang

    (Duke University Medical Center)

  • Jianxin Hu

    (Cardiovascular Research Institute, University of California)

  • Ravi Karra

    (Duke University Medical Center)

  • Amy L. Dickson

    (Duke University Medical Center)

  • Valerie A. Tornini

    (Duke University Medical Center)

  • Gregory Nachtrab

    (Duke University Medical Center)

  • Matthew Gemberling

    (Duke University Medical Center)

  • Joseph A. Goldman

    (Duke University Medical Center)

  • Brian L. Black

    (Cardiovascular Research Institute, University of California)

  • Kenneth D. Poss

    (Duke University Medical Center)

Abstract

How tissue regeneration programs are triggered by injury has received limited research attention. Here we investigate the existence of enhancer regulatory elements that are activated in regenerating tissue. Transcriptomic analyses reveal that leptin b (lepb) is highly induced in regenerating hearts and fins of zebrafish. Epigenetic profiling identified a short DNA sequence element upstream and distal to lepb that acquires open chromatin marks during regeneration and enables injury-dependent expression from minimal promoters. This element could activate expression in injured neonatal mouse tissues and was divisible into tissue-specific modules sufficient for expression in regenerating zebrafish fins or hearts. Simple enhancer-effector transgenes employing lepb-linked sequences upstream of pro- or anti-regenerative factors controlled the efficacy of regeneration in zebrafish. Our findings provide evidence for ‘tissue regeneration enhancer elements’ (TREEs) that trigger gene expression in injury sites and can be engineered to modulate the regenerative potential of vertebrate organs.

Suggested Citation

  • Junsu Kang & Jianxin Hu & Ravi Karra & Amy L. Dickson & Valerie A. Tornini & Gregory Nachtrab & Matthew Gemberling & Joseph A. Goldman & Brian L. Black & Kenneth D. Poss, 2016. "Modulation of tissue repair by regeneration enhancer elements," Nature, Nature, vol. 532(7598), pages 201-206, April.
    • Handle: RePEc:nat:nature:v:532:y:2016:i:7598:d:10.1038_nature17644
    DOI: 10.1038/nature17644
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    Citations

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    Cited by:

    1. Aiko Kawasumi-Kita & Sang-Woo Lee & Daisuke Ohtsuka & Kaori Niimi & Yoshifumi Asakura & Keiichi Kitajima & Yuto Sakane & Koji Tamura & Haruki Ochi & Ken-ichi T. Suzuki & Yoshihiro Morishita, 2024. "hoxc12/c13 as key regulators for rebooting the developmental program in Xenopus limb regeneration," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Lily L. Wong & Christina G. Bruxvoort & Nicholas I. Cejda & Matthew R. Delaney & Jannette Rodriguez Otero & David J. Forsthoefel, 2022. "Intestine-enriched apolipoprotein b orthologs are required for stem cell progeny differentiation and regeneration in planarians," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Valentina Cigliola & Adam Shoffner & Nutishia Lee & Jianhong Ou & Trevor J. Gonzalez & Jiaul Hoque & Clayton J. Becker & Yanchao Han & Grace Shen & Timothy D. Faw & Muhammad M. Abd-El-Barr & Shyni Var, 2023. "Spinal cord repair is modulated by the neurogenic factor Hb-egf under direction of a regeneration-associated enhancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Eudald Pascual-Carreras & Marta Marín-Barba & Sergio Castillo-Lara & Pablo Coronel-Córdoba & Marta Silvia Magri & Grant N. Wheeler & Jose Luis Gómez-Skarmeta & Josep F. Abril & Emili Saló & Teresa Ade, 2023. "Wnt/β-catenin signalling is required for pole-specific chromatin remodeling during planarian regeneration," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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