A Physical Mechanism for Coupling Bone Resorption and Formation in Adult Human Bone
Open accessAbstract
During skeletal remodeling, pre-osteoclasts and pre-osteoblasts are targeted to critical sites of the bone to resorb and reconstruct bone matrix, respectively. Coordination of site-specific recruitment of these two cell types is a prerequisite to maintain the specific architecture of each bone within strict limits throughout adult life. Here, we determined that the bone marrow microanatomy adjacent to remodeling areas is a central player in this process. By using histomorphometry and multiple immunostainings, we demonstrated in biopsies exhibiting coupled bone resorption and formation that osteoclasts and osteoblasts on the bone surface were always covered by a canopy of flat cells expressing osteoblast markers. In contrast, in biopsies in which this canopy was disrupted, bone formation was deficient. Three-dimensional visualizations revealed that this canopy covered the entire remodeling site and was associated with capillaries, thereby forming a previously unrecognized microanatomical entity. Furthermore, pre-osteoclasts were positioned along these capillaries. These findings led to a model that implicates vasculature in the site-specific recruitment of osteoclasts and osteoblasts and embraces the current knowledge on the molecular mechanism of bone remodeling.
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Bone remodeling occurs due to coordinated actions of osteoclasts, osteoblasts, osteocytes, and bone lining cells which together form the basic multicellular unit (BMU).
“This process occurs due to coordinated actions of osteoclasts, osteoblasts, osteocytes, and bone lining cells which together form the temporary anatomical structure called basic multicellular unit (BMU) [12–14].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [14]
Bone lining cells participate in osteoclast differentiation by producing OPG and RANKL.
“Bone lining cells functions are not completely understood, but it has been shown that these cells prevent the direct interaction between osteoclasts and bone matrix, when bone resorption should not occur, and also participate in osteoclast differentiation, producing osteoprotegerin (OPG) and the receptor activator of nuclear factor kappa-B ligand (RANKL) [14, 53].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [14]
Bone lining cells prevent the direct interaction between osteoclasts and bone matrix when bone resorption should not occur.
“Bone lining cells functions are not completely understood, but it has been shown that these cells prevent the direct interaction between osteoclasts and bone matrix, when bone resorption should not occur, and also participate in osteoclast differentiation, producing osteoprotegerin (OPG) and the receptor activator of nuclear factor kappa-B ligand (RANKL) [14, 53].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [14]
The BRC seems to be connected to bone lining cells on bone surface, which in turn are in communication with osteocytes enclosed within the bone matrix.
“The BRC seems to be connected to bone lining cells on bone surface, which in turn are in communication with osteocytes enclosed within the bone matrix [13, 14].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [14]
When the remodeling starts, BME cells and BLCs form a protective structure known as the canopy, which separates osteoclasts and osteoblasts from bone marrow.
“When the remodeling starts, BME cells and BLCs form a protective structure known as the canopy, which separates osteoclasts and osteoblasts from bone marrow117 (Fig. 3).”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [117]
The tight link between BRCs and capillaries coated with pericytes allows capillary-BRC canopy interactions to induce BMU development at bone remodeling sites.
“The tight link between BRCs and capillaries, which are coated with pericytes, allows capillary-BRC canopy interactions to induce BMU development at bone remodeling sites117 (Fig. 3).”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [117]
The osteoclast-canopy interface is the physical site where coupling of bone resorption to bone formation occurs.
“The osteoclast-canopy interface is therefore the physical site where the coupling of bone resorption to bone formation occurs.117”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [117]
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Self-citation
- Authors
- Andersen, T. L., Sondergaard, T. E., Skorzynska, K. E., Dagnaes-Hansen, F., Plesner, T. L., Hauge, E. M., Plesner, T., & Delaisse, J.-M.
- Affiliations
- University of Southern Denmark (DK)
- Aarhus University Hospital (DK)
- Corresponding author
- Andersen, Thomas Levin
- Venue
- The American Journal of Pathology
- Publisher
- Elsevier BV
- Published
- 2009-01
- Volume
- 174
- Issue
- 1
- Pages
- 239-247
- ISSN
- 0002-9440 (ISSN-L)
- PMC
- PMC2631336
- OpenAlex
- W1989343687
- Cited by
- 325
- References
- 51
- Citations by year
- 2026: 9 · 2025: 15 · 2024: 18 · 2023: 23 · 2022: 11 · 2021: 26 · 2020: 28 · 2019: 16 · 2018: 20 · 2017: 19 · 2016: 12 · 2015: 17 · 2014: 27 · 2013: 27 · 2012: 12
- FWCI
- 5.89
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal Of Pathology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
- 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
- bone remodeling, bone resorption, bone formation, osteoclasts, osteoblasts, osteoclast precursors, preosteoblasts, bone marrow vasculature, capillaries
- MeSH terms
- Animals, Bone and Bones, Bone Marrow, Bone Marrow Cells, Bone Regeneration, Bone Resorption, Humans, Immunohistochemistry, Multiple Myeloma, Osteoblasts, Osteoclasts, Rabbits, Stem Cells, Cell Lineage
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