Structural and functional changes in the alveolar bone osteoclasts of estrogen‐treated rats
Open accessAbstract
This study investigated structural and functional features of apoptotic alveolar bone osteoclasts in estrogen‐treated rats. For this purpose, 15 female rats 22 days old were divided into three groups: Estrogen (EG), Sham (SG) and Control (CG). The rats of EG received daily intramuscular injection of estrogen for 7 days. The SG received only the oil vehicle. Maxillary fragments containing alveolar bone were removed and processed for light and transmission electron microscopy. Area (OcA) and number of nuclei (OcN) and bone resorption surface per TRAP‐positive osteoclasts (BS/OC) were obtained. Vimentin, caspase‐3 and MMP‐9 immunoreactions, TUNEL/TRAP and MMP‐9/TUNEL combined reactions were performed. In EG, the OcA, OcN and BS/Oc were reduced. Moreover, osteoclasts showed cytoplasm immunolabelled by caspase‐3 and a different pattern of vimentin expression in comparison with CG and SG. MMP‐9 expression was not affected by estrogen and the TUNEL‐positive osteoclasts were MMP‐9‐immunolabelled. In EG, ultrastructural images showed that apoptotic osteoclasts did not exhibit ruffled borders or clear zones and were shedding mononucleated portions. TRAP‐positive structures containing irregular and dense chromatin were partially surrounded by fibroblast‐like cells. In conclusion, the reduction in the BS/Oc may be due to reduction in OcA and OcN; these effects seem to be related to vimentin disarrangement rather than to an interference of estrogen with osteoclast MMP‐9 expression. Osteoclast apoptosis involves caspase‐3 activity and vimentin degradation; these cells release portions containing one apoptotic nucleus and, subsequently, undergo fragmentation, giving rise to apoptotic bodies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Estrogen suppresses osteoclast formation and activity.
“The estrogen suppresses the osteoclast formation and activity as well as induces osteoclast apoptosis [16, 76, 104, 154].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [104]
Estrogen induces osteoclast apoptosis.
“The estrogen suppresses the osteoclast formation and activity as well as induces osteoclast apoptosis [16, 76, 104, 154].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [104]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
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
How Matrix Metalloproteinases Regulate Cell Behavior
Sternlicht, M. D., & Werb, Z. (2001) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.17.1.463 · Cited by 3,959 · 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
Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis
Byun, Y., Chen, F., Chang, R., Trivedi, M., Green, K. J., & Cryns, V. L. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400840 · Cited by 339 · see citing works
Bord, S., Ireland, D. C., Beavan, S. R., & Compston, J. E. (2003) · Bone · doi:10.1016/s8756-3282(02)00953-5 · Cited by 333 · see citing works
The apoptosis cascade — morphological and immunohistochemical methods for its visualization
Huppertz, B., Frank, H., & Kaufmann, P. (1999) · Anatomy and Embryology · doi:10.1007/s004290050254 · Cited by 325 · see citing works
αvβ3and macrophage colony‐stimulating factor: partners in osteoclast biology
Ross, F. P., & Teitelbaum, S. L. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00331.x · Cited by 303 · 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
Rogers, A., Saleh, G., Hannon, R. A., Greenfield, D., & Eastell, R. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020396 · Cited by 200 · see citing works
Local RANKL gene transfer to the periodontal tissue accelerates orthodontic tooth movement
Kanzaki, H., Chiba, M., Arai, K., Takahashi, I., Haruyama, N., Nishimura, M., & Mitani, H. (2006) · Gene Therapy · doi:10.1038/sj.gt.3302707 · Cited by 192 · 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
Characterization of osteoclasts derived from CD14+ monocytes isolated from peripheral blood
Sørensen, M. G., Henriksen, K., Schaller, S., Henriksen, D. B., Nielsen, F. C., Dziegiel, M. H., & Karsdal, M. A. (2006) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-006-0725-9 · Cited by 143 · 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
Lees, R. L., Sabharwal, V. K., & Heersche, J. N. M. (2001) · Bone · doi:10.1016/s8756-3282(00)00433-6 · Cited by 113 · see citing works
Ito, M., Amizuka, N., Nakajima, T., & Ozawa, H. (1999) · Bone · doi:10.1016/s8756-3282(99)00197-0 · Cited by 90 · see citing works
DEDD regulates degradation of intermediate filaments during apoptosis
Lee, J. C., Schickling, O., Stegh, A. H., Oshima, R. G., Dinsdale, D. D., Cohen, G. M., & Peter, M. E. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200112124 · 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
Akisaka, T., Yoshida, H., Suzuki, R., & Takama, K. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0552-x · Cited by 63 · see citing works
Miller, S. C., & Bowman, B. M. (2007) · The Anatomical Record · doi:10.1002/ar.20403 · Cited by 60 · see citing works
Alam, M. S., Ohsako, S., Tay, T. W., et al. (2010) · Anatomia Histologia Embryologia · doi:10.1111/j.1439-0264.2010.00993.x · Cited by 57 · see citing works
Cerri, P. S., Boabaid, F., & Katchburian, E. (2003) · Journal of Periodontal Research · doi:10.1034/j.1600-0765.2003.02006.x · Cited by 57 · see citing works
Self-citationEstradiol inhibits adhesion and promotes apoptosis in murine osteoclasts in vitro
Saintier, D., Khanine, V., Uzan, B., Ea, H., de Vernejoul, M. C., & Cohen-Solal, M. E. (2006) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2006.01.009 · Cited by 56 · see citing works
Liu, C.-C., & Howard, G. A. (1991) · The Anatomical Record · doi:10.1002/ar.1092290211 · Cited by 50 · see citing works
Teitelbaum, S. L. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1346.017 · Cited by 49 · 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-citationActivity‐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
THE EFFECTS OF HORMONES ON BONE IN GROWING RATS
Tapp, E. (1966) · Journal of Bone and Joint Surgery - British Volume · doi:10.1302/0301-620x.48b3.526 · Cited by 43 · see citing works
Liu, B.-Y., Wu, P., Bringhurst, F. R., & Wang, J. (2002) · Endocrinology · doi:10.1210/endo.143.2.8614 · Cited by 42 · see citing works
Decrease 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-citationCruzoé‐Souza, M., Sasso‐Cerri, E., & Cerri, P. S. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2009.01158.x · Cited by 38 · see citing works
Self-citationDifferences in regulation of pHi in large (≥10 nuclei) and small (≤5 nuclei) osteoclasts
Lees, R. L., & Heersche, J. N. M. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.3.c751 · Cited by 38 · see citing works
Cerri, P. S., Pereira‐Júnior, J. A., Biselli, N. B., & Sasso‐Cerri, E. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01249.x · Cited by 34 · see citing works
Self-citationEffects of oestrogen deficiency on osteoclastogenesis in the rat periodontium
Kawamoto, S., Ejiri, S., Nagaoka, E., & Ozawa, H. (2002) · Archives of Oral Biology · doi:10.1016/s0003-9969(01)00086-3 · Cited by 33 · 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
Hu, Y., Ek‐Rylander, B., Karlström, E., Wendel, M., & Andersson, G. N. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.11.008 · Cited by 27 · see citing works
Further investigations concerning the influence of estrogen on skeletal tissues
Silberberg, M., & Silberberg, R. (1941) · American Journal of Anatomy · doi:10.1002/aja.1000690206 · Cited by 26 · 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
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-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Rhoades RA, Tanner GA. Medical Physiology. Boston: Little, Brown and Company; 1995. [Google Scholar]
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-citationCimetidine Reduces Alveolar Bone Loss in Induced Periodontitis in Rat Molars
Longhini, R., Aparecida de Oliveira, P., Sasso‐Cerri, E., & Cerri, P. S. (2014) · Journal of Periodontology · doi:10.1902/jop.2013.130453 · Cited by 35 · 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
- Faloni, A. P. D. S., Sasso‐Cerri, E., Rocha, F. R. G., Katchburian, E., & Cerri, P. S.
- Affiliations
- Universidade Federal de São Paulo (BR)
- Universidade Estadual Paulista (Unesp) (BR)
- Corresponding author
- Cerri, Paulo Sérgio
- Venue
- Journal of Anatomy
- Publisher
- Wiley
- Published
- 2011-11-16
- Volume
- 220
- Issue
- 1
- Pages
- 77-85
- ISSN
- 0021-8782 (ISSN-L)
- 1469-7580
- PMC
- PMC3248665
- OpenAlex
- W1522615306
- Cited by
- 31
- References
- 38
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 2 · 2018: 3 · 2016: 1 · 2015: 3 · 2014: 1 · 2013: 3 · 2012: 1
- FWCI
- 0.65
- 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)
- Americanae (AECID Library) (submittedVersion)
- UNESP Institutional Repository (São Paulo State University) (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- 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
- osteoclast apoptosis, estrogen, alveolar bone, bone resorption, vimentin, caspase-3, MMP-9, TUNEL, osteoclast ultrastructure, apoptotic bodies, ruffled border, female rats
- MeSH terms
- Alveolar Process, Animals, Bone Resorption, Cell Nucleus, Estrogens, Female, Injections, Intramuscular, Osteoclasts, Vimentin, Rats, Sprague-Dawley, Apoptosis, Matrix Metalloproteinase 9, Microscopy, Electron, Transmission, Rats, Caspase 3
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
