Cited by 705Bone Metabolism and DiseasesBone health and osteoporosis researchEstrogen and related hormone effects

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Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-α

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Cenci, Simone, Weitzmann, M. Neale, Roggia, Cristiana, Namba, Noriyuki, Novack, Deborah, Woodring, Jessica, Pacifici, Roberto·2000·Journal of Clinical Investigation

DOI 10.1172/jci11066PMC PMC381439

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Abstract

Physiologic osteoclast renewal results from the differentiation of bone marrow monocytes (BMMs) into osteoclasts, a process induced by the simultaneous stimulation of osteoclast precursors by macrophage colonystimulating factor (M-CSF) and a TNF-related factor known as receptor activator of NF-κB ligand (RANKL; also known as OPGL, TRANCE, or ODF) (1-3).Although upregulation of osteoclast formation is recognized as the main mechanism by which estrogen deficiency induces bone loss (4, 5), the responsible cells and cytokines are not completely understood.Bone marrow stromal cells are essential for physiologic osteoclast renewal because they represent a major source of RANKL and M-CSF and provide a physical support for nascent osteoclasts (6).However, in stimulated conditions additional bone marrow cells contribute to regulate osteoclast formation by producing soluble and membrane-bound pro-and antiosteoclastogenic cytokines.Among them are activated T cells, which stimulate osteoclast formation through increased production of RANKL, a phenomenon that contributes to inflammation-induced bone loss (7).T cells express estrogen receptors, and estrogen directly regulates T-cell function and cytokine production (8-11).Moreover, T-cell subset alterations occur in women with postmenopausal osteoporosis (12, 13).Taken together, these findings suggest that T cells may contribute to enhanced osteoclast formation and induce bone loss not only during inflammation, but also in conditions of estrogen deficiency.In this study we have investigated the role of T cells in ovariectomy-induced bone loss.We report that ovariectomy-enhanced T-cell production of TNF-α, which, acting through the TNF-α receptor p55, augments M-CSF-and RANKL-induced osteoclastogenesis.We also show that ovariectomy failed to induce bone loss, stimulate bone resorption, and increase osteoclast formation in T-cell deficient mice, establishing T cells as essential mediators of the bone-wasting effects of estrogen deficiency in vivo. Methods Experimental protocol.All animal procedures were approved by the Animal Care and Use Committee of Barnes-Jewish Hospital.Wild-type C57BL/6 mice, C57BL/6 homozygous (nu/nu) athymic nude mice (14), and heterozygous (nu/+) euthymic control littermates were obtained from Taconic Farms Inc. (Germantown, New York, USA).C57BL/6 mice lacking either TNF-α receptor 1 (p55 -/-) or TNF-α receptor II (p75 -/-) and wild-type controls of the same genetic background were obtained from Jackson Laboratories (Bar Harbor, Maine, USA).At 5 weeks of age mice were either sham operated or ovariectomized (OVX), and either left untreated or treated with 17β estradiol (0.16 µg/d) for 4 weeks as described (15,16).In vitro osteoclast generation, cytokine neutralization, and TNF-α assay.Bone marrow cells were either cultured unfractionated or depleted of stromal cells by adherence for 12 hours.The nonadherent fraction was used as a source of T cells and BMM precursors and was found to

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Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation.
Lacey, D. L., Timms, E., Tan, H.-L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81569-x · Cited by 5,439
Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL
Yasuda, H., Shima, N., Nakagawa, N., Yamaguchi, K., Kinosaki, M., Mochizuki, S.-I., Tomoyasu, A., Yano, K., Goto, M., Murakami, A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3597 · Cited by 4,224
OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph node organogenesis.
Kong, Y.-Y., Yoshida, H., Sarosi, I., Tan, H.-L., Timms, E., Capparelli, C., Morony, S., Oliveira-dos-Santos, A. J., Van, G., Itie, A., et al. (1999) · Nature · doi:10.1038/16852 · Cited by 3,351
Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification.
Bucay, N., Sarosi, I., Dunstan, C. R., Morony, S., Tarpley, J., Capparelli, C., Scully, S., Tan, H. L., Xu, W., Lacey, D. L., et al. (1998) · Genes & Development · doi:10.1101/gad.12.9.1260 · Cited by 2,483
Modulation of Osteoclast Differentiation and Function by the New Members of the Tumor Necrosis Factor Receptor and Ligand Families
Suda, T., Takahashi, N., Udagawa, N., Jimi, E., Gillespie, M. T., & Martin, T. J. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0367 · Cited by 2,345
Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand.
Kong, Y.-Y., Feige, U., Sarosi, I., Bolon, B., Tafuri, A., Morony, S., Capparelli, C., Li, J., Elliott, R., McCabe, S., et al. (1999) · Nature · doi:10.1038/46303 · Cited by 1,856
Bone Marrow, Cytokines, and Bone Remodeling — Emerging Insights into the Pathophysiology of Osteoporosis
Manolagas, S. C., & Jilka, R. L. (1995) · New England Journal of Medicine · doi:10.1056/nejm199502023320506 · Cited by 1,670
Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand.
Hsu, H., Lacey, D. L., Dunstan, C. R., Solovyev, I., Colombero, A., Timms, E., Tan, H.-L., Elliott, G., Kelley, M. J., Sarosi, I., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3540 · Cited by 1,636
Tumor Necrosis Factor α Stimulates Osteoclast Differentiation by a Mechanism Independent of the Odf/Rankl–Rank Interaction
Kobayashi, K., Takahashi, N., Jimi, E., Udagawa, N., Takami, M., Kotake, S., Nakagawa, N., Kinosaki, M., Yamaguchi, K., Shima, N., et al. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.2.275 · Cited by 1,309
Bone histomorphometry : techniques and interpretation
Recker, R. R. (1983) · CRC Press eBooks · Cited by 1,160

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Self-citation
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Yogesha, S. D., Khapli, S. M., & Wani, M. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410828200 · Cited by 44
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Malet, A., Bournaud, E., Lan, A., Mikogami, T., Tomé, D., & Blais, A. (2011) · Bone · doi:10.1016/j.bone.2011.02.002 · Cited by 44
Production of IL-7 is increased in ovariectomized mice, but not RANKL mRNA expression by osteoblasts/stromal cells in bone, and IL-7 enhances generation of osteoclast precursors in vitro
Sato, T., Watanabe, K., Masuhara, M., Hada, N., & Hakeda, Y. (2006) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-006-0723-y · Cited by 41
Liver-derived IGF-I is permissive for ovariectomy-induced trabecular bone loss
Lindberg, M. K., Svensson, J., Venken, K., Chavoshi, T. M., Andersson, N., Skrtic, S., Isaksson, O. G. P., Vanderschueren, D., Carlsten, H., & Ohlsson, C. (2005) · Bone · doi:10.1016/j.bone.2005.07.027 · Cited by 41
Linkage disequilibrium between polymorphisms in the human TNFRSF1B gene and their association with bone mass in perimenopausal women
Albagha, O. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.19.2289 · Cited by 42
Role of cytokines in postmenopausal bone loss
Pfeilschifter, J. (2003) · Current Osteoporosis Reports · doi:10.1007/s11914-003-0009-4 · Cited by 41
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Kim, J., Park, S., Baek, J. M., Erkhembaatar, M., Kim, M. S., Yoon, K., Oh, J., & Lee, M. S. (2015) · Journal of Natural Products · doi:10.1021/acs.jnatprod.5b00233 · Cited by 41
Does systemic inflammation and immune activation contribute to fracture risk in HIV?
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Local Regulators of Bone: IL-1, TNF, Lymphotoxin, Interferon-γ, IL-8, IL-10, IL-4, the LIF/IL-6 Family, and Additional Cytokines
Horowitz, M., & Lorenzo, J. (2002) · Elsevier eBooks · doi:10.1016/b978-012098652-1.50155-4 · Cited by 60
Decrease in the number and apoptosis of alveolar bone osteoclasts in estrogen‐treated rats
Faloni, A. P. S., Sasso‐Cerri, E., Katchburian, E., & Cerri, P. S. (2007) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2006.00932.x · Cited by 40
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Colaianni, G., Sun, L., Zaidi, M., & Zallone, A. Z. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00040.2014 · Cited by 41
Mice Lacking the Integrin 5 Subunit Have Accelerated Osteoclast Maturation and Increased Activity in the Estrogen-Deficient State
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O’Gradaigh, D., & Compston, J. E. (2003) · Rheumatology · doi:10.1093/rheumatology/keg447 · Cited by 38
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Bernardi, A. I., Andersson, A., Stubelius, A., Grahnemo, L., Carlsten, H., & Islander, U. (2015) · Immunobiology · doi:10.1016/j.imbio.2015.05.009 · Cited by 38
Cellular and molecular interactions between immune system and bone.
Grčević, D., Katavić, V., Lukić, I. K., Kovačić, N., Lorenzo, J. A., & Marušić, A. (2001) · PubMed · Cited by 36
Effects of activated T cells on osteoclastogenesis depend on how they are activated
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Exercise for improving bone health in women treated for stages I–III breast cancer: a systematic review and meta-analyses
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Self-citation

Authors: Cenci, S., Weitzmann, M. N., Roggia, C., Namba, N., Novack, D., Woodring, J., & Pacifici, R.
Affiliations: Barnes-Jewish Hospital (US)
Corresponding author: Pacifici, Roberto
ORCID: Cenci, Simone
Weitzmann, M. Neale
Roggia, Cristiana
Namba, Noriyuki
Novack, Deborah
Pacifici, Roberto
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2000-11-15
Volume: 106
Issue: 10
Pages: 1229-1237
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci11066
PMC: PMC381439
OpenAlex: W2133281510
Cited by: 705
References: 57
Citations by year: 2026: 30 · 2025: 30 · 2024: 14 · 2023: 25 · 2022: 23 · 2021: 27 · 2020: 35 · 2019: 25 · 2018: 19 · 2017: 34 · 2016: 33 · 2015: 37 · 2014: 32 · 2013: 32 · 2012: 28
FWCI: 7.12
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Arthritis Foundation
Eli Lilly and Company
National Institutes of Health
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR041412, AR41412, AR-13534)
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Keywords: estrogen deficiency, bone loss, ovariectomy, T cells, TNF-α, osteoclastogenesis, RANKL, macrophage colony-stimulating factor, TNF receptor p55, postmenopausal osteoporosis, bone resorption, nude mice, estrogen receptor, mesenchymal stem cells, T cell deficiency
MeSH terms: Animals, Bone Resorption, Carrier Proteins, Cells, Cultured, Estrogens, Membrane Glycoproteins, Mice, Inbred C57BL, Mice, Nude, Osteoclasts, Ovariectomy, T-Lymphocytes, Tumor Necrosis Factor-alpha, Antigens, CD, Macrophage Colony-Stimulating Factor, Receptors, Tumor Necrosis Factor, Mice, Knockout, Receptors, Tumor Necrosis Factor, Type I, Receptors, Tumor Necrosis Factor, Type II, Mice, RANK Ligand, Receptor Activator of Nuclear Factor-kappa B

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Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-α

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