Notch Inhibition Enhances Cardiac Reprogramming by Increasing MEF2C Transcriptional Activity

Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhanc...

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Vydané v:	Stem cell reports Ročník 8; číslo 3; s. 548 - 560
Hlavní autori:	Abad, Maria, Hashimoto, Hisayuki, Zhou, Huanyu, Morales, Maria Gabriela, Chen, Beibei, Bassel-Duby, Rhonda, Olson, Eric N.
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States Elsevier Inc 14.03.2017 Elsevier
Predmet:	Animals Calcium Signaling - drug effects cardiomyocytes Cell Differentiation cell-fate conversion Cellular Reprogramming - drug effects Cellular Reprogramming - genetics DAPT Diamines - pharmacology direct cellular reprogramming Electrophysiological Phenomena - drug effects Gene Expression Profiling Gene Expression Regulation, Developmental heart regeneration MEF2 Transcription Factors - metabolism Mice Myocytes, Cardiac - cytology Myocytes, Cardiac - drug effects Myocytes, Cardiac - metabolism Notch signaling Proto-Oncogene Proteins c-akt - genetics Proto-Oncogene Proteins c-akt - metabolism Receptors, Notch - metabolism regenerative medicine Sarcomeres - drug effects Sarcomeres - metabolism Signal Transduction Thiazoles - pharmacology Transcriptional Activation Transcriptome transdifferentiation cardiomyocytes direct cellular reprogramming heart regeneration Notch signaling regenerative medicine transdifferentiation cell-fate conversion DAPT
ISSN:	2213-6711, 2213-6711
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Abstract	Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies. [Display omitted] •Notch activation is a barrier for GHMT-induced cardiac cell reprogramming•Notch blockade by DAPT improves GHMT-induced cardiac reprogramming•DAPT increases sarcomere organization, calcium flux, and beating in GHMT reprogramming•DAPT enhances transcriptional activity of MEF2C in GHMT reprogramming In this article, Olson and colleagues show that Notch signaling activation is a critical barrier for cardiac cell reprogramming. Notch signaling blockade by DAPT, a γ-secretase inhibitor, enhances fibroblast conversion to cardiomyocytes by increasing calcium flux, sarcomere structure, and beating. Mechanistically, Notch inhibition enhances the transcriptional activity of the cardiogenic transcription factor MEF2C, thereby enhancing expression of cardiac genes.
AbstractList	Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies. Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies. • Notch activation is a barrier for GHMT-induced cardiac cell reprogramming • Notch blockade by DAPT improves GHMT-induced cardiac reprogramming • DAPT increases sarcomere organization, calcium flux, and beating in GHMT reprogramming • DAPT enhances transcriptional activity of MEF2C in GHMT reprogramming In this article, Olson and colleagues show that Notch signaling activation is a critical barrier for cardiac cell reprogramming. Notch signaling blockade by DAPT, a γ-secretase inhibitor, enhances fibroblast conversion to cardiomyocytes by increasing calcium flux, sarcomere structure, and beating. Mechanistically, Notch inhibition enhances the transcriptional activity of the cardiogenic transcription factor MEF2C, thereby enhancing expression of cardiac genes. Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies.Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies. Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far this process remains inefficient and little is known about its molecular mechanisms. Here we show that DAPT, a classical Notch inhibitor, enhances the conversion of mouse fibroblasts into induced cardiac-like myocytes by the transcription factors GATA4, HAND2, MEF2C, and TBX5. DAPT cooperates with AKT kinase to further augment this process, resulting in up to 70% conversion efficiency. Moreover, DAPT promotes the acquisition of specific cardiomyocyte features, substantially increasing calcium flux, sarcomere structure, and the number of spontaneously beating cells. Transcriptome analysis shows that DAPT induces genetic programs related to muscle development, differentiation, and excitation-contraction coupling. Mechanistically, DAPT increases binding of the transcription factor MEF2C to the promoter regions of cardiac structural genes. These findings provide mechanistic insights into the reprogramming process and may have important implications for cardiac regeneration therapies. [Display omitted] •Notch activation is a barrier for GHMT-induced cardiac cell reprogramming•Notch blockade by DAPT improves GHMT-induced cardiac reprogramming•DAPT increases sarcomere organization, calcium flux, and beating in GHMT reprogramming•DAPT enhances transcriptional activity of MEF2C in GHMT reprogramming In this article, Olson and colleagues show that Notch signaling activation is a critical barrier for cardiac cell reprogramming. Notch signaling blockade by DAPT, a γ-secretase inhibitor, enhances fibroblast conversion to cardiomyocytes by increasing calcium flux, sarcomere structure, and beating. Mechanistically, Notch inhibition enhances the transcriptional activity of the cardiogenic transcription factor MEF2C, thereby enhancing expression of cardiac genes.
Author	Hashimoto, Hisayuki Chen, Beibei Bassel-Duby, Rhonda Olson, Eric N. Abad, Maria Zhou, Huanyu Morales, Maria Gabriela
AuthorAffiliation	4 Cell Plasticity and Cancer Group, Vall d'Hebron Institute of Oncology (VHIO), c/Natzaret, 115-117, Barcelona 08035, Spain 1 Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA 2 Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA 3 Department of Clinical Sciences, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
AuthorAffiliation_xml	– name: 1 Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – name: 2 Hamon Center for Regenerative Science and Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – name: 3 Department of Clinical Sciences, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – name: 4 Cell Plasticity and Cancer Group, Vall d'Hebron Institute of Oncology (VHIO), c/Natzaret, 115-117, Barcelona 08035, Spain
Author_xml	– sequence: 1 givenname: Maria surname: Abad fullname: Abad, Maria email: mabad@vhio.net organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 2 givenname: Hisayuki surname: Hashimoto fullname: Hashimoto, Hisayuki organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 3 givenname: Huanyu surname: Zhou fullname: Zhou, Huanyu organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 4 givenname: Maria Gabriela surname: Morales fullname: Morales, Maria Gabriela organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 5 givenname: Beibei surname: Chen fullname: Chen, Beibei organization: Department of Clinical Sciences, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 6 givenname: Rhonda surname: Bassel-Duby fullname: Bassel-Duby, Rhonda organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA – sequence: 7 givenname: Eric N. surname: Olson fullname: Olson, Eric N. email: eric.olson@utsouthwestern.edu organization: Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390, USA
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Snippet	Conversion of fibroblasts into functional cardiomyocytes represents a potential means of restoring cardiac function after myocardial infarction, but so far...
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SubjectTerms	Animals Calcium Signaling - drug effects cardiomyocytes Cell Differentiation cell-fate conversion Cellular Reprogramming - drug effects Cellular Reprogramming - genetics DAPT Diamines - pharmacology direct cellular reprogramming Electrophysiological Phenomena - drug effects Gene Expression Profiling Gene Expression Regulation, Developmental heart regeneration MEF2 Transcription Factors - metabolism Mice Myocytes, Cardiac - cytology Myocytes, Cardiac - drug effects Myocytes, Cardiac - metabolism Notch signaling Proto-Oncogene Proteins c-akt - genetics Proto-Oncogene Proteins c-akt - metabolism Receptors, Notch - metabolism regenerative medicine Sarcomeres - drug effects Sarcomeres - metabolism Signal Transduction Thiazoles - pharmacology Transcriptional Activation Transcriptome transdifferentiation
Title	Notch Inhibition Enhances Cardiac Reprogramming by Increasing MEF2C Transcriptional Activity
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