ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis

The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple‐negative breas...

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Vydáno v:EMBO molecular medicine Ročník 6; číslo 2; s. 278 - 294
Hlavní autoři: Romagnoli, Mathilde, Mineva, Nora D, Polmear, Michael, Conrad, Catharina, Srinivasan, Srimathi, Loussouarn, Delphine, Barillé‐Nion, Sophie, Georgakoudi, Irene, Dagg, Áine, McDermott, Enda W, Duffy, Michael J, McGowan, Patricia M., Schlomann, Uwe, Parsons, Maddy, Bartsch, Jörg W, Sonenshein, Gail E
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 01.02.2014
Wiley Open Access
Blackwell Publishing Ltd
Springer Nature
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ISSN:1757-4676, 1757-4684, 1757-4684
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Abstract The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple‐negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF‐A and transendothelial cell migration via β1‐integrin activation. In vivo , treatment with an anti‐ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non‐essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination. Synopsis The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer The transmembrane ADAM8 protein is expressed in primary human breast tumors compared to normal breast tissue, and especially in triple‐negative breast cancers (TNBC), which currently have no targeted therapies. High levels of ADAM8 expression predict poor breast cancer clinical outcome and are detected in half of patient metastases. ADAM8 promotes tumor growth and dissemination in an orthotopic mouse model by stimulating angiogenesis (via the release of VEGF‐A and other pro‐angiogenic growth factors) and tumor cell intra/extravasation (via activation of β1‐integrin). Treatment of mice with a monoclonal antibody targeting ADAM8 extracellular domains initiated at the time of TNBC cell implantation in the mammary fat pad significantly reduces tumor growth, angiogenesis and metastasis. Treatment of pre‐existing tumors with the ADAM8 antibody in a neoadjuvant setting profoundly reduces metastases in a mouse resection model, further validating ADAM8 as a therapeutic target of TNBC. Graphical Abstract The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer.
AbstractList Abstract The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple‐negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF‐A and transendothelial cell migration via β1‐integrin activation. In vivo, treatment with an anti‐ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non‐essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination.
The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple‐negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF‐A and transendothelial cell migration via β1‐integrin activation. In vivo, treatment with an anti‐ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non‐essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination. Synopsis The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer The transmembrane ADAM8 protein is expressed in primary human breast tumors compared to normal breast tissue, and especially in triple‐negative breast cancers (TNBC), which currently have no targeted therapies. High levels of ADAM8 expression predict poor breast cancer clinical outcome and are detected in half of patient metastases. ADAM8 promotes tumor growth and dissemination in an orthotopic mouse model by stimulating angiogenesis (via the release of VEGF‐A and other pro‐angiogenic growth factors) and tumor cell intra/extravasation (via activation of β1‐integrin). Treatment of mice with a monoclonal antibody targeting ADAM8 extracellular domains initiated at the time of TNBC cell implantation in the mammary fat pad significantly reduces tumor growth, angiogenesis and metastasis. Treatment of pre‐existing tumors with the ADAM8 antibody in a neoadjuvant setting profoundly reduces metastases in a mouse resection model, further validating ADAM8 as a therapeutic target of TNBC. The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer.
The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple-negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF-A and transendothelial cell migration via β1-integrin activation. In vivo, treatment with an anti-ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non-essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination.
The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple-negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanisti-cally, ADAM8 stimulated both angiogenesis through release of VEGF-A and transendothelial cell migration via β1-integrin activation. In vivo, treatment with an anti-ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non-essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination.
The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple‐negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF‐A and transendothelial cell migration via β1‐integrin activation. In vivo , treatment with an anti‐ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non‐essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination. Synopsis The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer The transmembrane ADAM8 protein is expressed in primary human breast tumors compared to normal breast tissue, and especially in triple‐negative breast cancers (TNBC), which currently have no targeted therapies. High levels of ADAM8 expression predict poor breast cancer clinical outcome and are detected in half of patient metastases. ADAM8 promotes tumor growth and dissemination in an orthotopic mouse model by stimulating angiogenesis (via the release of VEGF‐A and other pro‐angiogenic growth factors) and tumor cell intra/extravasation (via activation of β1‐integrin). Treatment of mice with a monoclonal antibody targeting ADAM8 extracellular domains initiated at the time of TNBC cell implantation in the mammary fat pad significantly reduces tumor growth, angiogenesis and metastasis. Treatment of pre‐existing tumors with the ADAM8 antibody in a neoadjuvant setting profoundly reduces metastases in a mouse resection model, further validating ADAM8 as a therapeutic target of TNBC. Graphical Abstract The transmembrane protein ADAM8 is shown to be a crucial player in multiple steps of breast tumorigenesis, notably in angiogenesis and cancer cell adhesion to the endothelium. The results validate ADAM8 as novel target for the treatment of aggressive triple‐negative breast cancer.
The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple-negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF-A and transendothelial cell migration via β1-integrin activation. In vivo, treatment with an anti-ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non-essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination. Subject Category Cancer
The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple-negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF-A and transendothelial cell migration via β1-integrin activation. In vivo, treatment with an anti-ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non-essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination.The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we report that ADAM8 is abundantly expressed in breast tumors and derived metastases compared to normal tissue, especially in triple-negative breast cancers (TNBCs). Furthermore, high ADAM8 levels predicted poor patient outcome. Consistently, ADAM8 promoted an aggressive phenotype of TNBC cells in culture. In a mouse orthotopic model, tumors derived from TNBC cells with ADAM8 knockdown failed to grow beyond a palpable size and displayed poor vascularization. Circulating tumor cells and brain metastases were also significantly reduced. Mechanistically, ADAM8 stimulated both angiogenesis through release of VEGF-A and transendothelial cell migration via β1-integrin activation. In vivo, treatment with an anti-ADAM8 antibody from the time of cell inoculation reduced primary tumor burden and metastases. Furthermore, antibody treatment of established tumors profoundly decreased metastases in a resection model. As a non-essential protein under physiological conditions, ADAM8 represents a promising novel target for treatment of TNBCs, which currently lack targeted therapies and frequently progress with fatal dissemination.
Author McDermott, Enda W
Sonenshein, Gail E
Polmear, Michael
Parsons, Maddy
Romagnoli, Mathilde
Barillé‐Nion, Sophie
Schlomann, Uwe
Bartsch, Jörg W
Conrad, Catharina
McGowan, Patricia M.
Georgakoudi, Irene
Dagg, Áine
Srinivasan, Srimathi
Duffy, Michael J
Mineva, Nora D
Loussouarn, Delphine
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Issue 2
Keywords breast cancer
ADAM8
therapeutic target
cancer progression
metastasis
triple‐negative
triple- negative breast cancer Subject Category Cancer
Language English
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Snippet The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we...
The transmembrane metalloprotease-disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components. Here, we...
Abstract The transmembrane metalloprotease‐disintegrin ADAM8 mediates cell adhesion and shedding of ligands, receptors and extracellular matrix components....
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StartPage 278
SubjectTerms ADAM Proteins - chemistry
ADAM Proteins - metabolism
ADAM8
Animals
Antibodies, Monoclonal - pharmacology
breast cancer
Breast Neoplasms - blood supply
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
cancer progression
Cell Adhesion - drug effects
Cell Hypoxia - drug effects
Cell Movement - drug effects
Cell Proliferation - drug effects
EMBO03
Endothelial Cells - drug effects
Endothelial Cells - metabolism
Endothelial Cells - pathology
Female
Gene Knockdown Techniques
Humans
Integrin beta1 - metabolism
Life Sciences
Membrane Proteins - chemistry
Membrane Proteins - metabolism
metastasis
Mice
Models, Biological
Neoplasm Invasiveness
Neoplasm Metastasis
Neoplastic Cells, Circulating - drug effects
Neoplastic Cells, Circulating - metabolism
Neoplastic Cells, Circulating - pathology
Neovascularization, Pathologic - pathology
Phenotype
Prognosis
Protein Structure, Tertiary
Research Article
therapeutic target
Triple Negative Breast Neoplasms - pathology
triple‐negative
Tumor Cells, Cultured
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Title ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis
URI https://link.springer.com/article/10.1002/emmm.201303373
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