Cited by 1,440Bone Metabolism and DiseasesOsteomyelitis and Bone Disorders ResearchRheumatoid Arthritis Research and Therapies

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TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand

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Lam, Jonathan, Takeshita, Sunao, Barker, Jane E., Kanagawa, Osami, Ross, F. Patrick, Teitelbaum, Steven L.·2000·Journal of Clinical Investigation

DOI 10.1172/jci11176PMC PMC387259

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Abstract

While TNF-alpha is pivotal to the pathogenesis of inflammatory osteolysis, the means by which it recruits osteoclasts and promotes bone destruction are unknown. We find that a pure population of murine osteoclast precursors fails to undergo osteoclastogenesis when treated with TNF-alpha alone. In contrast, the cytokine dramatically stimulates differentiation in macrophages primed by less than one percent of the amount of RANKL (ligand for the receptor activator of NF-kappaB) required to induce osteoclast formation. Mirroring their synergistic effects on osteoclast differentiation, TNF-alpha and RANKL markedly potentiate NF-kappaB and stress-activated protein kinase/c-Jun NH(2)-terminal kinase activity, two signaling pathways essential for osteoclastogenesis. In vivo administration of TNF-alpha prompts robust osteoclast formation in chimeric animals in which ss-galactosidase positive, TNF-responsive macrophages develop within a TNF-nonresponsive stromal environment. Thus, while TNF-alpha alone does not induce osteoclastogenesis, it does so both in vitro and in vivo by directly targeting macrophages within a stromal environment that expresses permissive levels of RANKL. Given the minuscule amount of RANKL sufficient to synergize with TNF-alpha to promote osteoclastogenesis, TNF-alpha appears to be a more convenient target in arresting inflammatory osteolysis.

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Inhibitory effect of sulphated polysaccharide porphyran (isolated from Porphyra yezoensis ) on RANKL ‐induced differentiation of RAW264.7 cells into osteoclasts
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“from mature monocytes and macrophages (Kikuta & Ishii, 2013; Lam et al., 2000; Nakashima et al., 2011; Udagawa, et al., 1990).”
Background
TNF‐α has both stimulatory and inhibitory effects on mouse monocyte‐derived osteoclastogenesis
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“Other studies have clearly shown that TNF-alpha promote proliferation and differentiation of osteoclasts in rats with erosive arthritis, suggesting that TNF-alpha appears to be a more convenient target in arresting inflammatory osteolysis [16].”
Result
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“The synergistic effects of TNF-α and RANKL significantly elevate the activation of NF-κB and stress-activated protein kinase/c-Jun NH2-terminal kinase, thereby enhancing osteo-clast differentiation [126].”
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“…factors, acting through an increase in RANKL expression by stromal/osteoblastic cells or lymphoid cells (Roux and Brown, 2009), or synergistically with or independently of RANKL, as has been reported for IL-1, TNF α (Kobayashi et al., 2000; Lam et al., 2000), IL-6 and IL-11 (Kudo et al., 2003).”
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Rac1 inhibition via Srgap2 restrains inflammatory osteoclastogenesis and limits the clastokine, SLIT3
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TNF-α is responsible for the contribution of stromal cells to osteoclast and odontoclast formation during orthodontic tooth movement
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Self-citation
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“additively with RANKL or directly (48, 49).”
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Organization of transcriptional regulatory machinery in osteoclast nuclei: Compartmentalization of Runx1
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“This protein consists of two subunits, which become translocated to the nucleus upon stimulation by RANKL, TNF-a, or other activators of NF-kB (Lam et al., 2000; Wei et al., 2001).”
Background
BAP1 promotes osteoclast function by metabolic reprogramming
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“Glutathione S-transferase (GST)-RANKL was expressed in our laboratory as described 52 .”
Self-citation
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Background
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Background
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Background
Intestinal Inflammation Promotes MDL-1+ Osteoclast Precursor Expansion to Trigger Osteoclastogenesis and Bone Loss
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BackgroundInfluential
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“The medium was changed every 2 to 3 d. Tartrate-resistant acid phosphatase (TRAP) staining was performed (Lam et al. 2000).”
BackgroundMethodInfluential

Authors: Lam, J., Takeshita, S., Barker, J. E., Kanagawa, O., Ross, F. P., & Teitelbaum, S. L.
Affiliations: Washington University in St. Louis (US)
Barnes-Jewish Hospital (US)
Corresponding author: Teitelbaum, Steven L.
ORCID: Kanagawa, Osami
Teitelbaum, Steven L.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2000-12-15
Volume: 106
Issue: 12
Pages: 1481-1488
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci11176
PMC: PMC387259
OpenAlex: W2132933661
Cited by: 1,440
References: 0
Citations by year: 2026: 45 · 2025: 63 · 2024: 48 · 2023: 53 · 2022: 60 · 2021: 72 · 2020: 57 · 2019: 61 · 2018: 59 · 2017: 75 · 2016: 61 · 2015: 56 · 2014: 49 · 2013: 64 · 2012: 58
FWCI: 11.22
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: National Institutes of Health
National Institute of General Medical Sciences (T32GM007200)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK027726)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-32788, AR-07033, R01AR032788, R37AR046523, T32AR007033, R01AR046852, AR46523, R01AR046523)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Health Sciences › Medicine › Rheumatology › Osteomyelitis and Bone Disorders Research
Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
Keywords: TNF-α, osteoclastogenesis, RANK ligand, macrophages, osteoclast precursors, NF-κB signaling, JNK signaling, inflammatory osteolysis, bone destruction, chimeric mice, cytokine synergy
MeSH terms: Animals, Carrier Proteins, Cell Differentiation, Cells, Cultured, Drug Synergism, Enzyme Activation, Flow Cytometry, Histocytochemistry, Macrophages, Membrane Glycoproteins, Osteoclasts, Stem Cells, Tumor Necrosis Factor-alpha, Bone Marrow Transplantation, NF-kappa B, Mitogen-Activated Protein Kinases, JNK Mitogen-Activated Protein Kinases, Mice, RANK Ligand, Receptor Activator of Nuclear Factor-kappa B

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TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand

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