Cited by 1,272Bone Metabolism and DiseasesBone health and osteoporosis researchBone health and treatments

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Disorders of Bone Remodeling

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Feng, Xu, McDonald, Jay M.·2011·Annual Review of Pathology: Mechanisms of Disease

DOI 10.1146/annurev-pathol-011110-130203PMC PMC3571087

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Abstract

The skeleton provides mechanical support for stature and locomotion, protects vital organs, and controls mineral homeostasis. A healthy skeleton must be maintained by constant bone modeling to carry out these crucial functions throughout life. Bone remodeling involves the removal of old or damaged bone by osteoclasts (bone resorption) and the subsequent replacement of new bone formed by osteoblasts (bone formation). Normal bone remodeling requires a tight coupling of bone resorption to bone formation to guarantee no alteration in bone mass or quality after each remodeling cycle. However, this important physiological process can be derailed by a variety of factors, including menopause-associated hormonal changes, age-related factors, changes in physical activity, drugs, and secondary diseases, which lead to the development of various bone disorders in both women and men. We review the major diseases of bone remodeling, emphasizing our current understanding of the underlying pathophysiological mechanisms.

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“As evidenced by disturbed bone homeostasis, altered bone microstructure, and reduced bone strength, OP arises from the imbalance of bone formation and bone resorption, resulting from excessive absorption by OC or impaired generation of OB (17, 20).”
Background
Pleiotropic physiological functions of Piezo1 in human body and its effect on malignant behavior of tumors
Zhang, Y., Zou, W., Dou, W., Luo, H., & Ouyang, X. (2024) · Frontiers in Physiology · doi:10.3389/fphys.2024.1377329 · Cited by 16
“Bone homeostasis depends on the overall balance between bone resorption and bone formation (Feng and McDonald, 2011).”
Background
Muscle–bone and fat–bone interactions in regulating bone mass: do PTH and PTHrP play any role?
Datta, N. S. (2014) · Endocrine · doi:10.1007/s12020-014-0273-3 · Cited by 16
“Age-related bone loss is associated with changes in bone remodeling with decreased bone formation relative to bone resorption, resulting in bone fragility, increased risk of fractures and osteoporosis [1–3].”
Background
Identification and in silico characterization of a novel p.P208PfsX1 mutation in V-ATPase a3 subunit associated with autosomal recessive osteopetrosis in a Pakistani family
Ajmal, M., Mir, A., Wahid, S., Khor, C. C., Foo, J. N., Siddiqi, S., Kauser, M., Malik, S. A., & Nasir, M. (2017) · BMC Medical Genetics · doi:10.1186/s12881-017-0506-4 · Cited by 16
“The condition lead to bone fragility and an increased vulnerability to fractures [3].”
Background
Sex-Specific Associations of Blood-Based Nutrient Profiling With Body Composition in the Elderly
Konz, T., Santoro, A., Goulet, L., Bazzocchi, A., Battista, G., Nicoletti, C., Kadi, F., Ostan, R., Goy, M., Monnard, C., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01935 · Cited by 16
“This observation is in agreement with the known sex-specific bone remodeling with the higher bone resorption rate reported in females (Feng and McDonald, 2011).”
Result
PSTP-3,5-Me Inhibits Osteoclast Differentiation and Bone Resorption
Cho, E., Chen, Z., Lee, J., Lee, S., & Lee, T. (2019) · Molecules · doi:10.3390/molecules24183346 · Cited by 16
“Excessive bone degradation by osteoclasts occurs due to estrogen deficiency in women and age-related increases in oxidative stress [5].”
BackgroundInfluential
How can nitric oxide help osteogenesis?
Nascimento, M. H. M., Pelegrino, M. T., Pieretti, J. C., & Seabra, A. B. (2020) · AIMS molecular science · doi:10.3934/molsci.2020003 · Cited by 16
Tabersonine ameliorates osteoblast apoptosis in rats with dexamethasone-induced osteoporosis by regulating the Nrf2/ROS/Bax signalling pathway
Sun, X., Gan, L., Li, N., Sun, S., & Li, N. (2020) · AMB Express · doi:10.1186/s13568-020-01098-0 · Cited by 16
PMSA prevents osteoclastogenesis and estrogen-dependent bone loss in mice
Cho, E., Chen, Z., Ding, M., Seong, J., Lee, S., Min, S. H., Choi, D. K., & Lee, T. (2020) · Bone · doi:10.1016/j.bone.2020.115707 · Cited by 16
Chicago sky blue 6B (CSB6B), an allosteric inhibitor of macrophage migration inhibitory factor (MIF), suppresses osteoclastogenesis and promotes osteogenesis through the inhibition of the NF-κB signaling pathway
Jin, K., Zheng, L., Ye, L., Xie, Z., Gao, J., Lou, C., Pan, W., Pan, B., Liu, S., Chen, Z., et al. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114734 · Cited by 16
Association between the dietary inflammatory index and bone markers in postmenopausal women
Song, D., Kim, J., Kang, M., Park, J., Lee, H., Kim, D., Park, S. Y., & Lim, H. (2022) · PLoS ONE · doi:10.1371/journal.pone.0265630 · Cited by 17
“Women’s bone loss accelerates as the bone resorption rate and increases faster than bone formation with estrogen decline [3, 4].”
Background
Association of the I264T Variant in the Sulfide Quinone Reductase-Like (SQRDL) Gene with Osteoporosis in Korean Postmenopausal Women
Jin, H., Kim, J., Park, S., Park, E., Kim, B. Y., Vit-Na, C., Yoo, Y.-H., Kim, B.-T., & Jeong, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135285 · Cited by 16
“We investigated whether the alteration of the amino acid residue at the 264 position of the SQRDL protein (I264T) influenced osteoblast and/or osteoclast differentiation, which is essential for bone remodeling [1, 2, 4].”
Background
Interleukin-3 plays dual roles in osteoclastogenesis by promoting the development of osteoclast progenitors but inhibiting the osteoclastogenic process
Hong, H., Shi, Z., Qiao, P., Li, H., McCoy, E. M., Mao, P., Xu, H., Feng, X., & Wang, S. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.09.098 · Cited by 16
“Bone remodeling can be divided into four major stages [2].”
Self-citation
Expressions and clinical significance of serum bone Gla-protein, bone alkaline phosphatase and C-terminal telopeptide of type I collagen in bone metabolism of patients with osteoporosis
Zhao, D., Wang, J., Liu, Y., & Liu, X. (2014) · Pakistan Journal of Medical Sciences · doi:10.12669/pjms.311.6143 · Cited by 16
Daily intake of polyamine-rich Saccharomyces cerevisiae S631 prevents osteoclastic activation and bone loss in ovariectomized mice
Yamada, T., Park, G., Node, J., Ozaki, K., Hiraiwa, M., Kitaguchi, Y., Kaneda, K., Hiramoto, S., & Hinoi, E. (2019) · Food Science and Biotechnology · doi:10.1007/s10068-019-00561-4 · Cited by 16
Dual regulation of phaseol on osteoclast formation and osteoblast differentiation by targeting TAK1 kinase for osteoporosis treatment
Tan, L., Miao, Z., Zhao, Y., Liang, Y., Xu, N., Chen, X., Tu, Y., & He, C. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.12.009 · Cited by 16
“An inequilibrium between osteoblast-mediated osteogenesis and osteoclast-driven bone absorption lead to pathological bone loss, which may cause osteoporosis, rheumatoid arthritis, bone metastasis, and fragility fractures [34–36].”
Ziyuglycoside I Upregulates RUNX2 through ERK1/2 in Promoting Osteoblast Differentiation and Bone Mineralization
Park, K., Lee, J. Y., Cho, M., & Yun, H. (2021) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x21500427 · Cited by 15
RETRACTED: In vitro and in silico anti-osteoporosis activities and underlying mechanisms of a fructan, ABW90-1, from Achyranthes bidentate
Li, T., Hou, X., Huang, Y., Wang, C., Chen, H., & Yan, C. (2021) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2021.118730 · Cited by 15
Retracted
Reduced Serum Levels of Bone Formation Marker P1NP in Psoriasis
Mentzel, J., Kynast, T., Kohlmann, J., Kirsten, H., Blüher, M., Simon, J. C., Kunz, M., & Saalbach, A. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.730164 · Cited by 14
Disrupted Sleep Architecture Is Associated With Incident Bone Loss in Indian Postmenopausal Women: A Prospective Study
Cherian, K. E., Kapoor, N., & Paul, T. V. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4662 · Cited by 15
“Bone remodeling occurs throughout life as a tightly regulated process in which bone resorption is coupled to bone formation.((20)) Bone turnover markers have been shown to increase during the night, peaking in the early morning hours and decreasing throughout the day, with a nadir being achieved in the late afternoon…”
Background
A microphysiological system for studying human bone biology under simultaneous control of oxygen tension and mechanical loading
Scheinpflug, J., Höfer, C. T., Schmerbeck, S. S., Steinfath, M., Doka, J., Tesfahunegn, Y. A., Violet, N., Renko, K., Gulich, K., John, T., et al. (2023) · Lab on a Chip · doi:10.1039/d3lc00154g · Cited by 19
Major vault protein (MVP) suppresses aging- and estrogen deficiency-related bone loss through Fas-mediated apoptosis in osteoclasts
Wang, R., Yang, Y., Zhang, Z., Zhao, N., Wiemer, E. A. C., Ben, J., Ma, J., & Yuan, L. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05928-4 · Cited by 15
“The unbalanced bone remodeling, specifically bone resorption over bone formation, leads to osteoporosis [2].”
Background
Molecular Mechanism of Thiazolidinedione-Mediated Inhibitory Effects on Osteoclastogenesis
Zhao, D., Shi, Z., Warriner, A. H., Qiao, P., Hong, H., Wang, Y., & Feng, X. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102706 · Cited by 14
“Osteoclasts, the multinucleated bone-resorbing cells, not only play a crucial role in skeletal development and adult bone remodeling but are also implicated in the pathogenesis of various bone disorders [33,34].”
BackgroundSelf-citation
Retracted
Effects of yuja peel extract and its flavanones on osteopenia in ovariectomized rats and osteoblast differentiation
Jeon, E. J., Lee, D.-H., Kim, Y.-J., Ahn, J., Kim, M. J., Hwang, J., Hur, J., Kim, M. K., Jang, Y. J., Ha, T. Y., et al. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600257 · Cited by 15
Barley Seedling Extracts Inhibit RANKL‐Induced Differentiation, Fusion, and Maturation of Osteoclasts in the Early‐to‐Late Stages of Osteoclastogenesis
Choi, S., Kim, S., Lee, K., Kang, H. J., Lee, M., Park, K., Lee, J. H., Park, K. D., & Seo, W. D. (2017) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2017/6072573 · Cited by 15
“Most bone metabolic disorders induce the activation of osteoclasts; consequently, bone resorption can exceed bone formation and lead to pathological bone-resorbing activity resulting in osteopenic disorderswith increased risk of fracture [4, 5].”
Background
A RANKL-based Osteoclast Culture Assay of Mouse Bone Marrow to Investigate the Role of mTORC1 in Osteoclast Formation
Dai, Q., Han, Y., Xie, F., Ma, X., Xu, Z., Liu, X., Zou, W., & Wang, J. (2018) · Journal of Visualized Experiments · doi:10.3791/56468 · Cited by 15
Impact of prenatal hypoxia on fetal bone growth and osteoporosis in ovariectomized offspring rats
Yang, Y., Fan, X., Tao, J., Xu, T., Zhang, Y., Zhang, W., Li, L., Li, X., Ding, H., Sun, M., et al. (2018) · Reproductive Toxicology · doi:10.1016/j.reprotox.2018.02.010 · Cited by 15
Dry-Fermented Soybean Food (Cheonggukjang) Ameliorates Senile Osteoporosis in the Senescence-Accelerated Mouse Prone 6 Model
Kim, J., Lee, H., Nirmala, F. S., Jung, C. H., Jang, Y. J., Ha, T. Y., & Ahn, J. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2018.4335 · Cited by 15
“Aging is associated with sustained bone loss, 1,4 which occurs as a result of two key processes: periosteal alignment outside the bone and bone resorption inside the bone.”
lncRNA TUG1 promotes proliferation and differentiation of osteoblasts by regulating the miR-545-3p/CNR2 axis
Hao, R., Wang, B., Wang, H., Huo, Y., & Lu, Y. (2020) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20209798 · Cited by 15
“Bone is an organ dynamically regulated by osteoblasts and osteoclasts, which emerge as crucial regulators in bone turnover (1).”
Background
lncRNA LINC01535 upregulates BMP2 expression levels to promote osteogenic differentiation via sponging miR‑3619‑5p
Zhao, Y., Chen, Y., Hu, X., Zhang, N., & Wang, F. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11635 · Cited by 14
Liver X receptors and skeleton: Current state-of-knowledge
Goel, D., & Vohora, D. (2020) · Bone · doi:10.1016/j.bone.2020.115807 · Cited by 15
Sorting Nexin 10 as a Key Regulator of Membrane Trafficking in Bone-Resorbing Osteoclasts: Lessons Learned From Osteopetrosis
Elson, A., Stein, M., Rabie, G., Barnea, M., Winograd-Katz, S. E., Reuven, N. B., Shalev, M., Sekereš, J., Kanaan, M. N., Tuckermann, J. P., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.671210 · Cited by 15
“Bones can be shaped or re-shaped also through the independent actions of these two cell types (Seeman, 2009; Feng and McDonald, 2011; Langdahl et al., 2016).”
Background
Extraction and characterization of matrix protein from pacific oyster ( Crassostrea gigs ) shell and its anti-osteoporosis properties in vitro and in vivo
Xue, F., Jiang, S., Zhang, F., Wang, R., Zhang, T., Zhao, Y., & Zeng, M. (2021) · Food & Function · doi:10.1039/d1fo00010a · Cited by 15
Biological Mechanisms of Paeonoside in the Differentiation of Pre-Osteoblasts and the Formation of Mineralized Nodules
Park, K.-R., Lee, J. Y., Cho, M., Hong, J. T., & Yun, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136899 · Cited by 14
“Bone tissue is dynamically and continuously renewed through various cellular events in bone cells including osteoblasts, osteocytes, and osteoclasts to maintain a healthy skeleton [1,2].”
Background
Nanodelivery Systems Face Challenges and Limitations in Bone Diseases Management
Giordano, F., Lenna, S., Rampado, R., Brozovich, A., Hirase, T., Tognon, M. G., Martini, F., Agostini, M., Yustein, J. T., & Taraballi, F. (2021) · Advanced Therapeutics · doi:10.1002/adtp.202100152 · Cited by 17
Mitochondrial Fus1/Tusc2 and cellular Ca2+ homeostasis: tumor suppressor, anti-inflammatory and anti-aging implications
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“Thus, it is possible that Fus1/Tusc2 loss in vivo could also affect bone remodeling, shifting it towards bone deposition that would reduce tissue repair potential [106] corroborating with accelerated aging and development of age-related disorders in Fus1 mice [23].”
Background
(S)-Equol Is More Effective than (R)-Equol in Inhibiting Osteoclast Formation and Enhancing Osteoclast Apoptosis, and Reduces Estrogen Deficiency–Induced Bone Loss in Mice
Tanaka, M., Fujii, S., Inoue, H., Takahashi, N., Ishimi, Y., & Uehara, M. (2022) · Journal of Nutrition · doi:10.1093/jn/nxac130 · Cited by 16
Design, Synthesis and Biological Evaluation of New Quinazolinone-Benzopyran-Indole Hybrid Compounds Promoting Osteogenesis Through BMP2 Upregulation
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NUMBL Interacts with TAK1, TRAF6 and NEMO to Negatively Regulate NF-κB Signaling During Osteoclastogenesis
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Nox4 Expression Is Not Required for OVX ‐Induced Osteoblast Senescence and Bone Loss in Mice
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“process in which osteoblast bone formation and osteoclast bone resorption are uncoupled.((1)) Acceptable explanations for the”
Background
Epigenetic and transcriptional regulation of osteoclastogenesis in the pathogenesis of skeletal diseases: A systematic review
Sharma, S., Mahajan, A., Mittal, A., Gohil, R., Sachdeva, S., Khan, S., & Dhillon, M. S. (2020) · Bone · doi:10.1016/j.bone.2020.115507 · Cited by 14
Three-dimensional labeling of newly formed bone using synchrotron radiation barium K-edge subtraction imaging
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Recent progress in immunomodulation-based strategies for bone repair
Yuqiang, W., Ziyan, Z., Xuedi, S., & Piao, C. (2025) · Regenerative Therapy · doi:10.1016/j.reth.2025.101054 · Cited by 15
“In contrast, persistent high levels of inflammatory signals chronically activate nuclear factor κ B (NF-κ B) and mitogen-activated protein kinase (MAPK) pathways, markedly suppressing osteogenic transcriptional programs and reducing mineralization capacity [103].”
A vascularized bone-on-a-chip model development via exploring mechanical stimulation for evaluation of fracture healing therapeutics
Das, B., Seesala, V. S., Pal, P., Roy, T., Ray, P. G., & Dhara, S. (2021) · In vitro models · doi:10.1007/s44164-021-00004-7 · Cited by 16

Authors: Feng, X., & McDonald, J. M.
Affiliations: University of Alabama at Birmingham (US)
ORCID: Feng, Xu
Venue: Annual Review of Pathology: Mechanisms of Disease
Publisher: Annual Reviews
Published: 2011-02-28
Volume: 6
Issue: 1
Pages: 121-145
ISSN: 1553-4006 (ISSN-L)
1553-4014
DOI: 10.1146/annurev-pathol-011110-130203
PMC: PMC3571087
OpenAlex: W2166266977
Cited by: 1,272
References: 171
Citations by year: 2026: 59 · 2025: 109 · 2024: 102 · 2023: 124 · 2022: 135 · 2021: 142 · 2020: 107 · 2019: 117 · 2018: 86 · 2017: 68 · 2016: 59 · 2015: 47 · 2014: 36 · 2013: 37 · 2012: 29
FWCI: 3.28
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Annual Review of Pathology Mechanisms of Disease (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA109119)
National Institute of Neurological Disorders and Stroke (R21NS061677, NS061677)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (5P30 AR0406031, R01AR047830, AR 47830, R01AR050235)
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 › Oncology › Bone health and treatments
Keywords: bone remodeling, bone resorption, bone formation, osteoclasts, osteoblasts, bone disease, menopause, hormonal changes, age-related bone loss, physical activity, drug-induced bone loss, mineral homeostasis, pathophysiology
MeSH terms: Animals, Bone Diseases, Humans, Bone Remodeling

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