Breast cancer cells induce osteolytic bone lesions in vivo through a reduction in osteoblast activity in mice
Bone metastases are severely debilitating and have a significant impact on the quality of life of women with metastatic breast cancer. Treatment options are limited and in order to develop more targeted therapies, improved understanding of the complex mechanisms that lead to bone lesion development...
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Published in | PloS one Vol. 8; no. 9; p. e68103 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
12.09.2013
Public Library of Science (PLoS) |
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Abstract | Bone metastases are severely debilitating and have a significant impact on the quality of life of women with metastatic breast cancer. Treatment options are limited and in order to develop more targeted therapies, improved understanding of the complex mechanisms that lead to bone lesion development are warranted. Interestingly, whilst prostate-derived bone metastases are characterised by mixed or osteoblastic lesions, breast-derived bone metastases are characterised by osteolytic lesions, suggesting unique regulatory patterns. This study aimed to measure the changes in bone formation and bone resorption activity at two time-points (18 and 36 days) during development of the bone lesion following intratibial injection of MDA-MB-231 human breast cancer cells into the left tibiae of Severely Combined Immuno-Deficient (SCID) mice. The contralateral tibia was used as a control. Tibiae were extracted and processed for undecalcified histomorphometric analysis. We provide evidence that the early bone loss observed following exposure to MDA-MB-231 cells was due to a significant reduction in mineral apposition rate, rather than increased levels of bone resorption. This suggests that osteoblast activity was impaired in the presence of breast cancer cells, contrary to previous reports of osteoclast-dependent bone loss. Furthermore mRNA expression of Dickkopf Homolog 1 (DKK-1) and Noggin were confirmed in the MDA-MB-231 cell line, both of which antagonise osteoblast regulatory pathways. The observed bone loss following injection of cancer cells was due to an overall thinning of the trabecular bone struts rather than perforation of the bone tissue matrix (as measured by trabecular width and trabecular separation, respectively), suggesting an opportunity to reverse the cancer-induced bone changes. These novel insights into the mechanisms through which osteolytic bone lesions develop may be important in the development of new treatment strategies for metastatic breast cancer patients. |
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AbstractList | Bone metastases are severely debilitating and have a significant impact on the quality of life of women with metastatic breast cancer. Treatment options are limited and in order to develop more targeted therapies, improved understanding of the complex mechanisms that lead to bone lesion development are warranted. Interestingly, whilst prostate-derived bone metastases are characterised by mixed or osteoblastic lesions, breast-derived bone metastases are characterised by osteolytic lesions, suggesting unique regulatory patterns. This study aimed to measure the changes in bone formation and bone resorption activity at two time-points (18 and 36 days) during development of the bone lesion following intratibial injection of MDA-MB-231 human breast cancer cells into the left tibiae of Severely Combined Immuno-Deficient (SCID) mice. The contralateral tibia was used as a control. Tibiae were extracted and processed for undecalcified histomorphometric analysis. We provide evidence that the early bone loss observed following exposure to MDA-MB-231 cells was due to a significant reduction in mineral apposition rate, rather than increased levels of bone resorption. This suggests that osteoblast activity was impaired in the presence of breast cancer cells, contrary to previous reports of osteoclast-dependent bone loss. Furthermore mRNA expression of Dickkopf Homolog 1 (DKK-1) and Noggin were confirmed in the MDA-MB-231 cell line, both of which antagonise osteoblast regulatory pathways. The observed bone loss following injection of cancer cells was due to an overall thinning of the trabecular bone struts rather than perforation of the bone tissue matrix (as measured by trabecular width and trabecular separation, respectively), suggesting an opportunity to reverse the cancer-induced bone changes. These novel insights into the mechanisms through which osteolytic bone lesions develop may be important in the development of new treatment strategies for metastatic breast cancer patients. |
Audience | Academic |
Author | Gregory, Laura S Choi, Wilson Burke, Leslie Clements, Judith A |
AuthorAffiliation | 1 Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia 2 Skeletal Biology and Forensic Anatomy Research Program, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, Queensland, Australia 3 School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, Queensland, Australia Rutgers - New Jersey Medical School, United States of America |
AuthorAffiliation_xml | – name: 1 Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia – name: 2 Skeletal Biology and Forensic Anatomy Research Program, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, Queensland, Australia – name: Rutgers - New Jersey Medical School, United States of America – name: 3 School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, Queensland, Australia |
Author_xml | – sequence: 1 givenname: Laura S surname: Gregory fullname: Gregory, Laura S organization: Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia ; Skeletal Biology and Forensic Anatomy Research Program, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, Queensland, Australia – sequence: 2 givenname: Wilson surname: Choi fullname: Choi, Wilson – sequence: 3 givenname: Leslie surname: Burke fullname: Burke, Leslie – sequence: 4 givenname: Judith A surname: Clements fullname: Clements, Judith A |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24069136$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1186_s13058_019_1117_0 crossref_primary_10_1016_j_addr_2014_08_009 crossref_primary_10_1097_MD_0000000000002670 crossref_primary_10_1007_s11914_017_0403_y crossref_primary_10_1016_j_bone_2015_06_002 crossref_primary_10_4062_biomolther_2015_105 crossref_primary_10_1038_s41416_022_01764_z crossref_primary_10_1371_journal_pone_0150085 crossref_primary_10_1089_ten_tea_2016_0153 crossref_primary_10_1590_1678_775720140158 crossref_primary_10_1016_j_bone_2015_10_004 crossref_primary_10_1155_2018_7120979 |
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Copyright | COPYRIGHT 2013 Public Library of Science 2013 Gregory et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Gregory et al 2013 Gregory et al |
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Notes | Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: LSG LB JAC. Performed the experiments: LSG WC. Analyzed the data: LSG WC. Contributed reagents/materials/analysis tools: LSG JAC. Wrote the manuscript: LSG WC LB JAC. |
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Snippet | Bone metastases are severely debilitating and have a significant impact on the quality of life of women with metastatic breast cancer. Treatment options are... |
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SubjectTerms | Animals Apoptosis Apposition Biocompatibility Biomedical materials Bone (trabecular) Bone cancer Bone density Bone growth Bone lesions Bone loss Bone matrix Bone Neoplasms - pathology Bone Neoplasms - secondary Bone resorption Bones Breast cancer Breast Neoplasms - complications Breast Neoplasms - pathology Cancellous bone Cancer Cancer cells Cancer metastasis Cancer therapies Cancer treatment Cell Line, Tumor Dkk1 protein Female Gene expression Homology Humans Injection Lesions Metastases Metastasis Mice Mice, SCID Mycoplasma Noggin protein Osteoblasts Osteoblasts - pathology Osteogenesis Osteolysis Pathogenesis Perforation Prostate Quality of life Reduction Struts Studies Tibia Womens health |
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Title | Breast cancer cells induce osteolytic bone lesions in vivo through a reduction in osteoblast activity in mice |
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