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A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice

Abrams, Michael J. and Tan, Fayth Hui and Li, Yutian and Basinger, Ty and Heithe, Martin L. and Sarma, Anish and Lee, Iris T. and Condiotte, Zevin J. and Raffiee, Misha and Dabiri, John O. and Gold, David A. and Goentoro, Lea (2021) A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice. eLife, 10 . Art. No. e65092. ISSN 2050-084X. PMCID PMC8782573. doi:10.7554/eLife.65092. https://resolver.caltech.edu/CaltechAUTHORS:20201123-131615362

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Abstract

Can limb regeneration be induced? Few have pursued this question, and an evolutionarily conserved strategy has yet to emerge. This study reports a strategy for inducing regenerative response in appendages, which works across three species that span the animal phylogeny. In Cnidaria, the frequency of appendage regeneration in the moon jellyfish Aurelia was increased by feeding with the amino acid L-leucine and the growth hormone insulin. In insects, the same strategy induced tibia regeneration in adult Drosophila. Finally, in mammals, L-leucine and sucrose administration induced digit regeneration in adult mice, including dramatically from mid-phalangeal amputation. The conserved effect of L-leucine and insulin/sugar suggests a key role for energetic parameters in regeneration induction. The simplicity by which nutrient supplementation can induce appendage regeneration provides a testable hypothesis across animals.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.65092DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8782573/PubMed CentralArticle
https://doi.org/10.22002/D1.2076DOIData
https://doi.org/10.22002/D1.2157DOIData
https://doi.org/10.22002/D1.1790DOIData
https://doi.org/10.1101/2020.11.21.392720DOIDiscussion Paper
ORCID:
AuthorORCID
Abrams, Michael J.0000-0003-1864-1706
Tan, Fayth Hui0000-0002-2160-5311
Dabiri, John O.0000-0002-6722-9008
Gold, David A.0000-0003-0135-4022
Goentoro, Lea0000-0002-3904-0195
Alternate Title:Amino acid and sugar supplement induces appendage regeneration in cnidarian, insect, and mammal, A conserved strategy for inducing appendage regeneration
Additional Information:© 2021, Abrams 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. Preprinted: 22 November 2020; Received: 22 November 2020; Accepted: 22 November 2021; Published: 07 December 2021. The authors thank Kiersten Darrow and Michael Schaadt at the Cabrillo Marine Aquarium, Cabrillo, CA for the gifts of Aurelia polyps and help with jellyfish culture, Patrick Leahy at the Caltech’s Kerckhoff Marine Laboratory, Corona Del Mar, CA for the help with setting up Aurelia experiments in natural habitat, Matthew Hunt from the Kavli Nanoscience Institute at Caltech for help with SEM imaging, James McGehee, Angela Stathopolous, Peter Lee, Kai Zinn for sharing Drosophila strains, Yujing Yang and Long Cai for help with imaging, and Carlos Lois for demonstration of digit amputation. The authors thank Gertrud Schupbach, Natalie Andrew, and Aki Ohdera for comments on the manuscript; and Katalina Fejes-Toth, Luis del Peso, Aditya Saxena, and Marta Truchado Garcia for discussion. This work was supported by the National Science Foundation Graduate Research Fellowship Program (1144469; to MJA), the James E and Charlotte Fedde Cordes Postdoctoral Fellowship in Biology (to DAG); the James S McDonnell Foundation for Complex Systems Science (220020365; to LG), the Center for Environmental Microbial Interactions at Caltech (to ZC and LG), the Center of Evolutionary Sciences at Caltech (to YL and LG), the Summer Undergraduate Research Fellowships (to IL and LG), and Charles Trimble and Caltech’s Biology and Biological Engineering Chair’s Council Inducing Regeneration Fund (to LG). Data availability: All data generated or analysed during this study are included in the manuscript and supporting files, as well as deposited to the open repository CaltechDATA. Author contributions: Michael J Abrams, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing – review and editing; Fayth Hui Tan, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing – review and editing; Yutian Li, Conceptualization, Data curation, Investigation, Methodology, Validation, Visualization, Writing – review and editing; Ty Basinger, Iris T Lee, Zevin J Condiotte, Data curation, Investigation, Methodology, Validation, Writing – review and editing; Martin L Heithe, Data curation, Formal analysis, Investigation, Methodology, Validation, Writing – review and editing; Anish Sarma, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Writing – review and editing; Misha Raffiee, Investigation, Writing – review and editing; John O Dabiri, Supervision, Writing – review and editing; David A Gold, Investigation, Methodology, Writing – review and editing; Lea Goentoro, Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft. Competing interests: Michael J Abrams, Fayth Hui Tan, Ty Basinger, Martin L Heithe, Lea Goentoro: Inventor in patent rights application for findings in the manuscript. The other authors declare that no competing interests exist.
Group:Kavli Nanoscience Institute, Caltech Center for Environmental Microbial Interactions (CEMI), GALCIT
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipDGE-1144469
James E. and Charlotte Fedde Cordes Postdoctoral FellowshipUNSPECIFIED
James S. McDonnell Foundation220020365
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Caltech Summer Undergraduate Research Fellowship (SURF)UNSPECIFIED
Charles TrimbleUNSPECIFIED
Caltech Division of Biology and Biological EngineeringUNSPECIFIED
Subject Keywords:Regeneration, appendage, limb, amino acid, leucine, sugar, insulin, jellyfish, Drosophila, mouse
PubMed Central ID:PMC8782573
DOI:10.7554/eLife.65092
Record Number:CaltechAUTHORS:20201123-131615362
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201123-131615362
Official Citation:A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice. Abrams, Tan, Li, et al. eLife 2021; 10:e65092; DOI: 10.7554/eLife.65092
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106788
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Nov 2020 22:26
Last Modified:10 May 2022 20:35

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