Inhibition of the epigenetic suppressor EZH2 primes osteogenic differentiation mediated by BMP2
Bone-stimulatory therapeutics include bone morphogenetic proteins (e.g. BMP2), parathyroid hormone, and antibody-based suppression of WNT antagonists. Inhibition of the epigenetic enzyme enhancer of zeste homolog 2 (EZH2) is both bone anabolic and osteoprotective. EZH2 inhibition stimulates key comp...
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| Published in: | The Journal of biological chemistry Vol. 295; no. 23; pp. 7877 - 7893 |
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| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Language: | English |
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05-06-2020
American Society for Biochemistry and Molecular Biology |
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| Abstract | Bone-stimulatory therapeutics include bone morphogenetic proteins (e.g. BMP2), parathyroid hormone, and antibody-based suppression of WNT antagonists. Inhibition of the epigenetic enzyme enhancer of zeste homolog 2 (EZH2) is both bone anabolic and osteoprotective. EZH2 inhibition stimulates key components of bone-stimulatory signaling pathways, including the BMP2 signaling cascade. Because of high costs and adverse effects associated with BMP2 use, here we investigated whether BMP2 dosing can be reduced by co-treatment with EZH2 inhibitors. Co-administration of BMP2 with the EZH2 inhibitor GSK126 enhanced differentiation of murine (MC3T3) osteoblasts, reflected by increased alkaline phosphatase activity, Alizarin Red staining, and expression of bone-related marker genes (e.g. Bglap and Phospho1). Strikingly, co-treatment with BMP2 (10 ng/ml) and GSK126 (5 μm) was synergistic and was as effective as 50 ng/ml BMP2 at inducing MC3T3 osteoblastogenesis. Similarly, the BMP2–GSK126 co-treatment stimulated osteogenic differentiation of human bone marrow–derived mesenchymal stem/stromal cells, reflected by induction of key osteogenic markers (e.g. Osterix/SP7 and IBSP). A combination of BMP2 (300 ng local) and GSK126 (5 μg local and 5 days of 50 mg/kg systemic) yielded more consistent bone healing than single treatments with either compound in a mouse calvarial critical-sized defect model according to results from μCT, histomorphometry, and surgical grading of qualitative X-rays. We conclude that EZH2 inhibition facilitates BMP2-mediated induction of osteogenic differentiation of progenitor cells and maturation of committed osteoblasts. We propose that epigenetic priming, coupled with bone anabolic agents, enhances osteogenesis and could be leveraged in therapeutic strategies to improve bone mass. |
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| AbstractList | Bone-stimulatory therapeutics include bone morphogenetic proteins (e.g. BMP2), parathyroid hormone, and antibody-based suppression of WNT antagonists. Inhibition of the epigenetic enzyme enhancer of zeste homolog 2 (EZH2) is both bone anabolic and osteoprotective. EZH2 inhibition stimulates key components of bone-stimulatory signaling pathways, including the BMP2 signaling cascade. Because of high costs and adverse effects associated with BMP2 use, here we investigated whether BMP2 dosing can be reduced by co-treatment with EZH2 inhibitors. Co-administration of BMP2 with the EZH2 inhibitor GSK126 enhanced differentiation of murine (MC3T3) osteoblasts, reflected by increased alkaline phosphatase activity, Alizarin Red staining, and expression of bone-related marker genes (e.g. Bglap and Phospho1). Strikingly, co-treatment with BMP2 (10 ng/ml) and GSK126 (5 μm) was synergistic and was as effective as 50 ng/ml BMP2 at inducing MC3T3 osteoblastogenesis. Similarly, the BMP2–GSK126 co-treatment stimulated osteogenic differentiation of human bone marrow–derived mesenchymal stem/stromal cells, reflected by induction of key osteogenic markers (e.g. Osterix/SP7 and IBSP). A combination of BMP2 (300 ng local) and GSK126 (5 μg local and 5 days of 50 mg/kg systemic) yielded more consistent bone healing than single treatments with either compound in a mouse calvarial critical-sized defect model according to results from μCT, histomorphometry, and surgical grading of qualitative X-rays. We conclude that EZH2 inhibition facilitates BMP2-mediated induction of osteogenic differentiation of progenitor cells and maturation of committed osteoblasts. We propose that epigenetic priming, coupled with bone anabolic agents, enhances osteogenesis and could be leveraged in therapeutic strategies to improve bone mass. Bone-stimulatory therapeutics include bone morphogenetic proteins ( e.g. BMP2), parathyroid hormone, and antibody-based suppression of WNT antagonists. Inhibition of the epigenetic enzyme enhancer of zeste homolog 2 (EZH2) is both bone anabolic and osteoprotective. EZH2 inhibition stimulates key components of bone-stimulatory signaling pathways, including the BMP2 signaling cascade. Because of high costs and adverse effects associated with BMP2 use, here we investigated whether BMP2 dosing can be reduced by co-treatment with EZH2 inhibitors. Co-administration of BMP2 with the EZH2 inhibitor GSK126 enhanced differentiation of murine (MC3T3) osteoblasts, reflected by increased alkaline phosphatase activity, Alizarin Red staining, and expression of bone-related marker genes ( e.g. Bglap and Phospho1). Strikingly, co-treatment with BMP2 (10 ng/ml) and GSK126 (5 μ m ) was synergistic and was as effective as 50 ng/ml BMP2 at inducing MC3T3 osteoblastogenesis. Similarly, the BMP2–GSK126 co-treatment stimulated osteogenic differentiation of human bone marrow–derived mesenchymal stem/stromal cells, reflected by induction of key osteogenic markers ( e.g. Osterix/SP7 and IBSP). A combination of BMP2 (300 ng local) and GSK126 (5 μg local and 5 days of 50 mg/kg systemic) yielded more consistent bone healing than single treatments with either compound in a mouse calvarial critical-sized defect model according to results from μCT, histomorphometry, and surgical grading of qualitative X-rays. We conclude that EZH2 inhibition facilitates BMP2-mediated induction of osteogenic differentiation of progenitor cells and maturation of committed osteoblasts. We propose that epigenetic priming, coupled with bone anabolic agents, enhances osteogenesis and could be leveraged in therapeutic strategies to improve bone mass. Bone-stimulatory therapeutics include bone morphogenetic proteins ( BMP2), parathyroid hormone, and antibody-based suppression of WNT antagonists. Inhibition of the epigenetic enzyme enhancer of zeste homolog 2 (EZH2) is both bone anabolic and osteoprotective. EZH2 inhibition stimulates key components of bone-stimulatory signaling pathways, including the BMP2 signaling cascade. Because of high costs and adverse effects associated with BMP2 use, here we investigated whether BMP2 dosing can be reduced by co-treatment with EZH2 inhibitors. Co-administration of BMP2 with the EZH2 inhibitor GSK126 enhanced differentiation of murine (MC3T3) osteoblasts, reflected by increased alkaline phosphatase activity, Alizarin Red staining, and expression of bone-related marker genes ( Bglap and Phospho1). Strikingly, co-treatment with BMP2 (10 ng/ml) and GSK126 (5 μm) was synergistic and was as effective as 50 ng/ml BMP2 at inducing MC3T3 osteoblastogenesis. Similarly, the BMP2-GSK126 co-treatment stimulated osteogenic differentiation of human bone marrow-derived mesenchymal stem/stromal cells, reflected by induction of key osteogenic markers ( Osterix/SP7 and IBSP). A combination of BMP2 (300 ng local) and GSK126 (5 μg local and 5 days of 50 mg/kg systemic) yielded more consistent bone healing than single treatments with either compound in a mouse calvarial critical-sized defect model according to results from μCT, histomorphometry, and surgical grading of qualitative X-rays. We conclude that EZH2 inhibition facilitates BMP2-mediated induction of osteogenic differentiation of progenitor cells and maturation of committed osteoblasts. We propose that epigenetic priming, coupled with bone anabolic agents, enhances osteogenesis and could be leveraged in therapeutic strategies to improve bone mass. |
| Author | Cool, Simon M. Galeano-Garces, Daniela Westendorf, Jennifer J. Larson, A. Noelle Kloen, Peter Paradise, Christopher R. Thaler, Roman Hevesi, Mario van Wijnen, Andre J. Mol, Merel O. Galeano-Garces, Catalina Pichurin, Oksana Dudakovic, Amel Zan, Pengfei Samsonraj, Rebekah M. Galvan, M. Lizeth Begun, Dana L. Karperien, Marcel |
| Author_xml | – sequence: 1 givenname: Amel surname: Dudakovic fullname: Dudakovic, Amel organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 2 givenname: Rebekah M. surname: Samsonraj fullname: Samsonraj, Rebekah M. organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 3 givenname: Christopher R. orcidid: 0000-0002-5882-709X surname: Paradise fullname: Paradise, Christopher R. organization: Mayo Clinic Graduate School of Biomedical Sciences, Mayo Clinic, Rochester, Minnesota, USA – sequence: 4 givenname: Catalina orcidid: 0000-0003-1882-6858 surname: Galeano-Garces fullname: Galeano-Garces, Catalina organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 5 givenname: Merel O. surname: Mol fullname: Mol, Merel O. organization: Department of Orthopedic Surgery, Amsterdam University Medical Center, Amsterdam, The Netherlands – sequence: 6 givenname: Daniela orcidid: 0000-0003-0954-6352 surname: Galeano-Garces fullname: Galeano-Garces, Daniela organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 7 givenname: Pengfei surname: Zan fullname: Zan, Pengfei organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 8 givenname: M. Lizeth surname: Galvan fullname: Galvan, M. Lizeth organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 9 givenname: Mario orcidid: 0000-0001-6208-878X surname: Hevesi fullname: Hevesi, Mario organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 10 givenname: Oksana surname: Pichurin fullname: Pichurin, Oksana organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 11 givenname: Roman surname: Thaler fullname: Thaler, Roman organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 12 givenname: Dana L. surname: Begun fullname: Begun, Dana L. organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 13 givenname: Peter surname: Kloen fullname: Kloen, Peter organization: Department of Orthopedic Surgery, Amsterdam University Medical Center, Amsterdam, The Netherlands – sequence: 14 givenname: Marcel surname: Karperien fullname: Karperien, Marcel organization: Department of Developmental BioEngineering, University of Twente, Enschede, The Netherlands – sequence: 15 givenname: A. Noelle surname: Larson fullname: Larson, A. Noelle organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 16 givenname: Jennifer J. orcidid: 0000-0002-4464-6108 surname: Westendorf fullname: Westendorf, Jennifer J. organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA – sequence: 17 givenname: Simon M. surname: Cool fullname: Cool, Simon M. organization: Glycotherapeutics Group, Institute of Medical Biology, Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 18 givenname: Andre J. orcidid: 0000-0002-4458-0946 surname: van Wijnen fullname: van Wijnen, Andre J. email: vanwijnen.andre@mayo.edu organization: Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32332097$$D View this record in MEDLINE/PubMed |
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| Keywords | histone methylation BMP2 methyltransferase mesenchymal stem cells (MSCs) chromatin regulation enhancer of zeste homolog bone development bone morphogenetic protein (BMP) osteoblast osteogenesis epigenetics Ezh2 |
| Language | English |
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| SubjectTerms | 3T3 Cells Animals BMP2 bone development bone morphogenetic protein (BMP) Bone Morphogenetic Protein 2 - administration & dosage Bone Morphogenetic Protein 2 - metabolism Cell Differentiation - drug effects Cells, Cultured chromatin regulation enhancer of zeste homolog Enhancer of Zeste Homolog 2 Protein - antagonists & inhibitors Enhancer of Zeste Homolog 2 Protein - metabolism epigenetics Ezh2 Gene Regulation histone methylation Humans Indoles - administration & dosage Indoles - pharmacology mesenchymal stem cells (MSCs) methyltransferase Mice osteoblast Osteoblasts - drug effects osteogenesis Osteogenesis - drug effects Pyridones - administration & dosage Pyridones - pharmacology |
| Title | Inhibition of the epigenetic suppressor EZH2 primes osteogenic differentiation mediated by BMP2 |
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