Dynamic Transcriptional Responses to Injury of Regenerative and Non-regenerative Cardiomyocytes Revealed by Single-Nucleus RNA Sequencing

The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-...

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Published inDevelopmental cell Vol. 53; no. 1; pp. 102 - 116.e8
Main Authors Cui, Miao, Wang, Zhaoning, Chen, Kenian, Shah, Akansha M., Tan, Wei, Duan, Lauren, Sanchez-Ortiz, Efrain, Li, Hui, Xu, Lin, Liu, Ning, Bassel-Duby, Rhonda, Olson, Eric N.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 06.04.2020
Subjects
Animals
Animals, Newborn
Cell Cycle - physiology
Cell Proliferation - physiology
cell survival
Gene Expression Regulation, Developmental - genetics
Heart - physiology
heart regeneration
ischemia
Myocardial Infarction - metabolism
Myocytes, Cardiac - cytology
NFE2L1
NFYa
Regeneration - physiology
Transcription Factors - metabolism
transcriptional response to injury
transcriptional response to injury
cell survival
heart regeneration
NFYa
NFE2L1
ischemia
Online AccessGet full text
ISSN1534-5807
1878-1551
1878-1551
DOI10.1016/j.devcel.2020.02.019

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Abstract The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured, and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on nuclear transcription factor Y subunit alpha (NFYa) and nuclear factor erythroid 2-like 1 (NFE2L1) transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury. [Display omitted] •Neonatal cardiomyocytes (CMs) in mice are heterogeneous•Immature CMs enriched in regenerative hearts enter the cell cycle upon injury•Defined transcriptome changes occur in regenerating CMs in response to injury•NFYa and NFE2L1 exert proliferative and protective functions, respectively, in CMs Using single-nucleus RNA sequencing, Cui et al. identified a unique immature cardiomyocyte population associated with heart regeneration in newborn mice. The NFYa and NFE2L1 factors are activated in these cardiomyocytes after injury and can confer protection against ischemic injury in mature mouse hearts that are otherwise non-regenerative.
AbstractList The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured, and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on nuclear transcription factor Y subunit alpha (NFYa) and nuclear factor erythroid 2-like 1 (NFE2L1) transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury.The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured, and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on nuclear transcription factor Y subunit alpha (NFYa) and nuclear factor erythroid 2-like 1 (NFE2L1) transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury.
The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured, and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on nuclear transcription factor Y subunit alpha (NFYa) and nuclear factor erythroid 2-like 1 (NFE2L1) transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury.
The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured, and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on nuclear transcription factor Y subunit alpha (NFYa) and nuclear factor erythroid 2-like 1 (NFE2L1) transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury. [Display omitted] •Neonatal cardiomyocytes (CMs) in mice are heterogeneous•Immature CMs enriched in regenerative hearts enter the cell cycle upon injury•Defined transcriptome changes occur in regenerating CMs in response to injury•NFYa and NFE2L1 exert proliferative and protective functions, respectively, in CMs Using single-nucleus RNA sequencing, Cui et al. identified a unique immature cardiomyocyte population associated with heart regeneration in newborn mice. The NFYa and NFE2L1 factors are activated in these cardiomyocytes after injury and can confer protection against ischemic injury in mature mouse hearts that are otherwise non-regenerative.
The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week of life. The molecular mechanisms that mediate the regenerative response and its blockade in later life are not understood. Here, by single-nucleus RNA sequencing, we map the dynamic transcriptional landscape of five distinct cardiomyocyte populations in healthy, injured and regenerating mouse hearts. We identify immature cardiomyocytes that enter the cell-cycle following injury and disappear as the heart loses the ability to regenerate. These proliferative neonatal cardiomyocytes display a unique transcriptional program dependent on NFYa and NFE2L1 transcription factors, which exert proliferative and protective functions, respectively. Cardiac overexpression of these two factors conferred protection against ischemic injury in mature mouse hearts that were otherwise non-regenerative. These findings advance our understanding of the cellular basis of neonatal heart regeneration and reveal a transcriptional landscape for heart repair following injury. Using single-nucleus RNA sequencing, Cui and Wang et al. identified a unique immature cardiomyocyte population associated with heart regeneration in newborn mice. The NFYa and NFE2L1 factors are activated in these cardiomyocytes after injury and can confer protection against ischemic injury in mature mouse hearts that are otherwise nonregenerative.
Author Bassel-Duby, Rhonda
Olson, Eric N.
Sanchez-Ortiz, Efrain
Liu, Ning
Wang, Zhaoning
Chen, Kenian
Tan, Wei
Duan, Lauren
Xu, Lin
Cui, Miao
Li, Hui
Shah, Akansha M.
AuthorAffiliation 3 Lead Contact
1 Department of Molecular Biology, the Hamon Center for Regenerative Science and Medicine, and Sen. Paul D. Wellstone Muscular Dystrophy Cooperative Research Center, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
2 Quantitative Biomedical Research Center, Department of Population & Data Sciences and Department of Pediatrics, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
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– sequence: 8
  givenname: Hui
  surname: Li
  fullname: Li, Hui
  organization: Department of Molecular Biology, The Hamon Center for Regenerative Science and Medicine and Sen. Paul D. Wellstone Muscular Dystrophy Cooperative Research Center, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
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  givenname: Lin
  surname: Xu
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  surname: Bassel-Duby
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  givenname: Eric N.
  surname: Olson
  fullname: Olson, Eric N.
  email: eric.olson@utsouthwestern.edu
  organization: Department of Molecular Biology, The Hamon Center for Regenerative Science and Medicine and Sen. Paul D. Wellstone Muscular Dystrophy Cooperative Research Center, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32220304$$D View this record in MEDLINE/PubMed
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IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Keywords transcriptional response to injury
cell survival
heart regeneration
NFYa
NFE2L1
ischemia
Language English
License Copyright © 2020 Elsevier Inc. All rights reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4449-a38abee36f4cafadad6eaaf77cc770b2f216de1c90df2ddbb712127cd7b02a683
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
AUTHOR CONTRIBUTIONS
These authors contributed equally to this work.
M.C., Z.W., W.T. A.M.S., L.D., E.S., and H.L. designed and performed experiments; M.C., K.C., and Z.W. performed the data analysis; L.X. and N.L. contributed to discussion; M.C., R.B.-D., and E.N.O. wrote the manuscript.
OpenAccessLink http://www.cell.com/article/S1534580720301465/pdf
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33290696 - Dev Cell. 2020 Dec 7;55(5):665-667
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Snippet The adult mammalian heart is incapable of regeneration following injury. In contrast, the neonatal mouse heart can efficiently regenerate during the first week...
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SubjectTerms Animals
Animals, Newborn
Cell Cycle - physiology
Cell Proliferation - physiology
cell survival
Gene Expression Regulation, Developmental - genetics
Heart - physiology
heart regeneration
ischemia
Myocardial Infarction - metabolism
Myocytes, Cardiac - cytology
NFE2L1
NFYa
Regeneration - physiology
Transcription Factors - metabolism
transcriptional response to injury
Title Dynamic Transcriptional Responses to Injury of Regenerative and Non-regenerative Cardiomyocytes Revealed by Single-Nucleus RNA Sequencing
URI https://dx.doi.org/10.1016/j.devcel.2020.02.019
https://www.ncbi.nlm.nih.gov/pubmed/32220304
https://www.proquest.com/docview/2384216050
https://pubmed.ncbi.nlm.nih.gov/PMC7365574
Volume 53
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