Pannexin-1 and P2X7-Receptor Are Required for Apoptotic Osteocytes in Fatigued Bone to Trigger RANKL Production in Neighboring Bystander Osteocytes
Open accessAbstract
Osteocyte apoptosis is required to induce intracortical bone remodeling after microdamage in animal models, but how apoptotic osteocytes signal neighboring “bystander” cells to initiate the remodeling process is unknown. Apoptosis has been shown to open pannexin-1 (Panx1) channels to release adenosine diphosphate (ATP) as a “find-me” signal for phagocytic cells. To address whether apoptotic osteocytes use this signaling mechanism, we adapted the rat ulnar fatigue-loading model to reproducibly introduce microdamage into mouse cortical bone and measured subsequent changes in osteocyte apoptosis, receptor activator of NF-κB ligand (RANKL) expression and osteoclastic bone resorption in wild-type (WT; C57Bl/6) mice and in mice genetically deficient in Panx1 (Panx1KO). Mouse ulnar loading produced linear microcracks comparable in number and location to the rat model. WT mice showed increased osteocyte apoptosis and RANKL expression at microdamage sites at 3 days after loading and increased intracortical remodeling and endocortical tunneling at day 14. With fatigue, Panx1KO mice exhibited levels of microdamage and osteocyte apoptosis identical to WT mice. However, they did not upregulate RANKL in bystander osteocytes or initiate resorption. Panx1 interacts with P2X7R in ATP release; thus, we examined P2X7R-deficient mice and WT mice treated with P2X7R antagonist Brilliant Blue G (BBG) to test the possible role of ATP as a find-me signal. P2X7RKO mice failed to upregulate RANKL in osteocytes or induce resorption despite normally elevated osteocyte apoptosis after fatigue loading. Similarly, treatment of fatigued C57Bl/6 mice with BBG mimicked behavior of both Panx1KO and P2X7RKO mice; BBG had no effect on osteocyte apoptosis in fatigued bone but completely prevented increases in bystander osteocyte RANKL expression and attenuated activation of resorption by more than 50%. These results indicate that activation of Panx1 and P2X7R are required for apoptotic osteocytes in fatigued bone to trigger RANKL production in neighboring bystander osteocytes and implicate ATP as an essential signal mediating this process. © 2016 American Society for Bone and Mineral Research.
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The same phenotype was observed in mice treated with an inhibitor of the P2X7 receptor (P2X7R), which is a coactivator of PANX1.
“The same phenotype was observed in mice treated with an inhibitor of the P2X7 receptor (P2X7R), which is a coactivator of PANX1.67”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [67]
ATP from apoptotic osteocytes might bind P2Y2 receptors expressed on bystander osteocytes, which in turn might activate RANKL production and release.
“Indeed, ATP from apoptotic osteocytes might bind P2Y2 receptors expressed on bystander osteocytes, which in turn might activate RANKL production and release67 (Fig. 2).”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [67]
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- [20]Elliott M Chekeni FB Trampont PC Lazarowski ER Kadl A Walk SF Park D Woodson RI Ostankovich M Sharma P Lysiak JJ Harden TK Leitinger N Ravichandran KS Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance Nature 2009 461 7261 282 286 19741708 PMC2851546
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BackgroundInfluential
- Authors
- Cheung, W. Y., Fritton, J. C., Morgan, S. A., Seref-Ferlengez, Z., Basta-Pljakic, J., Thi, M. M., Suadicani, S. O., Spray, D. C., Majeska, R. J., & Schaffler, M. B.
- Affiliations
- City College of New York (US)
- Rutgers, The State University of New Jersey (US)
- Department of Biomedical EngineeringCity College of New YorkNew YorkNYUSA
- Albert Einstein College of Medicine (US)
- Corresponding author
- Schaffler, Mitchell B
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-11-10
- Volume
- 31
- Issue
- 4
- Pages
- 890-899
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- PMC
- PMC4915221
- OpenAlex
- W2138486361
- Cited by
- 89
- References
- 71
- Citations by year
- 2026: 10 · 2025: 3 · 2024: 7 · 2023: 14 · 2022: 8 · 2021: 9 · 2020: 15 · 2019: 9 · 2018: 4 · 2017: 6 · 2016: 4
- FWCI
- 2.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Rutgers University Community Repository (Rutgers University) (acceptedVersion)
- Rutgers University Community Repository (Rutgers University)
- Funders
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR041210 and AR057139)
- National Institutes of Health (DK091466 and DK081435)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Keywords
- osteocyte apoptosis, pannexin 1, P2X7 receptor, RANKL, bone fatigue, microcracks, ATP release, osteoclast resorption, cortical bone, Brilliant Blue G, microdamage
- MeSH terms
- Animals, Nerve Tissue Proteins, Osteocytes, Apoptosis, Connexins, Mice, Knockout, Bystander Effect, Mice, Rats, RANK Ligand, Receptors, Purinergic P2X7
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