Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization

The miR200 family regulates EMT through E-cadherin modulation and has been proposed to contribute to metastasis thusly. This report identifies a promoting role of miR-200 in metastatic colonization that involves a novel target, the tumor secretome. The correlation between miR-200 and metastasis in p...

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Vydáno v:	Nature medicine Ročník 17; číslo 9; s. 1101 - 1108
Hlavní autoři:	Korpal, Manav, Ell, Brian J, Buffa, Francesca M, Ibrahim, Toni, Blanco, Mario A, Celià-Terrassa, Toni, Mercatali, Laura, Khan, Zia, Goodarzi, Hani, Hua, Yuling, Wei, Yong, Hu, Guohong, Garcia, Benjamin A, Ragoussis, Jiannis, Amadori, Dino, Harris, Adrian L, Kang, Yibin
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	New York Nature Publishing Group US 01.09.2011 Nature Publishing Group
Témata:	631/337/384/331 631/67/322 631/80/79/1902 692/699/67/1347 Animals Biomedical and Life Sciences Biomedicine Breast cancer Cadherins - metabolism Cancer Cancer Research Cell adhesion & migration Cell Line, Tumor Colonization Female Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic - physiology Humans Infectious Diseases Mass Spectrometry Metabolic Diseases Metastasis Mice Mice, Inbred BALB C Microarray Analysis MicroRNAs - metabolism Molecular Medicine Neoplasm Metastasis - physiopathology Neurosciences Proteins Statistics, Nonparametric Vesicular Transport Proteins - metabolism United States
ISSN:	1078-8956, 1546-170X, 1546-170X
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Abstract	The miR200 family regulates EMT through E-cadherin modulation and has been proposed to contribute to metastasis thusly. This report identifies a promoting role of miR-200 in metastatic colonization that involves a novel target, the tumor secretome. The correlation between miR-200 and metastasis in people with cancer supports the relevance of this biphasic, multifaceted role of miR-200. Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis-suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin–dependent epithelial traits and Sec23a-mediated tumor cell secretome.
AbstractList	Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis- suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin-dependent epithelial traits and Sec23a-mediated tumor cell secretome. Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis-suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin-dependent epithelial traits and Sec23a-mediated tumor cell secretome. [PUBLICATION ABSTRACT] The miR200 family regulates EMT through E-cadherin modulation and has been proposed to contribute to metastasis thusly. This report identifies a promoting role of miR-200 in metastatic colonization that involves a novel target, the tumor secretome. The correlation between miR-200 and metastasis in people with cancer supports the relevance of this biphasic, multifaceted role of miR-200. Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis-suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin–dependent epithelial traits and Sec23a-mediated tumor cell secretome. Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis-suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin-dependent epithelial traits and Sec23a-mediated tumor cell secretome.Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here we have used clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. miR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis-suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin-dependent epithelial traits and Sec23a-mediated tumor cell secretome. Although the role of miR-200s in regulating E-cadherin expression and epithelial-mesenchymal transition is well established, their influence on metastatic colonization remains controversial. Here, we use clinical and experimental models of breast cancer metastasis to discover a pro-metastatic role of miR-200s that goes beyond their regulation of E-cadherin and epithelial phenotype. Overexpression of miR-200s is associated with increased risk of metastasis in breast cancer and promotes metastatic colonization in mouse models, phenotypes that cannot be recapitulated by E-cadherin expression alone. Genomic and proteomic analyses revealed global shifts in gene expression upon miR-200 overexpression toward that of highly metastatic cells. MiR-200s promote metastatic colonization partly through direct targeting of Sec23a, which mediates secretion of metastasis suppressive proteins, including Igfbp4 and Tinagl1, as validated by functional and clinical correlation studies. Overall, these findings suggest a pleiotropic role of miR-200s in promoting metastatic colonization by influencing E-cadherin-dependent epithelial traits and Sec23a-mediated tumor cell secretome.
Audience	Academic
Author	Khan, Zia Blanco, Mario A Amadori, Dino Korpal, Manav Harris, Adrian L Ell, Brian J Kang, Yibin Mercatali, Laura Goodarzi, Hani Garcia, Benjamin A Hua, Yuling Ibrahim, Toni Wei, Yong Celià-Terrassa, Toni Ragoussis, Jiannis Hu, Guohong Buffa, Francesca M
AuthorAffiliation	5 Department of Computer Science, Princeton University, Princeton, NJ 08544, USA 4 Department of Cell Biology, Institut de Biologia Molecular de Barcelona, CSIC, Barcelona Scientific Park, Baldiri i Reixac 15-21, 08028 Barcelona, Spain 8 Genomic Instability and Tumor Progression Program, Cancer Institute of New Jersey, New Brunswick, NJ 08903, USA 1 Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA 3 Osteoncology Center, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori (I.R.S.T.), Meldola, Italy 2 Cancer Research UK, Molecular Oncology Laboratories, Weatherall Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital, Headington, Oxford, United Kingdom 7 Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom 6 The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA
AuthorAffiliation_xml	– name: 1 Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA – name: 6 The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA – name: 5 Department of Computer Science, Princeton University, Princeton, NJ 08544, USA – name: 2 Cancer Research UK, Molecular Oncology Laboratories, Weatherall Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital, Headington, Oxford, United Kingdom – name: 8 Genomic Instability and Tumor Progression Program, Cancer Institute of New Jersey, New Brunswick, NJ 08903, USA – name: 3 Osteoncology Center, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori (I.R.S.T.), Meldola, Italy – name: 4 Department of Cell Biology, Institut de Biologia Molecular de Barcelona, CSIC, Barcelona Scientific Park, Baldiri i Reixac 15-21, 08028 Barcelona, Spain – name: 7 Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, United Kingdom
Author_xml	– sequence: 1 givenname: Manav surname: Korpal fullname: Korpal, Manav organization: Department of Molecular Biology, Princeton University – sequence: 2 givenname: Brian J surname: Ell fullname: Ell, Brian J organization: Department of Molecular Biology, Princeton University – sequence: 3 givenname: Francesca M surname: Buffa fullname: Buffa, Francesca M organization: Cancer Research UK, Molecular Oncology Laboratories, Weatherall Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital – sequence: 4 givenname: Toni surname: Ibrahim fullname: Ibrahim, Toni organization: Osteoncology Center, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori – sequence: 5 givenname: Mario A surname: Blanco fullname: Blanco, Mario A organization: Department of Molecular Biology, Princeton University – sequence: 6 givenname: Toni surname: Celià-Terrassa fullname: Celià-Terrassa, Toni organization: Department of Molecular Biology, Princeton University, Department of Cell Biology, Institut de Biologia Molecular de Barcelona, Consejo Superior de Investegaciones Cientificas – sequence: 7 givenname: Laura surname: Mercatali fullname: Mercatali, Laura organization: Osteoncology Center, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori – sequence: 8 givenname: Zia surname: Khan fullname: Khan, Zia organization: Department of Computer Science, Princeton University, The Lewis-Sigler Institute for Integrative Genomics, Princeton University – sequence: 9 givenname: Hani surname: Goodarzi fullname: Goodarzi, Hani organization: Department of Molecular Biology, Princeton University, The Lewis-Sigler Institute for Integrative Genomics, Princeton University – sequence: 10 givenname: Yuling surname: Hua fullname: Hua, Yuling organization: Department of Molecular Biology, Princeton University – sequence: 11 givenname: Yong surname: Wei fullname: Wei, Yong organization: Department of Molecular Biology, Princeton University – sequence: 12 givenname: Guohong surname: Hu fullname: Hu, Guohong organization: Department of Molecular Biology, Princeton University – sequence: 13 givenname: Benjamin A surname: Garcia fullname: Garcia, Benjamin A organization: Department of Molecular Biology, Princeton University – sequence: 14 givenname: Jiannis surname: Ragoussis fullname: Ragoussis, Jiannis organization: Wellcome Trust Centre for Human Genetics, University of Oxford – sequence: 15 givenname: Dino surname: Amadori fullname: Amadori, Dino organization: Osteoncology Center, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori – sequence: 16 givenname: Adrian L surname: Harris fullname: Harris, Adrian L organization: Cancer Research UK, Molecular Oncology Laboratories, Weatherall Institute of Molecular Medicine, University of Oxford, John Radcliffe Hospital – sequence: 17 givenname: Yibin surname: Kang fullname: Kang, Yibin email: ykang@princeton.edu organization: Department of Molecular Biology, Princeton University, Genomic Instability and Tumor Progression Program, Cancer Institute of New Jersey
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21822286$$D View this record in MEDLINE/PubMed
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Snippet	The miR200 family regulates EMT through E-cadherin modulation and has been proposed to contribute to metastasis thusly. This report identifies a promoting role... Although the role of miR-200s in regulating E-cadherin expression and epithelial-to-mesenchymal transition is well established, their influence on metastatic... Although the role of miR-200s in regulating E-cadherin expression and epithelial-mesenchymal transition is well established, their influence on metastatic...
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SubjectTerms	631/337/384/331 631/67/322 631/80/79/1902 692/699/67/1347 Animals Biomedical and Life Sciences Biomedicine Breast cancer Cadherins - metabolism Cancer Cancer Research Cell adhesion & migration Cell Line, Tumor Colonization Female Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic - physiology Humans Infectious Diseases Mass Spectrometry Metabolic Diseases Metastasis Mice Mice, Inbred BALB C Microarray Analysis MicroRNAs - metabolism Molecular Medicine Neoplasm Metastasis - physiopathology Neurosciences Proteins Statistics, Nonparametric Vesicular Transport Proteins - metabolism
Title	Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization
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