Effects of oestrogen deficiency on osteoclastogenesis in the rat periodontium
Abstract
This study was designed to investigate quantitative changes in osteoclast generation in rat periodontium following ovariectomy. Wistar rats, aged 9 weeks, were subjected to either ovariectomy (OVX) or sham surgery. Osmotic pumps were implanted in 24 rats and either 17beta-oestradiol or vehicle solution were infused continuously. The rats were assigned to one of the following groups: (1) OVX+vehicle; (2) sham+vehicle; or (3) OVX+ 17beta-oestradiol. On the days 7 and 14 after surgery, four rats in each group were killed. Mandibles were demineralized and embedded in paraffin. Frontal sections of alveolar bone in the region of the first molar were cut for enzyme histochemistry and immunohistochemistry. On day 7, there was no significant difference in the number of tartrate-resistant acid phosphatase (TRAP)-positive cells located on bone surfaces in either group. However, the number of TRAP-positive mononuclear cells that were separated from the bone surface was significantly higher in group 1 than in groups 2 and 3. On the day 14, the number of TRAP-positive cells in group 1, which were attached to the bone surface, was significantly higher than had been apparent on day 7. There were also significant increases in the number of nuclei of TRAP-positive cells attached to the bone in group 1 compared with groups 2 and 3 on day 14. These findings demonstrate that oestrogen deficiency induces of osteoclastogenesis in the rat periodontium and that quantitative changes in osteoclastogenesis could be prevented by E2 infusion.
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Estrogen stimulates osteoblasts and osteocytes to produce osteoprotegerin (OPG), which inhibits osteoclastogenesis.
“Moreover, estrogen stimulates these bone cells to produce osteoprotegerin (OPG), a decoy receptor of RANK in osteoclast, thus inhibiting osteoclastogenesis [19, 155–159].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [156]
Cites
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 · see citing works
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 · see citing works
Hofbauer, L. C., Khosla, S., Dunstan, C. R., Lacey, D. L., Boyle, W. J., & Riggs, B. L. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.1.2 · Cited by 1,167 · see citing works
Bone acid phosphatase: Tartrate-resistant acid phosphatase as a marker of osteoclast function
Minkin, C. (1982) · Calcified Tissue International · doi:10.1007/bf02411252 · Cited by 992 · see citing works
Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis
Pacifici, R. (1996) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650110802 · Cited by 741 · see citing works
Cathepsin K, but Not Cathepsins B, L, or S, Is Abundantly Expressed in Human Osteoclasts
Drake, F. H., Dodds, R. A., James, I. E., Connor, J. R., Debouck, C. M., Richardson, S. B., Lee-Rykaczewski, E., Coleman, L., Rieman, D. J., Barthlow, R., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.21.12511 · Cited by 721 · see citing works
Udagawa, N., Takahashi, N., Akatsu, T., Sasaki, T., Yamaguchi, A., KODAMA, H., Martin, T. J., & Suda, T. (1989) · Endocrinology · doi:10.1210/endo-125-4-1805 · Cited by 492 · see citing works
Dynamic histomorphometry of alveolar bone remodeling in the adult rat
Vignery, A., & Baron, R. (1980) · The Anatomical Record · doi:10.1002/ar.1091960210 · Cited by 260 · see citing works
Tsukii, K., Shima, N., Mochizuki, S.-I., Yamaguchi, K., Kinosaki, M., Yano, K., Shibata, O., Udagawa, N., Yasuda, H., Suda, T., et al. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.8610 · Cited by 237 · see citing works
Generation of osteoclasts from isolated hematopoietic progenitor cells
Kurihara, N., Suda, T., Miura, Y., Nakauchi, H., Kodama, H., Hiura, K., Hakeda, Y., & Kumegawa, M. (1989) · Blood · doi:10.1182/blood.v74.4.1295.1295 · Cited by 202 · see citing works
Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine
Krall, E. A., García, R. I., & Dawson‐Hughes, B. (1996) · Calcified Tissue International · doi:10.1007/bf00369206 · Cited by 201 · see citing works
Localization of cathepsin K in human osteoclasts by in situ hybridization and immunohistochemistry
Littlewood-Evans, A. J., Kokubo, T., Ishibashi, O., Inaoka, T., Wlodarski, B., Gallagher, J. A., & Bilbe, G. (1997) · Bone · doi:10.1016/s8756-3282(96)00351-1 · Cited by 190 · see citing works
Marks, S. C. (1983) · Journal of Oral Pathology and Medicine · doi:10.1111/j.1600-0714.1983.tb00337.x · Cited by 172 · see citing works
Kribbs, P. J., Smith, D. E., & Chesnut, C. H. (1983) · Journal of Prosthetic Dentistry · doi:10.1016/0022-3913(83)90215-9 · Cited by 167 · see citing works
Roles of osteoclasts in alveolar bone remodeling
Omi, M., & Mishina, Y. M. (2022) · genesis · doi:10.1002/dvg.23490 · Cited by 139 · see citing works
Postmenopausal Estrogen Replacement and Tooth Retention
Krall, E. A., Dawson‐Hughes, B., Hannan, M. T., Wilson, P. W. F., & Kiel, D. P. (1997) · The American Journal of Medicine · doi:10.1016/s0002-9343(97)00045-4 · Cited by 132 · see citing works
Sminia, T., & Dijkstra, C. D. (1986) · Calcified Tissue International · doi:10.1007/bf02555216 · Cited by 87 · see citing works
Ejiri, S. (1983) · Archivum histologicum japonicum · doi:10.1679/aohc.46.533 · Cited by 82 · see citing works
Self-citationOvariectomy decreases the bone area fraction of the rat mandible
Elovic, R. P., Hipp, J. A., & Hayes, W. C. (1995) · Calcified Tissue International · doi:10.1007/bf00318051 · Cited by 68 · see citing works
Changes of cancellous bone mass in rat mandibular condyle following ovariectomy
Tanaka, M. W., Ejiri, S., Nakajima, M., Kohno, S., & Ozawa, H. (1999) · Bone · doi:10.1016/s8756-3282(99)00179-9 · Cited by 61 · see citing works
Self-citationShevde, N., & Pike, J. (1996) · Blood · doi:10.1182/blood.v87.7.2683.bloodjournal8772683 · Cited by 51 · see citing works
Most, W., van der Wee-Pals, L. J. A., EDERVEEN, A. G. H., Papapoulos, S. E., & Löwik, C. W. G. M. (1997) · Bone · doi:10.1016/s8756-3282(96)00309-2 · Cited by 49 · see citing works
The knive-edge tendency in mandibular residual ridges in women
Nishimura, I., Hosokawa, R., & Atwood, D. A. (1992) · Journal of Prosthetic Dentistry · doi:10.1016/0022-3913(92)90592-x · Cited by 42 · see citing works
Ikeda, T., Yamaguchi, A., Yokose, S., Nagai, Y., Yamato, H., Nakamura, T., Tsurukami, H., Tanizawa, T., & Yoshiki, S. (1996) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650110609 · Cited by 39 · see citing works
Effect of ovariectomy on the local residual ridge remodeling
Jahangiri, L., Kim, A., & Nishimura, I. (1997) · Journal of Prosthetic Dentistry · doi:10.1016/s0022-3913(97)70169-0 · Cited by 31 · see citing works
Comparative bone morphometric analysis of mandibles and 2nd metacarpals
von Wowern, N., & Stoltze, K. (1979) · European Journal Of Oral Sciences · doi:10.1111/j.1600-0722.1979.tb00694.x · Cited by 30 · see citing works
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Florencio-Silva, R., Sasso, G. R. D. S., Sasso-Cerri, E., Simões, M. J., & Cerri, P. S. (2015) · BioMed Research International · doi:10.1155/2015/421746 · Cited by 2,044 · see citing works
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Johnston, B. D., & Ward, W. E. (2015) · BioMed Research International · doi:10.1155/2015/635023 · Cited by 113 · see citing works
Garcia, V. G., Longo, M., Gualberto, E. C., Bosco, Á. F., Nagata, M. J. H., Ervolino, E., & Theodoro, L. H. (2013) · Journal of Periodontal Research · doi:10.1111/jre.12138 · Cited by 94 · see citing works
Hatakeyama, J., Sreenath, T., Hatakeyama, Y., Thyagarajan, T., Shum, L., Gibson, C. W., Wright, J. T., & Kulkarni, A. B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306284200 · Cited by 94 · see citing works
Estrogen Modulates Cytokine Expression in Human Periodontal Ligament Cells
Shu, L., Guan, S., Fu, S., Guo, T., Cao, M., & Ding, Y. (2008) · Journal of Dental Research · doi:10.1177/154405910808700214 · Cited by 82 · see citing works
Liu, S., Cheng, Y., Wang-min, X., & Bian, Z. (2010) · Journal of Endodontics · doi:10.1016/j.joen.2010.01.011 · Cited by 71 · see citing works
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Nardone, V., D’Asta, F., & Brandi, M. L. (2014) · Clinics · doi:10.6061/clinics/2014(06)12 · Cited by 62 · see citing works
Wang, Y., Yan, M., Yu, Y., Wu, J., Yu, J., & Fan, Z. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1604-z · Cited by 59 · see citing works
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Liu, S., Cheng, Y., Fan, M., Chen, D., & Bian, Z. (2010) · Journal of Dental Research · doi:10.1177/0022034509358822 · Cited by 52 · see citing works
Implant surface roughness influences osteoclast proliferation and differentiation
Marchisio, M., Carmine, M. D., Pagone, R., Piattelli, A., & Miscia, S. (2005) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.30287 · Cited by 48 · see citing works
Garcia, V. G., Gualberto, E. C., Fernandes, L. A., Bosco, Á. F., Nagata, M. J. H., Casatti, C. A., Ervolino, E., & Theodoro, L. H. (2012) · Journal of Periodontology · doi:10.1902/jop.2012.120163 · Cited by 41 · see citing works
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Pizzo, G., Guiglia, R., Licata, M. E., Pizzo, I., Davis, J., & Giuliana, G. (2011) · Medical Science Monitor · doi:10.12659/msm.881700 · Cited by 38 · see citing works
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Chen, F., Wang, K.-C., & Huang, J. (2009) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/s1028-4559(09)60323-5 · Cited by 31 · see citing works
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Liu, Z., Liu, L., Chen, K., Xie, Q., Zhang, B., & Li, Y. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3891 · Cited by 20 · see citing works
Gopalakrishnan, V., Arunakaran, J., Aruldhas, M. M., & Srinivasan, N. (2006) · Biochemistry and Cell Biology · doi:10.1139/o06-066 · Cited by 19 · see citing works
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Wu, Y., Liu, F., Zhang, X., & Shu, L. (2014) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2014.07.002 · Cited by 19 · see citing works
Oestrogen inhibits osteoclast formation induced by periodontal ligament fibroblasts
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Machado, G. J. R., Dias, S. M. D., Bosco, Á. F., Okamoto, T., de Castro, J. C. B., & Dornelles, R. C. M. (2010) · Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.joms.2010.04.018 · Cited by 14 · see citing works
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Said, F., Ghoul, S., Khemiss, F., Ayeb, H. E., Saïdane, D., Berdal, A., & Ruhin, B. (2011) · Journal of Periodontology · doi:10.1902/jop.2011.110242 · Cited by 10 · see citing works
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Nebel, D., Bratthall, G., Warfvinge, G., & Nilsson, B. (2008) · Acta Odontologica Scandinavica · doi:10.1080/00016350802443474 · Cited by 7 · see citing works
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Tsolakis, A. I., Khaldi, L., Bitsanis, I., Alexandridis, C., Triantafyllou, Α., Spyropoulos, M. N., & Dontas, I. A. (2018) · Europe PMC (PubMed Central) · Cited by 3 · see citing works
Johnston, B. D. (2015) · Brock University Digital Repository (Brock University)
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- Authors
- Kawamoto, S., Ejiri, S., Nagaoka, E., & Ozawa, H.
- Affiliations
- Kagoshima University (JP)
- Niigata University (JP)
- Matsumoto Dental University (JP)
- Corresponding author
- Kawamoto, S
- ORCID
- Ozawa, H
- Venue
- Archives of Oral Biology
- Publisher
- Elsevier BV
- Published
- 2002-01
- Volume
- 47
- Issue
- 1
- Pages
- 67-73
- ISSN
- 0003-9969 (ISSN-L)
- OpenAlex
- W2040784057
- Cited by
- 33
- References
- 26
- Citations by year
- 2021: 1 · 2020: 1 · 2018: 1 · 2015: 4 · 2014: 5 · 2013: 2 · 2012: 1
- FWCI
- 0.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Archives of Oral Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (10771091)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Keywords
- estrogen deficiency, osteoclastogenesis, periodontium, ovariectomy, estradiol, alveolar bone, tartrate-resistant acid phosphatase, bone resorption, estrogen replacement therapy
- MeSH terms
- Tartrate-Resistant Acid Phosphatase, Acid Phosphatase, Alveolar Process, Animals, Bone Resorption, Carrier Proteins, Cathepsins, Cell Adhesion, Cell Count, Cell Nucleus, Cysteine Endopeptidases, Estradiol, Estrogens, Female, Follow-Up Studies, Immunohistochemistry, Infusion Pumps, Isoenzymes, Ligands, Mandible, Membrane Glycoproteins, Osteoclasts, Ovariectomy, Periodontium, Statistics as Topic, Tumor Necrosis Factor-alpha, Pharmaceutical Vehicles, Biomarkers, NF-kappa B, Rats, Wistar, Rats, RANK Ligand, Cathepsin K
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