Immunohistochemical detection of estrogen receptor β in alveolar bone cells of estradiol‐treated female rats: possible direct action of estrogen on osteoclast life span
Open accessAbstract
The role of estrogen in bone resorption has been specifically related to the effect of estrogen on the signalling pathway that inhibits the formation of osteoclasts. However, osteoclast apoptosis and a significant reduction in the number of these cells have been observed in the alveolar bone of female rats treated with estradiol. In the present study, the expression of estrogen receptor β (ERβ) in the cells of alveolar bone was evaluated in estradiol‐treated and ‐untreated female rats. In order to test the possible direct action of estrogen on osteoclasts, the relationship between apoptosis and ERβ expression in these cells was also analysed. The animals received estradiol for 14 days and the alveolar bone fragments were embedded in paraffin for the quantification of tartrate‐resistant acid phosphatase‐positive osteoclasts. The expression of ERβ and apoptosis in the osteoclasts were evaluated by ERβ immunohistochemistry and Terminal deoxynucleotidyl transferase‐mediated dUTP Nick‐End Labelling (TUNEL) methods, respectively. To confirm osteoclast death by apoptosis, these cells were analysed under transmission electron microscopy. Some osteoclasts from estradiol‐treated animals were found to be undergoing apoptosis and the number of tartrate‐resistant acid phosphatase‐positive osteoclasts was significantly reduced. ERβ immunolabelling was observed in the cytoplasm and nuclei of active osteoblasts, osteocytes and osteoclasts in both groups, suggesting a direct participation of estrogen on alveolar bone cells. However, following estradiol treatment, a strong ERβ immunolabelling was often observed in the TUNEL‐positive osteoclasts. Therefore, these results indicate that, in addition to the other signalling pathway, the reduction of alveolar bone resorption is also related to a direct action of estrogen on osteoclasts, promoting apoptosis in these cells, via ERβ.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Enhanced immunoexpression observed in TUNEL-positive osteoclasts indicates that estrogen participates in the control of osteoclast life span directly by estrogen receptors.
“Moreover, the enhanced immunoexpression observed in TUNEL-positive osteoclasts indicates that estrogen participates in the control of osteoclast life span directly by estrogen receptors [163].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [163]
Osteoclast is a direct target for estrogen.
“Moreover, it has been shown that osteoclast is a direct target for estrogen [163, 164].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [163]
Cites
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444 · see citing works
Molecular basis of agonism and antagonism in the oestrogen receptor
Brzozowski, A. M., Pike, A. C. W., Dauter, Z., Hubbard, R. E., Bonn, T., Engström, O., Öhman, L., Greene, G. L., Gustafsson, J.-Å., & Carlquist, M. (1997) · Nature · doi:10.1038/39645 · Cited by 3,355 · see citing works
Mechanisms of estrogen action.
Nilsson, S., Mäkelä, S., Treuter, E., Tujague, M., Thomsen, J., Andersson, G., Enmark, E., Pettersson, K., Warner, M., & Gustafsson, J.-Å. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.4.1535 · Cited by 2,059 · see citing works
Estrogen promotes apoptosis of murine osteoclasts mediated by TGF–β
Hughes, D. E., Dai, A., Tiffee, J. C., Li, H. H., Mundy, G. R., & Boyce, B. F. (1996) · Nature Medicine · doi:10.1038/nm1096-1132 · Cited by 813 · cited 2× · see citing works
“In-vivo (Hughes et al. 1996; Faloni et al. 2007) and in-vitro (Kameda et al. 1997; Stern, 2007) studies have demonstrated that estrogen induces osteoclast apoptosis and this process of cell death has been related, at least in part, to the reduction of the osteoclast number in the alveolar bone of…”
BackgroundJensen, E. V., & DeSombre, E. R. (1973) · Science · doi:10.1126/science.182.4108.126 · Cited by 756 · see citing works
Integration of the extranuclear and nuclear actions of estrogen
Levin, E. R. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0390 · Cited by 708 · see citing works
Role of receptor activator of nuclear factor-κB ligand and osteoprotegerin in bone cell biology
Hofbauer, L. C., & Heufelder, A. E. (2001) · Journal of Molecular Medicine · doi:10.1007/s001090100226 · Cited by 586 · see citing works
Manolagas, S. C. (2002) · Recent Progress in Hormone Research · doi:10.1210/rp.57.1.385 · Cited by 523 · see citing works
Estrogen Inhibits Bone Resorption by Directly Inducing Apoptosis of the Bone-resorbing Osteoclasts
Kameda, T., Mano, H., Yuasa, T., Mori, Y., Miyazawa, K., Shiokawa, M., Nakamaru, Y., 広井, 恵., Hiura, K., Kameda, A., et al. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.4.489 · Cited by 519 · see citing works
Mitochondrial localization of estrogen receptor β
Yang, S.-H., Liu, R., Perez, E., Wen, Y., Stevens, S. M., Valencia, T. G., Brun‐Zinkernagel, A., Prókai, L., Will, Y., Dykens, J. A., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306948101 · Cited by 501 · see citing works
The mechanisms of estrogen regulation of bone resorption
Riggs, B. L. (2000) · Journal of Clinical Investigation · doi:10.1172/jci11468 · Cited by 447 · see citing works
Reversal of Bone Loss in Mice by Nongenotropic Signaling of Sex Steroids
Kousteni, S., Chen, J.-R., Bellido, T., Han, L., Ali, A. A., O'Brien, C. A., Plotkin, L., Fu, Q., Mancino, A. T., Wen, Y., et al. (2002) · Science · doi:10.1126/science.1074935 · Cited by 420 · see citing works
The Death of Osteocytes via Apoptosis Accompanies Estrogen Withdrawal in Human Bone
Tomkinson, A., REEVE, J., Shaw, R. W., & Noble, B. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.9.4200 · Cited by 417 · see citing works
Tracking the estrogen receptor in neurons: Implications for estrogen-induced synapse formation
McEwen, B. S., Akama, K. T., Alves, S. E., Brake, W. G., Bulloch, K., Lee, S. D., Li, C., Yuen, G. S., & Milner, T. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.121146898 · Cited by 311 · see citing works
Estrogen Receptors α and β Are Differentially Expressed in Developing Human Bone1
Bord, S., Horner, A. A., Beavan, S. R., & Compston, J. E. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.5.7513 · Cited by 300 · see citing works
Mitochondrial localization of ERα and ERβ in human MCF7 cells
Chen, J. Q., Delannoy, M., Cooke, C., & Yager, J. D. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00508.2003 · Cited by 272 · see citing works
Interaction between osteoblast and osteoclast: impact in bone disease.
Phan, T. C. A., Xu, J., & Zheng, M. (2004) · PubMed · doi:10.14670/hh-19.1325 · Cited by 207 · see citing works
Michael, H., Härkönen, P. L., Väänänen, H. K., & Hentunen, T. A. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.050803 · Cited by 200 · see citing works
Mechanism of osteoclast mediated bone resorption—rationale for the design of new therapeutics
VAANANEN, K. (2005) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2004.12.018 · Cited by 176 · see citing works
Chen, J.-Q., Yager, J., & Russo, J. (2005) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2005.08.001 · Cited by 173 · see citing works
Localization of Estrogen Receptor β Protein Expression in Adult Human Bone
Braidman, I. P., Hainey, L., Batra, G., Selby, P. L., Saunders, P. T. K., & Hoyland, J. A. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.2.214 · Cited by 172 · see citing works
Expression and Localization of Estrogen Receptor-β in Murine and Human Bone
Vidal, O., Kindblom, L., & Ohlsson, C. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.6.923 · Cited by 167 · see citing works
Regulation of apoptosis in osteoclasts and osteoblastic cells
Xing, L., & Boyce, B. F. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.11.072 · Cited by 163 · see citing works
Khurana, S., Ranmal, S. A., & Ben‐Jonathan, N. (2000) · Endocrinology · doi:10.1210/endo.141.12.7823 · Cited by 162 · see citing works
Estrogen actions on mitochondria—Physiological and pathological implications
Simpkins, J. W., Yang, S., Sarkar, S. N., & Pearce, V. P. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.04.013 · Cited by 158 · see citing works
Parikka, V., Lehenkari, P. P., Sassi, M.-L., Halleen, J. M., Risteli, J., Härkönen, P. L., & Väänänen, H. K. (2001) · Endocrinology · doi:10.1210/endo.142.12.8533 · Cited by 118 · see citing works
Estrogen-induced Spermatogenic Cell Apoptosis Occurs via the Mitochondrial Pathway
Mishra, D. P., & Shaha, C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405970200 · Cited by 117 · see citing works
Apoptosis in bone physiology and disease.
Hughes, D. E., & Boyce, B. F. (1997) · Molecular Pathology · doi:10.1136/mp.50.3.132 · Cited by 108 · see citing works
Mitochondrial estrogen receptors – new insights into specific functions
Yager, J. D., & Chen, J. Q. (2007) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2007.02.006 · Cited by 108 · see citing works
Estrogen Receptors and Are Differentially Expressed in Developing Human Bone
Bord, S. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.5.2309 · Cited by 101 · see citing works
Cammarata, P. R., Chu, S., Moor, A. N., Wang, Z., Yang, S., & Simpkins, J. W. (2004) · Experimental Eye Research · doi:10.1016/j.exer.2003.09.027 · Cited by 82 · see citing works
17 beta-estradiol stimulates cancellous bone formation in female rats.
Chow, J. W., Lean, J. M., & Chambers, T. J. (1992) · Endocrinology · doi:10.1210/endo.130.5.1572310 · Cited by 82 · see citing works
Apoptotic bone cells may be engulfed by osteoclasts during alveolar bone resorption in young rats
Boabaid, F., Cerri, P. S., & Katchburian, E. (2001) · Tissue and Cell · doi:10.1054/tice.2001.0179 · Cited by 53 · see citing works
Self-citationLiu, C.-C., & Howard, G. A. (1991) · The Anatomical Record · doi:10.1002/ar.1092290211 · Cited by 50 · see citing works
Sørensen, M. G., Henriksen, K., Dziegiel, M., Tankó, L. B., & Karsdal, M. (2006) · DNA and Cell Biology · doi:10.1089/dna.2006.25.475 · Cited by 48 · see citing works
Osteoblasts engulf apoptotic bodies during alveolar bone formation in the rat maxilla
Cerri, P. S. (2005) · The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology · doi:10.1002/ar.a.20220 · Cited by 45 · see citing works
Self-citationApoptosis in Bone for Tissue Engineering
Bran, G. M., Stern‐Straeter, J., Hörmann, K., Riedel, F., & GOESSLER, U. R. (2008) · Archives of Medical Research · doi:10.1016/j.arcmed.2008.02.007 · Cited by 45 · see citing works
Activity‐induced fiber regeneration in rat soleus muscle
Wanek, L., & Snow, M. H. (2000) · The Anatomical Record · doi:10.1002/(sici)1097-0185(20000201)258:2 · Cited by 43 · see citing works
Tirado, Ò. M., Selva, D. M., Torán, N., et al. (2004) · Journal of Andrology · doi:10.1002/j.1939-4640.2004.tb02762.x · Cited by 40 · see citing works
Apoptosis in the epithelial cells of the rests of Malassez of the periodontium of rat molars
Cerri, P. S., & Katchburian, E. (2005) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2005.00810.x · Cited by 40 · see citing works
Self-citationDecrease in the number and apoptosis of alveolar bone osteoclasts in estrogen‐treated rats
Faloni, A. P. S., Sasso‐Cerri, E., Katchburian, E., & Cerri, P. S. (2007) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2006.00932.x · Cited by 40 · see citing works
Self-citationAlteration of mitochondrial function and cell sensitization to death
Gogvadze, V. G., & Zhivotovsky, B. (2007) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-006-9054-x · Cited by 34 · see citing works
Antiresorptive agents and osteoclast apoptosis
Stern, P. H. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21311 · Cited by 34 · see citing works
Blumer, M. J. F., Longato, S., & Fritsch, H. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00958.x · Cited by 30 · see citing works
Bisphosphonate acts on osteoclasts independent of ruffled borders in osteosclerotic (oc/oc) mice
Ito, M., Amizuka, N., Nakajima, T., & Ozawa, H. (2001) · Bone · doi:10.1016/s8756-3282(01)00429-x · Cited by 28 · see citing works
Apoptosis during the seasonal spermatogenic cycle of Rana catesbeiana
Sasso‐Cerri, E., Cerri, P. S., Freymüller, E. H., et al. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00582.x · Cited by 28 · see citing works
Self-citationPiva, R., Penolazzi, L., Lambertini, E., Giordano, S., & Gambari, R. (2005) · APOPTOSIS · doi:10.1007/s10495-005-0618-8 · Cited by 27 · see citing works
17 beta-estradiol stimulates cancellous bone formation in female rats
Chow, J. W. M. (1992) · Endocrinology · doi:10.1210/en.130.5.3025 · Cited by 26 · see citing works
Tang, X., Meng, H., Han, J., et al. (2007) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2007.01031.x · Cited by 21 · see citing works
Testosterone‐immunopositive primordial germ cells in the testis of the bullfrog, Rana catesbeiana
Sasso‐Cerri, E., Freymüller, E. H., & Miraglia, S. M. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00419.x · Cited by 15 · see citing works
Self-citationStein, G. S., van Wijnen, A. J., Stein, J. L., Lian, J. B., McNeil, S. M., & Pockwinse, S. M. (1999) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(1999)75:32+ · Cited by 9 · see citing works
Eine Neue Theorie über die Blutgerinnung
Fuchs, H. J. (1930) · Journal of Molecular Medicine · doi:10.1007/bf01765180 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells
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
Self-citationExtra-gonadal sites of estrogen biosynthesis and function
Barakat, R., Oakley, O., Kim, H., Jin, J., & Ko, C. J. (2016) · BMB Reports · doi:10.5483/bmbrep.2016.49.9.141 · Cited by 215 · see citing works
Estrogens: Two nuclear receptors, multiple possibilities
Biason-Lauber, A., & Lang-Muritano, M. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111710 · Cited by 49 · see citing works
Structural and functional changes in the alveolar bone osteoclasts of estrogen‐treated rats
Faloni, A. P. D. S., Sasso‐Cerri, E., Rocha, F. R. G., Katchburian, E., & Cerri, P. S. (2012) · Journal of Anatomy · doi:10.1111/j.1469-7580.2011.01449.x · Cited by 31 · see citing works
Self-citationLonghini, R., de Oliveira, P. A., de Souza Faloni, A. P., Sasso‐Cerri, E., & Cerri, P. S. (2013) · Journal of Anatomy · doi:10.1111/joa.12011 · Cited by 23 · see citing works
Self-citation
- Authors
- Cruzoé‐Souza, M., Sasso‐Cerri, E., & Cerri, P. S.
- Affiliations
- Universidade Federal de São Paulo (BR)
- Universidade Estadual Paulista (Unesp) (BR)
- Corresponding author
- Cerri, Paulo S.
- Venue
- Journal of Anatomy
- Publisher
- Wiley
- Published
- 2009-11-17
- Volume
- 215
- Issue
- 6
- Pages
- 673-681
- ISSN
- 0021-8782 (ISSN-L)
- 1469-7580
- PMC
- PMC2796790
- OpenAlex
- W2077065930
- Cited by
- 38
- References
- 52
- Citations by year
- 2025: 5 · 2024: 3 · 2023: 3 · 2022: 1 · 2021: 3 · 2020: 5 · 2018: 2 · 2017: 1 · 2016: 3 · 2015: 3 · 2014: 2 · 2013: 2 · 2012: 1
- FWCI
- 0.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Anatomy (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Acervo Digital da Universidade Estadual Paulista (Universidade Estadual Paulista) (submittedVersion, other-oa)
- Americanae (AECID Library) (submittedVersion, other-oa)
- Americanae (AECID Library) (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação para o Desenvolvimento da UNESP
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Oncology › Bone health and treatments
- Keywords
- estrogen receptor beta, estradiol, osteoclasts, osteoclast apoptosis, alveolar bone, bone resorption, osteoblasts, osteocytes, female rats
- MeSH terms
- Alveolar Process, Animals, Estradiol, Female, Microscopy, Electron, Osteoclasts, Apoptosis, In Situ Nick-End Labeling, Estrogen Receptor beta, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
