Parathyroid Hormone Directs Bone Marrow Mesenchymal Cell Fate
Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue...
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| Published in | Cell metabolism Vol. 25; no. 3; pp. 661 - 672 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
07.03.2017
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1550-4131 1932-7420 1932-7420 |
| DOI | 10.1016/j.cmet.2017.01.001 |
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| Abstract | Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa B ligand (Rankl) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1+RANKL+ marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotic patients. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH’s therapeutic action through its ability to direct mesenchymal cell fate.
[Display omitted]
•PTH1R regulates lineage allocation in the marrow•Bone marrow adipocytes compose a unique adipose depot and produce RANKL•PTH reduced marrow adipogenesis in mice and humans
Fan et al. show that PTH regulates mesenchymal stem cell fate between bone and adipocyte in the marrow. Bone marrow adipocytes have distinct origins and properties from other adipocytes and are responsive to PTH, underlying the reduction in marrow adiposity in mouse models and idiopathic osteoporosis patients treated with PTH. |
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| AbstractList | Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa B ligand (Rankl) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1
RANKL
marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotic patients. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH's therapeutic action through its ability to direct mesenchymal cell fate. Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP Receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa-B ligand ( Rankl ) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1 + RANKL + marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotics. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH’s therapeutic action through its ability to direct mesenchymal cell fate. XXX et al show that PTH regulates mesenchymal stem cell fate between bone and adipocyte in the marrow. Bone marrow adipocytes have distinct origins and properties from other adipocytes and are responsive to PTH, underlying the reduction in marrow adiposity in mouse models and idiopathic osteoporosis patients treated with PTH. Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa B ligand (Rankl) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1+RANKL+ marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotic patients. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH's therapeutic action through its ability to direct mesenchymal cell fate.Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa B ligand (Rankl) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1+RANKL+ marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotic patients. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH's therapeutic action through its ability to direct mesenchymal cell fate. Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor (PTH1R) in mesenchymal stem cells using Prx1Cre and found low bone formation, increased bone resorption, and high bone marrow adipose tissue (BMAT). Bone marrow adipocytes traced to Prx1 and expressed classic adipogenic markers and high receptor activator of nuclear factor kappa B ligand (Rankl) expression. RANKL levels were also elevated in bone marrow supernatant and serum, but undetectable in other adipose depots. By cell sorting, Pref1+RANKL+ marrow progenitors were twice as great in mutant versus control marrow. Intermittent PTH administration to control mice reduced BMAT significantly. A similar finding was noted in male osteoporotic patients. Thus, marrow adipocytes exhibit osteogenic and adipogenic characteristics, are uniquely responsive to PTH, and secrete RANKL. These studies reveal an important mechanism for PTH’s therapeutic action through its ability to direct mesenchymal cell fate. [Display omitted] •PTH1R regulates lineage allocation in the marrow•Bone marrow adipocytes compose a unique adipose depot and produce RANKL•PTH reduced marrow adipogenesis in mice and humans Fan et al. show that PTH regulates mesenchymal stem cell fate between bone and adipocyte in the marrow. Bone marrow adipocytes have distinct origins and properties from other adipocytes and are responsive to PTH, underlying the reduction in marrow adiposity in mouse models and idiopathic osteoporosis patients treated with PTH. |
| Author | Bilezikian, John P. Wu, Joy Y. Rosen, Clifford J. Fan, Yi Baron, Roland Zhou, Xuedong Bronson, Roderick T. Mannstadt, Michael Lanske, Beate Hanai, Jun-ichi Bi, Ruiye DeMambro, Victoria Dempster, David W. Le, Phuong T. Maridas, David Kir, Serkan Figueroa, Carolina A. Horowitz, Mark C. |
| AuthorAffiliation | 6 Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, 02215, USA 9 Division of Endocrinology, Stanford University School of Medicine, Stanford, CA, 94305, USA 4 Maine Medical Center Research Institute, Scarborough, ME, 04074, USA 1 Division of Bone and Mineral Research, Harvard School of Dental Medicine, Boston, MA, 02115, USA 10 Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA 2 State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, 610041, China 11 Department of Pathology, College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA 7 Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, 02215, USA 8 Department of Orthopaedics and Rehabilitation, Yale School of Medicine, New Haven, CT, 06510, USA 5 Endocrine Unit, Massachusetts General Hospital and Department of Medicine, Harvard Medical |
| AuthorAffiliation_xml | – name: 4 Maine Medical Center Research Institute, Scarborough, ME, 04074, USA – name: 2 State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, 610041, China – name: 1 Division of Bone and Mineral Research, Harvard School of Dental Medicine, Boston, MA, 02115, USA – name: 7 Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, 02215, USA – name: 9 Division of Endocrinology, Stanford University School of Medicine, Stanford, CA, 94305, USA – name: 3 Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, 02215, USA – name: 10 Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA – name: 8 Department of Orthopaedics and Rehabilitation, Yale School of Medicine, New Haven, CT, 06510, USA – name: 5 Endocrine Unit, Massachusetts General Hospital and Department of Medicine, Harvard Medical School, Boston, MA, 02114, USA – name: 11 Department of Pathology, College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA – name: 6 Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, 02215, USA |
| Author_xml | – sequence: 1 givenname: Yi surname: Fan fullname: Fan, Yi organization: Division of Bone and Mineral Research, Harvard School of Dental Medicine, Boston, MA 02115, USA – sequence: 2 givenname: Jun-ichi surname: Hanai fullname: Hanai, Jun-ichi organization: Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02215, USA – sequence: 3 givenname: Phuong T. surname: Le fullname: Le, Phuong T. organization: Maine Medical Center Research Institute, Scarborough, ME 04074, USA – sequence: 4 givenname: Ruiye surname: Bi fullname: Bi, Ruiye organization: State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan 610041, China – sequence: 5 givenname: David surname: Maridas fullname: Maridas, David organization: Maine Medical Center Research Institute, Scarborough, ME 04074, USA – sequence: 6 givenname: Victoria surname: DeMambro fullname: DeMambro, Victoria organization: Maine Medical Center Research Institute, Scarborough, ME 04074, USA – sequence: 7 givenname: Carolina A. surname: Figueroa fullname: Figueroa, Carolina A. organization: Maine Medical Center Research Institute, Scarborough, ME 04074, USA – sequence: 8 givenname: Serkan surname: Kir fullname: Kir, Serkan organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 9 givenname: Xuedong surname: Zhou fullname: Zhou, Xuedong organization: State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan 610041, China – sequence: 10 givenname: Michael surname: Mannstadt fullname: Mannstadt, Michael organization: Endocrine Unit, Massachusetts General Hospital and Department of Medicine, Harvard Medical School, Boston, MA 02114, USA – sequence: 11 givenname: Roland surname: Baron fullname: Baron, Roland organization: Division of Bone and Mineral Research, Harvard School of Dental Medicine, Boston, MA 02115, USA – sequence: 12 givenname: Roderick T. surname: Bronson fullname: Bronson, Roderick T. organization: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02215, USA – sequence: 13 givenname: Mark C. surname: Horowitz fullname: Horowitz, Mark C. organization: Department of Orthopaedics and Rehabilitation, Yale School of Medicine, New Haven, CT 06510, USA – sequence: 14 givenname: Joy Y. surname: Wu fullname: Wu, Joy Y. organization: Division of Endocrinology, Stanford University School of Medicine, Stanford, CA 94305, USA – sequence: 15 givenname: John P. surname: Bilezikian fullname: Bilezikian, John P. organization: Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA – sequence: 16 givenname: David W. surname: Dempster fullname: Dempster, David W. organization: Department of Pathology, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA – sequence: 17 givenname: Clifford J. surname: Rosen fullname: Rosen, Clifford J. email: rosenc@mmc.org organization: Maine Medical Center Research Institute, Scarborough, ME 04074, USA – sequence: 18 givenname: Beate surname: Lanske fullname: Lanske, Beate email: beate_lanske@hsdm.harvard.edu organization: Division of Bone and Mineral Research, Harvard School of Dental Medicine, Boston, MA 02115, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28162969$$D View this record in MEDLINE/PubMed |
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| Keywords | lineage RANKL receptor PTH bone resorption |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Lead Contact Co-Corresponding author description: Dr. Lanske (lead contact): Dr. Lanske was involved in designing the original study, in generating the mutant mouse strains, planning the experiments, discovering and analyzing the phenotype of mice, supervising all in vivo and in vitro experiments performed at HSDM, setting up required collaborations for the completion of the study, writing and revising the manuscript. She has discussed all steps of the study with the postdoc and co-authors on a daily basis, reviewed the results, coordinated the experiments, and exchanged the design and ideas with Dr. Rosen on a regular basis. Dr. Rosen was involved in planning experiments, writing the manuscript with Dr. Lanske, and writing the revisions with Dr. Lanske. Specifically, Dr. Rosen focused on the marrow adipose phenotype and supervised the osmium micro CT analyses at MMCRI with and without PTH, the tibial histology for counting of the marrow adipocytes in mutant and controls, the human studies of marrow adiposity in iliac crest biopsies pre- and post PTH treatment, and the in vitro studies of PTH regulation of 3T3 L1 cells. He provided the methods that Dr. Fan used for isolating marrow adipocytes in the controls and mutants. He also developed the methods for sorting marrow progenitors for Pref-1 and RANKL using FACS that were adapted for this study by Dr. Fan, and supervised the adaptation of the TRAP technology for RANKL expression in inguinal adipose depots performed at MMCRI. Dr. Rosen discussed extensively with Dr. Jack Martin the role of Zfp467 in mediating RANKL expression in adipocytes. Co-correspondence |
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| Snippet | Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP... Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP receptor... Intermittent PTH administration builds bone mass and prevents fractures, but its mechanism of action is unclear. We genetically deleted the PTH/PTHrP Receptor... |
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| SubjectTerms | Adipocytes - metabolism Adipogenesis Adipose Tissue - metabolism Animals Biomarkers - metabolism Bone and Bones Bone Marrow Cells - cytology Bone Marrow Cells - drug effects Bone Marrow Cells - metabolism bone resorption Cell Count Cell Lineage - drug effects Humans Integrases - metabolism lineage Male Mesenchymal Stromal Cells - cytology Mesenchymal Stromal Cells - drug effects Mesenchymal Stromal Cells - metabolism Mice Osteoblasts - metabolism Osteoporosis - pathology Parathyroid Hormone - pharmacology Phenotype PTH RANK Ligand - metabolism RANKL receptor Receptor, Parathyroid Hormone, Type 1 - metabolism Signal Transduction Skull - cytology |
| Title | Parathyroid Hormone Directs Bone Marrow Mesenchymal Cell Fate |
| URI | https://dx.doi.org/10.1016/j.cmet.2017.01.001 https://www.ncbi.nlm.nih.gov/pubmed/28162969 https://www.proquest.com/docview/1865521115 https://pubmed.ncbi.nlm.nih.gov/PMC5342925 |
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