Increased presence of capillaries next to remodeling sites in adult human cancellous bone
Abstract
Vascularization is a prerequisite for osteogenesis in a number of situations, including bone development, fracture healing, and cortical bone remodeling. It is unknown whether a similar link exists between cancellous bone remodeling and vascularization. Here, we show an association between remodeling sites, capillaries, proliferative cells, and putative osteoblast progenitors. Iliac crest biopsies from normal human individuals were subjected to histomorphometry and immunohistochemistry to identify the respective positions of bone remodeling sites, CD34-positive capillaries, smooth muscle actin (SMA)-positive putative osteoblast progenitors, including pericytes, Ki67-positive proliferative cells, and bone remodeling compartment (BRC) canopies. The BRC canopy is a recently described structure separating remodeling sites from the bone marrow, consisting of CD56-positive osteoblasts at an early differentiation stage. We found that bone remodeling sites were associated with a significantly increased presence of capillaries, putative osteoblast progenitors, and proliferative cells in a region within 50 µm of the bone or the canopy surface. The increases were the highest above eroded surfaces and at the level of the light-microscopically assessed contact of these three entities with the bone or canopy surfaces. Between 51 and 100 µm, their densities leveled to that found above quiescent surfaces. Electron microscopy asserted the close proximity between BRC canopies and capillaries lined by pericytes. Furthermore, the BRC canopy cells were found to express SMA. These ordered distributions support the existence of an osteogenic-vascular interface in adult human cancellous bone. The organization of this interface fits the current knowledge on the mode of action of vasculature on osteogenesis, and points to the BRC canopy as a central player in this mechanism. We propose a model where initiation of bone remodeling coincides with the induction of proximity of the vasculature to endosteal surfaces, thereby allowing capillary-BRC canopy interactions that activate marrow events, including recruitment of osteoblast progenitors to bone remodeling sites. © 2013 American Society for Bone and Mineral Research.
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An increased presence of capillaries covering human cancellous bone is found at remodeling sites within 50 μm from the canopy surface.
“an increased presence of capillaries covering human cancellous bone has been found at remodeling sites in an area within 50 µm from the canopy surface.124”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [124]
Cites
A perivascular origin for mesenchymal stem cells in multiple human organs
Crisan, M., Yap, S., Casteilla, L., Chen, C.-W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.07.003 · Cited by 3,991 · see citing works
Bone Marrow Stromal Stem Cells: Nature, Biology, and Potential Applications
Bianco, P., Riminucci, M., Gronthos, S., & Robey, P. G. (2001) · Stem Cells · doi:10.1634/stemcells.19-3-180 · Cited by 1,944 · see citing works
Parfitt, A. M. (1994) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240550303 · Cited by 1,001 · see citing works
Maes, C., Kobayashi, T., Selig, M. K., Torrekens, S., Roth, S. I., Mackem, S., Carmeliet, G., & Kronenberg, H. M. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.07.010 · Cited by 940 · see citing works
CD34: structure, biology, and clinical utility [see comments]
Krause, D., Fackler, M., Civin, C., & May, W. S. (1996) · Blood · doi:10.1182/blood.v87.1.1.bloodjournal8711 · Cited by 939 · see citing works
Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche
Celso, C. L., Fleming, H. E., Wu, J. W., Zhao, C. X., Miake-Lye, S., Fujisaki, J., Côté, D. C., Rowe, D. W., Lin, C. P., & Scadden, D. T. (2008) · Nature · doi:10.1038/nature07434 · Cited by 917 · see citing works
Expression of the CD34 gene in vascular endothelial cells
Fina, L., Molgaard, H. V., Robertson, D. M., Bradley, N. J., Monaghan, P., Delia, D., Sutherland, D. R., Baker, M. A., & Greaves, M. F. (1990) · Blood · doi:10.1182/blood.v75.12.2417.2417 · Cited by 888 · see citing works
Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells
Kollet, Ó., Dar, A., Shivtiel, S., Kalinkovich, A., Lapid, K., Sztainberg, Y., Tesio, M., Samstein, R. M., Goichberg, P., Spiegel, A., et al. (2006) · Nature Medicine · doi:10.1038/nm1417 · Cited by 774 · see citing works
Nilsson, S. K., Johnston, H. M., & Coverdale, J. (2001) · Blood · doi:10.1182/blood.v97.8.2293 · Cited by 575 · see citing works
Vascular Pericytes Express Osteogenic Potential In Vitro and In Vivo
Doherty, M. J., Ashton, B. A., Walsh, S., Beresford, J. N., Grant, M. E., & Canfield, A. E. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.5.828 · Cited by 566 · see citing works
Díaz‐Flores, L., Gutiérrez, R., Madrid, J. F., Varela, H., Valladares, F., Acosta, E., Martı́n-Vasallo, P., & Díaz-Flores, L. (2009) · PubMed · doi:10.14670/hh-24.909 · Cited by 547 · see citing works
The physiological and cellular basis of metabolic bone disease
Rasmussen, H., & Bordier, P. (1973) · Medical Entomology and Zoology · Cited by 489 · see citing works
The hematopoietic stem cell niche: Low in oxygen but a nice place to be
Eliasson, P., & Jönsson, J. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21908 · Cited by 473 · see citing works
Burkhardt, R., Kettner, G., Böhm, W., Schmidmeier, M., Schlag, R., Frisch, B., Mallmann, B., Eisenmenger, W., & Gilg, T. (1987) · Bone · doi:10.1016/8756-3282(87)90015-9 · Cited by 452 · see citing works
The hematopoietic stem cell in its place
Adams, G. B., & Scadden, D. T. (2006) · Nature Immunology · doi:10.1038/ni1331 · Cited by 450 · see citing works
Regulation of Osteogenesis-Angiogenesis Coupling by HIFs and VEGF
Schipani, E., Maes, C., Carmeliet, G., & Semenza, G. L. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090602 · Cited by 407 · see citing works
Hauge, E. M., Qvesel, D., Eriksen, E. F., Mosekilde, L., & Melsen, F. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.9.1575 · Cited by 397 · see citing works
Angiogenesis in Fracture Repair
Glowacki, J. (1998) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-199810001-00010 · Cited by 386 · see citing works
Vascular Biology and the Skeleton
Brandi, M. L., & Collin‐Osdoby, P. (2006) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.050917 · Cited by 334 · see citing works
Manolagas, S. C., & Almeida, M. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0259 · Cited by 330 · see citing works
A Physical Mechanism for Coupling Bone Resorption and Formation in Adult Human Bone
Andersen, T. L., Sondergaard, T. E., Skorzynska, K. E., Dagnaes-Hansen, F., Plesner, T. L., Hauge, E. M., Plesner, T., & Delaisse, J.-M. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.080627 · Cited by 325 · see citing works
Self-citationThe Pericyte as a Possible Osteoblast Progenitor Cell
Brighton, C. T., Lorich, D. G., Kupcha, R., REILLY, T. M., JONES, A. R., & WOODBURY, R. A. (1992) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-199202000-00043 · Cited by 299 · see citing works
The mechanism of coupling: a role for the vasculature
PARFITT, A. M. (2000) · Bone · doi:10.1016/s8756-3282(00)80937-0 · Cited by 283 · see citing works
Arnett, T. R. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.07.021 · Cited by 265 · see citing works
Bone and the hematopoietic niche: a tale of two stem cells
Bianco, P. (2011) · Blood · doi:10.1182/blood-2011-01-315069 · Cited by 253 · see citing works
Colnot, C., Lu, C., Hu, D. P., & Helms, J. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.01.011 · Cited by 233 · see citing works
Zelzer, E., & Olsen, B. R. (2004) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(04)65006-x · Cited by 223 · see citing works
Expression of angiogenic factors during distraction osteogenesis
Pacicca, D. M., Patel, N., Lee, C., Palomares, K. T. S., Lehmann, W., Carvalho, R. S., Gerstenfeld, L. C., & Einhorn, T. A. (2003) · Bone · doi:10.1016/j.bone.2003.06.002 · Cited by 202 · see citing works
Osteal macrophages: A new twist on coupling during bone dynamics
Pettit, A. R., Chang, M. K., Hume, D. A., & Raggatt, L. J. (2008) · Bone · doi:10.1016/j.bone.2008.08.128 · Cited by 195 · see citing works
Compromised Bone Marrow Perfusion in Osteoporosis
Griffith, J. F., Yeung, D. K. W., Tsang, P. H., Choi, K. C., Kwok, T. C. Y., Ahuja, A. T., Leung, K., & Leung, P. (2008) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.080233 · Cited by 180 · see citing works
Intraosseous circulation from physiology to disease
Laroche, M. (2002) · Joint Bone Spine · doi:10.1016/s1297-319x(02)00391-3 · Cited by 173 · see citing works
Atherosclerosis and osteoporosis: age-dependent degenerative processes or related entities?
Anagnostis, P. G., Karagiannis, A. I., Kakafika, A. I., Τζιόμαλος, Κ., Athyros, V. G., & Mikhailidis, D. P. (2008) · Osteoporosis International · doi:10.1007/s00198-008-0648-5 · Cited by 171 · see citing works
The Bone Remodeling Compartment: A Circulatory Function for Bone Lining Cells
Parfitt, A. M. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.9.1583 · Cited by 169 · see citing works
Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population
Kalajzić, Ž., Li, H., Wang, L., Jiang, X., Lamothe, K., Adams, D. J., Aguila, H. L., Rowe, D. W., & Kalajzić, I. (2008) · Bone · doi:10.1016/j.bone.2008.04.023 · Cited by 167 · see citing works
Characterization of circulating osteoblast lineage cells in humans
Eghbali-Fatourechi, G. Z., Mödder, U. I., Charatcharoenwitthaya, N., Sanyal, A., Undale, A. H., Clowes, J. A., Tarara, J. E., & Khosla, S. (2007) · Bone · doi:10.1016/j.bone.2006.12.064 · Cited by 133 · see citing works
REEVE, J., ARLOT, M. E., Wootton, R., Edouard, C. M., Tellez, M., Hesp, R., Green, J. R., & Meunier, P. J. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-6-1124 · Cited by 124 · see citing works
Prisby, R. D., Guignandon, A., Vanden‐Bossche, A., Mac‐Way, F., Linossier, M., Thomas, M., Laroche, N., Malaval, L., Langer, M., Peter, Z., et al. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.459 · Cited by 114 · see citing works
Relationships between trabecular bone remodeling and bone vascularization: a quantitative study
Barou, O., Mekraldi, S., Vico, L., Boivin, G., Alexandre, C., & Lafage‐Proust, M. (2002) · Bone · doi:10.1016/s8756-3282(02)00677-4 · Cited by 96 · see citing works
Endl, E., & Gerdes, J. (2000) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(200003)182:3 · Cited by 89 · see citing works
Roche, B., David, V., Vanden‐Bossche, A., Peyrin, F., Malaval, L., Vico, L., & Lafage‐Proust, M. (2011) · Bone · doi:10.1016/j.bone.2011.09.051 · Cited by 83 · see citing works
Lee, Y., & Chuong, C. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650071211 · Cited by 60 · see citing works
Towler, D. A. (2008) · Current Osteoporosis Reports · doi:10.1007/s11914-008-0012-x · Cited by 58 · see citing works
Inoué, S., & Osmond, D. G. (2001) · The Anatomical Record · doi:10.1002/ar.1166 · Cited by 55 · see citing works
Changes in the vascular network during the formation of Haversian systems
Marotti, G., & Zallone, A. Z. (1980) · Cells Tissues Organs · doi:10.1159/000145171 · Cited by 54 · see citing works
Bourke, V. A., Watchman, C. J., Reith, J. D., Jorgensen, M., Dieudonné, A., & Bolch, W. E. (2009) · Blood · doi:10.1182/blood-2008-12-192922 · Cited by 54 · see citing works
Watchman, C. J., Bourke, V. A., Lyon, J. R., Knowlton, A. E., Butler, S. L., Grier, D. D., Wingard, J. R., Braylan, R. C., & Bolch, W. E. (2007) · Journal of Nuclear Medicine · doi:10.2967/jnumed.106.035337 · Cited by 50 · see citing works
Expression of smooth muscle actin in osteoblasts in human bone
Kinner, B., & Spector, M. (2002) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(01)00145-0 · Cited by 46 · see citing works
Regulatory pathways revealing new approaches to the development of anabolic drugs for osteoporosis
Martin, T. J., Sims, N. A., & Ng, K. W. (2008) · Osteoporosis International · doi:10.1007/s00198-008-0575-5 · Cited by 40 · see citing works
Jensen, P. R., Andersen, T. L., Søe, K., Hauge, E., Bollerslev, J., Amling, M., Barvencik, F., & Delaissé, J. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1490 · Cited by 37 · see citing works
Self-citationContribution of neural cell adhesion molecule (NCAM) to hemopoietic system in monkeys
Kato, J., Hisha, H., Wang, X., Mizokami, T., Okazaki, S., Li, Q., Song, C., Maki, M., Hosaka, N., Adachi, Y., et al. (2008) · Annals of Hematology · doi:10.1007/s00277-008-0513-9 · Cited by 20 · see citing works
Immunophenotypic characterization of human bone marrow endosteal cells
Sillaber, C., Walchshofer, S., Mosberger, I., Gaiger, A., Simonitsch, I., Chott, A., Lechner, K., & Valent, P. (1999) · Tissue Antigens · doi:10.1034/j.1399-0039.1999.530606.x · Cited by 10 · see citing works
Cellular isolation, culture and characterization of the marrow sac cells in human tubular bone.
Bi, L. X., Mainous, E. G., Yngve, D. A., & Buford, W. L. (2008) · PubMed · Cited by 10 · see citing works
Hypercalcaemia and azotaemia in multiple myeloma--clinical and biochemical parallels.
Goranova-Marinova, V. S. (1994) · PubMed · Cited by 1 · see citing works
Ultrastructural features in the structure of blood capillaries of the Haversian canal.
Baltadjiev, G. (1994) · PubMed · Cited by 1 · see citing works
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Fornetti, J., Welm, A. L., & Stewart, S. A. (2018) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3618 · Cited by 528 · see citing works
Feng, X., & Teitelbaum, S. L. (2013) · Bone Research · doi:10.4248/br201301003 · Cited by 541 · see citing works
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Croucher, P. I., McDonald, M. M., & Martin, T. J. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.44 · Cited by 475 · see citing works
It Takes Two to Tango: Coupling of Angiogenesis and Osteogenesis for Bone Regeneration
Grosso, A., Burger, M. G., Lunger, A., Schaefer, D. J., Banfi, A., & Maggio, N. D. (2017) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2017.00068 · Cited by 451 · see citing works
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Sims, N. A., & Martin, T. J. (2020) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021119-034425 · Cited by 286 · see citing works
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Drake, M. T., Clarke, B. L., Oursler, M. J., & Khosla, S. (2017) · Endocrine Reviews · doi:10.1210/er.2015-1114 · Cited by 282 · see citing works
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Martin, T. J., & Sims, N. A. (2015) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-014-9308-6 · Cited by 213 · see citing works
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Collins, F. L., Rios‐Arce, N. D., Schepper, J. D., Parameswaran, N., & McCabe, L. R. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.bad-0015-2016 · Cited by 188 · see citing works
Sims, N. A., & Martin, T. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00041 · Cited by 184 · see citing works
Delaissé, J. (2014) · BoneKEy Reports · doi:10.1038/bonekey.2014.56 · Cited by 168 · see citing works
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Lafage‐Proust, M., Roche, B., Langer, M., Cléret, D., Vanden‐Bossche, A., Olivier, T., & Vico, L. (2015) · BoneKEy Reports · doi:10.1038/bonekey.2015.29 · Cited by 154 · see citing works
Re-thinking the bone remodeling cycle mechanism and the origin of bone loss
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Self-citationOsteoclast-Derived Coupling Factors in Bone Remodeling
Henriksen, K., Karsdal, M. A., & Martin, T. J. (2013) · Calcified Tissue International · doi:10.1007/s00223-013-9741-7 · Cited by 145 · see citing works
Metabolic regulation of skeletal cell fate and function
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Understanding Coupling between Bone Resorption and Formation
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Burger, M. G., Grosso, A., Briquez, P. S., Born, G., Lunger, A., Schrenk, F., Todorov, A., Sacchi, V., Hubbell, J. A., Schaefer, D. J., et al. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.07.014 · Cited by 122 · see citing works
Osteoblast Recruitment Routes in Human Cancellous Bone Remodeling
Kristensen, H. B., Andersen, T. L., Marcussen, N., Rolighed, L., & Delaissé, J. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.11.022 · Cited by 88 · see citing works
Self-citationBisphosphonates impair the onset of bone formation at remodeling sites
Jensen, P. R., Andersen, T. L., Chavassieux, P., Roux, J.-P., & Delaissé, J. (2021) · Bone · doi:10.1016/j.bone.2021.115850 · Cited by 83 · see citing works
Self-citationRecent Advances in Osteoclast Biological Behavior
Sun, Y., Li, J., Xie, X., Gu, F., Sui, Z., Zhang, K., & Yu, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.788680 · Cited by 81 · see citing works
Abdelgawad, M. E., Delaisse, J.-M., Hinge, M., Jensen, P. R., Alnaimi, R. W., Rolighed, L., Engelholm, L. H., Marcussen, N., & Andersen, T. L. (2016) · Histochemistry and Cell Biology · doi:10.1007/s00418-016-1414-y · Cited by 76 · see citing works
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Martin, T. J. (2014) · Journal of Bone Metabolism · doi:10.11005/jbm.2014.21.1.8 · Cited by 72 · see citing works
Sayilekshmy, M., Hansen, R. B., Delaissé, J., Rolighed, L., Andersen, T. L., & Heegaard, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-41779-w · Cited by 73 · see citing works
Self-citationMuscle-bone interactions during fracture healing.
Davis, K. M., Griffin, K. S., Chu, T. G., Wenke, J. C., Corona, B. T., McKinley, T. O., & Kacena, M. A. (2015) · PubMed Central · Cited by 68 · see citing works
Cell‐to‐cell communication in guided bone regeneration: molecular and cellular mechanisms
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Jensen, P. R., Andersen, T. L., Hauge, E., Bollerslev, J., & Delaissé, J. (2014) · Bone · doi:10.1016/j.bone.2014.12.004 · Cited by 57 · see citing works
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Søe, K., Delaisse, J.-M., & Borggaard, X. G. (2021) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2020.05.016 · Cited by 49 · see citing works
Roche, B., Vanden‐Bossche, A., Malaval, L., Normand, M., Jannot, M., Chaux, R., Vico, L., & Lafage‐Proust, M. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2191 · Cited by 47 · see citing works
Eggers, B., Marciniak, J., Beisel-Memmert, S., Kramer, F., Deschner, J., & Nokhbehsaim, M. (2020) · Odontology · doi:10.1007/s10266-020-00487-y · Cited by 45 · see citing works
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Andersen, T. L., Hauge, E., Rolighed, L., Bollerslev, J., Kjærsgaard‐Andersen, P., & Delaissé, J. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.12.005 · Cited by 37 · see citing works
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Bone marrow blood vessel ossification and “microvascular dead space” in rat and human long bone
Prisby, R. D. (2014) · Bone · doi:10.1016/j.bone.2014.03.041 · Cited by 29 · see citing works
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Søe, K., Andersen, T. L., Hinge, M., Rolighed, L., Marcussen, N., & Delaissé, J. (2019) · Calcified Tissue International · doi:10.1007/s00223-019-00575-4 · Cited by 28 · see citing works
Self-citationIlas, D. C., Baboolal, T. G., Churchman, S. M., Jones, W. G., Giannoudis, P. V., Bühring, H., McGonagle, D., & Jones, E. (2020) · Scientific Reports · doi:10.1038/s41598-020-67998-0 · Cited by 27 · see citing works
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Ansari, N., & Sims, N. A. (2019) · Handbook of experimental pharmacology · doi:10.1007/164_2019_343 · Cited by 27 · see citing works
Jensen, P. R., Andersen, T. L., Pennypacker, B. L., Duong, L. T., Engelholm, L. H., & Delaissé, J. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.12.036 · Cited by 24 · see citing works
Self-citationPrisby, R. D. (2020) · Comprehensive physiology · doi:10.1002/cphy.c190009 · Cited by 30 · see citing works
A Critical Role of the Bone Marrow Envelope in Human Bone Remodeling
Andersen, T. L., Jensen, P. R., Sikjær, T., Rejnmark, L., Ejersted, C., & Delaissé, J. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4815 · Cited by 20 · see citing works
Self-citationAndreasen, C. M., Bakalova, L., Brüel, A., Hauge, E., Kiil, B. J., Delaissé, J., Kersh, M. E., Thomsen, J. S., & Andersen, T. L. (2019) · Bone · doi:10.1016/j.bone.2019.115127 · Cited by 20 · see citing works
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Neag, G., Finlay, M., & Naylor, A. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147253 · Cited by 19 · see citing works
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Zhang, Q., Nettleship, I., Schmelzer, E., Gerlach, J. C., Zhang, X., Wang, J., & Liu, C. (2019) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2019.0215 · Cited by 19 · see citing works
Andreasen, C. M., El-Masri, B. M., MacDonald, B., Laursen, K. S., Nielsen, M. H., Thomsen, J. S., Delaissé, J., & Andersen, T. L. (2023) · Bone · doi:10.1016/j.bone.2023.116787 · Cited by 16 · see citing works
Self-citationHong, H., Shi, Z., Qiao, P., Li, H., McCoy, E. M., Mao, P., Xu, H., Feng, X., & Wang, S. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.09.098 · Cited by 16 · see citing works
Martin, T. J., & Seeman, E. (2023) · Neurospine · doi:10.14245/ns.2346966.483 · Cited by 17 · see citing works
Beck-Broichsitter, B. E., Becker, S. T., Seitz, H., Wiltfang, J., & Warnke, P. H. (2015) · Journal of Cranio-Maxillofacial Surgery · doi:10.1016/j.jcms.2015.03.038 · Cited by 15 · see citing works
Sørensen, N. N., Andreasen, C. M., Jensen, P. R., Hauge, E., Bollerslev, J., Delaissé, J., Kassem, M. S., Jafari, A., Diaz‐delCastillo, M., & Andersen, T. L. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1232574 · Cited by 14 · see citing works
Self-citationde Moraes, P. H., Olate, S. M., Lauria, A., Asprino, L., de Moraes, M., & de Albergaria-Barbosa (2015) · PubMed Central · Cited by 14 · see citing works
Remodelling compartment in root cementum
Martins, J. F. B., Rodrigues, C. F. D., Diogo, P., Paulo, S., Palma, P., & Vale, F. (2020) · Folia Morphologica · doi:10.5603/fm.a2020.0134 · Cited by 13 · see citing works
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Panvini, F. M., Pacini, S., Montali, M., Barachini, S., Mazzoni, S., Morganti, R., Ciancia, E. M., Carnicelli, V., & Petrini, M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.596452 · Cited by 13 · see citing works
Tan, X., Zeng, Y., Tu, Z., Li, P., Chen, H., Cheng, L., Tu, S., & Jiang, L. (2020) · BioMed Research International · doi:10.1155/2020/7623635 · Cited by 12 · see citing works
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Kristensen, H. B., Andersen, T. L., Patriarca, A., Kallenbach, K., MacDonald, B., Sikjær, T., Ejersted, C., & Delaissé, J. (2021) · PLoS ONE · doi:10.1371/journal.pone.0250081 · Cited by 12 · see citing works
Self-citationSun, B., Zhao, B., Zhu, J., Sun, Z., Shi, Y., & Huang, F. (2018) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2018.3692 · Cited by 11 · see citing works
Pathophysiology of bone remodelling cycle: Role of immune system and lipids
Parolini, C. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.116844 · Cited by 10 · see citing works
Prisby, R. D. (2020) · Comprehensive physiology · doi:10.1002/j.2040-4603.2020.tb00132.x · Cited by 10 · see citing works
Coupling of bone formation and resorption
Sims, N. A., & Martin, T. J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814841-9.00010-5 · Cited by 9 · see citing works
Coupling: The Influences of Immune and Bone Cells
Sims, N. A., Martin, T. J., & Quinn, J. M. W. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800571-2.00010-4 · Cited by 9 · see citing works
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Vrahnas, C., & Sims, N. A. (2020) · Contemporary Endocrinology · doi:10.1007/978-3-319-69287-6_1 · Cited by 9 · see citing works
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Collins, F. L., Rios‐Arce, N. D., Schepper, J. D., Parameswaran, N., & McCabe, L. R. (2018) · ASM Press eBooks · doi:10.1128/9781555819705.ch9 · Cited by 8 · see citing works
Meertens, R. M., KNAPP, K. M., Strain, W. D., Casanova, F., Ball, S., Fulford, J., & Thorn, C. E. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.738239 · Cited by 8 · see citing works
Christiansen, P. V. D., Andreasen, C. M., El-Masri, B. M., Laursen, K. S., Delaissé, J., & Andersen, T. L. (2023) · Bone · doi:10.1016/j.bone.2023.116896 · Cited by 8 · see citing works
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Griffith, J. F., & van der Heijden, R. A. (2022) · Skeletal Radiology · doi:10.1007/s00256-022-04202-6 · Cited by 6 · see citing works
Rekrutierung osteogener Zellen an den Ort der Knochenbildung während Entwicklung und Frakturheilung
Böhm, A.-M., Dirckx, N., & Maes, C. (2016) · Zeitschrift für Rheumatologie · doi:10.1007/s00393-016-0065-7 · Cited by 6 · see citing works
Søe, K., Plesner, T., Jakobsen, E. H., Hansen, C. T., Jørgensen, H. B., & Delaissé, J. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1897 · Cited by 6 · see citing works
Lin, B., Huang, J.-F., Liu, X., Ma, X., Liu, X., Lu, Y., Zhou, Y., Guo, F., & Feng, T. (2017) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2017.04.018 · Cited by 6 · see citing works
Kahla, R. B., & Barkaoui, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-88467-9.00002-3 · Cited by 5 · see citing works
Beck-Broichsitter, B. E., Becker, S. T., Seitz, H., Wiltfang, J., & Warnke, P. H. (2017) · International Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.ijom.2017.01.010 · Cited by 5 · see citing works
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Martin, T. J. (2017) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3282 · Cited by 5 · see citing works
Lafage‐Proust, M., & Roche, B. (2018) · Primer on the metabolic bone diseases and disorders of mineral metabolism · doi:10.1002/9781119266594.ch127 · Cited by 5 · see citing works
Sekita, A., Matsugaki, A., & Nakano, T. (2016) · MATERIALS TRANSACTIONS · doi:10.2320/matertrans.m2016383 · Cited by 4 · see citing works
Gabusi, E., Manferdini, C., Paolella, F., Gambari, L., Kon, E., Filardo, G., Mariani, E., & Lisignoli, G. (2017) · BioMed Research International · doi:10.1155/2017/9036305 · Cited by 3 · see citing works
Cell Interaction and Mechanobiological Modeling of Bone Remodeling Process
Kahla, R. B., Barkaoui, A., Salah, F. Z. B., & Chafra, M. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.95045 · Cited by 3 · see citing works
Ischemic Stroke Reduces Bone Perfusion and Alters Osteovascular StructurePreprint
Hanne, N. J., Steward, A. J., Geeroms, C., Easter, E. D., Thornburg, H. L., Kerckhofs, G., Parac‐Vogt, T. N., Sheng, H., & Cole, J. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/729632 · Cited by 3 · see citing works
Miller, S. C. (2025) · The Anatomical Record · doi:10.1002/ar.25641 · Cited by 2 · see citing works
Ischemic stroke reduces bone perfusion and alters osteovascular structure
Hanne, N. J., Steward, A. J., Geeroms, C., Easter, E. D., Gensch, H. T., Kerckhofs, G., Parac‐Vogt, T. N., Sheng, H., & Cole, J. H. (2025) · Bone Reports · doi:10.1016/j.bonr.2025.101824 · Cited by 2 · see citing works
Recruitment of osteogenic cells to bone formation sites during development and fracture repair
Böhm, A.-M., Dirckx, N., & Maes, C. (2016) · Zeitschrift für Rheumatologie · doi:10.1007/s00393-015-1574-5 · Cited by 2 · see citing works
Multicolor Immunofluorescence Staining of Paraffin-Embedded Human Bone Marrow Sections
Panvini, F. M., Pacini, S., Mazzoni, S., & Méndez‐Ferrer, S. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1425-9_10 · Cited by 2 · see citing works
Mechanism Reversing Bone Resorption to Formation During Bone Remodeling
Delaissé, J., Andersen, T. L., Kristensen, H. B., & Jensen, P. R. (2021) · Springer eBooks · doi:10.1007/978-981-16-5613-2_6 · Cited by 2 · see citing works
Self-citationNovel Therapy for Bone Regeneration in Large Segmental Defects
Kacena, M. A., Anglen, J. O., & Chu, T. G. (2014) · doi:10.21236/ada612706 · Cited by 1 · see citing works
Hanne, N. J., Steward, A. J., Cox, J. M., Easter, E. D., Thornburg, H. L., Sessions, M. R., Pinnamaraju, S. V., & Cole, J. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/729624 · Cited by 1 · see citing works
Visualizing Normal and Malignant Human Stem and Progenitor Cells in Histological Sections
Kristensen, H. B., Patriarca, A., & Delaissé, J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.11159-6 · Cited by 1 · see citing works
Self-citationde Moraes, P. H., Olate, S. M., Lauria, A., Asprino, L., de Moraes, M., & Ricardo, J. R. D. S. (2015)
Sekita, A., Matsugaki, A., Ozasa, R., & Nakano, T. (2017) · Journal of the Japan Institute of Metals and Materials · doi:10.2320/jinstmet.j2017005
The hypoxia signaling pathway in the skeleton
Schipani, E., Sabini, E., & Giaccia, A. J. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-13683-2.00005-0
- Authors
- Kristensen, H. B., Andersen, T. L., Marcussen, N., Rolighed, L., & Delaisse, J.-M.
- Affiliations
- Department of Clinical Cell Biology, Lillebaelt/Vejle Hospital, IRS, University of Southern Denmark, Vejle, Denmark
- University of Southern Denmark (DK)
- Odense University Hospital (DK)
- Aarhus University Hospital (DK)
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-09-18
- Volume
- 28
- Issue
- 3
- Pages
- 574-585
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- OpenAlex
- W2158079848
- Cited by
- 97
- References
- 54
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 5 · 2022: 4 · 2021: 11 · 2020: 13 · 2019: 10 · 2018: 4 · 2017: 8 · 2016: 7 · 2015: 10 · 2014: 9 · 2013: 11
- FWCI
- 3.85
- Type
- journal article
- Language
- en
- Open access
- closed
- 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)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion)
- 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, trabecular bone, bone vascularization, capillaries, osteoblast progenitors, pericytes, CD34, smooth muscle actin, Ki-67, CD56, bone marrow, bone formation
- MeSH terms
- Adult, Bone and Bones, Capillaries, Humans, Immunohistochemistry, Microscopy, Electron
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