Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features
Some breast cancers have been shown to contain a small fraction of cells characterized by CD44⁺/CD24⁻/low cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells c...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 106; no. 33; pp. 13820 - 13825 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
18.08.2009
National Acad Sciences |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.0905718106 |
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| Abstract | Some breast cancers have been shown to contain a small fraction of cells characterized by CD44⁺/CD24⁻/low cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44⁺/CD24⁻/low and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44⁺/CD24⁻/low-MS signature. The CD44⁺/CD24⁻/low-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44⁺/CD24⁻/low-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. |
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| AbstractList | Some breast cancers have been shown to contain a small fraction of cells characterized by $CD44^ + /CD24^{ - /low} $ cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both $CD44^ + /CD24^{ - /low} $ and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this $CD44^ + /CD24^{ - /low} $-MS signature. The $CD44^ + /CD24^{ - /low} $-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both $CD44^ + /CD24^{ - /low} $-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. Some breast cancers have been shown to contain a small fraction of cells characterized by CD44 + /CD24 −/low cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44 + /CD24 −/low and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44 + /CD24 −/low -MS signature. The CD44 + /CD24 −/low -MS signature was found mainly in human breast tumors of the recently identified “claudin-low” molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44 + /CD24 −/low -MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin ( VIM ) in cytokeratin-positive epithelial cells metalloproteinase 2 ( MMP 2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. Some breast cancers have been shown to contain a small fraction of cells characterized by CD44 + /CD24 −/low cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44 + /CD24 −/low and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44 + /CD24 −/low -MS signature. The CD44 + /CD24 −/low -MS signature was found mainly in human breast tumors of the recently identified “claudin-low” molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44 + /CD24 −/low -MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin ( VIM ) in cytokeratin-positive epithelial cells metalloproteinase 2 ( MMP 2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. Some breast cancers have been shown to contain a small fraction of cells characterized by CD44+/CD24... cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44+/CD24... and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44+/CD24...-MS signature. The CD44+/CD24...-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44+/CD24...-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. (ProQuest: ... denotes formulae/symbols omitted.) Some breast cancers have been shown to contain a small fraction of cells characterized by CD44(+)/CD24(-/low) cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44(+)/CD24(-/low) and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44(+)/CD24(-/low)-MS signature. The CD44(+)/CD24(-/low)-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44(+)/CD24(-/low)-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients.Some breast cancers have been shown to contain a small fraction of cells characterized by CD44(+)/CD24(-/low) cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44(+)/CD24(-/low) and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44(+)/CD24(-/low)-MS signature. The CD44(+)/CD24(-/low)-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44(+)/CD24(-/low)-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. Some breast cancers have been shown to contain a small fraction of cells characterized by CD44⁺/CD24⁻/low cell-surface antigen profile that have high tumor-initiating potential. In addition, breast cancer cells propagated in vitro as mammospheres (MSs) have also been shown to be enriched for cells capable of self-renewal. In this study, we have defined a gene expression signature common to both CD44⁺/CD24⁻/low and MS-forming cells. To examine its clinical significance, we determined whether tumor cells surviving after conventional treatments were enriched for cells bearing this CD44⁺/CD24⁻/low-MS signature. The CD44⁺/CD24⁻/low-MS signature was found mainly in human breast tumors of the recently identified "claudin-low" molecular subtype, which is characterized by expression of many epithelial-mesenchymal-transition (EMT)-associated genes. Both CD44⁺/CD24⁻/low-MS and claudin-low signatures were more pronounced in tumor tissue remaining after either endocrine therapy (letrozole) or chemotherapy (docetaxel), consistent with the selective survival of tumor-initiating cells posttreatment. We confirmed an increased expression of mesenchymal markers, including vimentin (VIM) in cytokeratin-positive epithelial cells metalloproteinase 2 (MMP2), in two separate sets of postletrozole vs. pretreatment specimens. Taken together, these data provide supporting evidence that the residual breast tumor cell populations surviving after conventional treatment may be enriched for subpopulations of cells with both tumor-initiating and mesenchymal features. Targeting proteins involved in EMT may provide a therapeutic strategy for eliminating surviving cells to prevent recurrence and improve long-term survival in breast cancer patients. |
| Author | Sjolund, Ashley Fan, Cheng He, Xiaping Chang, Jenny C Rodriguez, Angel Renshaw, Lorna Rosen, Jeffrey M Creighton, Chad J Lewis, Michael T Li, Xiaoxian Zhang, Xiaomei Perou, Charles M Landis, Melissa Dixon, J. Michael Faratian, Dana Herschkowitz, Jason I Neumeister, Veronique M Rimm, David L Wong, Helen Gutierrez, M. Carolina Pavlick, Anne Hilsenbeck, Susan G Larionov, Alexey A |
| Author_xml | – sequence: 1 fullname: Creighton, Chad J – sequence: 2 fullname: Li, Xiaoxian – sequence: 3 fullname: Landis, Melissa – sequence: 4 fullname: Dixon, J. Michael – sequence: 5 fullname: Neumeister, Veronique M – sequence: 6 fullname: Sjolund, Ashley – sequence: 7 fullname: Rimm, David L – sequence: 8 fullname: Wong, Helen – sequence: 9 fullname: Rodriguez, Angel – sequence: 10 fullname: Herschkowitz, Jason I – sequence: 11 fullname: Fan, Cheng – sequence: 12 fullname: Zhang, Xiaomei – sequence: 13 fullname: He, Xiaping – sequence: 14 fullname: Pavlick, Anne – sequence: 15 fullname: Gutierrez, M. Carolina – sequence: 16 fullname: Renshaw, Lorna – sequence: 17 fullname: Larionov, Alexey A – sequence: 18 fullname: Faratian, Dana – sequence: 19 fullname: Hilsenbeck, Susan G – sequence: 20 fullname: Perou, Charles M – sequence: 21 fullname: Lewis, Michael T – sequence: 22 fullname: Rosen, Jeffrey M – sequence: 23 fullname: Chang, Jenny C |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/19666588$$D View this record in MEDLINE/PubMed |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: J.M.D., A.R., X.Z., A.P., M.C.G., A.A.L., J.M.R., and J.C.C. designed research; X.L., M.L., J.M.D., V.M.N., A.S., D.L.R., H.W., A.R., J.I.H., C.F., X.Z., A.P., M.C.G., L.R., C.M.P., M.T.L., and J.C.C. performed research; X.L., M.L., V.M.N., D.L.R., H.W., J.I.H., X.H., A.P., D.F., S.G.H., M.T.L., and J.M.R. contributed new reagents/analytic tools; C.J.C., X.L., M.L., V.M.N., A.S., D.L.R., H.W., A.R., J.I.H., C.F., X.H., A.P., M.C.G., L.R., A.A.L., D.F., S.G.H., C.M.P., M.T.L., J.M.R., and J.C.C. analyzed data; and C.J.C., X.L., M.L., A.S., D.L.R., A.R., S.G.H., C.M.P., M.T.L., J.M.R., and J.C.C. wrote the paper. 1C.J.C., X.L., and M.L. contributed equally to this work. 2M.T.L., J.M.R., and J.C.C. contributed equally to this work. Communicated by Robert A. Weinberg, Whitehead Institute for Biomedical Research, Cambridge, MA, May 26, 2009 |
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| SubjectTerms | antigens Biological Sciences Biopsy Breast cancer Breast neoplasms Breast Neoplasms - metabolism Breast Neoplasms - therapy Cancer CD24 Antigen - biosynthesis Cell Membrane - metabolism Cells Chemotherapy Claudin-1 Datasets drug therapy Epithelial cells Epithelium - pathology Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genes Humans Hyaluronan Receptors - biosynthesis Membrane Proteins - biosynthesis Mesoderm - metabolism Models, Biological neoplasm cells Neoplasm, Residual - etiology patients Polymerase Chain Reaction Signatures Studies Subpopulations Survival Survival analysis Treatment Outcome Tumors vimentin |
| Title | Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features |
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