Control of Bone Anabolism in Response to Mechanical Loading and PTH by Distinct Mechanisms Downstream of the PTH Receptor

Delgado-Calle, Jesus; Tu, Xiaolin; Pacheco-Costa, Rafael; McAndrews, Kevin; Edwards, Rachel; Pellegrini, Gretel G; Kuhlenschmidt, Kali; Olivos, Naomie; Robling, Alexander; Peacock, Munro; Plotkin, Lilian I; Bellido, Teresita

doi:10.1002/jbmr.3011

Cited by 114Bone Metabolism and DiseasesBone health and osteoporosis researchParathyroid Disorders and Treatments

Control of Bone Anabolism in Response to Mechanical Loading and PTH by Distinct Mechanisms Downstream of the PTH Receptor

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Delgado-Calle, Jesus, Tu, Xiaolin, Pacheco-Costa, Rafael, McAndrews, Kevin, Edwards, Rachel, Pellegrini, Gretel G, Kuhlenschmidt, Kali, Olivos, Naomie +4 more·2017·Journal of Bone and Mineral Research

DOI 10.1002/jbmr.3011PMC PMC8502039

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Abstract

Osteocytes integrate the responses of bone to mechanical and hormonal stimuli by poorly understood mechanisms. We report here that mice with conditional deletion of the parathyroid hormone (PTH) receptor 1 (Pth1r) in dentin matrix protein 1 (DMP1)-8kb–expressing cells (cKO) exhibit a modest decrease in bone resorption leading to a mild increase in cancellous bone without changes in cortical bone. However, bone resorption in response to endogenous chronic elevation of PTH in growing or adult cKO mice induced by a low calcium diet remained intact, because the increased bone remodeling and bone loss was indistinguishable from that exhibited by control littermates. In contrast, the bone gain and increased bone formation in cancellous and cortical bone induced by daily injections of PTH and the periosteal bone apposition induced by axial ulna loading were markedly reduced in cKO mice compared to controls. Remarkably, however, wild-type (WT) control littermates and transgenic mice overexpressing SOST injected daily with PTH exhibit similar activation of Wnt/β-catenin signaling, increased bone formation, and cancellous and cortical bone gain. Taken together, these findings demonstrate that Pth1r in DMP1-8kb–expressing cells is required to maintain basal levels of bone resorption but is dispensable for the catabolic action of chronic PTH elevation; and it is essential for the anabolic actions of daily PTH injections and mechanical loading. However, downregulation of Sost/sclerostin, previously shown to be required for bone anabolism induced by mechanical loading, is not required for PTH-induced bone gain, showing that other mechanisms downstream of the Pth1r in DMP1-8kb–expressing cells are responsible for the hormonal effect. © 2016 American Society for Bone and Mineral Research.

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SOST expression downregulation positively fine-tunes the bone remodeling balance by promoting osteoblast expansion.
“SOST expression downregulation positively fine-tunes the bone remodeling balance by promoting osteoblast expansion.78”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [78]

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[32]Tu X, Edwards R, Olivos N, Conditional deletion of the parathyroid hormone (PTH) receptor 1 from osteocytes results in decreased bone resorption and a progressive increase in cancellous bone mass. J Bone Miner Res. 2011; 26: S16.
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Low Intensity Pulsed Ultrasound for Bone Tissue Engineering
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PTH1R translocation to primary cilia in mechanically‐stimulated ostecytes prevents osteoclast formation via regulation of CXCL5 and IL‐6 secretion
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Postnatal deletion of β-catenin in osterix-expressing cells is necessary for bone growth and intermittent PTH-induced bone gain
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Pigment epithelium derived factor regulates human Sost/Sclerostin and other osteocyte gene expression via the receptor and induction of Erk/GSK-3beta/beta-catenin signaling
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The Transcription Factor Foxc1 Promotes Osteogenesis by Directly Regulating Runx2 in Response of Intermittent Parathyroid Hormone (1–34) Treatment
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CHIR99021-Treated Osteocytes with Wnt Activation in 3D-Printed Module Form an Osteogenic Microenvironment for Enhanced Osteogenesis and Vasculogenesis
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Functionalized 3D-Printed ST2/Gelatin Methacryloyl/Polcaprolactone Scaffolds for Enhancing Bone Regeneration with Vascularization
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Comparative study in estrogen-depleted mice identifies skeletal and osteocyte transcriptomic responses to abaloparatide and teriparatide
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Regulation of the Osteocyte Secretome with Aging and Disease
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Long-term use of proton pump inhibitors adversely affects minerals and vitamin metabolism, bone turnover, bone mass, and bone strength
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Plasma Membrane Receptors Involved in the Binding and Response of Osteoclasts to Noncellular Components of the Bone
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Disruption of the aldehyde dehydrogenase 2 gene increases the bone anabolic response to intermittent PTH treatment in an ovariectomized mouse model
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Loss of PTH 1 receptor signaling in periodontal cells drives cementum dysfunction and molar ankylosis in mice
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Paracrine parathyroid hormone–related protein in bone: physiology and pharmacology
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Engineering a Wnt-activated osteomimetic microenvironment with iPSC-derived MSCs for synergistic bone regeneration, angiogenesis, and neurogenesis
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Osteocyte Biology
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Matrix Competence Failure in Osteoporosis: Mechanosensing, Osteoimmune Crosstalk, and Fragility Beyond Bone Mineral Density
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Contributions of the intestinal microbiota to bone
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Resorption Controls Bone Anabolism Driven by Parathyroid Hormone (PTH) Receptor Signaling in Osteocytes
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Parathyroid Hormone Receptor Signaling Induces Bone Resorption in the Adult Skeleton by Directly Regulating the RANKL Gene in Osteocytes
Ben-awadh, A. N., Delgado-Calle, J., Tu, X., Kuhlenschmidt, K., Allen, M. R., Plotkin, L. I., & Bellido, T. (2014) · Endocrinology · doi:10.1210/en.2014-1046 · Cited by 114 · see citing works
Self-citation
Parathyroid hormone: anabolic and catabolic actions on the skeleton
Silva, B. C. C., & Bilezikian, J. P. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.03.005 · Cited by 564 · see citing works
Anabolic and Catabolic Regimens of Human Parathyroid Hormone 1–34 Elicit Bone- and Envelope-Specific Attenuation of Skeletal Effects in Sost-Deficient Mice
Robling, A. G., Kedlaya, R., Ellis, S. N., Childress, P., Bidwell, J. P., Bellido, T., & Turner, C. H. (2011) · Endocrinology · doi:10.1210/en.2011-0049 · Cited by 67 · see citing works
Self-citation
Contribution of rankl regulation to bone resorption induced by PTH receptor activation in osteocytes
Ben-awadh, A. N. (2012) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2093

Authors: Delgado-Calle, J., Tu, X., Pacheco-Costa, R., McAndrews, K., Edwards, R., Pellegrini, G. G., Kuhlenschmidt, K., Olivos, N., Robling, A., Peacock, M., Plotkin, L. I., & Bellido, T.
Affiliations: Roudebush Veterans Administration Medical CenterIndianapolisINUSA
Indiana University Indianapolis (US)
Department of Anatomy and Cell BiologySchool of MedicineIndiana UniversityIndianapolisINUSA
Richard L. Roudebush VA Medical Center (US)
Corresponding author: Bellido, Teresita
ORCID: Tu, Xiaolin
McAndrews, Kevin
Robling, Alexander
Peacock, Munro
Plotkin, Lilian I
Bellido, Teresita
Venue: Journal of Bone and Mineral Research
Publisher: Oxford University Press (OUP)
Published: 2016-10-05
Volume: 32
Issue: 3
Pages: 522-535
ISSN: 0884-0431 (ISSN-L)
1523-4681
DOI: 10.1002/jbmr.3011
PMC: PMC8502039
OpenAlex: W2528107193
Cited by: 114
References: 53
Citations by year: 2026: 10 · 2025: 6 · 2024: 8 · 2023: 7 · 2022: 9 · 2021: 9 · 2020: 20 · 2019: 18 · 2018: 10 · 2017: 14 · 2016: 2
FWCI: 7.62
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: Journal of Bone and Mineral Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
IUScholarWorks (Indiana University) (submittedVersion)
Funders: National Institutes of Health (NIH)
National Institute of Arthritis and Musculoskeletal and Skin Diseases [NIAMS] (R01-AR059357)
National Heart, Lung, and Blood Institute [NHLBI] (T35 HL110854-01)
Veterans Administration (1 I01 BX002104-01)
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 type 1 receptor, PTH1R, osteocytes, bone formation, bone resorption, mechanical loading, sclerostin, Wnt/β-catenin signaling, bone remodeling, low calcium diet, cortical bone, trabecular bone
MeSH terms: Fibroblast Growth Factor-23, Animals, Bone and Bones, Bone Resorption, Glycoproteins, Mice, Inbred C57BL, Models, Biological, Organ Size, Osteocytes, Parathyroid Hormone, Signal Transduction, Down-Regulation, Extracellular Matrix Proteins, Weight-Bearing, Bone Remodeling, Gene Deletion, Mice, Knockout, Intercellular Signaling Peptides and Proteins, Receptor, Parathyroid Hormone, Type 1, Adaptor Proteins, Signal Transducing

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Control of Bone Anabolism in Response to Mechanical Loading and PTH by Distinct Mechanisms Downstream of the PTH Receptor

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