Transcriptome and epigenome diversity and plasticity of muscle stem cells following transplantation

Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular musc...

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Published inPLoS genetics Vol. 16; no. 10; p. e1009022
Main Authors Evano, Brendan, Gill, Diljeet, Hernando-Herraez, Irene, Comai, Glenda, Stubbs, Thomas M, Commere, Pierre-Henri, Reik, Wolf, Tajbakhsh, Shahragim
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 30.10.2020
Public Library of Science (PLoS)
Subjects
Animals
Biology
Biology and life sciences
Cell differentiation
Cell Differentiation - genetics
Cell Lineage - genetics
Cell Plasticity - genetics
Cell Proliferation - genetics
Cell self-renewal
Deoxyribonucleic acid
DNA
DNA methylation
Engraftment
Enhancers
Epigenetics
Epigenome - genetics
Extremities - growth & development
Gene expression
Genetic aspects
Genetic Variation - genetics
Homeostasis
Humans
Investigations
Life Sciences
Medicine and Health Sciences
Mice
Mice, Inbred C57BL
Muscle Cells - cytology
Muscle Fibers, Skeletal
Muscle, Skeletal - cytology
Muscles
Myoblasts - cytology
Oculomotor system
Physical Sciences
Physiological aspects
Principal components analysis
Regeneration - genetics
Regenerative medicine
Research and Analysis Methods
Skeletal muscle
Software
Stem Cell Transplantation
Stem cells
Stem Cells - cytology
Stem Cells - metabolism
Transcription factors
Transcriptome - genetics
Transplantation
United Kingdom
United Kingdom > UK
France
Online AccessGet full text

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Abstract Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct DNA methylation signatures associated with enhancers of location-specific genes, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs expressed host-site specific positional Hox codes after engraftment and self-renewal within the host muscle. However, about 10% of EOM-specific genes showed engraftment-resistant expression, pointing to cell-intrinsic molecular determinants of the higher engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine.
AbstractList Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct DNA methylation signatures associated with enhancers of location-specific genes, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs expressed host-site specific positional Hox codes after engraftment and self-renewal within the host muscle. However, about 10% of EOM-specific genes showed engraftment-resistant expression, pointing to cell-intrinsic molecular determinants of the higher engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine.
Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct DNA methylation signatures associated with enhancers of location-specific genes, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs expressed host-site specific positional Hox codes after engraftment and self-renewal within the host muscle. However, about 10% of EOM-specific genes showed engraftment-resistant expression, pointing to cell-intrinsic molecular determinants of the higher engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine.
Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal, differentiation and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct DNA methylation signatures associated with enhancers of location-specific genes, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs expressed host-site specific positional Hox codes after engraftment and self-renewal within the host muscle. However, about 10% of EOM-specific genes showed engraftment-resistant expression, pointing to cell-intrinsic molecular determinants of the higher engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine. Adult skeletal muscles are regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in expression of key myogenic regulators and regeneration properties has been reported for MuSCs based on their anatomical location. Although MuSCs derived from extraocular muscles (EOM) have a higher regenerative capacity than those derived from limb muscles, the molecular determinants that govern these differences remain undefined. Here we show that EOM and limb MuSCs have distinct transcriptome and DNA methylation signatures, and that the EOM transcriptome is reprogrammed following transplantation into a limb muscle environment. Notably, EOM MuSCs adopted host-site specific positional Hox codes after engraftment within the host muscle. However, about 10% of EOM-specific genes were resistant to alterations following heterotopic engraftment, pointing to molecular determinants of the high engraftment potential of EOM MuSCs. Our results underscore the molecular diversity of distinct MuSC populations and molecularly define their plasticity in response to microenvironmental cues. These findings provide insights into strategies designed to improve the functional capacity of MuSCs in the context of regenerative medicine.
Audience Academic
Author Gill, Diljeet
Commere, Pierre-Henri
Comai, Glenda
Hernando-Herraez, Irene
Reik, Wolf
Evano, Brendan
Tajbakhsh, Shahragim
Stubbs, Thomas M
AuthorAffiliation 3 Epigenetics Programme, Babraham Institute, Cambridge, United Kingdom
Albert Einstein College of Medicine, UNITED STATES
4 Cytometry and Biomarkers, Center for Technological Resources and Research, Institut Pasteur, 28 rue du Dr. Roux, Paris, France
1 Stem Cells & Development, Department of Developmental & Stem Cell Biology, Institut Pasteur, 25 rue du Dr. Roux, Paris, France
2 CNRS UMR 3738, Institut Pasteur, Paris, France
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2020 Evano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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PMCID: PMC7657492
Current address: Chronomics Limited, 1 St James Court, Norwich.
I have read the journal's policy and the authors of this manuscript have the following competing interests: W.R. is a consultant and shareholder of Cambridge Epigenetix. T.S. is CEO and shareholder of Chronomics. All other authors declare no competing interests.
WR and ST also contributed equally to this work.
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pubmed_primary_33125370
PublicationCentury 2000
PublicationDate 2020-10-30
PublicationDateYYYYMMDD 2020-10-30
PublicationDate_xml – month: 10
  year: 2020
  text: 2020-10-30
  day: 30
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS genetics
PublicationTitleAlternate PLoS Genet
PublicationYear 2020
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
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Snippet Adult skeletal muscles are maintained during homeostasis and regenerated upon injury by muscle stem cells (MuSCs). A heterogeneity in self-renewal,...
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StartPage e1009022
SubjectTerms Animals
Biology
Biology and life sciences
Cell differentiation
Cell Differentiation - genetics
Cell Lineage - genetics
Cell Plasticity - genetics
Cell Proliferation - genetics
Cell self-renewal
Deoxyribonucleic acid
DNA
DNA methylation
Engraftment
Enhancers
Epigenetics
Epigenome - genetics
Extremities - growth & development
Gene expression
Genetic aspects
Genetic Variation - genetics
Homeostasis
Humans
Investigations
Life Sciences
Medicine and Health Sciences
Mice
Mice, Inbred C57BL
Muscle Cells - cytology
Muscle Fibers, Skeletal
Muscle, Skeletal - cytology
Muscles
Myoblasts - cytology
Oculomotor system
Physical Sciences
Physiological aspects
Principal components analysis
Regeneration - genetics
Regenerative medicine
Research and Analysis Methods
Skeletal muscle
Software
Stem Cell Transplantation
Stem cells
Stem Cells - cytology
Stem Cells - metabolism
Transcription factors
Transcriptome - genetics
Transplantation
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Title Transcriptome and epigenome diversity and plasticity of muscle stem cells following transplantation
URI https://www.ncbi.nlm.nih.gov/pubmed/33125370
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https://search.proquest.com/docview/2456414778
https://pasteur.hal.science/pasteur-03018737
https://pubmed.ncbi.nlm.nih.gov/PMC7657492
https://doaj.org/article/44796252406a407a85e793d21603b3eb
http://dx.doi.org/10.1371/journal.pgen.1009022
Volume 16
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