Functions of RANKL/RANK/OPG in bone modeling and remodeling

Boyce, Brendan F.; Xing, Lianping

doi:10.1016/j.abb.2008.03.018

Cited by 1,844Bone Metabolism and DiseasesBone health and osteoporosis researchBone and Dental Protein Studies

Functions of RANKL/RANK/OPG in bone modeling and remodeling

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Boyce, Brendan F., Xing, Lianping·2008·Archives of Biochemistry and Biophysics

DOI 10.1016/j.abb.2008.03.018PMC PMC2413418

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Abstract

The discovery of the RANKL/RANK/OPG system in the mid 1990s for the regulation of bone resorption has led to major advances in our understanding of how bone modeling and remodeling are regulated. It had been known for many years before this discovery that osteoblastic stromal cells regulated osteoclast formation, but it had not been anticipated that they would do this through expression of members of the TNF superfamily: receptor activator of NF-kappaB ligand (RANKL) and osteoprotegerin (OPG), or that these cytokines and signaling through receptor activator of NF-kappaB (RANK) would have extensive functions beyond regulation of bone remodeling. RANKL/RANK signaling regulates osteoclast formation, activation and survival in normal bone modeling and remodeling and in a variety of pathologic conditions characterized by increased bone turnover. OPG protects bone from excessive resorption by binding to RANKL and preventing it from binding to RANK. Thus, the relative concentration of RANKL and OPG in bone is a major determinant of bone mass and strength. Here, we review our current understanding of the role of the RANKL/RANK/OPG system in bone modeling and remodeling.

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OPG binds to RANKL, preventing the RANK/RANKL interaction and inhibiting osteoclastogenesis.
“On the other hand, another factor called osteoprotegerin (OPG), which is produced by a wide range of cells including osteoblasts, stromal cells, and gingival and periodontal fibroblasts [87–89], binds to RANKL, preventing the RANK/RANKL interaction and, consequently, inhibiting the osteoclastogenesis [87] (Figure 5).”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [87]
RANKL is routinely found as a membrane bound protein (mRANKL), but it can also be cleaved into a soluble form (sRANKL) or delivered via EVs.
“RANKL is routinely found as a membrane bound protein (mRANKL), but it can also be cleaved into a soluble form (sRANKL)49 or delivered via EVs.35”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [49]
In addition to osteocytes, other cells can be sources of OPG or RANKL; these cells are osteoprogenitors, osteoblasts or cells of the immune system (B and T cells), which are all simultaneously present in a BMU.
“In addition to osteocytes, other cells can be sources of OPG or RANKL; these cells are osteoprogenitors, osteoblasts49 or cells of the immune system (B and T cells),76 which are all simultaneously present in a BMU.”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [49]

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Determination of Three Isoforms of the Receptor Activator of Nuclear Factor-κΒ Ligand and Their Differential Expression in Bone and Thymus*
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Circulating Osteoprotegerin and Receptor Activator for Nuclear Factor κB Ligand: Clinical Utility in Metabolic Bone Disease Assessment
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Tumor Necrosis Factor-α Increases Circulating Osteoclast Precursor Numbers by Promoting Their Proliferation and Differentiation in the Bone Marrow through Up-regulation of c-Fms Expression
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Mechanisms of Disease: the link between RANKL and arthritic bone disease
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The RANK/RANKL/OPG triad in cancer-induced bone diseases
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Systemic tumor necrosis factor α mediates an increase in peripheral CD11bhigh osteoclast precursors in tumor necrosis factor α–transgenic mice
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The molecular scaffold Gab2 is a crucial component of RANK signaling and osteoclastogenesis
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Role of Cbfa1 in osteoblast differentiation and function
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Cyclosporine induces high bone turnover and may contribute to bone loss after heart transplantation
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Mechanisms of Disease: roles of OPG, RANKL and RANK in the pathophysiology of skeletal metastasis
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Effects of dissociated glucocorticoids on OPG and RANKL in osteoblastic cells.
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RGS10-null mutation impairs osteoclast differentiation resulting from the loss of [Ca2+]i oscillation regulationPreprint
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Murine and Chicken Chondrocytes Regulate Osteoclastogenesis by Producing RANKL in Response to BMP2
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Receptor activator of NF‐κB recruits multiple TRAF family adaptors and activates c‐Jun N‐terminal kinase
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NF-κB Specifically Activates BMP-2 Gene Expression in Growth Plate Chondrocytes in Vivo and in a Chondrocyte Cell Line in Vitro
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EBF2 Regulates Osteoblast-Dependent Differentiation of Osteoclasts
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Receptor Activator of NF-κB Ligand Regulates the Proliferation of Mammary Epithelial Cells via Id2
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Osteoclast Precursor Interaction with Bone Matrix Induces Osteoclast Formation Directly by an Interleukin-1-mediated Autocrine Mechanism
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Runx2/Cbfa1 stimulation by retinoic acid is potentiated by BMP2 signaling through interaction with Smad1 on the collagen X promoter in chondrocytes
Drissi, H., Li, X., Sheu, T. J., Zuscik, M. J., Schwarz, E. M., Puzas, J. E., Rosier, R. N., & O’Keefe, R. J. (2003) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10677 · Cited by 94 · see citing works
VEGF-C, a Lymphatic Growth Factor, Is a RANKL Target Gene in Osteoclasts That Enhances Osteoclastic Bone Resorption through an Autocrine Mechanism
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The receptor activator of nuclear factor (NF)κB ligand (RANKL) is a new chemotactic factor for human monocytes
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Regulation of bone remodeling and emerging breakthrough drugs for osteoporosis and osteolytic bone metastases
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IFN-γ Enhances Osteoclast Generation in Cultures of Peripheral Blood from Osteopetrotic Patients and Normalizes Superoxide Production
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Osteoclasts and Integrins
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Regulation of matrix metalloproteinase-9 gene expression and cell migration by NF-κB in response to CpG-oligodeoxynucleotides in RAW 264.7 cells
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Expression and function of RANK in human monocyte chemotaxis
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Specificity of RGS10A as a key component in the RANKL signaling mechanism for osteoclast differentiation
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Malignant Autosomal Recessive Osteopetrosis Caused by Spontaneous Mutation of Murine Rank
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Receptor Activator of Nuclear Factor-κB Ligand-Induced Nuclear Factor of Activated T Cells (C1) Autoregulates Its Own Expression in Osteoclasts and Mediates the Up-Regulation of Tartrate-Resistant Acid Phosphatase
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Positive regulatory domain I-binding factor 1 mediates repression of the MHC class II transactivator (CIITA) type IV promoter
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Osteoporosis and cardiovascular disease: benefit-risk of hormone replacement therapy.
Sammartino, A., Cirillo, D., Mandato, V. D., Carlo, C. D., & Nappi, C. (2005) · PubMed · Cited by 19 · see citing works

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International Journal of Molecular Sciences
Soni, N., Ross, A., Nookaew, I., Scheers, N., Gabrielsson, B., & Sandberg, A.-S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms · Cited by 10,136 · see citing works
Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells
Florencio-Silva, R., Sasso, G. R. D. S., Sasso-Cerri, E., Simões, M. J., & Cerri, P. S. (2015) · BioMed Research International · doi:10.1155/2015/421746 · Cited by 2,044 · see citing works
Osteoblast–osteoclast interactions
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Role of Inactivity in Chronic Diseases: Evolutionary Insight and Pathophysiological Mechanisms
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The Charcot Foot in Diabetes
Rogers, L. C., Frykberg, R. G., Armstrong, D. G., Boulton, A. J. M., EDMONDS, M. E., Van, G. H., Hartemann, A., Game, F. L., Jeffcoate, W. J., Jirkovská, A., et al. (2011) · Diabetes Care · doi:10.2337/dc11-0844 · Cited by 597 · see citing works
Osteocyte Wnt/β-Catenin Signaling Is Required for Normal Bone Homeostasis
Krämer, I., Halleux, C. M., Keller, H., Pegurri, M., Gooi, J. H., Weber, P. B., Feng, J. Q., Bonewald, L. F., & Kneissel, M. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01428-09 · Cited by 562 · see citing works
Nanosized hydroxyapatite and other calcium phosphates: Chemistry of formation and application as drug and gene delivery agents
Uskoković, V., & Uskokovic, D. P. (2010) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.31746 · Cited by 540 · see citing works
Bone remodeling: an operational process ensuring survival and bone mechanical competence
Bolamperti, S., Villa, I., & Rubinacci, A. (2022) · Bone Research · doi:10.1038/s41413-022-00219-8 · Cited by 482 · see citing works
Role and mechanism of action of sclerostin in bone
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Differences in tumor microenvironment dictate T helper lineage polarization and response to immune checkpoint therapy
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Genetics of Osteoporosis
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Tissue homeostasis and inflammation
Meizlish, M. L., Franklin, R. A., Zhou, X., & Medzhitov, R. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-061020-053734 · Cited by 364 · see citing works
Regulation of Osteoblast Differentiation by Cytokine Networks
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Internal Root Resorption: A Review
Patel, S., Ricucci, D., Durack, C., & Tay, F. R. (2010) · Journal of Endodontics · doi:10.1016/j.joen.2010.03.014 · Cited by 349 · see citing works
Immunoporosis: Immunology of Osteoporosis—Role of T Cells
Srivastava, R. K., Dar, H. Y., & Mishra, P. K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00657 · Cited by 329 · see citing works
No significant effect on bone mineral density by high doses of vitamin D3 given to overweight subjects for one year
Jorde, R., Sneve, M., Torjesen, P. A., Figenschau, Y., Hansen, J., & Grimnes, G. (2010) · Nutrition Journal · doi:10.1186/1475-2891-9-1 · Cited by 323 · see citing works
RANKL/RANK/OPG Pathway: A Mechanism Involved in Exercise-Induced Bone Remodeling
Tobeiha, M., Moghadasian, M. H., Amin, N., & Jafarnejad, S. (2020) · BioMed Research International · doi:10.1155/2020/6910312 · Cited by 309 · see citing works
Prostaglandins in bone: bad cop, good cop?
Blackwell, K. A., Raisz, L. G., & Pilbeam, C. C. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.12.004 · Cited by 309 · see citing works
Differential effects on lung and bone metastasis of breast cancer by Wnt signalling inhibitor DKK1
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Cytokine responses against periodontal infection: protective and destructive roles
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In Vitro Bone Cell Models: Impact of Fluid Shear Stress on Bone Formation
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The Mechanism of Osteoclast Differentiation Induced by IL-1
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Osseointegration – communication of cells
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Osteoporosis: Pathophysiology and therapeutic options
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Role of the calcium-sensing receptor in extracellular calcium homeostasis
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Interaction of staphylococci with bone
Wright, J. A., & Nair, S. P. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.10.003 · Cited by 258 · see citing works
Biomaterial delivery of morphogens to mimic the natural healing cascade in bone
Mehta, M., Schmidt‐Bleek, K., Duda, G. N., & Mooney, D. J. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.05.006 · Cited by 244 · see citing works
The Effect of Inflammation on Bone
Epsley, S., Tadros, S., Farid, A., Kargilis, D., Mehta, S., & Rajapakse, C. S. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2020.511799 · Cited by 242 · see citing works
Exercise and longevity
Grémeaux, V., Gayda, M., Lepers, R., Sosner, P., Juneau, M., & Nigam, A. (2012) · Maturitas · doi:10.1016/j.maturitas.2012.09.012 · Cited by 228 · see citing works
Extracellular Signal-Regulated Kinase 1 (ERK1) and ERK2 Play Essential Roles in Osteoblast Differentiation and in Supporting Osteoclastogenesis
Matsushita, T., Chan, Y. Y., Kawanami, A., Balmes, G. C., Landreth, G. E., & Murakami, S. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01549-08 · Cited by 232 · see citing works
Bone remodeling in rheumatic disease: a question of balance
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Inflammatory profile of chronic apical periodontitis: a literature review
Braz‐Silva, P. H., Bergamini, M., MARDEGAN, A. P., Rosa, C. S. D., Hasséus, B., & Jonasson, P. (2018) · Acta Odontologica Scandinavica · doi:10.1080/00016357.2018.1521005 · Cited by 229 · see citing works
Mechanism of alveolar bone destruction in periodontitis — Periodontal bacteria and inflammation
Usui, M., Onizuka, S., Sato, T., Kokabu, S., Ariyoshi, W., & Nakashima, K. (2021) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2021.09.005 · Cited by 239 · see citing works
Bone microenvironment signals in osteosarcoma development
Alfranca, A., Martínez-Cruzado, L., Tornín, J., Abarrategi, A., Amaral, A. T., de Álava, E., Menéndez, P. R., Garcı́a-Castro, J., & Rodrı́guez, R. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1918-y · Cited by 224 · see citing works
Receptor activator of nuclear factor-κB ligand (RANKL)/RANK/osteoprotegerin system in bone and other tissues (Review)
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Physiology of the Calcium-Parathyroid Hormone-Vitamin D Axis
Goltzman, D., Mannstadt, M., & Marcocci, C. (2018) · Frontiers of hormone research · doi:10.1159/000486060 · Cited by 214 · see citing works
Osteosarcoma: Cells‐of‐Origin, Cancer Stem Cells, and Targeted Therapies
Abarrategi, A., Tornín, J., Martínez-Cruzado, L., Hamilton, A., Martínez‐Campos, E., Rodrigo, J. P., González, M. V., Baldini, N., Garcı́a-Castro, J., & Rodrı́guez, R. (2016) · Stem Cells International · doi:10.1155/2016/3631764 · Cited by 211 · see citing works
Quercetin as an Agent for Protecting the Bone: A Review of the Current Evidence
Wong, S. K., Chin, K., & Soelaiman, I. N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176448 · Cited by 210 · see citing works
Gaucher Disease in Bone: From Pathophysiology to Practice
Hughes, D. A., Mikosch, P., Belmatoug, N., Carubbi, F., Cox, T., Göker-Alpan, Ö., Kindmark, A., Mistry, P. K., Poll, L. W., Weinreb, N. J., et al. (2019) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3734 · Cited by 203 · see citing works
Mutation Analysis of H3F3A and H3F3B as a Diagnostic Tool for Giant Cell Tumor of Bone and Chondroblastoma
Cleven, A. H. G., Höcker, S., Bruijn, I. H. B., Szuhai, K., Cleton-Jansen, A., & Bovée, J. V. M. G. (2015) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000512 · Cited by 200 · see citing works
Extracellular vesicles from adipose tissue‐derived stem cells alleviate osteoporosis through osteoprotegerin and miR‐21‐5p
Lee, K. S., Lee, J., Kim, H. K., Yeom, S. H., Woo, C. H., Jung, Y. J., Yun, Y. E., Park, S. Y., Han, J., Kim, E., et al. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12152 · Cited by 200 · see citing works
Calcitonin-gene-related peptide stimulates stromal cell osteogenic differentiation and inhibits RANKL induced NF-κB activation, osteoclastogenesis and bone resorption
Wang, L., Shi, X., Zhao, R., Halloran, B. P., Clark, D. J., Jacobs, C. R., & Kingery, W. S. (2010) · Bone · doi:10.1016/j.bone.2009.11.029 · Cited by 198 · see citing works
Exosomes derived from human menstrual blood-derived stem cells alleviate fulminant hepatic failure
Chen, L., Xiang, B.-Y., Wang, X.-J., & Xiang, C. (2017) · Stem cell research & therapeutics · doi:10.1186/s13287-016-0453-6 · Cited by 171 · see citing works
A review of the latest insights into the mechanism of action of strontium in bone
Marx, D., Yazdi, A. R., Papini, M., & Towler, M. R. (2020) · Bone Reports · doi:10.1016/j.bonr.2020.100273 · Cited by 196 · see citing works
Characterization of Regulatory Extracellular Vesicles from Osteoclasts
Huynh, N., VonMoss, L., Smith, D., Rahman, I., Felemban, M. F., Zuo, J., Rody, W. J., McHugh, K. P., & Holliday, L. S. (2016) · Journal of Dental Research · doi:10.1177/0022034516633189 · Cited by 196 · see citing works
The role of IL-1B in breast cancer bone metastasis
Tulotta, C., & Ottewell, P. D. (2018) · Endocrine Related Cancer · doi:10.1530/erc-17-0309 · Cited by 191 · see citing works
Toward the biomimetic implant surface: Biopolymers on titanium-based implants for bone regeneration
Tejero, R., Anitua, E., & Orive, G. (2014) · Progress in Polymer Science · doi:10.1016/j.progpolymsci.2014.01.001 · Cited by 187 · see citing works
The osteoclast, bone remodelling and treatment of metabolic bone disease
Boyce, B. F., Rosenberg, E., de Papp, A. E., & Duong, L. T. (2012) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2012.02717.x · Cited by 184 · see citing works
Self-citation
Receptor Activator of NF-kB (RANK) Expression in Primary Tumors Associates with Bone Metastasis Occurrence in Breast Cancer Patients
Santini, D., Schiavon, G., Vincenzi, B., Gaeta, L. M., Pantano, F., Russo, A. D., Ortega, C., Porta, C., Galluzzo, S., Armento, G., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019234 · Cited by 186 · see citing works
Effect of orthodontic forces on cytokine and receptor levels in gingival crevicular fluid: a systematic review
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Authors: Boyce, B. F., & Xing, L.
Affiliations: University of Rochester Medicine (US)
Corresponding author: Boyce, Brendan F.
ORCID: Boyce, Brendan F.
Xing, Lianping
Venue: Archives of Biochemistry and Biophysics
Publisher: Elsevier BV
Published: 2008-05
Volume: 473
Issue: 2
Pages: 139-146
ISSN: 0003-9861 (ISSN-L)
DOI: 10.1016/j.abb.2008.03.018
PMC: PMC2413418
OpenAlex: W1975953388
Cited by: 1,844
References: 107
Citations by year: 2026: 107 · 2025: 132 · 2024: 149 · 2023: 127 · 2022: 145 · 2021: 166 · 2020: 141 · 2019: 122 · 2018: 94 · 2017: 106 · 2016: 71 · 2015: 92 · 2014: 76 · 2013: 73 · 2012: 69
FWCI: 4.48
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Archives of Biochemistry and Biophysics (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Arthritis and Musculoskeletal and Skin Diseases (R21AR049305, R01AR043510)
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 › Rheumatology › Bone and Dental Protein Studies
Keywords: RANK/RANKL/OPG system, bone remodeling, bone modeling, osteoclastogenesis, osteoclast activation, osteoclast survival, bone resorption, TNF superfamily, receptor activator of NF-kappaB, osteoprotegerin, bone turnover
MeSH terms: Animals, Bone Resorption, Cell Differentiation, Humans, Osteoclasts, Osteogenesis, Signal Transduction, Bone Remodeling, Mice, Osteoprotegerin, RANK Ligand, Receptor Activator of Nuclear Factor-kappa B

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Functions of RANKL/RANK/OPG in bone modeling and remodeling

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