Bistable Epigenetic States Explain Age‐Dependent Decline in Mesenchymal Stem Cell Heterogeneity
The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen‐1 (Sca‐1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca‐1 express...
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| Published in | Stem cells (Dayton, Ohio) Vol. 35; no. 3; pp. 694 - 704 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Oxford University Press
01.03.2017
AlphaMed Press John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen‐1 (Sca‐1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca‐1 expression profiles regenerate the Sca‐1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca‐1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age‐dependent frequency due to persistent histone (de‐)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694–704
In young cells, expression of Sca‐1 is bistable. Frequent switches between high (Sca‐1H, red) and low (Sca‐1L, blue) expression states occur due to stochastic H3K4me3 (de‐) modification reactions at the gene promoter leading to gene expression heterogeneity. Accordingly, Sca‐1H and Sca‐1L populations regenerate the expression profile of their mother population (WCP) within a few days.During aging, gene activation by the underlying transcription factor network is reduced, stabilizing Sca‐1L states. Eventually, the system becomes monostable. |
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| AbstractList | The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen‐1 (Sca‐1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca‐1 expression profiles regenerate the Sca‐1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca‐1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age‐dependent frequency due to persistent histone (de‐)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. S
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2017;35:694–704 Abstract The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen‐1 (Sca‐1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca‐1 expression profiles regenerate the Sca‐1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca‐1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age‐dependent frequency due to persistent histone (de‐)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694–704 The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017; 35:694-704 In young cells, expression of Sca-1 is bistable. Frequent switches between high (Sca-1H, red) and low (Sca-1L, blue) expression states occur due to stochastic H3K4me3 (de-) modification reactions at the gene promoter leading to gene expression heterogeneity. Accordingly, Sca-1H and Sca-1L populations regenerate the expression profile of their mother population (WCP) within a few days.During aging, gene activation by the underlying transcription factor network is reduced, stabilizing Sca-1L states. Eventually, the system becomes monostable. The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694-704.The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694-704. The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694-704. The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen-1 (Sca-1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca-1 expression profiles regenerate the Sca-1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca-1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age-dependent frequency due to persistent histone (de-)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the membrane stem cell antigen‐1 (Sca‐1) in mouse bone marrow mesenchymal stem cell (MSC) clones. We show that subpopulations with varying Sca‐1 expression profiles regenerate the Sca‐1 profile of the mother population within a few days. However, after extensive replication in vitro, the expression profiles shift to lower values and the regeneration time increases. Study of the promoter of Ly6a unravels that the expression level of Sca‐1 is related to the promoter occupancy by the activating histone mark H3K4me3. We demonstrate that these findings can be consistently explained by a computational model that considers positive feedback between promoter H3K4me3 modification and gene transcription. This feedback implicates bistable epigenetic states which the cells occupy with an age‐dependent frequency due to persistent histone (de‐)modification. Our results provide evidence that MSC heterogeneity, and presumably that of other stem cells, is associated with bistable epigenetic states and suggest that MSCs are subject to permanent state fluctuations. Stem Cells 2017;35:694–704 In young cells, expression of Sca‐1 is bistable. Frequent switches between high (Sca‐1H, red) and low (Sca‐1L, blue) expression states occur due to stochastic H3K4me3 (de‐) modification reactions at the gene promoter leading to gene expression heterogeneity. Accordingly, Sca‐1H and Sca‐1L populations regenerate the expression profile of their mother population (WCP) within a few days.During aging, gene activation by the underlying transcription factor network is reduced, stabilizing Sca‐1L states. Eventually, the system becomes monostable. |
| Author | Charbord, Pierre Przybilla, Jens Fabian, Claire Rother, Karen Krinner, Axel Hopp, Lydia Stolzing, Alexandra Binder, Hans Galle, Joerg Hamidouche, Zahia Clay, Denis |
| AuthorAffiliation | 2 Faculty of Biology Mouloud Mammeri University Tizi‐ouzou Algeria 3 Interdisciplinary Center for Bioinformatics University Leipzig Germany 6 IBPS Laboratory of Developmental Biology University Pierre & Marie Curie Paris France 4 LIFE: Leipzig Research Center for Civilization Diseases University Leipzig Germany 5 Fraunhofer Institute for Cell Therapy and Immunology Leipzig Germany 1 INSERM U972, University Paris 11 Hôpital Paul Brousse Villejuif France |
| AuthorAffiliation_xml | – name: 3 Interdisciplinary Center for Bioinformatics University Leipzig Germany – name: 6 IBPS Laboratory of Developmental Biology University Pierre & Marie Curie Paris France – name: 5 Fraunhofer Institute for Cell Therapy and Immunology Leipzig Germany – name: 1 INSERM U972, University Paris 11 Hôpital Paul Brousse Villejuif France – name: 4 LIFE: Leipzig Research Center for Civilization Diseases University Leipzig Germany – name: 2 Faculty of Biology Mouloud Mammeri University Tizi‐ouzou Algeria |
| Author_xml | – sequence: 1 givenname: Zahia surname: Hamidouche fullname: Hamidouche, Zahia organization: Mouloud Mammeri University – sequence: 2 givenname: Karen surname: Rother fullname: Rother, Karen organization: University Leipzig – sequence: 3 givenname: Jens surname: Przybilla fullname: Przybilla, Jens organization: University Leipzig – sequence: 4 givenname: Axel surname: Krinner fullname: Krinner, Axel organization: University Leipzig – sequence: 5 givenname: Denis surname: Clay fullname: Clay, Denis organization: Hôpital Paul Brousse – sequence: 6 givenname: Lydia surname: Hopp fullname: Hopp, Lydia organization: University Leipzig – sequence: 7 givenname: Claire surname: Fabian fullname: Fabian, Claire organization: Fraunhofer Institute for Cell Therapy and Immunology – sequence: 8 givenname: Alexandra surname: Stolzing fullname: Stolzing, Alexandra organization: University Leipzig – sequence: 9 givenname: Hans surname: Binder fullname: Binder, Hans organization: University Leipzig – sequence: 10 givenname: Pierre surname: Charbord fullname: Charbord, Pierre organization: University Pierre & Marie Curie – sequence: 11 givenname: Joerg surname: Galle fullname: Galle, Joerg email: galle@izbi.uni-leipzig.de organization: University Leipzig |
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| Keywords | Aging Epigenetics FACS Methylation Mesenchymal stem cells |
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| Snippet | The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of the... Abstract The molecular mechanisms by which heterogeneity, a major characteristic of stem cells, is achieved are yet unclear. We here study the expression of... |
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| StartPage | 694 |
| SubjectTerms | Age Aging Aging - genetics Animals Antigens, Ly - metabolism Bone marrow Bone Marrow Cells - cytology Cell Differentiation - genetics Cell Proliferation Clone Cells Computer applications Epigenesis, Genetic Epigenetics FACS Feedback Gene Expression Profiling Genes Heterogeneity In vitro methods and tests Life Sciences Membrane Proteins - metabolism Mesenchymal stem cells Mesenchymal Stromal Cells - cytology Mesenchymal Stromal Cells - metabolism Mesenchyme Methylation Mice, Inbred C57BL Models, Biological Models, Genetic Molecular modelling Positive feedback Promoter Regions, Genetic Regeneration Replication Rodents Stem cell transplantation Stem cells Subpopulations Tissue‐Specific Stem Cells Transcription |
| Title | Bistable Epigenetic States Explain Age‐Dependent Decline in Mesenchymal Stem Cell Heterogeneity |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fstem.2514 https://www.ncbi.nlm.nih.gov/pubmed/27734598 https://www.proquest.com/docview/1906122190 https://www.proquest.com/docview/1835407626 https://www.proquest.com/docview/1877842827 https://cnrs.hal.science/hal-03977933 https://pubmed.ncbi.nlm.nih.gov/PMC5347872 |
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