The fibroblast Tiam1-osteopontin pathway modulates breast cancer invasion and metastasis
The tumor microenvironment has complex effects in cancer pathophysiology that are not fully understood. Most cancer therapies are directed against malignant cells specifically, leaving pro-malignant signals from the microenvironment unaddressed. Defining specific mechanisms by which the tumor microe...
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| Veröffentlicht in: | Breast cancer research : BCR 2016-01, Vol.18 (1), p.14-14, Article 14 |
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| creator | Xu, Kun Tian, Xuejun Oh, Sun Y Movassaghi, Mohammad Naber, Stephen P Kuperwasser, Charlotte Buchsbaum, Rachel J |
| description | The tumor microenvironment has complex effects in cancer pathophysiology that are not fully understood. Most cancer therapies are directed against malignant cells specifically, leaving pro-malignant signals from the microenvironment unaddressed. Defining specific mechanisms by which the tumor microenvironment contributes to breast cancer metastasis may lead to new therapeutic approaches against advanced breast cancer.
We use a novel method for manipulating three-dimensional mixed cell co-cultures, along with studies in mouse xenograft models of human breast cancer and a histologic study of human breast cancer samples, to investigate how breast cancer-associated fibroblasts affect the malignant behaviors of breast cancer cells.
Altering fibroblast Tiam1 expression induces changes in invasion, migration, epithelial-mesenchymal transition, and cancer stem cell characteristics in associated breast cancer cells. These changes are both dependent on fibroblast secretion of osteopontin and also long-lasting even after cancer cell dissociation from the fibroblasts, indicating a novel Tiam1-osteopontin pathway in breast cancer-associated fibroblasts. Notably, inhibition of fibroblast osteopontin with low doses of a novel small molecule prevents lung metastasis in a mouse model of human breast cancer metastasis. Moreover, fibroblast expression patterns of Tiam1 and osteopontin in human breast cancers show converse changes correlating with invasion, supporting the hypothesis that this pathway in tumor-associated fibroblasts regulates breast cancer invasiveness in human disease and is thus clinically relevant.
These findings suggest a new therapeutic paradigm for preventing breast cancer metastasis. Pro-malignant signals from the tumor microenvironment with long-lasting effects on associated cancer cells may perpetuate the metastatic potential of developing cancers. Inhibition of these microenvironment signals represents a new therapeutic strategy against cancer metastasis that enables targeting of stromal cells with less genetic plasticity than associated cancer cells and opens new avenues for investigation of novel therapeutic targets and agents. |
| doi_str_mv | 10.1186/s13058-016-0674-8 |
| format | Article |
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We use a novel method for manipulating three-dimensional mixed cell co-cultures, along with studies in mouse xenograft models of human breast cancer and a histologic study of human breast cancer samples, to investigate how breast cancer-associated fibroblasts affect the malignant behaviors of breast cancer cells.
Altering fibroblast Tiam1 expression induces changes in invasion, migration, epithelial-mesenchymal transition, and cancer stem cell characteristics in associated breast cancer cells. These changes are both dependent on fibroblast secretion of osteopontin and also long-lasting even after cancer cell dissociation from the fibroblasts, indicating a novel Tiam1-osteopontin pathway in breast cancer-associated fibroblasts. Notably, inhibition of fibroblast osteopontin with low doses of a novel small molecule prevents lung metastasis in a mouse model of human breast cancer metastasis. Moreover, fibroblast expression patterns of Tiam1 and osteopontin in human breast cancers show converse changes correlating with invasion, supporting the hypothesis that this pathway in tumor-associated fibroblasts regulates breast cancer invasiveness in human disease and is thus clinically relevant.
These findings suggest a new therapeutic paradigm for preventing breast cancer metastasis. Pro-malignant signals from the tumor microenvironment with long-lasting effects on associated cancer cells may perpetuate the metastatic potential of developing cancers. Inhibition of these microenvironment signals represents a new therapeutic strategy against cancer metastasis that enables targeting of stromal cells with less genetic plasticity than associated cancer cells and opens new avenues for investigation of novel therapeutic targets and agents.</description><identifier>ISSN: 1465-542X</identifier><identifier>ISSN: 1465-5411</identifier><identifier>EISSN: 1465-542X</identifier><identifier>DOI: 10.1186/s13058-016-0674-8</identifier><identifier>PMID: 26821678</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Breast cancer ; Breast Neoplasms - genetics ; Breast Neoplasms - pathology ; Cell Line, Tumor ; Cellular signal transduction ; Coculture Techniques ; Development and progression ; Epithelial-Mesenchymal Transition - genetics ; Female ; Fibroblasts ; Fibroblasts - metabolism ; Genetic aspects ; Guanine Nucleotide Exchange Factors - biosynthesis ; Guanine Nucleotide Exchange Factors - genetics ; Humans ; Lung Neoplasms - genetics ; Lung Neoplasms - pathology ; Lung Neoplasms - secondary ; Metastasis ; Mice ; Neoplasm Invasiveness - genetics ; Neoplasm Metastasis ; Osteopontin - biosynthesis ; Osteopontin - genetics ; Physiological aspects ; Signal Transduction ; Stromal Cells - pathology ; T-Lymphoma Invasion and Metastasis-inducing Protein 1 ; Tumor Microenvironment - genetics ; Xenograft Model Antitumor Assays</subject><ispartof>Breast cancer research : BCR, 2016-01, Vol.18 (1), p.14-14, Article 14</ispartof><rights>COPYRIGHT 2016 BioMed Central Ltd.</rights><rights>Copyright BioMed Central 2016</rights><rights>Xu et al. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c560t-a26674bdac811ec69c820ae8bc0979ef304e00b7b2067bfc527d5f5e360fac973</citedby><cites>FETCH-LOGICAL-c560t-a26674bdac811ec69c820ae8bc0979ef304e00b7b2067bfc527d5f5e360fac973</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4730665/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4730665/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,862,883,27911,27912,53778,53780</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26821678$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xu, Kun</creatorcontrib><creatorcontrib>Tian, Xuejun</creatorcontrib><creatorcontrib>Oh, Sun Y</creatorcontrib><creatorcontrib>Movassaghi, Mohammad</creatorcontrib><creatorcontrib>Naber, Stephen P</creatorcontrib><creatorcontrib>Kuperwasser, Charlotte</creatorcontrib><creatorcontrib>Buchsbaum, Rachel J</creatorcontrib><title>The fibroblast Tiam1-osteopontin pathway modulates breast cancer invasion and metastasis</title><title>Breast cancer research : BCR</title><addtitle>Breast Cancer Res</addtitle><description>The tumor microenvironment has complex effects in cancer pathophysiology that are not fully understood. Most cancer therapies are directed against malignant cells specifically, leaving pro-malignant signals from the microenvironment unaddressed. Defining specific mechanisms by which the tumor microenvironment contributes to breast cancer metastasis may lead to new therapeutic approaches against advanced breast cancer.
We use a novel method for manipulating three-dimensional mixed cell co-cultures, along with studies in mouse xenograft models of human breast cancer and a histologic study of human breast cancer samples, to investigate how breast cancer-associated fibroblasts affect the malignant behaviors of breast cancer cells.
Altering fibroblast Tiam1 expression induces changes in invasion, migration, epithelial-mesenchymal transition, and cancer stem cell characteristics in associated breast cancer cells. These changes are both dependent on fibroblast secretion of osteopontin and also long-lasting even after cancer cell dissociation from the fibroblasts, indicating a novel Tiam1-osteopontin pathway in breast cancer-associated fibroblasts. Notably, inhibition of fibroblast osteopontin with low doses of a novel small molecule prevents lung metastasis in a mouse model of human breast cancer metastasis. Moreover, fibroblast expression patterns of Tiam1 and osteopontin in human breast cancers show converse changes correlating with invasion, supporting the hypothesis that this pathway in tumor-associated fibroblasts regulates breast cancer invasiveness in human disease and is thus clinically relevant.
These findings suggest a new therapeutic paradigm for preventing breast cancer metastasis. Pro-malignant signals from the tumor microenvironment with long-lasting effects on associated cancer cells may perpetuate the metastatic potential of developing cancers. Inhibition of these microenvironment signals represents a new therapeutic strategy against cancer metastasis that enables targeting of stromal cells with less genetic plasticity than associated cancer cells and opens new avenues for investigation of novel therapeutic targets and agents.</description><subject>Animals</subject><subject>Breast cancer</subject><subject>Breast Neoplasms - genetics</subject><subject>Breast Neoplasms - pathology</subject><subject>Cell Line, Tumor</subject><subject>Cellular signal transduction</subject><subject>Coculture Techniques</subject><subject>Development and progression</subject><subject>Epithelial-Mesenchymal Transition - genetics</subject><subject>Female</subject><subject>Fibroblasts</subject><subject>Fibroblasts - metabolism</subject><subject>Genetic aspects</subject><subject>Guanine Nucleotide Exchange Factors - biosynthesis</subject><subject>Guanine Nucleotide Exchange Factors - genetics</subject><subject>Humans</subject><subject>Lung Neoplasms - genetics</subject><subject>Lung Neoplasms - pathology</subject><subject>Lung Neoplasms - secondary</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Neoplasm Invasiveness - genetics</subject><subject>Neoplasm Metastasis</subject><subject>Osteopontin - biosynthesis</subject><subject>Osteopontin - genetics</subject><subject>Physiological aspects</subject><subject>Signal Transduction</subject><subject>Stromal Cells - pathology</subject><subject>T-Lymphoma Invasion and Metastasis-inducing Protein 1</subject><subject>Tumor Microenvironment - genetics</subject><subject>Xenograft Model Antitumor Assays</subject><issn>1465-542X</issn><issn>1465-5411</issn><issn>1465-542X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><recordid>eNptUktLHTEYDaVSre0P6KYMdNPN2GQmz01BpC8Q3FzBXUgy33gjM8ltklH8981wrdUiWeTxnXPyneQg9IHgE0Ik_5JJj5lsMeEt5oK28hU6IpSzltHu6vWT9SF6m_MNxkRIJt-gw47LjnAhj9DVZgvN6G2KdjK5NBtvZtLGXCDuYig-NDtTtnfmvpnjsEymQG5sghXqTHCQGh9uTfYxNCYMzQylluo-v0MHo5kyvH-Yj9Hl92-bs5_t-cWPX2en561jHJfWdLx2bgfjJCHguHKywwakdVgJBWOPKWBshe2qQzs61omBjQx6jkfjlOiP0de97m6xMwwOQklm0rvkZ5PudTReP68Ev9XX8VZT0WPOWRX4_CCQ4u8FctGzzw6myQSIS9ZEcEJFJ4iq0E__QW_ikkK1t6KEwBIr-g91bSbQPoyx3utWUX1KqWBKKbL2ffICqo4BZu9igNHX82cEsie4FHNOMD56JFivcdD7OOgaB73GQcvK-fj0cR4Zf_-__wNcwbEf</recordid><startdate>20160128</startdate><enddate>20160128</enddate><creator>Xu, Kun</creator><creator>Tian, Xuejun</creator><creator>Oh, Sun Y</creator><creator>Movassaghi, Mohammad</creator><creator>Naber, Stephen P</creator><creator>Kuperwasser, Charlotte</creator><creator>Buchsbaum, Rachel J</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160128</creationdate><title>The fibroblast Tiam1-osteopontin pathway modulates breast cancer invasion and metastasis</title><author>Xu, Kun ; 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Most cancer therapies are directed against malignant cells specifically, leaving pro-malignant signals from the microenvironment unaddressed. Defining specific mechanisms by which the tumor microenvironment contributes to breast cancer metastasis may lead to new therapeutic approaches against advanced breast cancer.
We use a novel method for manipulating three-dimensional mixed cell co-cultures, along with studies in mouse xenograft models of human breast cancer and a histologic study of human breast cancer samples, to investigate how breast cancer-associated fibroblasts affect the malignant behaviors of breast cancer cells.
Altering fibroblast Tiam1 expression induces changes in invasion, migration, epithelial-mesenchymal transition, and cancer stem cell characteristics in associated breast cancer cells. These changes are both dependent on fibroblast secretion of osteopontin and also long-lasting even after cancer cell dissociation from the fibroblasts, indicating a novel Tiam1-osteopontin pathway in breast cancer-associated fibroblasts. Notably, inhibition of fibroblast osteopontin with low doses of a novel small molecule prevents lung metastasis in a mouse model of human breast cancer metastasis. Moreover, fibroblast expression patterns of Tiam1 and osteopontin in human breast cancers show converse changes correlating with invasion, supporting the hypothesis that this pathway in tumor-associated fibroblasts regulates breast cancer invasiveness in human disease and is thus clinically relevant.
These findings suggest a new therapeutic paradigm for preventing breast cancer metastasis. Pro-malignant signals from the tumor microenvironment with long-lasting effects on associated cancer cells may perpetuate the metastatic potential of developing cancers. Inhibition of these microenvironment signals represents a new therapeutic strategy against cancer metastasis that enables targeting of stromal cells with less genetic plasticity than associated cancer cells and opens new avenues for investigation of novel therapeutic targets and agents.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>26821678</pmid><doi>10.1186/s13058-016-0674-8</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Breast cancer Breast Neoplasms - genetics Breast Neoplasms - pathology Cell Line, Tumor Cellular signal transduction Coculture Techniques Development and progression Epithelial-Mesenchymal Transition - genetics Female Fibroblasts Fibroblasts - metabolism Genetic aspects Guanine Nucleotide Exchange Factors - biosynthesis Guanine Nucleotide Exchange Factors - genetics Humans Lung Neoplasms - genetics Lung Neoplasms - pathology Lung Neoplasms - secondary Metastasis Mice Neoplasm Invasiveness - genetics Neoplasm Metastasis Osteopontin - biosynthesis Osteopontin - genetics Physiological aspects Signal Transduction Stromal Cells - pathology T-Lymphoma Invasion and Metastasis-inducing Protein 1 Tumor Microenvironment - genetics Xenograft Model Antitumor Assays |
| title | The fibroblast Tiam1-osteopontin pathway modulates breast cancer invasion and metastasis |
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