Anti-Transforming Growth Factor ß Antibody Treatment Rescues Bone Loss and Prevents Breast Cancer Metastasis to Bone
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{"title"=>"Anti-transforming growth factor ß antibody treatment rescues bone loss and prevents breast cancer metastasis to bone", "type"=>"journal", "authors"=>[{"first_name"=>"Swati", "last_name"=>"Biswas", "scopus_author_id"=>"55031265200"}, {"first_name"=>"Jeffry S.", "last_name"=>"Nyman", "scopus_author_id"=>"7006598811"}, {"first_name"=>"Jo Ann", "last_name"=>"Alvarez", "scopus_author_id"=>"7402573996"}, {"first_name"=>"Anwesa", "last_name"=>"Chakrabarti", "scopus_author_id"=>"54413944300"}, {"first_name"=>"Austin", "last_name"=>"Ayres", "scopus_author_id"=>"54413880300"}, {"first_name"=>"Julie", "last_name"=>"Sterling", "scopus_author_id"=>"36127843700"}, {"first_name"=>"James", "last_name"=>"Edwards", "scopus_author_id"=>"55368709400"}, {"first_name"=>"Tapasi", "last_name"=>"Rana", "scopus_author_id"=>"22235303200"}, {"first_name"=>"Rachelle", "last_name"=>"Johnson", "scopus_author_id"=>"55501409900"}, {"first_name"=>"Daniel S.", "last_name"=>"Perrien", "scopus_author_id"=>"6506333256"}, {"first_name"=>"Scott", "last_name"=>"Lonning", "scopus_author_id"=>"6701725407"}, {"first_name"=>"Yu", "last_name"=>"Shyr", "scopus_author_id"=>"35431521800"}, {"first_name"=>"Lynn M.", "last_name"=>"Matrisian", "scopus_author_id"=>"7005390593"}, {"first_name"=>"Gregory R.", "last_name"=>"Mundy", "scopus_author_id"=>"56833794300"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"362904727", "doi"=>"10.1371/journal.pone.0027090", "sgr"=>"80855128847", "scopus"=>"2-s2.0-80855128847", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pmid"=>"22096521"}, "id"=>"5991d8dc-5b9f-3f3a-b237-6830d6fe1778", "abstract"=>"Breast cancer often metastasizes to bone causing osteolytic bone resorption which releases active TGFβ. Because TGFβ favors progression of breast cancer metastasis to bone, we hypothesized that treatment using anti-TGFβ antibody may reduce tumor burden and rescue tumor-associated bone loss in metastatic breast cancer. In this study we have tested the efficacy of an anti-TGFβ antibody 1D11 preventing breast cancer bone metastasis. We have used two preclinical breast cancer bone metastasis models, in which either human breast cancer cells or murine mammary tumor cells were injected in host mice via left cardiac ventricle. Using several in vivo, in vitro and ex vivo assays, we have demonstrated that anti-TGFβ antibody treatment have significantly reduced tumor burden in the bone along with a statistically significant threefold reduction in osteolytic lesion number and tenfold reduction in osteolytic lesion area. A decrease in osteoclast numbers (p = 0.027) in vivo and osteoclastogenesis ex vivo were also observed. Most importantly, in tumor-bearing mice, anti-TGFβ treatment resulted in a twofold increase in bone volume (p<0.01). In addition, treatment with anti-TGFβ antibody increased the mineral-to-collagen ratio in vivo, a reflection of improved tissue level properties. Moreover, anti-TGFβ antibody directly increased mineralized matrix formation in calverial osteoblast (p = 0.005), suggesting a direct beneficial role of anti-TGFβ antibody treatment on osteoblasts. Data presented here demonstrate that anti-TGFβ treatment may offer a novel therapeutic option for tumor-induced bone disease and has the dual potential for simultaneously decreasing tumor burden and rescue bone loss in breast cancer to bone metastases. This approach of intervention has the potential to reduce skeletal related events (SREs) in breast cancer survivors.", "link"=>"http://www.mendeley.com/research/antitransforming-growth-factor-%C3%9F-antibody-treatment-rescues-bone-loss-prevents-breast-cancer-metasta", "reader_count"=>32, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>3, "Student > Bachelor"=>2, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>3, "Student > Bachelor"=>2, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>19, "Medicine and Dentistry"=>4, "Veterinary Science and Veterinary Medicine"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Sweden"=>1, "United States"=>2, "United Kingdom"=>1, "Mexico"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/713788"], "description"=>"<p><b>Panel a:</b> Representative H&E sections (5×) of tibia from tumor-bearing mice treated with control antibody (13C4) or anti-TGFβ antibody (1D11). White line indicates the presence of tumor. <b>Panel b:</b> A boxplot of tumor burden in MDA-MB-231 tumor-bearing mice treated with either 13C4 (10 mg/kg) or 1D11(10 mg/kg) for 4 weeks, starting 1 day after tumor cell injection (N = at least 7) showing decrease in tumor burden. Wilcoxon rank-sum p-value = 0.001. Mean ± standard deviation = 13C4: 0.76±0.12, 1D11: 0.25±0.1. <b>Panel c:</b> Boxplots of tumor burden in MDA-MB-231 tumor bearing mice treated with either 13C4(10 mg/kg) or 1D11(10 mg/kg) starting two weeks after tumor cell injection and continued to be treated until the end of 4 weeks post tumor injection. Wilcoxon rank-sum p-value = 0.016. Mean ± standard deviation = 13C4:0.6461 ±0.3599, 1D11: 0.1114±0.1919. (N = at least 5). <b>Panel d:</b> Boxplot of tumor burden by group for the 4T1 tumor bearing mice (4T1 cells injected in Balb/c), treated 1 day post tumor cell injection and treated for 4 weeks shown decrease in tumor burden. Wilcoxon rank-sum p-value = 0.03. Mean ± standard deviation = 13C4: 0.0331±0.012, 1D11:0.006±0.002 (N = 4). <b>Panel e:</b> Decreased relative mRNA expression of Gli2 in MDA-MB-231 upon 1D11 treatment. Wilcoxon rank-sum p-value for TGFβ versus TGFβ+1D11 groups is 0.005. Mean ± standard deviation = TGFβ: 2.08±0.06, TGFβ + 1D11: 0.42±0.05. Results presented here are representative of at least two independent experiments. <b>Panel f:</b> Decreased relative mRNA expression of PTHrP in MDA-MB-231 upon treatment with 1D11. Wilcoxon rank-sum p-value for TGFβ versus TGFβ + 1D11 groups is 0.005. Mean ± standard deviation = TGFβ: 6.24±0.05, TGFβ + 1D11: 0.41±0.04. Results presented here are representative of at least two independent experiments.</p>", "links"=>[], "tags"=>["antibody", "decreases", "tumor-bearing"], "article_id"=>384126, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_TGF_946_antibody_treatment_decreases_tumor_burden_in_tumor_bearing_mice_/384126", "title"=>"Anti-TGFβ antibody treatment decreases tumor burden in tumor-bearing mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:47:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/714185"], "description"=>"<p>MDA-MB-231 cells were injected via intra-cardiac route in 4 week old female nude mice and 4T1 cells were injected in 4–5 week old female Balb/C mice. Mice were treated either with control antibody (13C4, 10 mg/kg) or anti-TGFβ antibody (1D11, 10 mg/kg) for 4 weeks, starting 1 day after tumor cell inoculation. Trabecular bone volume in the tibial metaphysis of tumor-bearing mice was analyzed by microCT. <b>Panel a:</b> Representative three dimensional reconstitutions of microCT images from both 13C4 and 1D11 treated groups from mice injected with MDA-MB-231 cells. <b>Panel b:</b> Boxplots of average BV/TV (bone volume/total volume) by group for the MDA-M<b>B</b>-231 tumor- bearing mice show significant increase in bone mass after treatment with anti-TGFβ antibody. Wilcoxon rank-sum p-value = <0.001. Mean ± standard deviation = 13C4: 0.06±0.04, 1D11: 0.32±0.09. N = at least 10. <b>Panel c.</b> Boxplots of average BV/TV (bone volume/total volume) by group for the 4T1 tumor- bearing mice show a significant increase in bone mass as a result of treatment with 1D11 as measured by BV/TV. Wilcoxon rank-sum p-value = 0.036. Mean ± standard deviation = 13C4: 0.09±0.01, 1D11: 0.11±0.01, N = at least 5. <b>Panel d:</b> Mouse calverial osteoblasts were isolated and cultured for 7–10 days as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027090#s2\" target=\"_blank\">Materials and Methods</a>, either in presence of anti-TGFβ antibody (1D11) or isotype control (13C4) and mineralized matrix formation was measured using Von Kossa staining as a surrogate for osteoblast differentiation. <b>Panel e:</b> Boxplot analysis reveals treatment with anti-TGFβ antibody (1D11) significantly increased percent areas of mineralized matrix. Images were taken from representative fields and quantified using Metamorph software. Wilcoxon rank-sum p-value = 0.005. Mean ± standard deviation = 13C4: 16±3.7, 1D11: 32.3±1. Data presented here is representative of two independent experiments.</p>", "links"=>[], "tags"=>["antibody", "increases", "bearing"], "article_id"=>384532, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_TGF_946_antibody_increases_bone_volume_in_tumor_bearing_mice_/384532", "title"=>"Anti-TGFβ antibody increases bone volume in tumor bearing mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:49:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/714326"], "description"=>"<p>Confocal raman spectroscopy was performed on mice bearing MDA-MB-231 tumors in bone treated for 4 weeks with 1D11 or 13C4 antibodies as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027090#s2\" target=\"_blank\">materials and methods</a> section. At least nine spectra were analyzed per specimen and the mean mineral-to-collagen ratio, Type-B carbonate substitution, and crystallinity were scored. Both mineral-to-collagen ratio and carbonate substitution increased significantly upon 1D11 treatments compared to control. Mean ± standard deviation is shown, p value was determined using Wilcoxon test.</p>", "links"=>[], "tags"=>["antibody", "1d11", "mineral-to-collagen"], "article_id"=>384674, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.t002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Suppression_of_TGF_946_by_anti_TGF_946_antibody_1D11_increased_the_mineral_to_collagen_ratio_/384674", "title"=>"Suppression of TGFβ by anti-TGFβ antibody 1D11 increased the mineral-to-collagen ratio.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 11:50:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/714283"], "description"=>"<p>MicroCT analysis of the tibiae from MDA-MB-231tumor-bearing mice treated for 4 weeks, starting one day after tumor cell inoculation, revealed that suppression of TGFβ by the antibody 1D11 increased trabecular bone volume through increases in trabecular number, and this improved the connectivity of the trabeculae (lack of fenestrations), compared to isotype control. Wilcoxon rank-sum test was used for this analysis. Means and standard deviations by group for the MDA-MB-231 four week data with p-values from Wilcoxon rank-sum tests. Quantitative analysis of microCT data from MDA-MB-231 tumor-bearing mice treated with 13C4 or 1D11 for weeks. Trabecular bone volume (BV/TV), trabecular thickness (Tb.Th*), trabecular number (Tb.N*), and connectivity density (Conn.D), and mean volumetric density of the mineralized tissue (Tb.TMD) were calculated using the Scanco evaluation software.</p>", "links"=>[], "tags"=>["antibody", "improves", "trabecular", "bearing", "mice", "tibia"], "article_id"=>384623, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_TGF_946_antibody_improves_trabecular_architecture_in_tumor_bearing_mice_tibia_and_femur_/384623", "title"=>"Anti-TGFβ antibody improves trabecular architecture in tumor bearing mice tibia and femur.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 11:49:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/713940"], "description"=>"<p>Mice were inoculated with MDA-MB-231 human breast cancer cells in the left cardiac ventricle and were treated with either isotype control (13C4, 10 mg/kg) or anti-TGFβ antibody (1D11, 10 mg/kg) for 4 weeks, starting from 1 day post tumor cell injection. At the end of the experiment, whole body X-ray images of mice from both control and anti-TGFβ antibody treated group were taken and osteolytic lesion area and osteolytic lesion counts were analyzed using image analysis software (Metamorph, Molecular Device). <b>Panel a:</b> Representative X-ray images of osteolytic bone lesions in the hind leg of mice treated for 4 weeks either with control antibody (13C4, left panel) or anti-TGFβ antibody (1D11, right panel). White arrows indicate presence of osteolytic lesions. <b>Panel b:</b> A boxplot representing the average lesion counts in mice inoculated with MDA-MB-231 cells in the left cardiac ventricle, treated with either control antibody (13C4, 10 mg/kg) or anti-TGFβ antibody (1D11, 10 mg/kg) for 4 weeks, starting 1 day after tumor cell injection shows decrease in lesion numbers after anti-TGFβ treatment (6.9±1.7 for control and 1.9±0.7 for 1D11; Wilcoxon rank-sum p-value = <.001, N = 9). <b>Panel c:</b> A boxplot representing the lesion area from the same experiment shows decrease in the lesion area after anti-TGFβ treatment (20520±6000 for control and 1497±888 for 1D11; Wilcoxon rank-sum p-value = <.001, N = at least 9). Lesion areas were measured using arbitrary pixel unit.</p>", "links"=>[], "tags"=>["antibody", "osteolytic", "lesions", "mda-mb-231", "cancer", "metastasis", "cardiac", "injection"], "article_id"=>384281, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_TGF_946_antibody_reduces_osteolytic_lesions_in_MDA_MB_231_breast_cancer_bone_metastasis_cardiac_injection_model_/384281", "title"=>"Anti-TGFβ antibody reduces osteolytic lesions in MDA-MB-231 breast cancer bone metastasis cardiac injection model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/714056"], "description"=>"<p><b>Panel a:</b> Boxplot of number of TRAP positive osteoclasts per millimeter of bone surface in MBA-MB-231 tumor-bearing tibiae, showing significantly decreased osteoclasts upon 1D11 treatment, compared to 13C4. Wilcoxon rank-sum p-value = 0.027. Mean ± standard deviation = 13C4: 0.7733±0.3002, 1D11: 0.4539±0.1141. N = at least 6). <b>Panel b:</b> To assess the effect of anti-TGFβ treatment directly on osteoclast population, an <i>ex vivo</i> osteoclastogenesis assay was performed using bone marrow mononuclear cells. Bone marrow mononuclear cells were isolated and cultured in presence of 13C4 (control antibody), 1D11(anti-TGFβ antibody), TGFβ+13C4 or TGFβ+1D11 in presence of both RANKL and MCSF. Both 13C4 and 1D11 was used at a concentration of 25 µg/ml. TGFβ as used at a concentration of 5 ng/ml. Osteoclasts were stained using using a Leucocyte acid phosphatase (TRAP) kit as per manufacturer's instruction (Sigma-Aldrich) and TRAP positive cells (reddish brown) were counted under microscope. Boxplots of number of osteoclasts by group for osteoclastogenesis assay show that treatment with 1D11 significantly reduced TGFβ-mediated osteoclast formation. Wilcoxon rank-sum p-value for TGFβ and TGFβ + 1D11 groups is 0.01. Mean ± standard deviation = TGFβ: 26.5±3.83, TGFβ + 1D11: 17.83±4.17. Data presented here is representative of two independent experiments. <b>Panel c:</b> To assess the effect of anti-TGFβ antibody on osteoblast-mediated osteoclastogenesis, bone marrow mononuclear cells were cultured on a layer of primary mouse calverial osteoblasts in the presence of either control antibody (13C4) or the anti-TGFβ antibody (1D11). After 7–10 days, TRAP staining was performed to identify mature osteoclasts (indicated by arrow). <b>Panel d:</b> Osteoblast mediated osteoclastogenesis increases significantly upon 1D11 treatment compared to control, Wilcoxon rank-sum p-value = 0.006. Mean ± standard deviation = 13C4: 26.5±11.31, 1D11: 4.83±2.48. Data presented here is representative of two independent experiments.</p>", "links"=>[], "tags"=>["antibody", "osteoclast", "numbers"], "article_id"=>384402, "categories"=>["Physiology", "Microbiology", "Cancer", "Developmental Biology", "Immunology"], "users"=>["Swati Biswas", "Jeffry S. Nyman", "JoAnn Alvarez", "Anwesa Chakrabarti", "Austin Ayres", "Julie Sterling", "James Edwards", "Tapasi Rana", "Rachelle Johnson", "Daniel S. Perrien", "Scott Lonning", "Yu Shyr", "Lynn M. Matrisian", "Gregory R. Mundy"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027090.g003", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anti_TGF_antibody_decreased_osteoclast_numbers_and_in_vitro_osteoclastogenesis_/384402", "title"=>"Anti-TGFβ antibody decreased osteoclast numbers and <i>in vitro</i> osteoclastogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:48:40"}

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Relative Metric

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