Hair follicle stem cell cultures reveal self‐organizing plasticity of stem cells and their progeny
Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single‐cell behaviors are coordinated on the population level. The self‐renewing hair follicle, maintained by a distinct stem cell population, rep...
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| Published in: | The EMBO journal Vol. 36; no. 2; pp. 151 - 164 |
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| Main Authors: | , , , , |
| Format: | Journal Article |
| Language: | English |
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London
Nature Publishing Group UK
17-01-2017
Blackwell Publishing Ltd John Wiley and Sons Inc |
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| Abstract | Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single‐cell behaviors are coordinated on the population level. The self‐renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell (HFSC) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an
in vitro
culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long‐term maintenance of murine multipotent HFSCs in the absence of heterologous cell types. Strikingly, this scheme promotes
de novo
generation of HFSCs from non‐HFSCs and vice versa in a dynamic self‐organizing process. This bidirectional interconversion of HFSCs and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population‐level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate.
Synopsis
An advanced
in vitro
culture system allows for enrichment and long‐term maintenance of multipotent mouse hair follicle stem cells (HFSCs), recapitulating key features of their
in vivo
regulation.
Combination of a 3D extracellular matrix environment and defined soluble components (FGF‐2, VEGF‐A, ROCK inhibitor Y27632) facilitates long‐term propagation of HFSCs.
HFSC expansion can be achieved from purified HFSCs as well as from total or HFSC‐depleted epidermal cell mixtures.
Cultured HFSCs retain multipotency, self‐renewal potential, and transcriptional identity.
Bidirectional interconversion of cultured HFSCs driven by BMP and Shh pathways leads to self‐organization into a dynamic equilibrium between HFSCs and their progeny.
Graphical Abstract
Cell culture conditions for enrichment and long‐term maintenance of multipotent mouse skin stem cells in population equilibrium. |
|---|---|
| AbstractList | Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single-cell behaviors are coordinated on the population level. The self-renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell (HFSC) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an in vitro culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long-term maintenance of murine multipotent HFSCs in the absence of heterologous cell types. Strikingly, this scheme promotes de novo generation of HFSCs from non-HFSCs and vice versa in a dynamic self-organizing process. This bidirectional interconversion of HFSCs and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population-level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate. Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single‐cell behaviors are coordinated on the population level. The self‐renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell (HFSC) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an in vitro culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long‐term maintenance of murine multipotent HFSCs in the absence of heterologous cell types. Strikingly, this scheme promotes de novo generation of HFSCs from non‐HFSCs and vice versa in a dynamic self‐organizing process. This bidirectional interconversion of HFSCs and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population‐level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate. Synopsis An advanced in vitro culture system allows for enrichment and long‐term maintenance of multipotent mouse hair follicle stem cells (HFSCs), recapitulating key features of their in vivo regulation. Combination of a 3D extracellular matrix environment and defined soluble components (FGF‐2, VEGF‐A, ROCK inhibitor Y27632) facilitates long‐term propagation of HFSCs. HFSC expansion can be achieved from purified HFSCs as well as from total or HFSC‐depleted epidermal cell mixtures. Cultured HFSCs retain multipotency, self‐renewal potential, and transcriptional identity. Bidirectional interconversion of cultured HFSCs driven by BMP and Shh pathways leads to self‐organization into a dynamic equilibrium between HFSCs and their progeny. Cell culture conditions for enrichment and long‐term maintenance of multipotent mouse skin stem cells in population equilibrium. Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single‐cell behaviors are coordinated on the population level. The self‐renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell ( HFSC ) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an in vitro culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long‐term maintenance of murine multipotent HFSC s in the absence of heterologous cell types. Strikingly, this scheme promotes de novo generation of HFSC s from non‐ HFSC s and vice versa in a dynamic self‐organizing process. This bidirectional interconversion of HFSC s and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population‐level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate. Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single‐cell behaviors are coordinated on the population level. The self‐renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell (HFSC) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an in vitro culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long‐term maintenance of murine multipotent HFSCs in the absence of heterologous cell types. Strikingly, this scheme promotes de novo generation of HFSCs from non‐HFSCs and vice versa in a dynamic self‐organizing process. This bidirectional interconversion of HFSCs and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population‐level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate. Synopsis An advanced in vitro culture system allows for enrichment and long‐term maintenance of multipotent mouse hair follicle stem cells (HFSCs), recapitulating key features of their in vivo regulation. Combination of a 3D extracellular matrix environment and defined soluble components (FGF‐2, VEGF‐A, ROCK inhibitor Y27632) facilitates long‐term propagation of HFSCs. HFSC expansion can be achieved from purified HFSCs as well as from total or HFSC‐depleted epidermal cell mixtures. Cultured HFSCs retain multipotency, self‐renewal potential, and transcriptional identity. Bidirectional interconversion of cultured HFSCs driven by BMP and Shh pathways leads to self‐organization into a dynamic equilibrium between HFSCs and their progeny. Graphical Abstract Cell culture conditions for enrichment and long‐term maintenance of multipotent mouse skin stem cells in population equilibrium. Understanding how complex tissues are formed, maintained, and regenerated through local growth, differentiation, and remodeling requires knowledge on how single-cell behaviors are coordinated on the population level. The self-renewing hair follicle, maintained by a distinct stem cell population, represents an excellent paradigm to address this question. A major obstacle in mechanistic understanding of hair follicle stem cell (HFSC) regulation has been the lack of a culture system that recapitulates HFSC behavior while allowing their precise monitoring and manipulation. Here, we establish an in vitro culture system based on a 3D extracellular matrix environment and defined soluble factors, which for the first time allows expansion and long-term maintenance of murine multipotent HFSCs in the absence of heterologous cell types. Strikingly, this scheme promotes de novo generation of HFSCs from non-HFSCs and vice versa in a dynamic self-organizing process. This bidirectional interconversion of HFSCs and their progeny drives the system into a population equilibrium state. Our study uncovers regulatory dynamics by which phenotypic plasticity of cells drives population-level homeostasis within a niche, and provides a discovery tool for studies on adult stem cell fate. Synopsis An advanced in vitro culture system allows for enrichment and long-term maintenance of multipotent mouse hair follicle stem cells (HFSCs), recapitulating key features of their in vivo regulation. Combination of a 3D extracellular matrix environment and defined soluble components (FGF-2, VEGF-A, ROCK inhibitor Y27632) facilitates long-term propagation of HFSCs. HFSC expansion can be achieved from purified HFSCs as well as from total or HFSC-depleted epidermal cell mixtures. Cultured HFSCs retain multipotency, self-renewal potential, and transcriptional identity. Bidirectional interconversion of cultured HFSCs driven by BMP and Shh pathways leads to self-organization into a dynamic equilibrium between HFSCs and their progeny. |
| Author | Chacón‐Martínez, Carlos Andrés Glauche, Ingmar Wickström, Sara A Niemann, Catherin Klose, Markus |
| AuthorAffiliation | 1 Paul Gerson Unna Group “Skin Homeostasis and Ageing” Max Planck Institute for Biology of Ageing Cologne Germany 4 Center for Molecular Medicine Cologne University of Cologne Cologne Germany 2 Institute for Medical Informatics and Biometry Carl Gustav Carus Faculty of Medicine Technische Universität Dresden Dresden Germany 3 Institute for Biochemistry II Medical Faculty University of Cologne Cologne Germany 5 Cologne Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD) University of Cologne Cologne Germany |
| AuthorAffiliation_xml | – name: 4 Center for Molecular Medicine Cologne University of Cologne Cologne Germany – name: 5 Cologne Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD) University of Cologne Cologne Germany – name: 1 Paul Gerson Unna Group “Skin Homeostasis and Ageing” Max Planck Institute for Biology of Ageing Cologne Germany – name: 2 Institute for Medical Informatics and Biometry Carl Gustav Carus Faculty of Medicine Technische Universität Dresden Dresden Germany – name: 3 Institute for Biochemistry II Medical Faculty University of Cologne Cologne Germany |
| Author_xml | – sequence: 1 givenname: Carlos Andrés surname: Chacón‐Martínez fullname: Chacón‐Martínez, Carlos Andrés organization: Paul Gerson Unna Group “Skin Homeostasis and Ageing”, Max Planck Institute for Biology of Ageing – sequence: 2 givenname: Markus surname: Klose fullname: Klose, Markus organization: Institute for Medical Informatics and Biometry, Carl Gustav Carus Faculty of Medicine, Technische Universität Dresden – sequence: 3 givenname: Catherin surname: Niemann fullname: Niemann, Catherin organization: Institute for Biochemistry II, Medical Faculty, University of Cologne, Center for Molecular Medicine Cologne, University of Cologne – sequence: 4 givenname: Ingmar surname: Glauche fullname: Glauche, Ingmar organization: Institute for Medical Informatics and Biometry, Carl Gustav Carus Faculty of Medicine, Technische Universität Dresden – sequence: 5 givenname: Sara A orcidid: 0000-0001-6383-6292 surname: Wickström fullname: Wickström, Sara A email: wickstroem@age.mpg.de organization: Paul Gerson Unna Group “Skin Homeostasis and Ageing”, Max Planck Institute for Biology of Ageing, Cologne Excellence Cluster on Cellular Stress Responses in Aging‐Associated Diseases (CECAD), University of Cologne |
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| SubjectTerms | Animals Cell culture Cell Culture Techniques - methods Cell Differentiation differentiation EMBO11 EMBO39 EMBO43 Extracellular matrix Hair Hair Follicle - cytology hair follicle stem cells Mice, Inbred BALB C Mice, Inbred C57BL niche Organ Culture Techniques - methods Plasticity reprogramming Rodents stem cell cultures Stem cells Stem Cells - physiology |
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| Title | Hair follicle stem cell cultures reveal self‐organizing plasticity of stem cells and their progeny |
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