Parathyroid Hormone Receptor Signaling Induces Bone Resorption in the Adult Skeleton by Directly Regulating the RANKL Gene in Osteocytes
Open accessAbstract
PTH upregulates the expression of the receptor activator of nuclear factor κB ligand (Rankl) in cells of the osteoblastic lineage, but the precise differentiation stage of the PTH target cell responsible for RANKL-mediated stimulation of bone resorption remains undefined. We report that constitutive activation of PTH receptor signaling only in osteocytes in transgenic mice (DMP1-caPTHR1) was sufficient to increase Rankl expression and bone resorption. Resorption in DMP1-caPTHR1 mice crossed with mice lacking the distal control region regulated by PTH in the Rankl gene (DCR−/−) was similar to DMP1-caPTHR1 mice at 1 month of age, but progressively declined to reach values undistinguishable from wild-type (WT) mice at 5 months of age. Moreover, DMP1-caPTHR1 mice exhibited low tissue material density and increased serum alkaline phosphatase activity at 5 month of age, and these indices of high remodeling were partially and totally corrected in compound DMP1-caPTHR1;DCR−/− male mice, and less affected in female mice. Rankl expression in bones from DMP1-caPTHR1 mice was elevated at both 1 and 5 months of age, whereas it was high, similar to DMP1-caPTHR1 mice at 1 month, but low, similar to WT levels at 5 months in compound mice. Moreover, PTH increased Rankl and decreased Sost and Opg expression in ex vivo bone organ cultures established from WT mice, but only regulated Sost and Opg expression in cultures from DCR−/− mice. PTH also increased RANKL expression in osteocyte-containing primary cultures of calvarial cells, in isolated murine osteocytes, and in WT but not in DCR−/− osteocyte-enriched bones. Thus, PTH upregulates Rankl expression in osteocytes in vitro, ex vivo and in vivo, and resorption induced by PTH receptor signaling in the adult skeleton requires direct regulation of the Rankl gene in osteocytes.
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When PTHR1 on osteocytes is activated by chronically high PTH concentrations or when PTHR1 is constitutively active, osteocytes initiate bone remodeling by expanding the osteoclast pool through the release of RANKL, particularly within the bone cortex.
“When PTHR1 on osteocytes is activated by chronically high PTH concentrations or when PTHR1 is constitutively active, osteocytes initiate bone remodeling by expanding the osteoclast pool through the release of RANKL,79 particularly within the bone cortex.80”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [79]
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- Authors
- Ben-awadh, A. N., Delgado-Calle, J., Tu, X., Kuhlenschmidt, K., Allen, M. R., Plotkin, L. I., & Bellido, T.
- Affiliations
- Departments of Anatomy and Cell Biology (A.N.B., J.D.-C., X.T., K.K., M.R.A., L.I.P., T.B.), Indianapolis, Indiana 46202
- Roudebush Veterans Administration Medical Center (J.D.-C., L.I.P., T.B.), Indianapolis, Indiana 46202
- Richard L. Roudebush VA Medical Center (US)
- Corresponding author
- Bellido, Teresita
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2014-08-01
- Volume
- 155
- Issue
- 8
- Pages
- 2797-2809
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC4098003
- OpenAlex
- W2084261817
- Cited by
- 114
- References
- 36
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 9 · 2023: 9 · 2022: 3 · 2021: 6 · 2020: 18 · 2019: 10 · 2018: 14 · 2017: 9 · 2016: 7 · 2015: 12 · 2013: 1
- FWCI
- 3.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IUScholarWorks (Indiana University) (submittedVersion)
- Purdue University Indianapolis (Indiana University) (submittedVersion)
- PMC
- Funders
- U.S. Department of Veterans Affairs (IK6 BX004596, I01 BX002104)
- National Institutes of Health (1s10rr023710-01)
- School of Medicine, Indiana University
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK076007)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR059357)
- National Center for Research Resources (S10‐RR023710)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Nephrology › Parathyroid Disorders and Treatments
- Keywords
- parathyroid hormone, RANKL, osteocytes, bone resorption, bone remodeling, sclerostin, OPG, osteoblasts, sex differences
- MeSH terms
- Animals, Bone Resorption, Disease Models, Animal, Female, Humans, Male, Mice, Transgenic, Organ Culture Techniques, Osteocytes, Parathyroid Hormone, Signal Transduction, Receptors, Parathyroid Hormone, Gene Expression Regulation, Developmental, Mice, RANK Ligand, Primary Cell Culture
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