Cited by 405Bone Metabolism and DiseasesBone health and osteoporosis researchAlkaline Phosphatase Research Studies

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What old means to bone

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Manolagas, Stavros C., Parfitt, A. Michael·2010·Trends in Endocrinology & Metabolism

DOI 10.1016/j.tem.2010.01.010PMC PMC2880220

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Abstract

The adverse effects of aging of other organs (ovaries at menopause) on the skeleton are well known, but ironically little is known of skeletal aging itself. Evidence indicates that age-related changes, such as oxidative stress, are fundamental mechanisms of the decline of bone mass and strength. Unlike the short-lived osteoclasts and osteoblasts, osteocytes--former osteoblasts entombed in the mineralized matrix--live as long as 50 years, and their death is dependent on skeletal age. Osteocyte death is a major contributor to the decline of bone strength with age, and the likely mechanisms are oxidative stress, autophagy failure and nuclear pore "leakiness". Unraveling these mechanisms should improve understanding of the age-related increase in fractures and suggest novel targets for its prevention.

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CSF‐1 in Osteocytes Inhibits Nox4‐mediated Oxidative Stress and Promotes Normal Bone Homeostasis
Werner, S. L., Sharma, R., Woodruff, K. A., Horn, D., Harris, S. E., Gorin, Y. C., Lee, D.-Y., Hua, R., Gu, S., Fajardo, R. J., et al. (2018) · JBMR Plus · doi:10.1002/jbm4.10080 · Cited by 32
The role of CDK8 in mesenchymal stem cells in controlling osteoclastogenesis and bone homeostasis
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Pyroptosis: A spoiler of peaceful coexistence between cells in degenerative bone and joint diseases
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“The increase in porosity resulting from the rise in resorption cavities and the accumulation of incompletely closed osteons, particularly contributes to the loss of cortical bone more obvious [222,223].”
Exosomes as a Novel Approach to Reverse Osteoporosis: A Review of the Literature
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“Bisphosphonates, the most common current therapy for osteoporosis, result in general side effects including gastrointestinal irritation, bone and joint pain and jaw osteonecrosis (Marx, 2003; Ruggiero et al., 2004).”
Background
Oxidative Stress and Antioxidants in the Risk of Osteoporosis — Role of the Antioxidants Lycopene and Polyphenols
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“Epidemiological evidence in humans and studies in animals indicate that aging and the associated increase in ROS are responsible for bone loss [64].”
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Regulating Mitochondrial Aging via Targeting the Gut‐Bone Axis in BMSCs With Oral Hydrogel Microspheres to Inhibit Bone Loss
Qu, X., Zhou, X., Zhang, J., Huang, Y., Zhao, R., Li, N., Wang, J., Chen, L., Cui, W., & Luo, X. (2024) · Small · doi:10.1002/smll.202409936 · Cited by 31
Milk, Fruit and Vegetable, and Total Antioxidant Intakes in Relation to Mortality Rates: Cohort Studies in Women and Men
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“The increased oxidative stress with aging and chronic low-grade inflammation is not only a pathogenic mechanism of cardiovascular disease and cancer in humans (9, 10) but also a mechanism of age-related bone loss and sarcopenia (10, 11).”
Background
Sub-chronic exposure to Kalach 360 SL, Glyphosate-based Herbicide, induced bone rarefaction in female Wistar rats
Hamdaoui, L., Oudadesse, H., Lefeuvre, B., Mahmoud, A., Naifer, M., Badraoui, R., Ayadi, F. M., & Rebaï, T. (2020) · Toxicology · doi:10.1016/j.tox.2020.152412 · Cited by 31
“Manolagas (2010) reported that oxidative stress, a shared mechanism of the pathogenesis related to several degenerative disorders associated with aging, including osteoporosis and an increase in ROS was involved in the decreased bone formation.”
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Energy Metabolism and Ketogenic Diets: What about the Skeletal Health? A Narrative Review and a Prospective Vision for Planning Clinical Trials on this Issue
Merlotti, D., Cosso, R., Eller-Vainicher, C., Vescini, F., Chiodini, I., Gennari, L., & Falchetti, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22010435 · Cited by 34
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Sharma, R., Callaway, D. A., Vanegas, D., Bendele, M., Lopez‐Cruzan, M., Horn, D., Guda, T., Fajardo, R. J., Abboud‐Werner, S. L., & Herman, B. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093696 · Cited by 31
“Recent studies implicate the accumulation of reactive oxygen species (ROS) and increased oxidative stress as key factors in agerelated osteoporosis [2,4,5].”
Background
Targeting Subchondral Bone Mesenchymal Stem Cell Activities for Intrinsic Joint Repair in Osteoarthritis
Ilas, D. C., Churchman, S. M., McGonagle, D., & Jones, E. (2017) · Future Science OA · doi:10.4155/fsoa-2017-0055 · Cited by 31
Low-dose PTH increases osteoblast activity via decreased Mef2c/Sost in senescent osteopenic mice
Saidak, Z., Hénaff, C. L., Azzi, S., Marty, C., & Marie, P. J. (2014) · Journal of Endocrinology · doi:10.1530/joe-14-0249 · Cited by 30
Effect of calcium glucoheptonate on proliferation and osteogenesis of osteoblast-like cells in vitro
Modi, P. K., Prabhu, A., Bhandary, Y. P., Sudheer Shenoy, P., Hegde, A., Sindhu Priya, E. S., Johnson, R. P., Das, S. P., Vazirally, S., & Rekha, P. D. (2019) · PLoS ONE · doi:10.1371/journal.pone.0222240 · Cited by 30
Osteoimmunology and aging: Mechanisms, implications, and therapeutic perspectives
Wang, Y.-T., Zheng, S.-Y., Luo, Y., Xiao, W., Huang, C., & Li, Y. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102822 · Cited by 35
Deletion of p16 prevents estrogen deficiency-induced osteoporosis by inhibiting oxidative stress and osteocyte senescence
Li, J., Karim, M. A., Che, H., Geng, Q., & Miao, D. (2020) · PubMed Central · doi:10.6094/unifr/166811 · Cited by 29
mTORC1 induces plasma membrane depolarization and promotes preosteoblast senescence by regulating the sodium channel Scn1a
Chen, A., Jin, J., Cheng, S., Liu, Z., Yang, C., Chen, Q., Liang, W., Li, K., Kang, D., Ouyang, Z., et al. (2022) · Bone Research · doi:10.1038/s41413-022-00204-1 · Cited by 29
“Bone formation requires an adequate number of mature osteoblastic cells, which are postmitotic cells that have a short lifespan and must be continually replaced with new cells.(6) Osteoblasts arise from preosteoblasts, which express the transcription factors Osterix (Osx) and Runx2.”
Background
Targeting the osteoblast: approved and experimental anabolic agents for the treatment of osteoporosis
Toulis, K. A., Anastasilakis, A. D., Pοlyzos, S. A., & Makras, P. (2011) · HORMONES · doi:10.14310/horm.2002.1308 · Cited by 28
“In a dose escalation study in healthy volunteers, SC PTHrP (1-36) was found safe in single doses up to 2.”
BackgroundMethodInfluential
Anti-Aging Potential of Platelet Rich Plasma (PRP): Evidence from Osteoarthritis (OA) and Applications in Senescence and Inflammaging
Vun, J. S. H., Iqbal, N., Jones, E., & Ganguly, P. (2023) · Bioengineering · doi:10.3390/bioengineering10080987 · Cited by 30
“In contrast, fibroblasts are reported to have a life span of 270 days in vitro [117], osteoblasts have a life span of 1–200 days, bone lining cells may live up to 1–10 years, and osteocytes can live up to 50 years [118].”
Background
Repression of Osteoblast Maturation by ERRα Accounts for Bone Loss Induced by Estrogen Deficiency
Gallet, M., Saïdi, S., Haÿ, E., Photsavang, J., Marty, C., Sailland, J., Carnesecchi, J., Tribollet, V., Barenton, B., Forcet, C., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054837 · Cited by 28
“Due to the global ageing of the human population worldwide, osteoporosis is now a major health problem, being the most common metabolic disorder of old age in humans [1,2].”
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Glucocorticoid‐Induced Autophagy Protects Osteocytes Against Oxidative Stress Through Activation of MAPK/ERK Signaling
Kar, R., Riquelme, M. A., Hua, R., & Jiang, J. X. (2018) · JBMR Plus · doi:10.1002/jbm4.10077 · Cited by 27
“Osteocyte cell death increases progressively with age in mice,((10)) and oxidative stress during aging is a major mechanism contributing to the death of bone cells (reviewed by((11,12))).”
Background
The Role of Chronic Inflammatory Bone and Joint Disorders in the Pathogenesis and Progression of Alzheimer's Disease
Culibrk, R. A., & Hahn, M. S. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.583884 · Cited by 28
“Increased autophagy is assumed critical in osteogenesis due to the requirement for rapid organelle recycling, preservation of nutrients, and the increased environmental susceptibility to hypoxia inherent to the osteoblast-to-osteocyte transition (Manolagas and Parfitt, 2010).”
Background
Synergistic stimulation of osteoblast differentiation of rat mesenchymal stem cells by leptin and 25(OH)D3 is mediated by inhibition of chaperone-mediated autophagy
He, Q., Qin, R., Glowacki, J., Zhou, S., Shi, J., Wang, S., Gao, Y., & Cheng, L. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02623-z · Cited by 27
Homer1 mediates CaSR-dependent activation of mTOR complex 2 and initiates a novel pathway for AKT-dependent β-catenin stabilization in osteoblasts
Rybchyn, M. S., Islam, K. S., Brennan‐Speranza, T. C., Cheng, Z., Brennan, S. C., Chang, W., Mason, R. S., & Conigrave, A. D. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006587 · Cited by 27
“Resistance to oxidative stress promotes bone quality in vivo (41).”
Background
Age-related increase of kynurenine enhances miR29b-1-5p to decrease both CXCL12 signaling and the epigenetic enzyme Hdac3 in bone marrow stromal cells
Elmansi, A. M., Hussein, K. A., Mas, S., Periyasamy‐Thandavan, S., Aguilar‐Perez, A., Kondrikova, G., Kondrikov, D., Eisa, N. H., Pierce, J. L., Kaiser, H., et al. (2020) · Bone Reports · doi:10.1016/j.bonr.2020.100270 · Cited by 28
“Bone is a heterogeneous tissue made up of extracellular matrix (ECM) and different cell populations including mesenchymal stem cells (MSCs), pre-osteoblasts, osteoblasts, osteocytes, bone lining cells, osteoclasts, a complex vasculature system, and the hematopoietic system (Schönherr and Hausser, 2000; Manolagas, 2000…”
Background
Elevated Intracellular Ca2+ Signals by Oxidative Stress Activate Connexin 43 Hemichannels in Osteocytes
Riquelme, M. A., & Jiang, J. X. (2013) · Bone Research · doi:10.4248/br201304006 · Cited by 27
Nutrition and Osteoporosis: Preliminary data of Campania Region of European PERsonalised ICT Supported Service for Independent Living and Active Ageing.
Vuolo, L., Barrea, L., Savanelli, M. C., Savastano, S., Rubino, M., Scarano, E., Soprano, M., Illario, M., Colao, A., & Somma, C. D. (2015) · Europe PMC (PubMed Central) · Cited by 26
Bone Sclerostin and Dickkopf-related protein-1 are positively correlated with bone mineral density, bone microarchitecture, and bone strength in postmenopausal osteoporosis
Peng, J., Zhang, D., Zhang, H., Aifei, W., Lianfu, D., & Xu, Y. (2021) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-021-04365-8 · Cited by 26
“Osteocytes constitute more than 90–95% of bone cells in the adult skeleton and are extremely long-lived cells that survive for up to decades in the bone matrix [40].”
Background
Acylated and unacylated ghrelin protect MC3T3-E1 cells against tert-butyl hydroperoxide-induced oxidative injury: pharmacological characterization of ghrelin receptor and possible epigenetic involvement
Dieci, E., Casati, L., Pagani, F., Celotti, F., & Sibilia, V. (2014) · Amino Acids · doi:10.1007/s00726-014-1734-y · Cited by 25
Focus on Pivotal Role of Dietary Intake (Diet and Supplement) and Blood Levels of Tocopherols and Tocotrienols in Obtaining Successful Aging
Rondanelli, M., Faliva, M. A., Peroni, G., Moncaglieri, F., Infantino, V., Naso, M., & Perna, S. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161023227 · Cited by 25
“The vitamin E component is a potent scavenger of free radicals, and it has been postulated that this vitamin may favorably influence bone and muscle mass due to its antioxidant properties [28,29,34,35].”
Background
Potential Effects of Exosomes and their MicroRNA Carrier on Osteoporosis
Li, Q.-C., Li, C., Zhang, W., Pi, W., & Han, N. (2022) · Current Pharmaceutical Design · doi:10.2174/1381612828666220128104206 · Cited by 25
Role of the nuclear envelope in the pathogenesis of age-related bone loss and osteoporosis
Vidal, C., Bermeo, S., Fatkin, D., & Duque, G. (2012) · BoneKEy Reports · doi:10.1038/bonekey.2012.62 · Cited by 25
Comparative high-resolution pQCT analysis of femoral neck indicates different bone mass distribution in osteoporosis and osteoarthritis
Rubinacci, A., Tresoldi, D., Scalco, E., Villa, I., Adorni, F., Moro, G. L., Fraschini, G., & Rizzo, G. (2011) · Osteoporosis International · doi:10.1007/s00198-011-1795-7 · Cited by 25
Aging of the Bone
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Combined low-dose LiCl and LY294002 for the treatment of osteoporosis in ovariectomized rats
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“The balance between bone formation and absorption is disrupted with age, and both the mechanical strength and mass of bone decrease because of the loss of bone cell function through bone tissue microstructural deterioration, decreased trace elements and salt levels, and increased osteoblast apoptosis, all of which inc…”
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Emerging therapeutic targets for osteoporosis
Gennari, L., Merlotti, D., Falchetti, A., Eller-Vainicher, C., Cosso, R., & Chiodini, I. (2020) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2020.1726889 · Cited by 25
Estrogen-Related Receptors and the control of bone cell fate
Carnesecchi, J., & Vanacker, J.-M. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.07.019 · Cited by 26
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“The decreased activity of osteoblasts is one of many reasons for delayed healing of bone fractures in older patients (Manolagas & Parfitt, 2010).”
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Strontium ranelate prevents the deleterious action of advanced glycation endproducts on osteoblastic cells via calcium channel activation
Fernández, J. M., Molinuevo, M. S., Sedlinsky, C., Schurman, L., Cortizo, A. M., & McCarthy, A. D. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.02.042 · Cited by 24
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Autophagy in osteoporosis: Relation to oxidative stress
Ezzat, S., Louka, M. L., Zakaria, Z. M., Nagaty, M. M., & Metwaly, R. G. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27552 · Cited by 23
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Background

Authors: Manolagas, S. C., & Parfitt, A. M.
Affiliations: Central Arkansas Veterans Healthcare System (US)
Corresponding author: Manolagas, Stavros C.
ORCID: Manolagas, Stavros C.
Venue: Trends in Endocrinology & Metabolism
Publisher: Elsevier BV
Published: 2010-06
Volume: 21
Issue: 6
Pages: 369-374
ISSN: 1043-2760 (ISSN-L)
DOI: 10.1016/j.tem.2010.01.010
PMC: PMC2880220
OpenAlex: W2088789328
Cited by: 404
References: 74
Citations by year: 2026: 11 · 2025: 17 · 2024: 20 · 2023: 30 · 2022: 25 · 2021: 30 · 2020: 30 · 2019: 39 · 2018: 32 · 2017: 30 · 2016: 24 · 2015: 25 · 2014: 25 · 2013: 23 · 2012: 17
FWCI: 1.82
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Trends in Endocrinology and Metabolism (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Department of Veterans Affairs
University of Arkansas for Medical Sciences
National Institutes of Health (P01 AG13918)
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 › Endocrinology, Diabetes and Metabolism › Alkaline Phosphatase Research Studies
Keywords: skeletal aging, osteocyte death, oxidative stress, bone loss, bone strength, osteoblasts, osteoclasts, menopause
MeSH terms: Aging, Animals, Bone and Bones, Bone Diseases, Humans, Menopause, Osteocytes, Cell Death

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